(Ettore Majorana International Science Series) Davide Csermely, Danilo Mainardi (Auth.), Alberto Oliverio, Michele Zappella (Eds.) - The Behavior of Human Infants-Springer US (1983)

The Behavior of
Human Infants
ETTORE MAJOR ANA INTERNATIONAL SCIENCE SERIES
Series Editor:
Antonino Zichichi
European Physical Society
Geneva, Switzerland
(LIFE SCIENCES)
Recent volumes in the series
Volume 4 SELECTED TOPICS IN EXERCISE CARDIOLOGY
AND REHABILITATION
Edited by A. Raineri, J. J. Kellermann, and V. Rulli
Volume 5 THE AGING BRAIN: Neurological and Mental Disturbances

Edited by G. Barbagallo-Sangiorgi and A. N. Exton-Smith
Volume 6 THE LUNG IN ITS ENVIRONMENT

Edited by G. Bonsignore and G. Cumming
Volume 7 INVESTIGATION OF BRAIN FUNCTION

Edited by A. W. Wilkinson
Volume 8 THE IMMUNOLOGY OF INFANT FEEDING

Edited by A. W. Wilkinson
Volume 9 ADVANCES IN NEPHROUROLOGY

Edited by M. Pavone-Macaluso and P. H. Smith
Volume 10 CELLULAR BIOLOGY OF THE LUNG

Edited by G. Cumming and G. Bonsignore
Volume 11 BIOELECTROCHEMISTRY I: Biological Redox Reactions

Edited by G. Milazzo and Martin Blank
Volume 12 SELECTED TOPICS IN PREVENTIVE CARDIOLOGY

Edited by Angelo Raineri and Jan J. Kellermann
Volume 13 THE BEHAVIOR OF HUMAN INFANTS

Edited by Alberto Oliverio and Michele Zap pella
A Continuation Order Plan is available for this series. A continuation order will bring
delivery of each new volume immediately upon publication. Volumes are billed only
upon actual shipment. For further information please contact the publisher.
The Behavior of
Human Infants
Edited by
Alberto Oliverio
University of Rome
Rome, Italy
and
Michele Zappella
Regional Hospital-Siena
Siena, Italy
Plenum Press • New York and London

Library of Congress Cataloging in Publication Data
Main entry under title
The Behavior of human infants.
(Ettore majorana international science series, Life sciences; v. 13)

"Proceedings of the first workshop of the International School of Ethology on the
Behavior of Human Infants, held August 22-27, 1981, in Erice, Sicily, Italy"-T.p.
verso.
Bibliography: p
Includes index.
1. Infant psychology-Congresses. I. Oliverio, Alberto. II. Zappella, Michele M. III.
Series.
BF719.B431983 83-13965
ISBN-13: 978-1-4613-3786-7 e-ISBN-13: 978-1-4613-3784-3
001: 10.1007/978-1-4613-3784-3
Proceedings of the First workshop on the International School of Ethology on

The Behavior of Human Infants, held August 22-27, 1981,
in Erice, Sicily, Italy
© 1983 Plenum Press, New York

Softcover reprint of the hardcover 1st edition 1983
A Division of Plenum Publishing Corporation
233 Spring Street, New York. N.Y. 10013
All rights reserved
No part of this book may be reproduced, stored in a retrieval system, or transmitted

in any form or by any means, electronic, mechanical, photocopying, microfilming,
recording, or otherwise, without written permission from the Publisher
PREFACE
The present workshop started with various requests on behalf of

several participants: some of us suggested the desirability of having
only a free discussion, leaving papers aside: others would have
preferred to stick to papers, though enlarging the discussion of each
of them to more general topics. Further, intermediate positions were
also present. From these different proposals came the hypothesis that
a common frame or red line to all of our discussions on behavioural
development would be to see what could be done by an interexchange
of differing but converging disciplines in favour of children, and
in particular of children with psychic handicaps, in terms of preven-
tion and cure. At the end of three days of prolonged meetings, where
each paper was given and extensively discussed, one feels that a
number of referral points have emerged. On the one side the plas-
ticity of behaviour, on the other is reciprocity (between mother and
child, father and child and perhaps we should add between mother and
father). The third point, which perhaps has been only partially
covered, concerns the relationship between these two variables, i.e.
in terms of treatment of a child, the potential plasticity of his
behaviour can be used to his great advantage if it is related to the
historical common needs of the reciprocal relationship, for example,
between the child and his parents.
If these three referral points are accepted as significant in the

process of child development, then one may envisage a child psychology
and a child psychiatry very different from the present one, having
always as a starting point a careful observation of behaviour and
ability to re-open concepts (using Papousek's words) continuously.
Perhaps one of the main contributions that ethology is currently
making to these allied disciplines (psychology and psychiatry) lies
in its attempt to read behaviour in terms of main functional systems,
such as approach and avoidance, etc., where there are embedded inborn
programme activities as well as learned, cognitive and, in a word,
cultural components. This approach is in line with the results of
psychobiological studies conducted on infant development with the
idea of a fundamental adaptive system composed of two sets of
mechanisms: one set for exploring, approaching and getting to know
reality, the opposite set involved in avoidance and reduction of
v
vi PREFACE
informational input. The psychobiological approach allows a better

understanding of reciprocal behaviour between the infant and the
adult both on a cognitive and an emotional-social point of view and
emphasizes the need for play and creativity in that system.
Following this approach we have been able, for example, to see

in a longitudinal perspective how rich can be the first drama which
is played between mother and child and in a cross-cultural perspective
we were able to see common traits of this relationship in quite
different cultures. One feels that by clarifying the inborn compo-
nents, which are a part of man's history, one is better confronted
with the cultural components of his life.
These data support the more recent interpretations of severe

psychiatric disorders of children and fit perfectly with the more
advanced therapeutic results obtained in treating autistic children.
It was apparently through the display of some largely inborn uncon-
scious parental qualities that a number of autistic children can
improve or be healed through the help chiefly of their parents. In
these studies, however, it became evident that in order to move those
unconscious parental qualities which are so helpful in breaking down
the 'autistic wall' and in the recovery of child's ability to relate
to people and to the world, it was usually necessary to touch some
important component of the parent's historical relationship with his
child. Thus again cultural and biological aspects of man's history
corne together.
At the end of the meeting it was apparent from the discussion

that political consequences may follow: if this is true, we would be
inclined to think, or to hope, that it would be in the direction of
an education and a health system where the balance of power should be
able to oscillate, and to open the world to the one or to the other
part of the relationship and to a general attitude towards different
cultures more humble than is usual on the part of industrialized
societies, but in being able to understand what are the teachings
which can be drawn from them in order to solve present day problems
of children's education and mental health.
CONTENTS
Infant Signals 1
D. Csermely and D. Mainardi
A Comparative Approach to Behavioral

Development 21
A. Oliverio and C. Castellano
A Developmental Analysis of Suckling

in the Rat 39
J. S. Rosenblatt
The Interpretation of Sensitive Periods 57

P. Bateson
Social Development in Rhesus Monkeys:

Consideration of Individual
Differences 71
S. J. Suomi
And What of Fetal Audition? 93

M.-C. Busnel and C. Granier-Deferre
Some Peculiarities of Electrical Brain

Activity Correlated with Behavioral
States in Infancy: A Review 127
C. Faienza
Interpersonal Abilities of Infants as

Generators for Transmission of
Language and Culture 145
C. Trevarthen
Patterns of Parent-Child Interaction in

a Cross-Cultural Perspective 177
I. Eibl-Eibesfeldt
vii
viii CONTENTS
The Psychobiology of the First Didactic

Programs and Toys in Human Infants 219
H. Papousek and M. Papousek
Development of Social Avoidance in

Autistic Children 241
J. Richer
Parental Affiliation as a Key Reference

in the Treatment of Infantile Autism 267
M. Zappella
Urbanization as a Factor Influencing

Child Behavior 283
C. Stroppa
Index 295
INFANT SIGNALS
Davide Csermely and Danilo Mainardi
Istituto di Zoologia
Universita di Parma
Parma, Italy
INTRODUCTION
If any of us can distinguish at first sight an infant mammal or

bird from an adult of the same species, this depends partly on the
fact that we possess an ability to recognize the distinctive signals
associated with that species member. This concept was explained for
the first time by Lorenz (1943). In his paper he suggests that the
altricial young of many homeothermous species possess some common
features, especially in the head, the so called "baby schema". Such
similarities suggest an evolutionary convergence phenomenon that
allows a young animal to be recognized such not only by its parents
but also by strange adults of its own or even different species.
We assign the status of infant to an animal only if we recognize

the presence of certain characters, largely unspecifiable; that is,
only if both behavior and appearance coincide with what German
Authors would call infant 'Gestalt'. This is not a defined, unitary
image. Rather, it is a combination of broad characters, applicable
to a large number of mammals and birds. Thus, the use of the label
"infant" or "immature" is the result of a decision which is taken
only after these characters have been examined.
Human "infant Gestalt" is quite similar to that of many other

species. Presumably, this is the reason why man, after becoming a
hunter, did not kill all the animals he met indiscriminately, but now
and then would spare or even adopt some, starting in some cases the
process of domestication.
The origin and evolution of infant form is evident when one

considers the natural situation in which this form is most effective,
2 D. CSERMELY AND D. MAINARDI
i.e. the moment of reproduction. An adult who has produced some

offspring will recognize his progeny only if it possesses specific
characters. Therefore, the infant -must use signals to communicate
with his parents, and the parents in turn must be able somehow to
receive his signals. These communication signals involve the entire
range of sensory capabilities: vision, hearing, smell, taste and
perhaps touch as well. When the signals fade out, or disappear, the
parents lose interest in their offspring. It is probable that wean-
ing is based upon a mechanism of this sort.
But adults are not always willing to provide parental care for
the young. In order for infant signals to be recognized and to evoke
the appropriate response, specific signals must be present. Tinbergen
(1969) found that herring gulls (Larus argentatus) completely ignore
or even eat a herring gull egg if the egg is presented to an indi-
vidual which is not breeding. However, the same egg will release
parental behavior if it is offered just prior to egg-laying. In
other cases, it is probably the presence or sight of the young that
triggers off parental response (Noirot, 1964a,b,c, 1965; Carlier and
Noirot, 1965; Gandelman, 1973). An extreme example of this is ma-
ternal imprinting in sheep: ewes recognize and accept their lambs
only after they have learnt their odor (Hafez, 1975).
The place where the infant is encountered may be especially

important. Gannets (genus Sula) generally accept strange chicks in
their nest, but viciously attack their own chicks if these approach
the nest from outside (Nelson, 1975). In the house mouse (Mus muscu-
lus), a highly territorial species in which parental care is well
developed (see for example Svare et al., 1977; Priestnall and Young,
1978; Csermely and Mainardi, 1981), Beilharz (1975) found that males
take care of strange pups, if these are found within their home
range. Otherwise, the young are ignored or even killed.
INFANT SIGNALS IN ADOPTION OF YOUNG
The young have evolved the ability to produce signals that evoke
recognition by adults and block aggression, probably also because
they are almost completely unprotected from adults (for example,
species with altricial young). The signals produced by the infants
not only increase the survival rate of the young who happen to en-
counter strange adults, but also raise the fitness of their parents.
This provides the basis for adoption, a highly developed behavior,
especially in rodents. An infant that has inadvertently become
separated from its parents not only blocks the aggressive behavior of
the adults that meet him, but also evokes a tendency to retrieving
and adoption. Infant signals, then, serve as releasing mechanisms.
In addition, different species have evolved similarities in the

key stimuli associated with their infants. Evolutionary convergence
INFANT SIGNALS 3
in infant signals further increased the species' genetic benefit (in

terms of fitness). Because the infant could be recognized, it could
block aggression and evoke parental care. Thus, infant signals must
be somewhat indefinite so that they can be adapted to a broad range
of animal groups.
Intraspecific and interspecific adoption in rodents has been an

active field of research for several years at the Institute of
Zoology, Parma. The aim was to identify which infant signals elicit
adoption mechanisms.
Initially, we set out to study interspecific adoption between

golden hamsters (Mesocricetus auratus) and house mice (Mus musculus
domesticus). The first set of experiments (Mainardi et al., 1970)
were carried out to see whether lactating female hamsters could be
brought to adopt young mice of exactly the same age as the young
hamsters. The experiments were carried out in the morning, after
waiting for the female to leave the nest for a while and putting the
young mice into it. Sixteen females at different stages of nursing,
with water and food "ad libitum", were tested with one or two young
mice aged between 3 and 12 days. The results obtained indicate that
the females readily adopted all the pups (27 individuals) (Table 1).
Although only 15 of these lived up to 20 days of age, after they had
been taken out of the nest, their death did not appear to depend upon
a lack of parental care.
A second parallel set of tests was done to see whether young of

different species could elicit maternal behavior in virgin female
hamsters - a phenomenon that had already been demonstrated in golden
hamsters put in contact with young of their own species (Noirot and
Richards, 1966; Richards, 1966; Rowell, 1961). The females were
divided into two groups. Those of the first group were put in con-
tact with a newborn mouse, then, ten days later, with one 6 day old
pup. The females of the second group were put in contact first with
one 6 day old pup, then, ten days later, with one newborn pup. All
the pups (20 individuals) were attacked, killed and eaten within a
short time: in no case did they evoke maternal care. Such cannibal-
istic behavior could not be due to insufficient nutrition of the
female, since these were fed "ad libitum" and could build a larder.
Hamsters, therefore, can recognize infant signals, but, in order to
do so, they must be in a specific physiological state.
Subsequent research (Mainardi et al., 1973) investigated several

factors influencing the mechanism of adoption. In the first set of
experiments, the females were tested with pups of the same age as
their own litter. These were placed in the female's nest at differ-
ent ages, from day 1 to day 15. The percentage of females performing
adoptions increased at first with the increasing age of pups, reached
100% from day 6 to day 12, and decreased to 80% on day 15 (Figure 1).
Statistical comparison of the results obtained on days 1 and 2 with
Table 1. Adoption of Mice by Golden Hamster Females and Relationship

Between Days Post-Partum and Pup's Age.
Females Days after Age of mouse Number of Adopted

birth tested mice mice
1 3 4 2 2
2 3 3 2 2
3 3 3 2 2
4 3 3 2 2
5 3 4 2 2
6 3 3 2 2
7 6 6 2 2
8 6 6 2 2
9 6 6 2 2
10 6 6 2 2
11 10 10 1 1
12 10 10 1 1
13 10 10 2 2
14 12 10 1 1
15 8 10 1 1
16 8 10 1 1
those obtained on days 3 to 12 was carried out using Fisher's test

and showed high significance (p = 0.008).
The second set of experiments was aimed at understanding whether

adoption was influenced by the age of the test pup or by postpartum
age of the mother female. The pups were divided into two groups: 6
day old pups (which had elicited 100% of adoptions in the previous
experiment) and newborns. The pups of the first group were placed in
the nest of females (10 individuals) who had given birth the day
before the beginning of the test (i.e. in a context that had produced
the lowest number of adoptions. in the previous experiment). The
pups of the second group were placed in the nest of females (10
individuals) who had given birth 6 days before. The results obtained
indicated a clear cut difference (p = 0.005): 40% of the newborns
were accepted and reared, while 100% of the 6 day old pups were
adopted even by mothers who were not very interested in providing
parental care. Therefore, the age of the pup, and perhaps its size,
are more effective than postpartum age of the mother for evoking
maternal behavior.
The third set of experiments was aimed at determining whether

the percentage of adoptions is influenced by where the pup is found
(inside or outside the nest). Again, the females who had given birth
to their litter on the day prior to the beginning of the test, were
divided into two groups. Each female was exposed to two mice pups,
INFANT SIGNALS 5
100
90
80
70
60
50
,/
I
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 days
Fig. 1. On the ordinate percentage of adoptions effected by

lactating female hamsters; on the abscissa age of mice and
hamster litters respectively.
inside and outside the nest. The females of one of the groups were
tested with newborns, while the females of the second group were
tested with 6 day old pups. When the pups were outside the nest, the
females accepted none of the newborns and only 23% of those aged 6
days. When the test pups were inside the nest, the females accepted
15% of the newborns and 70% of the 6 day old pups. Presumably, this
difference depends on the fact that the young mouse in the nest
absorbs the odor of the litter and consequently can conceal his
species. Once again, it is demonstrated that 6 day old mice rep-
resent a better stimulus for eliciting a maternal response in ham-
ster, than newborns.
"Abnormal behavior" of this sort is also found in intraspecific

contexts. When considering the evolutionary position of golden
hamsters, Richards (loc. cit.) suggests that this species may re-
cently have reduced its gestation period from about 20 to 16 days,
thus increasing the immaturity of their young. If, as this Author
suggests, the behavior of the female golden hamster has not "caught
up" with the newly acquired gestation length, we should expect
strange newborns to be treated as food, and killed. Accordingly,
nursing females and individuals who are not in the maternal physio-
logical state, such as males and virgin females, would tend to adopt
pups, at least 6 day old. On the other hand Siegel and Rosenblatt
(1980) have observed that males and naire females can be sensitized
to pups and are capable to show maternal responsiveness.
In the previous experiments it was possible to evoke retrieving,

as well as adoption. The test pups who had previously absorbed the
odor of the young hamsters were all newborn, hardly capable of
evoking maternal care. Once the female hamster had been lifted out
of the cage, on the day after delivery, two test pups were placed in
the nest for 15 minutes, then placed outside the nest. The female
was put back into the nest and her behavior observed. Retrieval of
the pups occurred in 27 times out of 34 pups used (79.4%). Thus,
olfactory cues, in addition to age and position of the pup, play an
essential role in eliciting maternal behavior and can compensate for
such negative factors as low postpartum age of the female and high
immaturity of the pup.
Another experiment (Mainardi et al., 1976) analyzed an interest-

ing behavior pattern exhibited by females tested as in the previous
set of experiments. In some cases the female picked up the mouse in
her mouth and deposited it just outside the nest or at some other
point within the cage. After a while she picked it up again and took
it to another point. In particular, three females deposited the
mouse in the foods tore (thus treating it as food), then covered it
with nest material, exhibiting a distinctive parental pattern.
Another female carried the mouse into the nest and began to eat it.
This provides an example of ambivalent "conflict" behavior, in which
the individual is torn between two opposing motivation, dependent on
recognition or non-recognition of the infant.
Another set of experiments (Favoriti et al., 1977) again inves-

tigated interspecific adoption, but the tests were carried out on
mice females. The test pups were young mice and hamsters of differ-
ent size and age. The female was lifted out of her cage and two pups
were put close to each other at the end opposite to the nest. The
female was put back into the nest and the order of retrieving re-
corded. The females were divided into three groups: group A, in
which both pups were the same size (hamsters were 4 days younger than
mice); group B, in which the pups were the same age (hamsters were
bigger); and group C. in which the hamsters were smaller and 8 to 10
days younger than the mice (Table 2). In group A hamsters and mice
were retrieved with equal frequency (41.7% against 40.0%, p>O.OS).
In group B mice were retrieved more frequently than hamsters (53.8%
against 28.8%, p<0.025). In group C mice were retrieved less fre-
quently than hamsters (49.2% against 26.6%, p<0.005). These results
clearly show that size is an important factor in determining adop-
tion, and can compensate for intraspecific differences.
Using nursing female mice we also studied intraspecific adoption

through experiments on preferential retrieving of strange pups versus
own pups, it has also been possible to assess whether the female
recognizes her own litter (Favoriti and Mainardi, 1976). As in the
previous set of experiments, two pups were placed at the end opposite
to the nest. The pups used belonged to Swiss and C57 BL/6 strains.
INFANT SIGNALS 7
Table 2. Number of Hamsters and Mice Retrieved First in Every Group.
No. of Retrievals of Hamsters Mice Void

tests hamsters mice killed killed tests
Group A 60 25 24 11 1*
(41.7%) (40.0%) (18.3%)
Group B 80 23 43 8 6
(28.8%) (53.8%) (10.0%) (7.5%)
Group C 128 63 34 5 4 22
(49.2%) (26.6%) (3.9%) (3.9%) (17.2%)
*Mouse killed immediately after the hamster.
For each pair, a record was kept of which pup was retrieved first.
The results indicate that the mother did not respond selectively to
the pups. This happened both within the Swiss strain and in cross-
tests with one Swiss and one C57 BL/6 pup. Similar results were
obtained when the female was tested on the 1st and on the 10th day
postpartum. Because the female did not appear to discriminate
between the pups, another experiment was undertaken, to determine
whether age is an important factor in releasing maternal preference
(Favoriti et al., 1979). Using the same procedure as the previous
experiment, 22 lactating females were tested for response to newborn
and to 8-10 day old pups. Although some females did not chose a
single pup, on the whole they showed a clear cut preference for pups
aged 1 day (X 2 = 23.33, p<O.Ol). Comparison between these results
and those obtained by Mainardi and co-workers (1973) reveals that the
mothers responded differently to homo- and heterospecific pups. In
fact, while hamster females preferred 6 day old pups versus 1 day old
ones, the reverse was true for mice females. The effect of the
signal, therefore, depends on the receiver.
A comparison between the natural situation of species with

altricial young and that of species with_precocious young may offer
an explanation. Altricial young are not mobile until sometime after
birth, therefore they constantly require the presence of at least the
mother. Thus, it makes sense that highest sensitivity to signals
given by conspecific infants takes place in this period. However,
once the demand for parental care decreases and the young begin to
come into contact with the external world, they face a higher risk of
heterospecific interactions. The development of pleasing signals to
heterospecific individuals, i.e. predators, takes place in this
period (as we can observe in man, if we look at him as a predator).
On the other hand, in the species with precocious young, these are
exposed to the risk of predation at the same time when they require
most parental care. In these species, therefore, we do not observe
any shift in time of the effect of infant signals for homo- or
heterospecific situations.
Another experiment was aimed at carrying out a detailed analysis
of age versus size. In fact, the effect of different sizes might
interfere with that of different ages in test pups. This might imply
differences in motor coordination, vocalizations, presence or absence
of fur. The test pups were taken from a strain of mutant mice, which
produces some individuals homozygous for the allele controlling
achondroplasia (cn/cn) (Mainardi et al., 1978). Just after birth,
these individualS-have a recognizable short and round skull, a thick
tail, and are smaller than their normal siblings. Thus we were able
to use subjects of same age, hence in the same physiological state,
but of different sizes (Figure 2). The experiment was carried out as
before, but the test pups (normal and cn/cn) now were the offspring
of the lactating females. These (16 individuals) were tested from
day 1 to day 10 postpartum. As expected, the females tended to
prefer achondroplastic versus non-achondroplastic pups (59.1% against
34.4%; X 2 = 5.00, p<O.05).
Besides being smaller, ~/~ pups also tend to develop a round

skull, a character that presumably becomes a supernormal releaser.
Probably, these two are not the only morphological patterns eliciting
maternal response but, undoubtedly, they are the only ones to become
Fig. 2. Two young mice belonging to the strain carrying the "cn"
mutation. On the left a 16 day old normal, on the right
an achondroplastic sibling (cn/cn).
INFANT SIGNALS 9
exaggerated in such individuals. In his well-known work on the

morphological characters typical of infants, Lorenz (loc. cit.)
showed that the dome shaped skull is an infant character present in
most homeothermous species. Since the individual possessing such
characters receives more attention than does an individual who lacks
them, these can be legitimately considered as signals. The charac-
ters include a large head in proportion to the body, large eyes below
the mid-line of the face, round cheeks, short limbs, a rounded body,
a soft body surface. In mammals, especially in canids, one might add
floppy ears. (In this connection, it is interesting to note an
oversight in the illustrations to Lorenz's paper: these include the
head of an adult gun dog with floppy ears) (Figure 3).
Other types of signals, besides body size, may encourage adop-

tion, Fairhust (1976), in her study of the bird colony of Bempton
Cliffs, Yorkshire, recorded some cases of gannets (Sula bassana)
adopting guillemots (Uria aalge). This Author suggested that the
black and white plumage pattern of guillemot chicks might be the
releaser for adoption in gannets. Instead, the white plumage of
gannet chicks would be a substimulus, since as previously reported
by Nelson (loc. cit.), these are attacked by adults round about if
they wander away from their nest. In sheep, Alexander (1977) and
Alexander and his co-workers (1977, 1978, 1979) have demonstrated
that Merino ewes accept their own lambs only if these possess
specific visual cues. In particular, ewes accept a lamb which has
been colored black, provided that its head has not been given the
same color. Furthermore, ewes tend to accept strange lambs, if these
have been colored, but only if they are their own color. Similarly,
importance of differences in coloration between infants and adults as
elicitor of parental care has been suggested by Alley (1980) in
primates.
The evolution of intraspecific detection of signals was followed

by adoption between different species, which in turn gave origin to
. --
~-. --------~---
- .. --- -- -- --
~ -~
----- ----- ------- -- --. - -. ----
Fig. 3. Lorenz's "baby schema". Note the floppy ears of the adult
gun dog.
the remarkable mechanism of brood parasitism. Following a co-

evolution mechanism, cuckoos (Cuculinae) have developed eggs which
closely resemble in appearance the host's own egg, and with a re-
duction of the incubation period. After hatching, the parasite
exploits exaggerated releasing mechanisms, or supernormal releasers.
In fact, the newly hatched cuckoo opens his beak over and over again
exposing its brilliant red lining, which is more marked than that of
the host's nestlings. Because these two cues are so exaggerated and
hosts cannot ignore them, the nestlings cuckoos are fed continuously
at the expense of their "stepbrothers", and are reared, even if they
differ greatly in appearance from host nestlings and adults. In
contrast, the females of some African weaverbirds (Genus Steganura)
have chosen the evolutionary path of mimetism. Instead of using
supernormal releasers, they have evolved a perfect copy of the mouth
"buttons" typical of their hosts' fledlings. Their hosts cannot
discriminate between their own nestlings and those of the parasite,
therefore they feed the individuals of both species.
In laboratory rats, overall motility of the pups is an important

visual cue. Cone (1974) points out that on the sixth day post-
partum, mothers retrieve their active young faster than their non-
active ones. Piccirillo and colleagues (1979) have obtained similar
results with pups in which hyperactivity was experimentally produced
by injecting 6-hydroxydopamine. Although Smart (1976) found no
difference in retrieving times between well-fed and under-fed pups,
he recorded that the former elicit more licking by their mothers.
Grota (1973) suggested that the acceptance of newborn rats,

immediately after birth, is mediated by olfactory signals. Using
litters whose delivery had been obtained surgically, he demonstrated
that the survival rate of pups is determined by the odor of the
amniotic fluid, which interacts with substances contained in the
placenta. If the mother does not contact these fluids, she ignores
her offspring. A phenomenon of this sort has been observed in ewes
who lost their lamb just after birth. These subjects could then be
brought to accept a strange lamb, aged at least 2 days, provided its
skin had been wiped with the placenta, or covered with the skin of
her own lamb (Gibson, 1951).
Finally, another category of infant signals involves the audi-

tory system. When the young of the red kangaroo Megaleia rufa are
far from their mother, they produce specific vocalizations whose
function is to call the mother and to signal their position (Ewer,
1973; Russell and Nicholls, 1974). Similar behavior has been ob-
served in cats (Haskins, 1977) and sheep (Poindron and Carrick,
1976), and has been especially well studied in rodents, whose sounds
are mostly in the 50 to 70 KHz range. In many species, including
mice, rats and hamsters, the young emit two types of sounds, clearly
different in purpose and in the time of occurrence (Noirot, 1966b,
1968, 1972; Sales and Pye, 1974). During the four days following
INFANT SIGNALS II
birth, the newborns produce many high frequency sounds in response to

lac tile stimulation. These ultrasounds decrease from the fifth day
on. Then, on the 6-7th day after birth, the pups begin to produce
sounds in response to low temperatures. In fact, at this age, these
species become homeothermous (while, immediately after birth, they
are poikilothermous). When exposed to cold, they may go rapidly into
a coma, thus blocking breathing and the production of calls. With
the help of equipment that could generate sounds similar to those
produced by the young, Smith (1976) was able to show that adult mice
are attracted mostly by sounds of 45 to 65 KHz and 80 msec in dur-
ation. A similar technique was used by Mal'tsev (1974, 1976) with
rats. He observed that the typical signals of 4 day old pups attract
the female more than those produced by 17 day rats. Busnel and
Lehmann (1977) have denied that infant ultrasounds might inhibit
aggression by adults or evoke maternal behavior, although Noirot
(1966a, 1972) states this effect is real. In general, it has been
observed that high-frequency calls of the pups stimulate and maintain
the hormonal state of the mother (Smotherman et al., 1978; Terkel et
al., 1979); while at the same time they may influence specific par-
ental activities, especially nest-building (Noirot, 1969, 1974).
In some situations, as when the litter is too large, infant

signals are not effective in blocking cannibalistic behavior by the
mother, considered to be normal in situations of this kind (Day and
Galef, 1977; Gandelman and Simon, 1978). However, in mice it has
been observed that the less developed pups are killed more often than
the better developed ones.
At a later age young mice produce calls to block aggression by

adults. In general the young may exhibit specific a~~asement be-
havior, such as food begging in both birds and mamma~ or they may
suppress the releasers of the aggressive tendency in aaults, for
example in species where plumage pattern of the young differs from
that of the adults. In both cases, the young obtains an additional
advantage. In the first, they not only reduce aggression, but obtain
food. In the second, their cryptic coloration gives them better
protection against their enemies. The importance of recognizing the
young stems from the fact that they do not participate in the social
system of adults, and consequently are not involved in dominance-
sub ordinance interations. An example of this can be seen in mute
swans (Cygnus olor) , whose young are normally grey. In a few cases,
however, the young exhibit the white color typical of adults. It has
been demonstrated in this species that territorial pairs attack the
white young more often than the grey ones (Immelmann, 1980).
INFANT SIGNALS IN ADULT AND SOCIAL BEHAVIOR
Behavioral patterns typical of the young are found in some adult

displays, called "infantilisms". This form of behavior emerges in
socio-sexual contexts and serves to maintain group cohesion or pair

bonding. There are many examples of this sort of "infantilistic"
behavior. To appease another member of his species, a defeated dog
lies on his back, in a posture which is typical of pups. When a
chimpanzee meets a species member, in sign of appeasement and greet-
ing, he extends his hand, palm up, seeking contact with the other,
who in turn extends his hand, palm down. As mutual trust grows, the
two shake hands, kiss and embrace one another. When frightened, an
adult chimp may embrace a young one and calm down (van Lawick-
Goodall, 1968). In all these cases, we clearly observe the emergence
of the infant search for bodily contact.
During the early stages of courtship, the males of some species

produce vocalizations very similar to those of the young (immelmann,
loco cit.). Many male birds offer food to the females which they
court. This behavior resembles parental feeding and serves to over-
come the fear of close contact in the sexual partner.
Parental feeding has undergone many changes, in the course of

evolution. Consequently we find a great diversity of patterns used
by animal species. All the patterns, however, are probably drived
from the same original pattern. Thus, in songbirds, the female have
retained food begging only during courtship. Or both partners may
engage in beak flirting, in which they rub their beaks together, a
pattern derived from parental trophallaxis. Interestingly, in the
cuckoo Clamata jacobinus, a brood parasite, beak flirting has not
been retained as a component of the repertoire of parental behavior,
but it is still found in sexual behavior (Eibl-Eibesfeldt, 1976).
In the jackal Thos mesomelas food begging, where the young push their
muzzles into the sides of their parent's mouth, has been retained as
a greeting gesture (Goodall and van Lawick-Goodall, 1973).
In the light of the previous discussion it is apparent that

infant signals serve mainly as inhibitors of aggression and releasers
of liking. The latter function has been especially favored by
natural selection, which has increased the generality of the signal.
This permitted detection of the signal by strange conspecific adults
or even by nonspecies members. Consequently, we find examples of
altruistic behavior (i.e. helping individuals not belonging to one's
own family) such as communal nests in mice (Orv, 1944; Werboff et
al., 1970) or helpers in several families of birds (for example
Brown, 1978; Collias and Collias, 1978; Ligon, 1978; Ervin, 1979;
Lennartz and Harlow, 1979) and in canids (Macdonald, 1979; Mochlman,
1979).
SENSITIVITY OF MAN TO INFANT SIGNALS
Another evolutionary phenomenon, which is related to sensitivity

to infant signals, is the domestication of many avian and mammal
INFANT SIGNALS 13
species. As we have already pointed out, this process certainly

started in the Neolithic age, when the first group-living hominids
hunted animals and occasionally encountered newborns of wild species
(Hale, 1969). Sensitivity to infant signals blocked the aggressive
behavior and favored adoption. Imprinting-like processes led to the
formation of social bonds, with the integration of the animal into
human society.
A clear-cut example of this process is provided by the house

dog, in which domestication and subsequent selection was facilitated
by infant signals. In fact man has preferred, more or less advert-
ently, adult individuals with infant traits. As a result, these
characters are exhibited by most existent races. Pet dogs are a
"concentration" of infant patterns: short and thick paws, large
head, floppy ears, elastic and soft body surface. In contrast, in
breeds that are meant to arouse fear or respect, as watchdogs, selec-
tion favored the individuals who lacked infant characters. In the
doberman or boxer, for example, man himself removes by surgery the
infantile characters, which have not yet been eliminated by selec-
tion.
Man's attitude toward infantilization was also directed towards

his own species. His strong sensitivity to infant signals may have
contributed to their exploitation in a broad range of activities, for
example the doll industry (Lorenz, 1980). A clear example of this is
provided by the characters in cartoons. It is easily observed that
pleasing characters, whether they represent animals or humans, con-
tain a "concentration" of infant signals, while these are lacking in
"unpleasant" characters. Gould (1979) carried out an interesting
study on the "physical" evolution of Mickey Mouse which Disney
artists have continued since his first appearance. Gould notes that
Mickey assumed a more and more childlike appearance: his head and
eyes increased substantially and assumed an increasingly "positive"
feature. This Author concludes that Walt Disney anticipated the
evolutionary path of man toward our present neoteny, which is already
apparent.
Ponzo (1977) suggests that in our society adults, particularly

mothers, may have created a stereotyped fictitious image of the baby
with a relatively large head, the so-called "walt Disney's baby".
By presenting various models of infant faces to adults and

registering their response, Sternglanz and co-workers (1977) were
able to draw what they consider the "ideal" baby face, the one which
seems to possess the best releasers of parental behavior. In the
drawing of the face most often preferred the eyes and iris are large,
a feature essential in determining our preference for faces (Hesse,
1975). A point-like iris will evoke hostility, and it has been used,
for example, in "The Village of the Damned", a science fiction movie
produced in England in 1960, in which the character "point-like iris"
served to evoke a conflict behavior towards the children of alien

invaders (Mainardi, 1980); in fact, these children in all other
aspects, exhibited many infant signals.
In man, Lorenz's idea (loc. cit.) that infant Gestalt may serve
as an innate releasing mechanism has been confirmed by Fullard and
Reiling (1976), who found a difference in the preference for slides
depicting infants versus adults. The preference begins at puberty
and, as Hess has already observed in adults (loc. cit.), it differs
in males and females, appearing earlier and stronger in the latter.
One possible explanation for this fact could be the superimposition
of social factors upon an innate predisposition. Because in many
societies parental care is an exclusive duty of females, these may
have become more effective than males in identifying the fundamental
physiological and psychological states that underlie crying in babies
(Vuorenkoski, 1975). Another explanatory factor could be experience.
In fact, multiparous mothers recognize better, and are more sensitive
than primiparous mothers to be signals given by the child during
lactation in the early hours of life (Thoman, 1975).
Some infant signals can induce physiological changes in the

observer. By showing pictures of crying infants to strange mothers,
Donovan and co-workers (1978) were able to measure differences in the
conductivity of the skin and in the frequency of heartbeat. They
also found that the subjects, after a while, ceased to smile. In
other cases, Klaus and Kennel (1976) observed the onset of the se-
cretion of maternal hormones.
Infantilisms can be found also in man. In humans, as in many

other primates, the search for bodily contact has soothing effects
after shock or in courtship interations. Kissing behavior, which is
performed more often by males, is clearly derived from parental
trophallaxis, very similar to this behavioral patter of primates, and
is still used in some human populations (Eibl-Eibesfeldt, loco cit.).
Finally, it seems of interest to point out the possibility that

other species could be sensitive to the signals given by human
infants. For example, Lorenz (1973) stated that dogs are perfectly
capable of discriminating between adults and children. Although
specific researches are not available, some indications could be
provided by the great deal of reports available on "wild" human
infants, adopted and reared by animals (Ludovico, 1979). Adoption of
this sort probably is released by the same mechanism which underlies
retrieval behavior observed in many laboratory species. Neverthe-
less, since generally the cases reported were neither scientifically
studied or clear cut, their interpretation remains quite speculative.
INFANT SIGNALS 15
ACKNOWLEDGEMENTS
Researches carried out at our Institute of Zoology were sup-

ported by C.N.R. (Progetto Finalizzato Biologia della Riproduzione).
REFERENCES
Alexander, G., 1977, Role of auditory and visual cues in mutual

recognition between ewes and lambs in Merino sheep, ~
Anim.Ethol., 3:65-81.
Alexander, G., and Shillito, E. E., 1977, Importance of visual clues
from various body regions in maternal recognition of the
young in Merino sheep (Ovis aries), Appl.Anim.Ethol., 3:137-
143.
Alexander, G., and Shillito, E. E., 1978, Maternal responses in
Merino ewes to artificially colored lambs, Appl.Anim.Ethol.,
4:141-152.
Alexander, G., and Stevens, D., 1979, Discrimination of colors and
grey shades by Merino ewes: tests using colored lambs,
Appl.Anim.Ethol., 5:215-231.
Alley, T. R., 1980, Infantile coloration as an elicitor of care-
taking behavior in old world primates, Primates, 21:416-429.
Beilharz, R. G., 1975, The aggressive response of male mice (Mus
musculus)(L.) to a variety of stimulus animals, Z.Tierpsychol.
39:141-149.
Brown, J. L., 1978, Avian communal breeding systems, Annu.Rev.Ecol.
Syst., 9:123-155.
Busnel, R. G., and Lehmann, A., 1977, Acoustic signals in mouse
maternal behavior: retrieving and cannibalism, Z.Tierpsychol.,
45:321-324.
Carlier, C., and Noirot, E., 1965, Effects of previous experience on
maternal retrieving by rats, Anim.Behav., 13:423-426.
Collias, N. E., and Collias, E. C., 1978, Cooperative breeding
behavior in the white-browned sparrow weaver, Auk, 95:472-484.
Cone, A. L., 1974, Maternal retrieving behavior in rats as predicted
by locomotor activity and weight of six-day-old pups, Bull.
Psychon.Soc., 4:233-234. -----
Csermely, D., and Mainardi, D., 1981, Influence of social status on
paternal behavior in mice, Boll.Zool., in press.
Day, C. S. D., and Galef, B. G., jr., 1977, Pup cannibalism: one
aspect of maternal behavior in golden hamsters, J.Comp.
Physiol.Psychol., 91:1179-1189.
Donovan, W. L., Leavitt, L. A., and Balling, J. D., 1978, Maternal
physiological response to infant signals, Phychophysiology,
15:68-74.
Eibl-Eibesfeldt, 1., 1975, "Ethology. The biology of behavior",
second edition, Holt Rinehart and Winston, New York.
Ervin, S., 1979, Bushtit helpers: accident or altruism?, Bird
Behavior, 1:93-97.
Ewer, R. F., 1973, "Ethology of mammals", Elek Science, London.

Fairhurst, J., 1976, Gannets brooding guillemot chicks, Bird Study,
23:285-286.
Favoriti, M. P., and Mainardi, D., 1976, Assenza di disciminazione
tra figli ed estranei nell'ambito dell'adozione nel topo,
Ateneo Parmense, 12:259-269.
Favoriti, M. P., Mainardi, D., Mainardi, M., and Csermely, D., 1977,
Variazioni nei primi giorni di vita del-l'efficacia dei
segnali infantili nel topo e nel criceto, Istituto Lombardo
(Rend.Sc.) j!), 111:61-68.
Favoriti, M. P., Scoccianti, V., Csermely, D., and Maidardi, M.,
1979, Influence of pups age on preferential adoption in Mus
musculus, Istituto Lombardo, (Rend.Sc.) (B), 113:24-38.
Fullard, W., and Reiling, A. M., 1976, An investigation of Lorenz's
"babyness", Child Dev., 47: 1191-1193.
Gandelman, R., 1973, Induction of maternal nest building in virgin
female mice by the presentation of young, Horm.Behav.,
4:191-197.
Gandelman, R., and Simon, N. G., 1978, Spontaneous pup-killing by
mice in response to large litters, Dev.Psychobiol., 11:235-
241.
Gibson, E. J., 1951, Maternal behavior in the domestic goat,
Anat.Rec., 111:483 (Abstract), cit. in: "Imprinting", E.H.
Hess, van Nostrand Reinhold Co., New York.
Gould, S. J., 1979, Mickey Mouse meets Konrad Lorenz, Nat.Hist. (NY),
May:30-36.
Grota, L. J., 1973, The effects of the placenta and foetal fluids on
the acceptance of foster young, Dev.Psychobiol., 6:495-502.
Hafez, E. S. E., ed., 1975, "The Behavior of Domestic Animals", Third
Edition, Baillere, Tindall & Cassell, London.
Hale, E. B., 1969, Domestication and the evolution of behavior, in:
The Behavior of Domestic Animals", Second edition, E.S.E.
Hafez, ed., Baillere, Tindall & Cassell, London.
Haskins, R., 1977, Effect of kitten vocalization on maternal behav-
ior, J.Comp.Physiol.Psychol., 91:830-838.
Hess, E. R., 1975, "The Tell-Tale Eye", van Nostrand Reinhold Co.,
New York.
Immelmann, K., 1980, "Introduction to Ethology", Plenum Press, New
York.
Klaus, M. H., and Kennel, J. H., eds., 1976, "Maternal-Infant
Bonding", Mosby Co., Saint Louis.
Lawick-Goodall, J. van, 1968, The behavior of free-living chimpanzees
in the Gombe Stream Reserve, Anim.Behav.Monogr., 1:161-311,
cit. in: "Ethology. The Biology of Behavior", 1.
Eibl-Eibesfeldt, Holt Rinehart and Winston, New York.
Lawick-Goodall, J. van, and Lawick, H. van, 1973, "Assassini
Innocenti", Rizzoli, Milano.
Lennartz, M. R., and Harlow, R. F., 1979, The role of parent and
helper red-cockaded woodpecker at the nest, Wilson Bull.,
91:331-335.
INFANT SIGNALS 17
Ligon, J. D., and Ligon, S. H., 1978, Communal breeding in green

wood-hoopoes as a case for reciprocity, Nature, 276:496-498.
Lockard, J. S., Daley, P. C., and Gunderson, V. M., 1979, Maternal
and paternal differences in infant carry: U.S. and African
data, Am.Nat., 113:235-246.
Lorenz, K., 1943, Die angeborenen Formen mog1icher Ehrfahrung,
Z.Tierpsycho1., 5:235-409.
Lorenz, K., 1973, "E l'uomo incontro i1 cane", Adelphi, Milano.
Lorenz, K., 1980, "L'etologia", Boringhieri, Torino.
Ludovico, A., 1979, "La scimmia cestita", Armando, Roma.
Macdonald, D. W., 1979, "Helpers" in fox society, Nature, 282:69-71.
Maclean, C., 1979, "The wolf children", Penguin Books, Harmondsworth.
Mainardi, D., 1980, I segnali infanti1i, Psico1ogia Contemporanea,
7: 15-21.
Mainardi, D., Mainardi, M., Pasquali, A., and Zandra, C. F., 1970,
Adoption of mice by golden hamsters, Atti Soc.ltal.Sci.Nat.
Mus.Civ.Stor.Nat.Milano, 110:150-154.
Mainardi, D., Mainardi, M., Pasquali, A., and Zadra, C. F., 1973,
Adoption of mice by golden hamsters: the effect of the age of
the mouse, the meeting place and the olfactory stimuli,
Ateneo Parmense, 9:3-11.
Mainardi, D., Mainardi, M., Favoriti, M. P., and Pasqua1i, A., 1976,
A conflict behavior in nursing female hamsters, Atti Soc.lta1.
Sci.Nar.Mus.Civ.Stor.Nat.Mi1ano, 117:59-68.
Mainardi, D., Mainardi, M., Favoriti, M. P., Scoccianti, V., and
Cserme1y, D., 1978, Preferential retrieving in mice: exper-
iments with cn/cn strain, Istituto Lonbardo (Rend.Sci) (B),
112:62-65. -- -- -
Mal'tsev, V. P., 1974, Differentiation by rats of acoustic pain
signals of their young. Zh.Vyssh.Nerbn.Deyat.I.P.Pavlova,
24:617-622.
Mal'tsev, V. P., 1976, Estimation of acoustic signal preference by
rat mother during search of the pups, Zh.Evol.Biokhim.Fiziol.,
12:263-266.
Moehlman, P. D., 1979, Jackal helpers and pup survival, Nature,
277: 382-383.
Nelson, J. B., 1975, Functional aspects of behavior in the Sulidae,
in: "Function and Evolution in Behavior", G. Baerends, and A.
Manning, eds., Clarendon Press, Oxford.
Noirot, E., 1964a, Changes in responsiveness to young in the adult
mouse. I. The problematical effect of hormones, Anim.Behav.,
12:52-58.
Noirot, E., 1964b, Changes in responsiveness to young in the adult
mouse. II. The effect of external stimuli, J.Comp.Physiol.
Psychol., 57:97-99.
Noirot, E., 1964c, Changes in responsiveness to young in the adult
mouse. IV. The effect of an initial contact with a strong
stimulus, Anim.Behav., 12:442-445.
Noirot, E., 1965, Changes in responsiveness to young in the adult
mouse. III. The effect of immediately proceding performances,
Behavior, 24:318-325.
Noirot, E., 1966a, Ultrasons et comportement maternels chez les

petits rongeurs, Ann.Soc.R.Zool.Belg., 95:47-56.
Noirot, E., 1966b, Ultrasounds in young rodents. I. Changes with age
in albino mice, Anim.Behav., 14:459-462.
Noirot, E., 1968, Ultrasounds in young rodents. II. Changes with age
in albino rats, Anim.Behav., 16:129-134.
Noirot, E., 1969, Selective priming of maternal responses by auditory
and olfactory cues from mouse pups, Dev.Psychobiol.,
2:273-276.
Noirot, E., 1972, Ultrasounds and maternal behavior in small rodents,
Dev.Psychobiol., 5:371-387.
Noirot, E., 1974, Nest-building by the virgin female mouse exposed to
ultrasounds from inaccessible pups, Anim.Behav., 22:410-420.
Noirot, E., and Richards, M. P. M., 1966, Maternal behavior in virgin
female golden hamsters: changes consequent upon initial
contact with pups, Anim.Behav., 14:7-10.
Orv, R. T., 1944, Communal nests of the house mouse, Wasmann
Collector, 6:35-57.
Piccirillo, M., Cohen, D. J., Shywitz, B. A., Alpet, J. E., and
Marinelli, D., 1979, Maternal care received by rat pups
treated with 6-Hydroxidopamine, Physiol.Behav. 22:69-75.
Poindron, P., and Carrick, M. J., 1976, Hearing recognition of the
lamb by its mother, Anim.Behav., 24:600-602.
Ponzo, E., ed., 1977, "Il bambino semplificato 0 inesistente",
Bulzoni, Roma.
Priestnall, R., and Young, S., 1978, An observational study of
caretaking behavior of male and female mice housed together,
Dev.Psychobiol., 11:23-30.
Richards, M. P. M., 1966, Maternal behavior in virgin female golden
hamsters (Mesocricetus auratus Waterhouse): the role of the
age of the test pup, Anim.Behav., 14:303-309.
Rowell, T. E., 1961, Maternal behavior in non maternal golden
hamsters (Mesocricetus auratus), Anim.Behav., 9:11-15.
Russell, E. M., and Nicholls, D. G., 1974, Distress vocalizations of
young of the red kangaroo Megaleia rufa (Marsupialia:
macropodidae), J.Aust.Mamm.Soc., 1:251-254.
Sales, G., and Pye, D., 1974, "Ultrasonic communication by animals",
Chapman and Hall, London.
Siegal, H. I., and Rosemblatt, J. S., 1980, Hormonal and behavioral
aspect of maternal care in the hamster: a review, Neurosci.
Biobehav.Rev., 4:17-26.
Smart, J. L., 1976, Maternal behavior of undernourished mother rats
toward well fed and underfed young, Physiol.Behav., 16:147-
149.
Smith, J. C., 1976, Responses of adult mouse to models of infant
calls, J.Comp.Physiol.Psychol., 90:1105-1115.
Smotherman, W. P., Bell, R. W., Herzshberger, W. A., and Coover, G.
D., 1978, Orientation to rat pup cues: effects of maternal
experiential history, Anim.Behav., 26:265-273.
INFANT SIGNALS 19
Sternglanz, S. H., Gray, J. L., and Murakami, M., 1977, Adult

preferences for infantile facial features: an ethological
approach, Anim.Behav., 25:108-115.
Svare, B., Bartke, A., and Gandelman, R., 1977, Individual differ-
ences in the maternal behavior of male mice: no evidence for a
relationship to circulating testosterone levels, Horm.Behav.,
8:372-376.
Terkel, J., Damassa, D. A., and Sawyer, C. H., 1979, Ultrasonic cues
from infant rats stimulate prolactine release in lactating
mothers, Horm.Behav., 12:95-102.
Thoman, E. B., 1975, The role of infant in early transfer of
information, Biol.Psychiatry, 10:161-169.
Tinbergen, N., 1969, !Il comportamento sociale degli animali",
Einaudi, Torino.
Vueronkoski, V., 1975, Maternal recognition of infant sounds,
Symp.Zool.Soc.London, 37:331-338.
Werboff, J., Steg, M., and Barnes, L., 1970, Communal nursing in
mice: strain specific effects of multiple mothers on growth
and behavior, Psychon.Sci., 19:269-271.
A COMPARATIVE APPROACH TO BEHAVIORAL DEVELOPMENT
Alberto Oliverio and Claudio Castellano
Istituto di Fisiologia Generale dell Universita di Roma

Istituto di Psicobiologia e Psicofarmacologia del C.N.R.
via Reno, 1-00198 Roma
INTRODUCTION
What is the usefulness of a comparative approach to the study

of behavioral development during infancy? A large amount of research
has been done on behavioral ontogeny using different approaches
ranging from the evolutionistic meaning of the development to the
maturation of the neurochemical and neurophysiological cerebral
systems, to the role of the genetic and environmental factors with
respect to the development and finally to the toxicological and
pharmacological aspects of brain development. The laboratory animal
represents a good tool for 1) a comparative approach, because pre-
cocial and altricial species are available, 2) the study of the role
of genetic factors, because a number of inbred strains are available
belonging to the same animal species, either when birds and rodents
or complex mammals are considered, 3) the study of neurochemical and
neurophysiological factors, since, mainly for some species, a large
body of experiments exists in the field of neuroscience, and finally
4) the study of the toxicological and pharmacological factors, which
can be accurately screened; this screening is obviously impossible in
our species. A comprehensive review of all these arguments cannot be
given in a single paper owing to the very large body of existing
ethological, psychobiological and psychopharmacological evidence.
In this review only those trends in behavioral development which

are more important for a knowledge of the development of human in-
fancy or those in which much recent progress has been made, will be
considered. Four main topics are covered: 1) the meaning of behav-
ioral ontogeny in evolutionary terms, 2) the role of genetic factors
in behavioral development, 3) perinatal behavioral toxicology, 4) the
development of neurophysiological and neurochemical systems.
21
22 A. OLIVERIO AND C. CASTELLANO
1. BEHAVIORAL ONTOGENY FROM AN EVOLUTIONARY POINT OF VIEW
In general, as indicated by Altman (1966) and MacLean (1975),

the behavioral abilities of different species may be determined more
or less rigorously according to their level of encephalization. At
the lowest level, protochordates such as the amphioxus are character-
ized by a spinomedullary nervous system and by "reflex" activities;
at intermediate level, protovertebrates such as amphibia or reptiles
depend on paleocephalic mechanisms and on "instinctive" processes; at
the highest level, protomammals and mammals are endowed with neen-
cephalic structures and respond with individual "intelligent" behav-
iors. However, among mammals, the importance of the role of "instinc-
tive" or "intelligent" processes depends on that of the paleoencepha-
lic or neencephalic mechanisms: some species are characterized by
fixed-action patterns and others are more plastic and rely on flexi-
ble strategies. At one extreme, the nervous structure, and the
behavior that this allows, confine the specialist animal to a rela-
tively narrow niche. At the other end of the continuum, structure
and behavior are more flexible and versatile and allow the animal to
exploit a greater array of environmental situations. These broad-
niched animals are known as generalists. What are the advantages of
these two conditions? In a slowly changing environment of low varia-
bility, behavioral specialization may represent an advantage for the
specialist. However, there is the evolutionary risk that the envi-
ronment might deviate too rapidly for the individual to adapt. On
the other hand, the generalist organism, with a reduced number of
behaviors organized with a minimum of personal experience, spends its
entire life solving problems that the specialist's genetic background
has solved for it. While specialist species rely on fixed-action
patterns and on other behaviors that are more structurally deter-
mined, generalist species are more flexible, depend on individual
experience for acquiring useful behavior, and are able temporarily to
link diverse responses in new ways to solve new problems (Mayr, 1974;
Parker, 1974).
The distinction between specialist and generalist species is

based not only on cerebral evolutionary correlates but also on the
different mechanisms that may produce response variability. In
addition to their brain development, the security from predators or
the fact of living in a nonagonist social framework - defined as a
hedonic mode by Chance (1975) - may be conducive to the generation of
variable behaviors. Other mechanisms that have been related to the
production of behavioral variability are (1) living under relaxed
motivational pressures (Parker, 1974), (2) play behavior, and (3)
paradoxical sleep. This last mechanism has been related to the
evolutionary level of different species, and it has been indicated
that paradoxical sleep plays a more important role in the most
evolved mammals (Jouvet, 1976; Rojas-Ramirez and Druker-Kolin, 1977).
Of course the possession of a diverse behavioral repertoire must not
passively be related to the level of adaptive behavior or intelli-
A COMPARATIVE APPROACH TO BEHAVIORAL DEVELOPMENT 23
gence, although this repertoire (and behavioral plasticity) repre-

sents the necessary starting point.
In addition to their relationships with the level of encepha-

lization, behavioral rigidity or plasticity (specialization or gener-
alization) may be considered from the point of view of the maturity
of mammals at birth. In the precocial species (such as guinea pigs
or ruminants), sensory and motor maturation at birth allows immediate
identification with the mother and the establishment of social and
mother-offspring relationships resembling imprinting in birds (Scott,
1958; Sluking, 1965). However, in nonprecocial (altricial) mammals,
which form a heterogeneous group ranging from other rodent species to
carnivores and primates, including humans, the immediate postnatal
period is characterized by great maternal dependency, by a later
onset of primary and social relationships, and by immaturity of
sensor and motor abilities.
From an evolutionary point of view, precocity at birth may, for

given aspects, be equated, to behavioral specialization, and immatu-
rity at birth, to behavioral plasticity and generalization. The
precocial species have the advantage that the ontogeny of the CNS is
achieved during the fetal period and that the newborn organism is
practically mature enough for independent life soon after birth. The
behavioral adaptation of a precocial species is largely set by its
innate mechanisms (Sedlacek, 1974). The immaturity of behavioral
functions in the altricial neonate, at birth and during the first
days, months and even years, of postnatal life, is compensated by
parental behavior. The immature brain passes through critical devel-
opmental periods under different influences from the external envi-
ronment, which may have positive (or negative) effects on the process
of brain and behavioral maturation. In other words, while precocial
species have the advantages of the "specialist" and rely to a greater
extent on innate patterns, altricial species have the advantages of
the "generalist", that is, they are more flexible and open to the
effects of the environment.
Different maturational and behavioral patterns during infancy

lead to specific interactions with the environment; similarly, the
stimulating or detrimental effects of the environment have a more
pronounced effect on those species that reach maturity at a later
age. Whether an adult animal is a specialist or a generalist depend
on these early mechanisms and behavioral categories, on the type of
interaction with the environment, and finally, on the evolutionary
genetic mechanisms setting the types of species-specific or individu-
al cerebral and behavioral organization.
In general, behavioral precocity or immaturity cannot be con-

sidered in terms of phylogenetic progression. In fact, some species,
e.g, hares, are precocious at birth, and other closely related
species, e.g. rabbits, are clearly immature. Also within primates
there are clear differences in precocity and immaturity and in the

resulting mechanisms of attachment to the mother. These different
patterns, which have been reviewed by Jolly (1972), cannot even be
interpreted solely in terms of ecological adaptation, as is indicate
by different findings reviewed by this author. Both strategies
(behavioral immaturity and maturity) are adaptive in evolutionary
terms. However, when learning strategies are "chosen", rather than
fixed action patterns, the period of postnatal brain development
tends to be longer and the brain is subjected to positive or negative
influences from the environment. The long period of immaturity,
which characterizes our species, and the long process of brain matu-
ration which terminates around 15-18 years of age, represent an
important mechanism in evolutionary terms: the processes such as
early experience, sexual orientation, learning, cultural transmission
and so forth, possible are typical of the human species also because
the brain circuitry and behavioral mechanism are not preformed at
birth. Therefore, even though our species has a much larger brain
endowed with unique abilities and is characterized by very long
postnatal maturational processes, a comparative approach may prove
useful for the study of maturational processes and adaptive mecha-
nisms common to mammals.
2. BEHAVIORAL ONTOGENY: A GENETIC APPROACH
From a comparative point of view the studies of brain and behav-

ioral mechanisms in mammals indicate that the mammalian brain is an
"original" product in relation to the reptilian and avian brain
(Altman, 1966). However, within mammals there are profound differ-
ences in the levels of encepha1isation and in the relation between
the role of pa1eoencepha1ic vs neoencepha1ic mechanisms.
In a behavioral genetic approach to the problem of ontogeny of

behavior, it is important to work with species characterized by 1)
clear phenotypic differences at brain and behavioral level, 2) dif-
ferences in relation to precocity and maturity at birth, and 3)
behavioral rigidity or plasticity in relation to a number of pa1eon-
cephalic (instinctive) or neencepha1ic (adaptive) patterns. From an
analysis of the data available from the literature, the mouse repre-
sents the main tool (Lindzey and Thiessen, 1970; Oliverio, 1977) for
any behavior genetic analysis, and some inbred lines characterized by
different patterns of behavioral plasticity or rigidity may represent
a useful model in this type of analysis.
A very large number of strains of mice is available today

(Green, 1966; Medvedev, 1958; Staats, 1972), their genetic homozy-
gosity resulting from a number of studies based on different immuno-
logical methods. Thirty-nine strains have also been characterized
for their alleles for as many as 16 polymorphic loci. The variabili-
ty among these strains is at least as great as in any single feral
population, a large group of inbred strains with unique alleles and

no overlapping pedigrees being available as the best group to screen
for a hoped-for variant (Roderick et aI" 1971), The existence of
clear intraspecific phenotypic differences at the level of peripheral
or central nervous system has also been assessed, For example, the
strains SECt lReJ and DBA/2 are characterized by high performance
levels in a number of learning tasks and by low levels of exploratory
behavior and running activity, while the C57BL/6J strain shows poor
avoidance performance and maze learning but is very active (Oliverio
et aI" 1972),
A number of findings are available today on these three strains

(C57BL/6, DBA/2 and SEC/IRe) which are also characterized by a number
of biochemical differences at brain level (Oliverio et aI" 1979),
At the present time it is important to point out that the reason for
assessing these biochemical estimates was related to the amount of
behavioral data indicating that these strains are different and
present a useful behavioral model, For the sake of clarity it is
worth recalling the main characteristics of these strains,
C57 mice are characterized by lower brain weight (Roderick et

al,. 1971) and thinner brain cortex and corpus callosum (Gozzo et
aI" 1979) than SEC or DBA mice, by greater aggressive behavior
(Puglisi-Allegra, unpublished results; Southwick and Clark. 1966) by
higher exploratory locomotor and wheel-running activity (Malorni et
aI" 1975; Oliverio and Castellano, 1977; Oliverio et aI" 1972; van
Abeelen, 1966); by more pronounced circadian wheel running and sleep
rhythmicity (Malorni et aI" 1975) and by lower levels of passive or
active avoidance and maze learning (Bovet et aI" 1969; Oliverio et
aI" 1972; Sprott, 1971) than DBA or SEC mice, Finally, the time
spent in non-REM and REM sleep is lower in the C57 strain than in the
other two strains (Valatx et aI" 1972),
Reasons of space obviously make it difficult to summarize the

large number of findings available, However, two main points emerge:
(1) The three strains considered are characterized by sharp pheno-
typic differences at brain and behavioral levels, and (2) within the
framework of the classification proposed by Altman (1966) (3), it is
possible, generally speaking to indicate that the behavioral patterns
of C57 mice are characterized to a large extent by the role of paleon-
cephalic or instinctive processes (circadian patterns, locomotor
activity, maternal behavior, emotional and aggressive behavior),
while the behavioral patterns of SEC (or DBA or BALB/c) mice are
characterized by a more relevant role of the neencephalic processes
or individual adaptation (escape and avoidance behavior, visual dis-
crimination, maze learning, etc,), These behavioral data have been
fitted into a tenative theoretical model in which the two strains are
considered in terms of innate contributions or of learning,
C57- like rig i d SEC-I ike plastic

programmi ng prog rammi ng
Neencep ha lic
instnune.ntal functions
I'Nt;:llte eontribution ... Contrlbutlon by learning ~
Fig. 1. A theoretical model for the role of innate contribution or

of learning in the reflex, catering and instrumental
functions of two strains of mice (C57BL/6 and SEC/IRe).
It was previously noted that maturity at birth in mammals repre-

sents an important point in evolutionary terms, since the behavior of
precocia1 species must be related in part to innate mechanisms, while
altricial species, in which brain and behavioral maturation occurs
later, are more plastic and are modifiable to a greater extent by the
environment. The strains of mice previously considered are also
different in their patterns of postnatal neurological and behavioral
development. If we consider the electrocorticographic activity,
which has been shown to parallel the different stages of maturation
of the cortex (Kobayashi et al., 1963), some strains, e.t. C57, are
found to be more mature at birth and other, e.g. SEC, less mature: at
8 days of age the electrical activity of the cortex of SEC mice is
similar to that found in the C57 strain on day 1 of postnatal life
(Oliverio et al., 1975). Similar developmental differences are also
evident when a number of reflex activities are considered. Reflexes
such as cliff aversion, righting, placing, grasping, or the startle
response appear at an earlier age (3 to 4 days sooner) in the C57
strain (Oliverio et a1., 1975). These findings indicate that there
are clear genetic differences in the intraspecific patterns of post-
natal maturation, which suggests that the individual genetic makeup
may also set the limits within which the environment is able to
affect the patterns of postnatal maturation.
It may well be that a strain that is more precocia1 at birth is

less reactive to environmental differences (1) because its behavior
is more "rigidly" determined and (2) because a more precocia1 brain
maturation leaves less room for the stimulating or detrimental ef-
fects of environmental situations. Independently of the mechanisms
.
.
EVES ....
OPEN
EARS ....
OPEN
. •
BAR ....
HOLDING
HAIR
GROW
....
VIBR ISSAE
PLACING • ....
CLIFF .....
5 10 15
DAYS OF POSTNATAL LIFE
Fig. 2. Some developmental measures occurring at different ages in

C57BL/6 (circles) and SEC/IRe (triangle) mice. It is
evident that the maturation of the SEC strain is delayed in
relation to C57BL/6 mice.
involved the effects connected with an early impoverished or enriched

environment have been shown to be less evident in the C57 strain than
in the SEC strain. In fact, SEC mice reared postnatally in an en-
riched or impoverished environment respectively attained a higher or
lower performance in different learning tasks in the adult stage.
However, the effects of the two environmental situations are less
evident in the C57 strain (Oliverio, 1977).
Two other findings indicate that the patterns of behavioral

ontogeny are clearly different in these two strains.
1) The recovery after lesions of the limbic system (septal

lesions) was studied in these two strains of mice (Oliverio, 1979):
since limbic-dependent responses are evident at an earlier age in
precocious rodents it was hypothesized that septal lesions in the
more precocious C57 mice would result in a more severe deficit than
in the less mature and "plastic" SEC mice. In fact, lesions produced
at 2 days of age permanently effected behavioral development of C57
mice. Septal lesions in infancy or adulthood enhanced the locomotor
behavior of C57 mice as well as avoidance responding or the number of
errors in a Lashley III maze. On the contrary, septal lesions pro-
duced during infancy did not modify the behavioral ontogeny of SEC
mice nor their behavior as measured in the adult age. As previously
indicated SEC mice are characterized by slower patterns of matura-
tional processes and by behavioral plasticity; thus it may be sugges-
ted that some form of recovery takes place in early operated SEC
mice, while in C57 mice, which are less precocious, the functions of
the damaged area are not compensated for.
2) Sexual preferences between perfumed and non-perfumed males

were assessed (Alleva et al., 1981) in adult female C57 and SEC mice
reared by parents whose odour was artificially altered; as in pre-
vious experiments by Mainardi et al., (1965), C57 females reared by
perfumed parents spent most of their time with a perfumed male, while
SEC females did not exhibit any clear-cut preference. Since C57 mice
are more mature at birth also this fact suggests that the strain
differences related to sexual choices may be explained in terms of a
higher sensitivity of C57 mice to early experience.
Thus, a number of biochemical and morphological differences at

brain level characterize strains that also differ in their pattern of
postnatal development and present clear-cut behavioral differences in
the adult. Other findings indicate that the strains considered are
not only different in their developmental rhythms, or characterized
to a larger extent by "instinctive" processes or by patterns of
individual adaptation, respectively, but are also characterized by
behavioral rigidity or plasticity in different environmental situa-
tions.
As previously noted, the paleoencephalic activities control a

number of circadian energy-deployment processes. As for the strains
considered in our theoretical model, it was shown that C57 mice are
characterized by clear-cut differences between the circadian patterns
of sleep, while no sharp differences are evident in the SEC strain
(Valatx et al., 1972). Recent data on these strains of mice also
indicate that free-running rhythms of sleep and activity may be
plastic or rigid, depending on the genetic factors involved in the
expression of circadian rhythmicity. Under 12-12 hour light-dark
(L-D) schedules it was shown that the external synchronizer induces
well-defined activity phases at night and lower levels during the
hours of light in C57 and SEC mice. However, when the running activ-
ity of the strains was assessed under constant light (L-L) or dark-
ness, it was shown that C57 mice (and other strains such as BALB/c)
do not show a clear-cut circadian rhythm (Ma1orni and Oliverio, 1978;
Oliverio, 1977).
A clearer demonstration of the importance of the genetic factors

in modulating the plasticity or rigidity of those two (and other)
strains was afforded by studying wheel running and sleep under L-D
schedules shorter than 12-12 hours. The effects of 12-12-hour,
6-6-hour, 3-3-hour, and 1-lhour L-D cycles and of constant light
(L-L) were studied in C57 and SEC mice (Oliverio and Malorni, 1979).
Wheel-running activity and sleep were inhibited by light and enhanced
by darkness; however, in the C57 strain the L-D induced changes were
less pronounced and were superimposed on a clear circadian rhythm.
Under the subsequent L-L schedule, clear patterns of daily rhythm-

icity were evident in the C57 strain but not in the SEC strain. A
second finding was rather interesting: SEC mice shifted from a short
L-D schedule on to a condition of constant light, for a short time,
retain the experience of their previous rhythmic performance, that
is, they show a rhythmic behavior similar to that induced by the
previous L-D schedule, which might indicate that a pace-maker is able
to "memorize" a rhythm determined by environmental cues. This find-
ing and the absence of rhythmicity of SEC mice under constant light
indicate that there are nonspecific structures that may assume a
transient pacemaker function when the circadian rhythms are not
rigidly programmed. Therefore, it seems likely that some strains are
more plastic and are influenced by the environment not only for a
number of acquired "neencephalic" behavioral activities but also for
such instinctive paleoencephalic behavioral processes as sleep or
locomotor activity.
Do these findings mean that these patterns of circadian rhythm-

icity respond essentially to inborn mechanisms, and that we must
consider that the C57-type of circadian rigidity is determined by an
inborn mechanism? Generally it is assumed that a number of circadian
functions respond to strict inborn mechanisms; however, it may be
that for some individuals or species these mechanisms can be modulat-
ed by early experience as well. The rhythms of animals have been
studied for generations under constant conditions and also under
unusual daylight schedules to ascertain whether behavioral rhythms
are learned early in life or whether they respond to inborn mecha-
nisms (Aschoff, 1960). The problem is rather difficult since, under
conditions of constant light, mammals could bequeath circadian
rhythms to their young by rhythms of maternal activity. These
rhythms may be transmitted to the young mammals through successive
generations despite constant or anomalous environmental conditions.
Since C57 mice arp. more mature at birth than SEC mice, this fact may
play an important role in a number of precocious interactions with
the environment: it might also be that in an altricial species such
as Mus musculus imprinting-like phenomena play an important role, and
that this role is more evident in those strains that are more mature
at birth. As a matter of fact, the relationships between early expe-
rience and sexual preferences in the mouse were assessed by Mainardi
et al., (1965) and recently were discussed by Bateson (1980).
The experiments on circadian rhythmicity support the existence

of imprinting-like mechanisms and indicate that rearing in constant
light or imprinting to 12-12-hour L-D cycles can affect wheel-running
activity. As was previously noted, a clear circadian rhythm is
characteristic of C57 mice reared under 12-12-h L-D cycles when their
activity rhythm is allowed to free run in continuous light, while no
evidence of circadian rhythmicity is evident in the SEC mice. On the
contrary, C57 and SEC mice reared under constant light do not show a
clear pattern of daily rhythmicity under continuous light. C57 mice
GENETIC MODE OF ENVIfONMENTAL PHENOTYPE

FACTORS ..TERACTION
IRAIN BIOCHEMICAL BEHAVIORAL

DIFFERENCES PRECOCITY RIGID BEHAVIORAL
PROCESSES
-.nNT1NG - LIKE
IRAIN STRUCTURAL PROCESSES
DIFFERENCES
BEHAVIORAL
IMMATURITY PLASTIC BEHAVIORAL
BRAIN AND BEHAVIORAL PROCESSES
MATURITY OR IMMATURITY LEAR_ca
PROCESSES
Fig. 3. A theoretical model for the role of genetic and

environmental factors related to behavioral rigidity or
plasticity.
imprinted to 12-12-h L-D cycles during days 15 to 18 show a clear

circadian pattern under constant light. As expected no evidence for
the imprinting-like phenomenon was evident in the SEC mice (Malorni
and Oliverio, 1978).
In general the findings reported in this section emphasize the

existence of rigid or plastic behavioral mechanisms within the same
species and also in relation to paleoencephalic mechanisms, which
should be strictly set by the genetic makeup. Again the possibility
that cerebral precocity or maturity at birth influences behavioral
specialization or generalization cannot be ignored.
3. BEHAVIORAL DEVELOPMENT TERATOGENY
There is growing evidence that nervous tissue, especially the

brain, is more sensitive to many foreign chemical substances than had
previously been suspected.
The detection of toxic processes and their cumulative effects

with time may be greatly facilitated by sensitive and reliable behav-
ioral evaluation procedures (Spyker, 1975). Changes in behavior can
serve as early indicators of potential damage to the organism and its
environment. It is fairly well accepted that an individual is more
vulnerable to certain adverse factors during the period of develop-
ment than in any other time in life. As indicated by a number of
studies (see Spyker, 1975), distinguishing features contributing to
making developing organisms more vulnerable to environmental insults
than the mature organism include a number of physiological patterns
such as differences in metabolizing enzymes, the development of
protecting systems such as the blood-brain barrier or binding capaci-
ties of the serum and time processes.
It was previously believed that the fetus was protected by a

placental barrier. Although the maternal organism may metabolize a
chemical or reduce its concentration, the function of the placenta as
a barrier is limited, and molecules of most substances - from nutri-
tionals to addicting drugs - can cross the "barrier". Consequently
many chemicals to which the pregnant organism is exposed will ulti-
mately reach the fetus. Furthermore, the immature organism does not
have the same capacity as an adult for metabolizing noxious sub-
stances. It has been shown that the fetus and the newborn have not
yet developed the mechanisms to detoxify and excrete a variety of
drugs and environmental chemicals.
The vulnerability of the newborn is evident from the large and

increasing amount of congenital malformations and severe functional
deficits, resulting from prenatal exposure to drugs, toxic agents and
other chemicals of the environment. Assessment of the functional
consequences of an insult has been named "behavioral teratology".
This term suggests that teratogens may have special affinities for
developing fetal brain centers, that the developing brain is very
vulnerable to insults and finally that alterations in neural develop-
ment result in alterations in behavior. Although many questions
remain to be answered concerning the behavioral consequences of
teratogens, it appears that these factors that determine the type and
extent of structural abnormality also influence the type and extent
'of behavioral abnormality. In this regard five basic factors have
been outlined, as follows: 1) a given genetic predisposition, associ-
ated with 2) a particular teratogen, administered at a given 3)
dosage level during a specific 4) stage of development. In addition,
since the maternal organism provides the environment for the develop-
ing organisms, maternal/fetal offspring interaction is also a factor
that has been considered.
One of the main fields within behavioral toxicology is related

to the different types of malnutrition resulting in cerebral and be-
havioral damage. Generally it has been assumed that caloric-proteic
malnutrition represents the main problem, while a number of recent
findings also indicate that lipidic malnutrition results in many
subtle damages, since lipids play an essential role in myelinogenesis
and in the formation of synaptic membranes, of neurons and glia.
A growing number of experiments and clinical findings suggest

that malnutrition during pregnancy affects brain growth and exerts
negative effects on postnatal behavioral development, resulting in
the stunting of many essential behavioral patterns such as learning
(Dobbing and Smart, 1974). From an experimental point of view the
use of the inbred strains of mice represents a useful tool in the
study of the effects of early malnutrition on electrophysiological
and behavioral development, since it is possible to ascertain the
effects of malnutrition on particular brain systems and behavioral
abilities characteristic of contrasting inbred strains. As a case in
point, mice from a random bred strain and from SEC/IRe and C57BL/6
strains were used, and the effects of malnutrition were assessed by

artificially altering the litter size at birth, using small (four
pup), intermediate (eight pup), or large (16 pup) litters (Oliverio
et al., 1975). An analysis of the effects of early malnutrition on
brain and body weight showed that clear cut deficits were evident
from the first weeks after birth. Mice from large litters were
characterized at 16 and 24 days of age by body and brain weights that
were, respectively, 50 and 30% lower than those evident in mice
belonging to the small litters. This deficit was still evident in
adult 60-day-old mice.
When the development of a number of reflex activities was con-

sidered. it was evident that in well-nourished mice reflexes such as
the rooting reflex were mature from the first day in all strains and
other reflexes such as cliff aversion or righting appeared on the
third day. whereas still other reflexes appeared at a later age.
Early malnutrition exerted a negative effect on the development of
some of these reflexes; although the rooting reflex was unaffected.
cliff aversion. righting, placing. and grasping appeared at a later
age in the large litters. Some differences were evident between
C57BL/6 and SEC/IRe mice; reflexes such as righting and placing. for
example. were more affected in C57 mice than in the SEC strain.
The measures of ECoG activity showed that the postnatal matura-

tion of the ECoG activity was delayed by malnutrition in all strains.
For example, random-bred mice belonging to well-nourished litters
showed a rhythmic pattern (6 to 10 cycles/sec) from the fourth day of
age. and the tracing increased in voltage at 16 days and reached its
highest amplitude by the 24th day. In contrast. electrical activity
was extremely low at 4 or 8 days in the large litters. which showed.
only after 16 days of age, a pattern similar to that evident at 4
days in well-nourised mice. When inbred mice were considered. it was
evident that ECoG maturation was more precocious in well-nourised C57
mice than in SEC mice; thus a delay in the ECoG maturation was evi-
dent at an earlier stage (day 4 to 8) in the C57 strain. since small
litters from the SEC strain showed barely detectable ECoG activity at
this stage. However, the ECoG maturation of the mice belonging to
intermediate and large litters of both strains reached adult level
only at 24 to 30 days of age, without displaying those intermediate
patterns evident in the small litters at 8 (C57BL/6) or 16 days
(SEC/IRe).
The detrimental effects of malnutrition on brain development

were evident when locomotor activity and avoidance learning were
assessed in adult mice malnourished during the suckling period.
These measurements were taken in 60-day-old mice following dietary
rehabilitation. With respect to the locomotor activity. the C57BL/6
mice belonging to small litters were more active than SEC/IRe mice.
as previously demonstrated (Oliverio et al., 1972); a general trend
toward an increased exploratory activity, independently of the strain
considered, was observed as litter size increased. In contrast,
avoidance learning of Swiss and SEC mice was greatly impaired in

early malnourished mice. No obvious effect following dietary depriv-
ation was detectable in the poor avoiding C57BL/6 mice.
A more selective and interesting type of malnutrition is that

derived from diets deprived of essential fatty acids (EFA). It must
be emphasized that the advantage of this method is that the use of
EFA malnutrition during pregnancy avoids the possible pitfalls con-
nected with an altered mother-offspring ratio, as in experiments in
which malnutrition is obtained by varying the litter size.
The results show that brain and body growth patterns were only
slightly affected in mice born from females fed EFA-deprived diets
during pregnancy. However, a number of reflexes, for example, the
placing reflex, appeared later in the EFA group than in control mice;
similarly, grasping and bar holding were also delayed by 2 to 3 days,
as in mice malnourished during the suckling period (Castellano and
Oliverio, 1976; Oliverio et al., 1975). The reflexes delayed in
their maturation (righting, placing, grasping, and bar holding re-
flexes) were those involving motor abilities normally evident during
the first 2 weeks after birth, suggesting that the administration of
an EFA-deprived diet affects the myelinization of the nervous motor
system tracts.
The EcoG recordings also showed a clear cut delay in the matura-
tion of brain electrical activity of EFA-deprived mice, compared with
the controls. However, the ECoG of control and EFA-deprived animals
was similar, starting from the third week of age. Using this type of
malnutrition, it was also possible to show that the avoidance-
-learning ability was impaired after 2 months of rehabilitation in
mice fed by females that were EFA deprived during pregnancy. The
selective deprivation of fatty acids seems therefore to affect the
patterns of brain development permanently (D'Udine and Oliverio,
1976; Galli et al., 1975). A morphological analysis of brain matura-
tion has indicated that in the animals fed EFA-deprived diets there
is a delay of myelination processes in a number of myelinated struc-
tures that may result in long-lasting effects on learning ability
(Gozzo and D'Udine, 1977).
If it is possible to stunt or delay the development of the brain

and learning abilities through the use of diets deprived of free
fatty acids, it is also possible to accelerate the development of a
number of reflex activities and of the ECoG by feeding diets charac-
terized by odd-chain fatty acids during pregnancy and lactation
(Gozzo et al., 1977). Some of the reflexes considered appeared from
4 to 6 days earlier than in control mice. Similarly a clear-cut
acceleration in the maturation of the cortical activity was also
evident. These findings are particularly interesting because they
indicate that it is possible to alter brain and behavioral ontogeny
in one direction or the other and to modify learning ability as
assessed in the adult.
4. BEHAVIORAL ONTOGENY AND THE DEVELOPMENT OF NEUROCHEMICAL SYSTEMS
Postnatal behavioral development involves maturation of several

systems and excitatory and inhibitory mechanisms which appear to
control behavioral maturation and arousal in mammals. Evidence
suggests that these mechanisms are modulated by various components of
the reticular system and by forebrain structures such as the frontal
cortex an hippocampus (Campbell and Mabry, 1972). At the neuro-
chemical level, it has been shown that among neuronal pathways there
exist major differences in the time of their appearance and the rate
of their differentiation and that the availability of neurotransmit-
ters at the synaptic cleft exhibits different rates of development
within a particular neuronal group (Coyle, 1977). In this regard the
ontogeny of stereotyped behavior is a reliable indicator of the
development of cerebral catecholaminergic processes (Coyle, 1977).
The use of a number of pharmacological agents acting on cate-

cholaminergic processes may represent a useful way of evaluating the
patterns of behavioral ontogeny related to maturation of different
neurophysiological and neurochemical mechanisms. For example, when
the effects of amphetamine on locomotor activity and stereotyped
behavior were considered (Lal and Sourkes, 1973), it was possible to
indicate a number of developmental stages related to maturation of
excitatory and inhibitory systems. The sterotyped behaviors observed
were different, including activity such as rearing (when the mouse
leaned with both forepaws on the wall of the cage), sniffing, and
gnawing. The results indicated that the dopaminergic mechanisms
which are responsible for the outcome of these stereotyped behaviors
are not mature at birth and reach their full development at about 2
months of age, when mice are almost adult. Also when locomotor
activity was considered there were differences in the magnitude of
behavioral arousal through ages. In both control and amphetamine-
injected mice a sharp rise in activity between day 8 and 16 and a
subsequent fall between day 16 and day 32 was evident; this fact had
been previously related to the time course for maturation of excit-
atory and inhibitory structures in the eNS of altricial mammals (Fox,
1965; Sedlacek et al., 1961; Campbell and Mabry, 1972; Oakley and
Plotkin, 1975).
Our findings indicate that after this decline in behavioral

arousal during the juvenile period, and increase in activity was
evident in adult mice (90 days old) while a subsequent decrease
paralleled the aging process. Though it is possible that the fall of
activity evident after the second week of postnatal life is related
to the maturation of inhibitory (serotonergic) structures in the CNS
(Mabry and Campbell, 1974), our findings suggest that other mechan-
isms may be involved in the regulation of the "arousal motivational
systems". Since amphetamine exerts both noradrenergic (arousal) or
dopaminergic (SB) effects it is possible to use this drug in order to
assess the ontogeny of the different catecholaminergic processes and
to indicate that different receptor sites do not develop at similar
ages (Coyle, 1977).
Another example of the developmental changes which are evident

for a number of neurophysiological systems is related to the matura-
tion of opiate receptors. In the mouse, morphine induced hyper-
activity is evident at many postnatal ages except in three weeks old
mice, in which a catatonic effect is evident. This finding has been
interpreted by suggesting that the neurophysiological and inhibitory
systems responsible for the non analgesic effects of morphine are not
characterized by the same developmental patterns (Filibeck et al.,
1981).
These are examples of some findings which provide a picture of

the developmental changes occurring at the level of specific systems
which mediate arousal mechanisms, pain reactions, and other fundamen-
tal forms of the interaction between the newborn and the environment.
The human brain has a particularly long prenatal phase in which

the main groups of neurons differentiate throughout it. All the
motivational and coordinating systems are present at birth but func-
tion in a rudimentary way. At this time much of the refined anatomy
of the cortex and the reticular integrative networks are incomplete.
As indicated by Trevarthen (1979) the integrative neurons of the
cortex, the long association fibers and neuropil, mature after birth,
when cultural skills are acquired. Before birth the human individual
is characterized by complete immaturity of visual, somesthetic,
auditory, motor and reticular mechanisms. These different essential
patterns are almost complete at 2 years of age. However, the reti-
cular system and the long cortical association fibers which cross
through the corpus calosum, are characterized by a much longer devel-
opment, which is achieved after 15 years of age. The maturation of
these important systems is paralleled by the emergence of a number of
typical human abilities, such as language, reading and writing.
However, these cultural activities only emerge when the underlying
neurophysiological systems are mature. It seems therefore essential
that developmental psychology be correlated with a psychological
approach and that comparative studies be extended in order to reach a
better understanding of the genetic and environmental factors affect-
ing the maturation of important neurophysiological systems.
REFERENCES
Alleva, E., D'Udine, B., and Oliverio, A., 1981, Effet d'une
experience olfactive precoce sur les preferences sexuelles de
deux souches de souris consanguines, Biology of Behaviour,
6:73.
Altman, J., 1966, Organic Foundations of Animal Behavior, Holt
Rinehart and Winston, New York.
Aschoff, J., 1960, Exogenous and endogenous components in circadian
rhythms, Symp.Quant.Biol.(Cold Springs Harbor), 25:11.
Bateson, P. P. G., 1980, Early experience and sexual preferences, in:

"Biological Determinants of Sexual Behaviour," J. B.
Hutchison, ed., Wiley, London, 29-53.
Bovet, D., Bovet-Nitti, F., and Oliverio, A., 1969, Genetic aspects
of learning and memory in mice, Science 163:139.
Campbell, B. A., and Mabry, P. D., 1972, Ontongeny of behavioral
arousal: a comparative study, J.Comp.Physiological Psychology,
81:371-379.
Castellano, C., and Oliverio, A., 1976, Early malnutrition and
postnatal changes in brain and behavior in the mouse, Brain
Res., 101:317-325.
Chance, M. R. A., 1975, Social cohesion and the structure of
attention, in: "Biosocial Anthropology," R. Fox, ed., Wiley,
New York.
Coyle, J. T., 1977, Biochemical aspects of neurotransmission in the
developing brain, Int.Rev.Neurobiol., 20:65-107.
Dobling, J., and Smart, J. L., 1974, Vulnerability of developing
brain and behaviour, Br.Med.Bull., 30:164.
D'Ddine, B., and Oliverio, A., 1976, Lipid malnutrition and early
development, Behav. Processes, 1:183-190.
Filibeck, D., Castellano, C., and Oliverio, A., 1981, Development of
morphine-induced changes of activity in the mouse,
Develop.Brain Res.in press.
Fox, M. W., 1965, Reflex ontogeny and behavioral development of the
mouse, Animal Behavior, 13:234-241.
Galli, G., Messeri, P., Oliverio, A., and Paoletti, R., 1975,
Deficiency of essential fatty acids during pregnancy and
avoidance learning in the progeny. Pharmacol., Res. Commun.,
7: 71-80.
Gozzo, S., and D'Ddine, B., 1977, Lipid malnutrition and postnatal
brain myelination ontogeny, NeuroscLLett. (In preparation).
Gozzo, S., Oliverio, A., Salvati, S., Serlupi-Crescenzi, G.,
Tagliamonte, B., and Tomassi, G., 1977, Nurtitional studies of
the lipid fraction of n-alkane grown yeast, IV, Effects on
behavioral development, Nutr.Rep.lntl., (In press).
Gozzo, S. Renzi, P., and D'Udine, B., 1979, Morphological differences
in cerebral cortex and corpus callosum are genetically deter-
mined in two different strains of mice. Int.J. Neurosci.,
9:91.
Green, E. L.. , 1966, Biology of the Laboratory Mouse, ed. 2, McGraw-
Hill, New York.
Jolly, A., 1972, The evolution of primate behavior, MacMillan,
London.
Jouvet, M., 1976, L'histoire nature lie du reve, Institut de France,
Paris.
Kobayashi, T., Inman, 0., and Buno, W., 1963, A multidisciplinary
study of changes in mouse brain with age, Recent Adv.Biol.
Psychiat., 5:293.
Lal, S., and Sourkes, T., 1973, Ontogeny of stereotyped behavior
induced by apomorphine and amphetamine in the rat, Arch. Int.
Pharmacodyn., 202:171-182.
Lindzey, G., and Thiessen, D. D., 1970, Contributions to Behavior-

Genetic Analysis. The Mouse as a Prototype, Appleton-Century-
Crofts, New York.
Mabry, P. D., and Campbell, B. A., 1973, Serotonergic inhibition of
catecholamine induced behavioral arousal, Brain Res., 49:
381-391.
MacLean, P. D., 1975, The imitative-creative interplay of our three
mentalities, in: "Astride the Two Cultures," H. Harris, ed.,
Hutchinson, London, 187-213.
Mainardi, D., Marsan, M., and Pasquali, A., 1965, Caustion of sexual
preferences of the house mouse. The behavior of mice reared
by parents whose odour was artificially altered. Atti Soc. It.
Sc. Nat.,104:325.
Malorni, W., and Oliverio, A., 1978, Imprinting to light-dark cycle
or rearing in constant light affect circadian locomotor rhythm
of mice, Neurosci. Letters, 9:93.
Malorni, W., Oliverio, A., and Bovet, D., 1975, Analyse g~n~tique
d'activite circadienne chez la souris, CR Acad. Sc., Paris,
281:1479.
Mayr, E., 1974, Behavior programs and evolutionary strategies, Amer.
Scient., 62: 650: 650-659. --
Medvedev, N. N., 1958, On the breeding of the laboratory strain mice,
Biulletini Moskoskogo Obestva Ispitateki Prirodvi, 63:117-133.
Oakley, D. A., and Ploktin, H. C., 1975, Ontogeny of spontaneous
locomotor activity in rabbit, rat and guinea pig., J. Compo
Physiol. Psychol., 89(3): 267-273.
Oliverio, A., 1977, Genetics, Environment and Intelligence,
Elsevier/North-Holland, Amsterdam.
Oliverio, A., 1977, La maturation de l'EEG et du sommeil: Facterus
genetiques et du milieu, Rev. EEG Neurophysiol., 7:263-268.
Oliverio, A., 1979, Functional consequences of infant septal lesions
in two strains of mice Brain Res., 175:131.
Oliverio, A., and Castellano, C., 1977, Postnatal brain maturation
and learning in the mouse, in: "Genetics, Environment and
Intelligence," A. Oliverio-,-ed., Elsevier/North-Holland,
Amsterdam, 117-131.
Oliverio, A., Castellano, C., and Messeri, P., 1972, A genetic
analysis of avoidance, maze and wheel running behavior in the
mouse, J. Compo Physiol. Psychol., 79:459-473.
Oliverio, A., Castellano, C., and Puglisi-Allegra, S., 1975, Effects
of genetic and nutritional factors on post-natal reflex and
behavioral development in the mouse, Exp. Agric. Res., 1:
41-56.
Oliverio, A., Castellano, C., and Renzi, P., 1975, Genotype or
prenatal drug experience affect brain maturation in the mouse,
Brain Res., 90:357-360.
Oliverio, A., Castellano, C., and Puglisi-Allegra, S., 1979, A
genetic approach to behavioral plasticity and rigidity, in:
"Theoretical Advances in Behavioral Genetics," J. R. Royce,
ed., NATO Advanced Study Institute, Sijthoff and Noordhoff,
Alphen aan den Rijn, The Netherlands, Germantown, Maryland,

USA, 139-165.
Parker, C. R., 1974, Behavioral diversity in ten species of non human
primates, J. Compo Physiol. Psychol., 87:930-937.
Roderick, T. R., Ruddle, F. R., Chapman, V. M., et al., 1971,
Biochemical polymorphism in feral and inbred mice, Mus mus-
culus, Biochem. Genet., 5:457-466.
Rojas-Ramirez, J. A., and Drucker-Colin, R. D., 1977, Phylogenetic
correlations between sleep and memory, in Drucker-Colin, R.
R., J. L Mc-Gaugh, eds., Academic Press, New York.
Sedlacek, J., 1974, The significance of the perinatal period in the
neural and behavioral development of precocial mammals, in:
"Aspects of Neurogenesis," G. Gottlieb, ed., Academic Press,
New York, 245-273.
Sedlacek, J., Svehlova, Sedlackova, M., Marsala, J., and Kapras, J.,
1961, New results in the ontogenesis of reflex activity,
Plzensky lekarsky Sbornik, Suppl. 3: 167-173.
Southwick, C. R., and Clark, L. R., 1966, Aggressive behavior and
exploratory activity in fourteen mouse strains, Amer. Zool.,
6:559.
Sprott, R. L., 1971, Inheritance of avoidance learning, The Jackson
Laboratory's Annual Report, 42:78.
Spyker, J. M., 1975, Assessing the impact of low level chemicals on
development: behavioral and latent effects, Federation Proc.,
34:1835-1844.
Staats, J. L., 1972, Standard nomenclature for inbred strains of
mice: fifth listing, Cancer. Res., 32:1609-1646.
Trevarthen, C., 1979, Brain growth and the nature of infancy, in:
"Developmental Psychology and Society, " J. Sants, ed. , -
MacMillan, London.
Valatx, J. L., Bugat, R., and Jouvet, M., 1972, Genetic studies of
sleep in mice, Nature, 238: 226-227.
Van Abeelen, J. H. F., 1966, Effects of genotype on mouse behavior,
Anim. Behav., 14: 218-225.
A DEVELOPMENTAL ANALYSIS OF SUCKLING IN THE RAT
Jay S. Rosenblatt
Institute of Animal Behavior

Rutgers University, 101 Warren Street
Newark, New Jersey 07102
Suckling and its development in the newly born rat has been the
subject of a burst of research activity in which several investi-
gators in my own laboratory have played an important role. In this
article I want to review this research because I believe it is rel-
evant to the study of behavioral development among all mammalian
newborn. Although mammals are classified by the possession of mam-
mary glands they could equally well be classified by the capacity for
suckling possessed by the young. The development of this capacity
and its decline are principal features of infancy among mammalian
young and playa central role in their behavioral development.
In the first section of this article the normal development of

suckling and the role of experience in this development will be
discussed. The next section will deal with nutritional and non-
nutritional factors in the regulation of suckling. The third section
will discuss the regulation of milk intake during suckling and the
fourth will present the sensory control of suckling in the rat pup.
The final section will discuss the question of the relationship
between suckling and independent feeding during weaning in the rat
pup.
NORMAL DEVELOPMENT OF SUCKLING: THE ROLE OF EXPERIENCE
Suckling is initiated by the newly born rat pup during the final
phase of parturition and in the early post-partum period when the
mother lies with her litter, resting after the rigors of the lengthy
parturition. During the first two weeks the mother initiates nurs-
ing sessions by entering the nest licking the young, adopting a
nursing posture draped over them or lying on her side with her
39
40 J. S. ROSENBLATT
ventrum facing the pups, the nipples, in two rows of six each, ac-
cessible for suckling. To suckle, during this period, the young must
locate and grasp a nipple: once grasped the nipple is sucked but the
pup receives milk only at intervals that may be as long as 15 minutes
or as short as 3-4 minutes. 3 The ejection of milk, caused by the
release of oxytocin, is signaled in the young by the stretch response
in which they pull strongly against the nipple with their legs out-
stretched and their backs arched and is indicated in the mother by a
sudden rise in her intramammary pressure.
The readiness with which pups attach to nipples, independently

of the mother's assistance, can be measured by anesthetizing the
mother and placing her in a supine position with nipple lines access-
ible, in a trough-shaped cage, and holding pups to her nipples or
placing them on her ventrum to find nipples by themselves. 3 ,4 At one
hour after birth, when brought to the nipples, only 21% attach and
suckle but after 12 hr of experience suckling from the awake mother
with her assistance, pups attach to nipples in 82% of the tests. s
The first 12 hours of suckling experience are important for the
development of nipple attachment with the anesthetized mother. Pups
removed from their mother 1 hour after birth and kept in a warm oven
without feeding, fail to improve and at 12 hr only 27% attach to
nipples. The experience they require to show improvement is not
necessarily receiving milk during suckling from the mother. Pups
suckling mothers with ligated nipples improve as much as those actu-
ally receiving milk during suckling but pups living with thelec-
tomized mothers (i.e. mothers whose nipples are surgically removed)
do not improve at 12 hr. The specific experience of searching for,
locating and grasping nipples is necessary for the improvement to
occur and general social contact or even maternal ano-genital stimu-
lation are not sufficient.
Even though suckling appears to be established quite securely

at 24 hr it can easily be disrupted by separating pups from their
mothers at 48 hr of age and feeding them by an implanted gastric
cannula until the fifth day.6 When returned to their anesthetized
mothers only 25% attached to nipples and suckled (nearly all of
littermates suckled under identical test conditions). Their suckling
latencies were nearly three times longer than those of their litter-
mates. The nipple grasping response was still present in nearly 75%
of the S-day old isolated pups as shown when they were brought di-
rectly in contact with the nipple but nipple localization was absent
and these pups were unable to suckle for 1~-2 days after they were
returned to their mothers, littermates and nests despite their
mothers' assistance.
As in the previous study during the first 12 hr post-partum, in

this study also the kind of experience required to prevent the de-
terioration of suckling between day 2 and 5 was shown to be more than
simply nipple attachment and suckling. In order for their suckling
A DEVELOPMENTAL ANALYSIS OF SUCKLING IN THE RAT 41
to be restored to normal levels at 5 days of age, pups had to find

nipples by themselves and they had to have the experience of grasping
the nipples and sucking even if they did not receive milk.
Although they appear to have preserved normal suckling the

isolated pups, given nipple searching and grasping experience between
days 2 and 5, are not as secure in their suckling as pups that have
remained with the mother throughout the first 5 days. If both kinds
of pups are removed from their mothers on the fifth day and are
raised in isolation with feeding by implanted gastric cannulas, on
day 10 the previously isolated pups attach in only 29% of the cases
when placed on their anesthetized mother's vent rum whereas those
is10ated for the first time are unaffected by the isolation at 10,
and also at 15 and 20 days of age.
The initiation of nursing by the mother gradually declines in

the second week as nursing occurs less frequently and for shorter
durations though nursing continues to be the predominant mode of
feeding by the pups. It has been shown that the mother's contact
with the young during the first two weeks is governed in large part
by her own thermoregulatory needs - to prevent excessive heat loss
from her relatively furless ventrum combined apparently with her
elevated thermal set point. Ventral contact with her litter during
nursing enables her to reduce hear loss by insulating her against the
ambient temperature. A decline in ventral and core temperature when
she is away from the litter stimulates her to enter the nest and
settle her ventrum on the pups that have themselves become cool
during the mother's absence. Nursing usually occurs at this time and
during nursing the mother's core and ventral body temperature rise
and the temperature of the litter also rises.
During the third week, therefore, pups begin to initiate suck-

ling sessions by approaching the mother outside the nest and pinning
her down to nurse. At first the mother accepts these approaches but
after the third week she becomes increasingly refractory and begins
to evade the pups' nursing approaches or to actively reject them and
during the fourth week the pups are virtually weaned.
NUTRITIONAL AND NONNUTRITIONAL FACTORS IN THE REGULATION OF SUCKLING
It is reasonable to believe that suckling is regulated by the

nutritional needs of the young because it serves these nutritional
needs until the beginning of the third week. Recent research indi-
cates that this may not be the case. To test whether nutritional
factors govern the initiation of suckling making attachment more
rapid in suckling deproved pups than in recently fed, nondeprived
pups, pups were suparated from their mothers for 22 hr and tested
with an anesthetized mother. The pups that were recently separated
from their mothers, nondeprived pups, had short latencies that were
42 J. S. ROSENBLATT
equal to those of deprived pups during the first 10 days and the same
proportion of each group attached to nipples during the first of
three daily tests. The response to recent feeding changed after the
10th day and from the 11th-13th day on fewer pups attached to nipples
and their latencies increased to 4 minutes of the 5-minute test.
Latencies of the suckling-deprived pups continued to decline during
the second and third weeks and the proportion of pups that attached
increased to 100 percent by the 14th day. It appeared, therefore,
that after an early period during which nutritional state plated no
apparent role in the initiation of suckling (and in the duration of
suckling since at all ages pups that attached to nipples remained
attached to the end of the test) there was a period, starting after
the 10th day in which the initiation of suckling increasingly came
under the control of the pups nutritional state. Nutritional state
was not altered during tests with the anesthetized mother because
there was no milk ejection in these females. We will return to these
observations at a later point.
During the third week a second change occurred in the regulation

of suckling. Nondeprived pups no longer attached to nipples at
initial testing after day 23 and in subsequent tests on a given day
their latencies were very long, nearly 5 minutes. Deprived pups
showed an increase in suckling latencies and by day 35, although they
continued to attach to nipples their latencies were longer than 3
minutes. By the end of testing at 35 days pups are eating solid food
which begins around day 16 and increases thereafter. If they are
severely food deprived however and given no other source of food than
the mother's nipples (which were "dry" during the tests) they re-
vealed that they were still able to initiate suckling although not
very readily.
The increased latencies for initiating suckling of the recently

suckled pups and the reduced number that suckled could be based upon
the nutritional sufficiency caused by the recent feeding, upon the
gastric distention caused by the milk load, independent of the nu-
tritional effect or upon oral-pharyngeal stimulation received during
suckling. Conversely, the shorter latencies of the deprived pups
could reflect nutritional deficiency, absence of gastric fill, or
deprivation of oral-pharyngeal sensory stimulation.
To study gastric fill, gastric pre10ads of milk were given to S-

and 10-day pups immediately before or during suckling (to m1n1m1ze
nutritional effects) on an anesthetized mother but at neither age did
the gross gastric distention interfere with nipple attachmentJ The
relative contribution of oral stimuli of suckling and the nutritional
effects of gastric pre loads was studied in 20- and 25-day old pups
undergoing the transition from suckling to independent feeding, i.e.
weaning,IO At 20 and 25 days of age pups were separated from their
mothers for 22 to 24 hrs with no access to food while isolated. In
separate groups gastric preloads of milk amounting to the normal
intake of a pup during a suckling session (i.e. about 5% of body

weight) were given at 60 min or 3 min prior to testing with an anes-
thetized mother. The 60 min preload tested the influence of nu-
tritional factors while the 3 min preload tested the effect of
stomach fill as possible inhibitors of the initiation of suckling.
It was found that preloaded pups were not inhibited in their nipple
attachment, their attachment latencies were comparable to those of
non-preloaded pups at either of the two ages. All pups attached at
both ages and latencies and durations of suckling were equal among
all groups at each age. Despite the preloads, and their nutritional
and gastric stimulus effects, pups were highly motivated to initiate
suckling and to remain attached to nipples. In two recent studies
gastric preloading with milk of pups 1- to 20-days and 11- to 13-days
did not increase latencies for suckling nor shorten durations) 1,12
There remained oral-pharyngeal sensory stimuli associated with

suckling or with food intake to be investigated in pups. 20 and 25
days of age, for their effect on the initiation of suckling. To do
this one group at each age was totally deprived of all food and
suckling for 22-24 hr (total deprivation) while a second group was
given sweetened condensed milk in a dish. Purina Rat Chow pellets and
water but had no opportunity to suckle from the mother (food only).
A third group suckled from the mother and in addition had rat show
pellets and water available (food and suckling).
At 20 days of age food alone did not inhibit suckling although

pups gained as much weight while suckling-deprived as when they
remained with their mothers. Food and suckling did reduce suckling
in these 20-day old pups causing an increase in latency to attach to
a nipple and a decrease in the duration of "dry" suckling. Oral
stimulation gained during suckling was therefore the crucial com-
ponent of suckling for reducing the pup's readiness to attach to a
nipple but at this age oral stimulation received during earing food
pellets was not effective.
At 25 days pups given food alone or food and suckling prior to

testing were significantly inhibited in initiating attachment to
nipples (suckling latencies) and in the duration of their dry suck-
ling. At this age. therefore, (when gastric preloading of an ad-
equate milk load that circumvented the normal oral-pharyngeal stimu-
lation received during suckling did not inhibit suckling initiation
and duration) the addition of suckling stimulation. but more import-
ant, the addition of a quite different kind of oral stimulation
received during eating food pellets were sufficient to inhibit suck-
ling. This latter phenomenon was shown very clearly in a further
study in which 25-day old were unfed for 21-23 hours as above. but
during the last hour they had access to food pellets prior to the
suckling test. These pups consumed more than 6% of their body weight
in food and their suckling was severely inhibited. Earlier it was
noted that an equivalent preload of milk 1 hour before a suckling
44 J. S. ROSENBLATT
test does not inhibit dry suckling. It was, therefore, not the
gastric loading but rather the oral stimulation which inhibited
suckling during the test. As expected in this study when 21-23 hour
deprived 20-day old pups ate food pellets one hour before a suckling
test their suckling was not inhibited in any manner.
The second transition in the regulation of suckling between 20

and 25 days does not change the predominant role of oral stimulation
in suckling. Rather these studies " •.• demonstrate that oral stimu-
lation remains of primary importance in controlling the pups' suck-
ling behavior, but by 25 days of age there is no longer anything
specific or special about stimulation provided by suckling; oral
stimulation from solid food ingestion is equally effective in in-
hibiting suckling."(lO, p.477) Of course this sets the stage for
weaning to occur since eating solid food inhibits the pups' readiness
to suckle when the opportunity subsequently presents itself.
The studies described above were undertaken to analyze the

underlying bases for the transition in suckling at 11-13 days and the
subsequent transition after 20 days when suckling declines and inde-
pendent feeding of food pellets increases. It is quite clear that
the first transition is not based upon a growing importance of nu-
tritional factors in the regulation of suckling. As late as 20 days
it has been shown that nutritional pre loads do not inhibit suckling
initiation or duration although at this age they begin to influence
the amount of milk that is ingested during suckling. Pups when they
have not received oral stimulation for some time and they are less
ready to suckle when they have recently received this stimulation.
Functionally, of course, this means that they are more ready to
suckle when they are food deprived than when they are recently fed.
The oral stimulation they seek is obtained specifically by suckling
and the oral stimulation which reduces their readiness to suckle is
specifically suckling stimulation through 20 days of age.
After 20 days there is a decline in the readiness to suckle in

both deprived and nondeprived pups as weaning progresses. One factor
which reduces suckling is the inhibiting influence of oral stimu-
lation received during eating or suckling which first appears between
21 and 25 days. A second, more important factor is the decline in
suckling itself at 25 days. This appeared in one experiment cited
above but it was not clear in that experiment whether 25-day old pups
found their mothers less attractive for suckling during testing than
20-day old pups found their mothers. To examine this possibility
20-day old pups were tested with 25-day post-partum mothers and
25-day old pups with 20-day post-partum mothers. Pups of both ages
were either totally deprived of food, given access to milk, food
pellets and water in isolation, or allowed to suckle from the mother
with access to food pellets and water as before. The results were
identical with those found earlier when pups were tested with their
own mothers. The decline in suckling at 25 days was not due to a
change in the relative attractiveness of the mothers at different

post-partum periods. This suggested that it was based upon develop-
ments in the pups between the two ages. These developments however
could reflect the influence of the events in litter over that period.
Normally pups are prevented from suckling by the mother's avoid-

ance and physical rejection of them during the period from 20 to 25
days. They may, therefore, prefer to feed from dishes and eat food
pellets and this may reduce their tendency to suckle from the anes-
thetized mother even when they are food-deprived at 25 days of age.
To examine this possibility pups were forcibly weaned from their
mothers at 15-16 or 20-21 days and given access to wet mash, dry food
pellets and water. The aim was to see whether an interval of 5 or 10
days without suckling would reduce suckling in the suckling test and
whether the absence of suckling between 15 to 20 days was equal in
its effect to the absence of suckling between 20 and 25 days.
Five days without suckling between 15 and 20 days did not reduce
suckling of either the deprived or the nondeprived pups but it had a
strong effect when suckling was prevented between days 20 and 25.
Even deprived pups suckled for less than 10 minutes of the 30 minute
test. When both intervals were spent in isolation (days 15 to 25)
then pups hardly suckled at all on day 25.
There may, therefore, be a maturational influence as well as an

experiential one on the timing of weaning. Suckling deprivation more
effectively reduces suckling when it occurs after day 20 than when it
occurs before day 20.
REGULATION OF MILK INTAKE DURING SUCKLING
Study of the regulation of milk intake during early development

requires special techniques for controlling milk flow during suck-
ling. Two procedures have been devised: the first procedure in-
volves periodic injections of oxytocin to anesthetized mothers while
pups are suckling.3 Milk is ejected shortly after the injection
method involves the use of a tongue cannula inserted through the
lower jaw and tongue and entering far back on the tongue where the
mother normally ejects her milk. Pups can be fed through the
cannula while they are attached and suckling the dry nipples of an
anesthetized mother. The second method gives the experimenter
greater control over the milk supply and the rate of delivery and it
has been shown that results obtained with artificial diet are similar
to those obtained with natural diet: pups exhibit the stretch re-
sponse at every milk injection and the response given is identical to
that given when the mother ejects milk.
The control of milk intake during suckling was studied by allow-

ing pups at ages 5, 10, 15, and 20 days to attach to nipples of an
46 J. S. ROSENBLATT
anesthetized mother and delivering pulses of milk into their mouths
through tongue cannulas that has been implanted shortly before. 13
Pups had been deprived of feeding from their mothers and all other
sources of food for 8 hours prior to the test. The termination of
milk intake for a particular pup was indicated during a test by its
failure to reattach to a nipple after releasing it, for a period of 3
minutes following a milk delivery. At this time various measures of
the pups responsiveness were made and its milk intake was determined.
Throughout the suckling period pups suckling from the mother

normally take about 6 per cent of their body weight at each lengthy
feeding: in the suckling test, with the cannula providing milk, pups
at 5 and 10 days of age ingested nearly twice that amount (i.e. 10 to
12 per cent) and at 15 days they ingested one-and-a-half times that
amount. Only when they reached the age of 20 days did they limit
their intake to 6% of their body weight as they do with the mother at
all ages.
The younger pups (5 and 10 days of age) were unable to limit

their intake by releasing the nipple before they were forced to do so
by the reflux of milk that jeopardized their respiration. At 5 and
10 days nearly all pups ingested milk until the stretch response
waned and the milk began to dribble from their mouths as they were
unable to swallow it. At these ages, therefore, there was virtually
no control over intake other than the mechanical effects of gastric
filling. After the 10th day pups began to control their intake and
more than half released the nipple before the stretch response had
waned. The younger pups were ready to grasp the nipple again after
they had released it but this declined with age. The adult post-
prandial pattern of grooming, exploration and then sleep was absent
until 15-20 days - the younger pups neither explored nor groomed but
fell asleep rather quickly no doubt due to the general inhibition
induced by their filled stomachs.
During studies of gastric preloading with milk diet and suckling

it was noted that milk intake was limited when the preload filled a
good part of the stomach. In a systematic study it has been shown
that at all ages up to 20 days pups regulate intake principally with
reference to gastric volume'! I In this respect artificial diet and
natural colostrum were equally effective in I-day old pups and diet
alone effective up to 20 days: pups achieve a remarkably constant
gastrointestinal volume through suckling and at 4% body weight pre-
load they suppress further ingestion. At no age tested did the
preload affect suckling latencies.
Nutritional control over the termination of suckling (as well as

the initiation of suckling) and the regulation of milk intake by this
means develops slowly in rat pups. It first appears in a few IS-day
old pups but not until 20 days is it present in a majority of the
pups.1 3 ,14 However under normal conditions when pups suckle from the
awake mother their intake is regulated and they ingest about 6 per
cent of their body weight. It has been shown recently that there is
a crude form of intake control during suckling in 5-, 10- and IS-day
old pups suckling from an anesthetized mother that is given 10
oxytocin injections at 4 min intervals. The pups had been deprived
0, 6 or 24 hr and at each age those deprived longest ingested twice
as much milk as those that were nondeprived and those deprived of
milk intake for 6 hr were intermediate. When pups of the same age
were suckling-deprived for 12 hr and were given an unlimited number
of milk ejections, at 5 and 10 days they no longer could control
their intake and overloaded themselves until they could not hold on
to the nipples. At all ages, therefore, pups can directly control
the rate of milk ingestion during suckling but control over the
volume of their intake appears to be indirect.
In view of the difficulty pups have regulating their intake when

they receive milk from a tongue cannula or when an anesthetized
mother gives unlimited amounts of milk at a rapid rate (i.e. every 4
min), how do they regulate their intake normally to about 5-6% of
their body weight from day 1 onward? Moreover, gastric preloads of
milk (and other fluids) do not impair their ability to regulate their
intake to the constant percentage of their body weight; they compen-
sate for the gastric volume of the preload by consuming less milk.
It has been suggested that the pup accomplishes this by regu-

lating its sucking rate in accord with the duration of suckling
deprivation and current milk intake. An analysis of the motor
components of sucking by electromyographic recording (EMG) has
singled out a particular rhythmic pattern of muscle activity ("rhyth-
mic" sucking) as against two other arrhythmic patterns ("bursts" and
"treadles") as having the dynamic characteristics to regulate milk
ingestion in relation to deprivation and milk intake. Rhythmic
sucking consists of slow deep evenly distributed sucks each lasting
about 2 sec and occurring in series lasting at least 5 sec with 2 sec
between peaks. A suckling deprivation of 20-24 hr increases three-
fold the pup's rate of rhythmic sucking compared to a 4 hr depri-
vation and associated with this increase is nearly 150% greater
consumption of milk via a tongue cannula while the pup is attached
to an anesthetized mother. The rhythmic sucking of a pup is sensi-
tive to the presence or absence of milk and at the same time it is
sensitive to gastric fill produced by a milk preload. Pups that are
deprived of suckling for 20-24 hr and receive milk via a cannula
perform rhythmic sucking at nearly twice the rate of pups that, in
addition, have been pre loaded with 5% body weight of milk. The
preload reduces milk intake presumably by reducing the rate of rhyth-
mic sucking. Rhythmic sucking after 20-24 hr suckling deprivation is
not as rapid without milk delivery as when milk delivery occurs and
under this condition at 5% body weight gastric preload does not
decrease rhythmic sucking. The higher rate of rhythmic sucking of
these pups reflects their state of suckling deprivation quite
48 J. S. ROSENBLATT
directly without the additional influence of milk intake. Because

the preload does not reduce further the high rate of rhythmic sucking
(under the dry suckling condition) it has been suggested that the
high rate of rhythmic sucking is in response to deprivation of oral
suckling stimulation over the 20-24 hr period of maternal depri-
vation. There is strong support for this proposal since sucking on a
dry nipple which supplies oral stimulation reduces the rate of rhyth-
mic sucking to that of pups that have been suckling-deprived for only
2-6 hr. 16, 1 7
SENSORY CONTROL OF SUCKLING IN THE RAT PUP
The altricial status of the newly born rat dictates that its
searching, locating and grasping of the nipple for suckling are under
the control of proximate sensory systems, namely, tactile, thermal,
and 01factory-gustatory .l8 It is, by now, well-established that of
these systems, olfaction plays the most important role from the
beginning. Very early it was shown that anosmia produced by olfac-
tory bulbectomy or intranasal lavage or zinc sulfate as early as 2
days after birth and at any age within the first two weeks results
in a severe disturbance of suckling, with a consequent loss of weight
and a resultant high mortality within a few days among the younger
pups but less so among the older ones.l 9 ,20 Detailed observations
of anosmic pups reveal that by contrast with their intact siblings
contact with a nipple does not elicit nipple grasping in them.
The relevant olfactory stimulus at two weeks of age appears to

be an oxytocin-stimulated glandular secretion that has not yet been
isolated.21 ,22 Washing the mother's nipples with organic solvents
removes this chemical cue and prevents pups from attaching to the
nipples and either distilling the wash and reapplying it to the
nipple or injecting the mother with oxytocin restores the olfactory
cue and along with that, suckling by the pups.
At an earlier age, near birth, it has been shown that the first
suckling by newborn is in response to amniotic fluid that has been
deposited on the nipples during parturition. 23 This initial nipple
grasping and suckling is specific to amniotic fluid and does not
occur if other substances that might later be attractive to the pup,
having distinct odors, are applied to the washed nipple. Saliva from
the mother and amniotic fluid itself are the most effective suckling
stimuli but later pup saliva is also effective. This has been estab-
lished by washing the nipples before the first sucking, applying
these fluids to the nipples and comparing the pups' responses to
these fluids with their response before the nipple is washed or after
the wash has been distilled and distillate has been applied to the
nipple. 9
The initial attractiveness of amniotic fluid for eliciting

nipple grasping and sucking raises the question whether the response
to this odor may not be influences by experience in the uterus and

during parturition, prior to suckling. Pups may develop a mouthing
response in utero when they are known to swallow amniotic fluid. In
an ingenious series of experiments, it has recently been shown that
an artificial odor, lemon, can acquire the same efficacy as amniotic
fluid and, in fact, pups can develop a preference for it over amni-
otic fluid. In the initial attempts to establish, prenatal prefer-
ence, vanilla was introduced into the amniotic sac 2 days before
birth.24 This procedure failed to instill in the pups a response to
vanilla-coated nipples. Later lemon odor was introduced into the
amniotic sacs on day 20. Tests were later done in a lemon odor-
suffused chamber but newborn pups still did not attach to the washed
nipples of the mother when surrounded by a strong lemon odor. How-
ever, if the prenatal exposure of lemon odor was supplemented by
vigorous tactile stimulation of the newly emerged fetus, similar to
that which it received from the mother's licking during delivery, in
the presence of lemon odor, a procedure that was ineffective in
itself for stimulating later nipple attachment, then pups readily
attached to nipples in the lemon-odored chamber and they failed to
respond to amniotic fluid placed on the nipples. In addition to the
prenatal exposure to lemon odor, pups required postnatal exposure but
under conditions in which they received tactile stimulation and
consequent strong arousal. 25
Once they have initiated suckling in response to amniotic fluid

odor pups grasp nipples more readily on the basis of new features
which they have encountered. They may include other odors or even
washed nipples in which case pups may be responding to thermotactile
features of the nipples. Pups whose upper lips are desensitized by a
nerve block are unable to grasp a nipple even though they make snout
contact with it. 18 This suggests that tactile thermal sensory cues
may also play a role in nipple localization and grasping. This
suggestion has recently been confirmed in a study in which trigeminal
nerve section were performed on rat pups at 1, 7, 12, and 17 days of
age. 26
At all ages, snout denervation, leaving intact mouth, gums, and
tongue, lower lip, and lower jaw, caused disturbances of suckling.
Three of the newborn died during the first week and all failed to
gain any significant amount of body weight, indicating that they too
would eventually die. Seven- and 12-day old pups immediately began
to lose weight after snout denervation and among the younger pups all
died before the 12th day while 2 of 13 of the older pups died and the
remainder had severely reduced body weights. The oldest pups fared
best if they were allowed to feed from dishes but they also lost
weight if they were only able to obtain food by suckling. Denervated
pups when hand held to the nipple failed to attach to it and few
showed mouthing, licking and nosing of the nipple when brought into
contact with it.
50 J. S. ROSENBLATT
Suckling reinforcement for odor conditioning, for discrimination
learning in a Y maze, and for the instrumental task of crawling down
a runway. As early as 7 days of age pups learn to discriminate
between the two arms of a Y maze that lead them either to nipples
from which they can suckle or to the covered ventrum of a lactating
mother.28 When reinforced by milk, given by tongue cannula, for
choosing one arm of the Y maze they increase their choice of that arm
over the arm that leads only to dry suckling. 29 The age at which
they begin to make this discrimination is approximately the age at
which they begin to increase their latencies to suckle when they have
recently suckled from their mother nut continue to show short laten-
cies if they have been suckling-deprived for 22 hr.4 Since preload-
ing studies have shown that nutritional sufficiency is not the likely
cause for the slow responding by the recently suckled pups but the
case is, rather, the recent performance of suckling, 10 it might also
be that it is not the nutritional value of the milk but its stimu-
lational effect, which is greater than that of dry suckling, that
serves as reinforcement.
In a similar vein during odor conditioning 29 and for pups crawl-

ing down a runway to the mother, 30 milk enhances the reinforcing
value of suckling. 31 ,32 With regard to the latter, an order of
effective reinforcement can be demonstrated during learning (and
extinction) with a "lactating" anesthetized mother most effective, a
"dry" mother less effective, and, in decreasing order or effective-
ness, a male or non-lactating female, and a sibling or an empty goal
box. 33
The issue is not whether milk increases the reinforcing value of

suckling but whether it is the nutritional consequence of milk or its
added stimulus/arousal effect which is reinforcing. Thus far the
only behavioral effect of the nutritional aspect of milk ingestion
that has been demonstrated is the reduced intake at 20 days that
follows gastric preloads of milk as against saline,l4 This effect,
in turn, may be mediated by the reduced rhythmic sucking which occurs
when pups are preloaded with milk and suckle from a nipple while
receiving milk via a tongue cannula.
There is little doubt that pups are keyed to respond more

strongly to milk than to many other substances during suckling and,
moreover, that there is an immediate persisting effect of milk re-
ceived continuously or intermittently by the pups upon their rhythmic
sucking. 34 The frequency is increased and this increase continues
for some time after milk delivery no longer occurs. It persists for
24 hr after a relatively short period of milk delivery but may con-
tinue for a longer period and, in addition, pups remain attached to
nipples for longer periods of suckling if they have received milk
repeatedly over 5 days.34
Oral stimulation by milk, as during suckling, may be an es-

pecially effective way of arousing pups prior to any extensive learn-
ing of substitute stimuli. Another way is through tactile stimu-
lation which we have seen, is a necessary supplement for lemon odor
to become an effective suckling stimulusJ5 Recently tactile stimu-
lation at 3 days has been used to establish as association of suck-
ling with a novel odor. 35 This kind of tactile stimulation resembles
another natural stimulus, the mother's licking of the pups and this
is certainly arousing to pups.
Until conditioning and learning studies are done on neonates

whose nutritional needs have been met but who are aroused during
sucking we shall not be able to distinguish the nutritional from
stimulational aspects of the reinforcement which suckling milk pro-
vides.
RELATIONSHIP BETWEEN SUCKLING AND INDEPENDENT FEEDING DURING WEANING
In a series of studies examining the developing serotonergic

system in relation to suckling, methysergide, a serotonin blocking
agent, was found to prolong suckling beyond the age when it normally
declines. 36 ,37 Suckling was still present in nearly 80% of non
deprived pups at 30 days of age when normally it would be already
absent. Methysergide maintained suckling in suckling-deprived pups
until they were 35 days of age when normally even such pups are
unwilling to suckle from an active or an anesthetized mother. The
number of pups suckling and the duration of their suckling were
consistently greater in methysergide-treated than saline-treated
pups.
These findings suggested that the maturational component of

weaning, noted earlier in the study on oral factors in suckling,10
was very likely the development of the serotonin system. Normally
the development of this system inhibits the performance of suckling:
by blocking serotonin suckling was not inhibited. This study raises
the possibility that suckling and independent feeding are basically
mutually exclusive patterns of feeding; weaning is not a smooth
transition from one pattern to the other but the suppression of
suckling by independent feeding.
If this is the case then quipazine, a serotonergic agonist that

acts by stimulating serotonin receptors, might accelerate weaning by
inhibiting suckling and facilitating independent feeding. Ten- and
20-day-old suckling-deprived pups were injected with quipazine and
only a small percentage suckled. 36 ,37 Those that suckled remained
attached to nipples for less than 15 min compared to 60 min suckling
for most of the saline-treated pups. As an indication that quipazine
and methysergide act at serotonin receptor sites, methysergide was
given to pups that were subsequently treated with quipazine and
suckling was facilitated rather than inhibited in these pups.
52 J. S. ROSENBLATT
The question arises whether methysergide acts by making pups

very hungry rather than suppressing independent feeding and facili-
tating suckling. To test this possibility pups were treated with
methysergide then given the choice of "feeding" from either an anes-
thetized mother that was not giving milk or a dish of food pellets.
The pups were 20 and 25 days of age and they were either food-
deprived or not: half of the pups were treated with methysergide and
half were treated with saline. Drug-treated pups at 20 days almost
exclusively suckled while saline-treated pups were divided between
suckling and eating pellets. Further into weaning, at 25 days the
majority of deprived pups suckled but 40% ate pellets and nearly the
same division occurred among the nondeprived pups. Saline-treated
pups favored pellet eating particularly when they had been deprived,
the opposite of the methysergide-treated pups. The choice of suck-
ling by drug-treated pups, therefore, was not based simply upon
stimulation of hunger for food which only the mother provides in the
suckling tests. It is a real preference for suckling, particularly
since the anesthetized mothers did not provide milk in the tests.
The emergence of independent feeding around 20 days and its

development into the major feeding system of the adult animal raises
questions about the development of this system during the suckling
period. Does it emerge full-blown at 20-25 days or are developmental
precursors discernible? An important lead in answering this question
was the discovery in newborn rat pups of another feeding system that
normally is not employed. When pups encounter a bit of fluid during
their crawling and nosing of the cage floor surface they lick it and
ingest it. 38 This only occurs at elevated ambient temperatures
normally found in the nest, huddle or when pups are in contact with
the mother or in her vicinity.
Unlike suckling in the newborn which is not regulated by depri-

vation this kind of feeding, which van also be elicited for exper-
imental purposes, by a lower jaw cannula inserted anteriorly so as to
stimulate swallowing, is already under nutritional regulation at 1
day of age. 39 Pups ingested less than 20% of the diet infusion when
they were food-deprived only 1 hr and this rose to nearly 40% when
they were deprived 7 hr and 70% after 24 hr deprivation. At compar-
able deprivations i-day old pups with the usual tongue cannulas
simulating ingestion during suckling took amounts of the infusion
that were unrelated to the prior deprivation.
An experimental analysis of this feeding pattern in the prewean-

ing has brought out many similarities between this form of feeding
and adult feeding. The motor aspects are more similar to the adult
pattern than in suckling and the pattern of terminating feeding
resembles, from the beginning, the postprandial pattern of the adult.
The investigators have speculated that: " ••• an ingestive system
that may be developmentally continuous with the adult feeding system
is present from birth in the infant. This system does not appear to
be the same system that sub serves suckling but is patterned and
regulated like the feeding system of adult rats."(40, p.754)
There is evidence, therefore, that during weaning there is a

shift in the relative dominance of suckling and this developing
system of independent feeding. There are many external influences
which affect the timing of this shift (e.g. separation at 20 days
from the mother weakens suckling and strengthens independent feeding)
but maturation plays an important role and beyond a certain age,
which is around 35 days, suckling can no longer be maintained and
independent feeding becomes firmly established.
REFERENCES
1. J. S. Rosenblatt, The basis of synchrony in the behavioral

interaction between the mother and her offspring in the
laboratory rat, in: "Determinants of Infant Behavior - III",
B.M. Poss, ed., Methuen, London (1965).
2. W. R. Holloway, Jr., M. J. Dollinger and V. H. Deneberg,
Parturition in the rat: description and assessment, in:
"Maternal Influences and Early Behavior," R.W. Bell and W.P.
Smotherman, eds., Spectrum, New York (1980).
3. D. W. Lincoln, A. Hill and J. B. Wakerley, The milk-ejection
reflex of the rat: an intermittent function not abolished by
surgical levels of anesthesia, J.Endocr. 57:459 (1973).
4. w. G. Hall, C. P. Cramer and E. M. Blass, Ontogeny of suckling
in rats: transitions toward adult ingestion, J.Comp.Physiol.
Psychol. 91:1141 (1977).
5. M. J. Dollinger, W. R. Holloway, Jr. and V. H. Denenberg, The
development of behavioral competence in the rat, in: "Ma-
ternal Influences and Early Behavior," R.W. Bell and W. P.
Smotherman, eds., Spectrum, New York (1980).
6. M. L. Stoloff, J. T. Kenny, E. M. Blass and W. G. Hall, The role
of experience in suckling maintenance in albino rats, J.Comp.
Physiol.Psychol. 94:847 (1980).
7. M. L. Leon, P. G. Croskerry and G. K. Smith, Thermal control of
mother-young contact in rats, Physiol.Behav. 21:793 (1978).
8. S. Reisbick, J. S. Roenblatt and A. D. Mayer, Decline of
maternal behavior in the virgin and lactating rat, J.Comp.
Physiol.Psychol. 89:722 (1975).
9. E. M. Blass, W. G. Hall and M. H. Teicher, The ontogeny of
suckling and ingestive behaviors, Prog.Psychobiol.Physiol.
Psychol. 8:243 (1979).
10. C. L. Williams, W. G. Hall and J. S. Rosenblatt, Changing oral
cues in suckling of weaning-age rats: possible contributions
of weaning, J.Comp.Physiol.Psychol. 94:472 (1980).
11. D. N. Lorenz, S. Ellis and A. N. Epstein, Differential effects
of GI preloads of colostrum on nipple attachment and milk
ingestion of rat neonates, Int.Soc.Dev.Psychobiol. Nov.,
Cincinnati, Ohio (1980).
54 J. S. ROSENBLATT
12. S. C. Brake, D. J. Sager, R. Sullivan and M. Hofer, Nutritive
and non-nutritive control of sucking and milk consumption in
11-13-day old rat pups, J.Comp.Physiol.Psychol. (submitted)
(1981).
13. W. G. Hall and J. S. Rosenblatt, Suckling behavior and intake
control in the developing rat pup, J.Comp.Physiol.Psychol.
91:1232 (1977).
14. W. G. Hall and J. S. Rosenblatt, Development of nutritional
control of food intake in suckling rat pups, Behav.Biol.
24:413 (1978).
15. C. P. Cramer, Infant rats control rate but not volume of milk
intake. Int.Soc.Dev.Psychobiol. Nov., Cincinnati, Ohio
(1980) •
16. S. C. Brake, V. Wolfson and M. A. Hofer, Electromyographic
patterns associated with non-nutritive sucking in 11-13-day-
old rat pups, J.Comp.Physiol.Psychol. 93:760 (1979).
17. S. C. Brake and M. A. Hofer, Maternal deprivation and prolonged
suckling in the absence of milk alter the frequency and
intensity of sucking responses in neonatal rat pups, Physiol.
Behav. 24:185 (1980).
18. J. S. Rosenblatt, The sensorimotor and motivational bases of
early behavioral development of selected altricial mammals,
in: "Ontogeny of Leaning and Memory," N.E. Spear and B.A.
Campbell, eds., L.Erlbaum, Hillsdale, N.J. (1979).
19. P.J. Singh and E. Tobach, Olfactory bulbectomy and nursing
behavior in rat pups (Wistar DAB), Dev.Psychobiol. 8:151
(1975) .
20. P. J. Singh, A. M. Tucker and M. A. Hofer, Effects of nasal
ZnS04 irrigation and olfactory bulbectomy on rat pups,
Physiol.Behav. 17:373 (1976).
21. M. A. Hofer, H. Shair and P. Singh, Evidence that maternal
ventral skin substances promote suckling in infant rats,
Physiol.Behav. 17:131 (1976).
22. P. J. Singh and M. A. Hofer, Oxytocin reinstates maternal
olfactory cues for nipple orientation and attachment in rat
pups. Physiol.Behav. 20:385 (1978).
23. M. H. Teicher and E. M. Blass, First suckling response of the
newborn albino rat: the role of olfaction and amniotic
fluid, Science, 198:635 (1977).
24. E. M. Blass and P. E. Pedersen, Alteration of the amniotic
environment: an attempt to influence the first nipple attach-
ment, (Abstract) Ann.Mtg.lnt.Soc.Dev.Psychobiol. Nov., 1-2
(1979) .
25. E. M. Blass and P. E. Pedersen, Weturn wright to the womb:
prenatal and postnatal influences on the first suckling
episode, Int.Soc.Dev.Psychobiol. Nov., Cincinnati, Ohio.
26. M. A. Hofer, A. Fisher and H. Shair, Effects of infraorbital
nerve section on survival, growth and suckling behaviors of
developing rats, J.Comp.Physiol.Psychol. 95:123 (1981).
27. J. T. Kenny and E. M. Blass. Suckling as incentive to

instrumental learning in preweaning rats. Science 196:898
(1977) •
28. E. M. Blass. J. T. Kenny. M. Stolnoff. J. P. Bruno. M. H.
Teicher and W. G. Hall. Motivation. learning and memory in
the ontogeny of suckling in albino rats. in: "Ontogeny of
Learning and Memory." N.E. Spear and B.A. Campbell. eds •• L.
Erlbaum. Hillsdale. N.J. (1979).
29. s. C. Brake. Suckling infant rats learn a preference for a novel
olfactory stimulus paired with milk delivery. Science 211:506
(1981) •
30. A. Amsel. D. R. Burdette and R. Letz. Appetitive learning.
patterned alternation, and extinction in 10-day-old rats with
non-lactating suckling as reward, Nature 262:816 (1976).
31. M. Stanton. W. Dailey and A. Amsel. Patterned (single)
alternation in 11- and 14-day-old rats under various reward
conditions. J.Comp.Physiol.Psychol. 94:459 (1980).
32. M. Stanton and A. Arosel. Adjustment to reward reduction (but no
negative contrast) in rats 11. 14. and 16 days of age.
J.Comp.Physiol.Psychol. 94:446 (1980).
33. A. Arosel. R. Letz, D. R. Burdette. Appletitive learning and
extinction in 11-day-old rat pups: effects of various rein-
forcement conditions, J.Comp.Physiol.Psychol. 91:1156 (1977).
34. s. C. Brake. R. Sullivan, D. J. Sager and M. Hofer. Effects of
varying milk-delivery contingencies on sucking and nipple
attachment in preweaning and weaning rat pups. J.Comp.
Physiol.Psychol. (Submitted).
35. P. E. Pedersen and C. L. Williams. Nipple attachment elicited by
a novel odor: a demonstration of early olfactory learning in
young pups, Int.Soc.Dev.Psychobiol. Nov •• Cincinnati. Ohio.
36. C. L. Williams. J. S. Rosenblatt and W. G. Hall. Inhibition of
suckling in weaning-age rats: a possible serotonergic mechan-
ism. J.Comp.Physiol.Psychol. 93:414 (1979).
37. B. Nock. C. L. Williams and W. G. Hall. Suckling behavior of the
infant rat: modulation by a developing neurotransmitter
system. Pharm.Biochem.Behav. 8:277 (1978).
38. w. G. Hall, Feeding and behavioral activation in infant rats.
Science 205:206 (1979).
39. w. G. Hall, The ontogeny of feeding in rats: I. Ingestive and
behavioral responses to oral infusions, J.Comp.Physiol.
Psychol. 93:977 (1979).
40. w. G. Hall and T. E. Bryan, The ontogeny of feeding in rats: II.
Independent ingestive behavior, J.Comp.Physiol.Psychol.
94:746 (1980).
THE INTERPRETATION OF SENSITIVE PERIODS
Patrick Bateson
University of Cambridge
Sub-Department of Animal Behaviour
Madingley, Cambridge, England
INTRODUCTION
Many people who study the development of behavior in humans feel

uncomfortable or even hostile, when the topic of sensitive periods is
mentioned in their presence. It is as though the term is tainted
with rigid determinism and the worst excesses of biologists intent on
taking over the social sciences. It is a great pity that such atti-
tudes are so prevalent because the phenomena encompassed by the term
can provide highly promising gateways to an understanding of develop-
mental processes. "Sensitive period", or one of its numerous syn-
onyms, ought merely to refer descriptively to the evidence that an
individual's characteristics may be most strongly influenced by a
given event at a certain stage of development. It should not suggest
that other events exert their maximum influence at the same stage.
Nor should it carry implications about what might have given rise to
the particular sensitive period that has been described.
Before proceeding any further, it is only fair to point out that

the unease generated by talk of sensitive periods is not rooted in a
total misreading of the literature. Oyama (1979) has explored with
great clarity and penetration how the term came to be associated with
the nature side of the futile nature-nurture battle. Certainly,
those who have treated sensitive periods as explanatory concepts
rather than described programming metaphors and have made strong
claims for universal biological principles. Scot~ (1978, p.5) goes
so far as to assert that a "decision" is made within the critical
period (as he prefers to call it) and the decision cannot be repeated
or reversed later in development. Such views deeply embedded in the
thinking about development in general, and human childhood in par-
ticular. Clarke and Clarke (1976) vigorously attacked such conven-
57
58 P. BATESON
tional thought and, at the end of their book devoted to examining the
available evidence, stated that virtually no behavioral deficit
induced by early experience was irreversible. Rutter (1980) agreed
that the notion of fixed and absolute "critical periods" no longer
warranted serious consideration with respect to human behavioral
development. However, he also pointed out that the notion of periods
of heightened responsiveness during development had obvious validity
in certain cases. If the child is too old, rehabilitation of certain
deficits could be difficult.
A reconciliation between the view that early experience is

important and the view that nothing is irreversible was already
implicit in psychoanalytical theory (e.g. Freud 1949). Freud (1910)
had followed a long tradition when he placed great emphasis on the
formative effects of early experience. Unusual at the time, though
was his view that seemingly irreversible influences of childhood
could be overcome in adults by the application of the psychoanalyti-
cal method. It is worth remembering this central notion of his
method of therapy when examining modern debates about sensitive
periods in development. The general point is that it may be possible
for the distinctive features of behavior to be formed in particular
stages in development, and yet the processes generating those fea-
tures can be reactivated at much later stages in the life-cycle.
EXPLANATION FOR SENSITIVE PERIODS
The variety of phenomena covered by the term sensitive period

means that it is virtually inconceivable that the same explanations
will apply to all of them. For instance, processes that regulate the
stage in childhood when language development can begin (see
Lennenberg, 1967) must surely be different from those regulating when
a mother is most likely to form a strong bond to her newly born child
(e.g. Hales et al., 1977). Yet the descriptive term, sensitive
period, has been applied to both cases.
Some sensitive periods can be explained in terms of increased

vulnerability to external influences at times of rapid change as
Scott (1978) has argued. This usage seems particularly apt in the
case of physical growth. A simple model can be devised which simu-
lates the catch-up effect by which a sick child can lose weight and
yet rapidly make good the loss as soon as it has recovered from the
illness, and get back to where it would have been if it had not been
ill at all (Bateson, 1976b). This model simulated plasticity in
development as well as elasticity so that if the discrepancy between
the true weight and the set-point for weight was more than a speci-
fied amount, the set-point would be reduced. The interesting effect
of this embellishment was that long term effects of starvation on
adult weight were much more pronounced if the starvation had occurred
during periods of rapid growth. This prediction is supported by
THE INTERPRETATION OF SENSITIVE PERIODS 59
evidence for growth in rats (Smart et al., 1977). However, it seems

far-fetched to suppose that such examples and the explanations for
them will tell us anything about what regulates sensitive periods for
learning.
IMPRINTING
Imprinting in birds is usually regarded as the archetypal ex-

ample of learning occurring at highly predictable stages in a life-
cycle. Notions of an internally controlled "window" opening and then
shutting again have been used but have also proved highly misleading
(see Bateson, 1979). Interactions between the animal's internal
organization and the external conditions are more interesting and
provide a more useful model for studies of human development than the
simple ideas about rigid internal control.
That having been said, the onset of sensitivity for filial

imprinting - the process by which precocial birds like ducklings
learn about the individual characteristics of their mother - seems to
be linked in part to the developmental stage of the young bird
(Landsberg, 1976). This does not mean that the time of increase in
sensitivity is rigidly linked to chronological age since the general
developmental state may be influenced by many external factors such
as temperature. Nevertheless, such factors affect many systems apart
from those specifically influencing imprinting. For instance, pat-
terned light generally accelerates the development of visually guided
behavior in domestic chicks and, in so doing, has an effect on when
filial imprinting can occur (Bateson and Wainwright, 1972; Bateson,
1976a). Part of the increase in sensitivity is attributable to
physiological changes in the efficiency of the visual system
(Paulson, 1965) and here the interaction between internal and exter-
nal factors is particularly easy to understand. Visual experience
with patterned light has a general facilitating effect on the devel-
opment of visually-guided behavior and may well serve to strengthen
connections in the underlying neural systems (e.g. Horn et al.,
1973). Other changes in internal state, particularly in levels of
corticosterones, appear to be associated with the changes in sensi-
tivity to imprinting objects (Martin, 1975; Landsberg and Weiss,
1976; Weiss et al., 1977), although the extent to which the hormonal
levels are dependent on preceding external events is not yet known.
Finally, an increase in the level of "arousal" has often been thought
to be important in imprinting (e.g. Kovach, 1970; Fischer, 1970;
Rajecki, 1973; Martin and Schutz, 1974). Increased arousal may be a
consequence of visual experience or other changes, but it may reflect
on endogenous increase in the excitability of the central nervous
system.
The important influence of an animal's internal state on the

onset of a sensitive period is emphasized by recent work on sexual
60 P. BATESON
imprinting - a process by which birds learn about their immediate kin

and so are able to choose an optimal mate when they are adult.
Sexual imprinting is not completed until the young birds have devel-
oped their adult plumage and, as a consequence, can subsequently
recognize their siblings and, of course, be recognized by them
(Bateson, 1979). The clearest indication that sexual imprinting
might be dissociated at least partly from filial imprinting comes
from a study of the domestic cockerel by Vidal (1980). He exposed
cockerels to a moving object from 0-15 days, 16-30 days, or 31-45
days after hatching. Subsequently they were isolated or reared with
a female until they were adult. Starting at 150 days they were given
a series of choice tests between familiar and novel objects. The
chicks that had been exposed for 31-45 days and then isolated, showed
the strongest sexual preference for the familiar object. These birds
had shown the least amount of filial behavior to the object during
the period of exposure.
The evidence for some internal control over the ending of the
sensitive period is much less satisfactory. By contrast, the power-
ful influence of external experience affecting behavior in specific
ways is compelling (Bateson, 1979). It should be remembered that
imprinting is a pre-emptive self-terminating process in the sense
that it narrows social preferences to that which is familiar, and
therefore tends to prevent fresh experience from further modifying
those social preferences. Moreover, while some experiences are such
more effective in restricting social preferences than others, birds
can eventually form preferences for the static cages in which they
have been isolated. It follows that if some birds are reared with
attractive stimuli such as their siblings, and some are reared in
isolation, it should be possible to imprint the isolated birds with
a novel object at an age when the socially reared birds escape from,
or are unresponsive to, new things. This has been demonstrated in
chicks and ducklings (Guiton, 1959; Sluckin and Salzen, 1961;
Asdourian, 1967; Smith and Knott, 1970). Furthermore, when a bird's
visual experience of patterned light is reduced or it is drugged, the
age at which it will respond socially to novel objects can be greatly
extended (Moltz and Stettner, 1961; McDonald, 1968). The influence
of external events on the ending of the sensitive period is, there-
fore, hard to deny. Experimenters have difficulty in getting older
birds to respond socially to an object at least in part because the
birds have developed a preference for something else. The first
preference to be formed is protected from disruption by subsequent
experience as a result of the animal being indifferent to novel
objects or, more especially, escaping from them. However, the escape
from a novel object can be habituated by repeatedly exposing the
animal to that object (Bateson, 1964; Ratner and Hoffman, 1974).
What is more, chicks that have developed a preference for, say, a
blue cloth ball, can be induced to change their preference by a
sufficiently long period of exposure to a green cloth ball (Salzen
and Meyer, 1968). In some conditions, then, the initial preference
is not completely stable and irreversible.
INTERNAL PROTECTION OF PREFERENCES
The notion that social preferences acquired by imprinting are

merely protected by escape from, or indifferences to novel objects is
not sufficient to account for what happens in certain cases of sexual
imprinting. Immelmann (1969) found that male zebra finches reared in
early life with Bengalese finches, and subsequently kept with their
OWll species, could breed successfully with female zebra finches.
However, when given the change, they would court Bengalese finches in
preference to zebra finches. The preference for the species with
which they had been reared surfaced despite the birds' considerable
sexual experience with their own species. Clearly their preference
for the Bengalese finch had not been protected by escape from or
indifference to, zebra finches.
Interestingly, a period of isolation can be crucial for the

latent sexual preference to show itself (see Immelmann, 1979;
Immelmann and Suomi, 1981). When some male zebra finches, which had
been reared with Bengalese finches, were given a choice between a
female of their own species and a Bengalese finch without first being
isolated, they initially preferred the zebra finch. After some days
of isolation, the preference for the Bengalese finch emerged.
Recently, a re-examination of the stability of filial prefer-

ences has shown that there is more to their protection than a mechan-
ism ensuring the bird's escape from strange things. Cherfas and
Scott (1981) replicating the experiment of Salzen and Meyer (1968),
confirmed that if chicks were exposed to one object for the first
three days of life and then exposed to a different object for the
next three days, the birds initially preferred the most recently seen
object when tested at six days after hatching. However, after three
further days of isolation, the birds' preferences showed a signifi-
cant return to the preference for the object seen first. As Cherfas
and Scott point out, their result could be interpreted either in
terms of a re-surfacing of the initial preference or in terms of
forgetting. The return to the original preference could merely be
a drift back to a naive preference. Bateson, Scott, Grice and
Florence (in prep.) exposed chicks to either green or blue colored
cloth balls for the first three days, the other color for the next
three days, and both colors for the final three days. With such an
experimental design, the chicks could hardly forget the ball color in
the final three days of the experiment. It was found that the resur-
facing of the preference for the colored ball was especially marked.
So these results from filial imprinting are analogous to those from
Immelmann's studies of sexual imprinting.
The studies of both filial and sexual imprinting might seem to

indicate that first experience is always more important than sub-
sequent experience. However, such a conclusion cannot be universally
true. Consider what would happen when the length of exposure of
62 P. BATESON
different groups of birds to the first imprinting object was progess-

ively reduced, keeping exposure to the second object constant.
Common sense suggests that there must be a period of exposure to the
first object which is so short as to be outweighed by the counter-
vailing effects of subsequent experience with the second object. It
is empirical matter to find out how long this period is, but the
length presumably depends on other independent variables such as the
length of exposure to the second object (Bateson, 1981). In the
course of his extensive studies, Immelmann (in preparation) has
varied both the length of the initial exposure of young zebra finches
to adult Bengalese finches, and the length of subsequent exposure to
adult zebra finches. When the male zebra finches were sexually
mature, they were given a choice between a female Bengalese finch and
a female zebra finch. The longer they had been exposed to a
Bengalese finch in early life the more they courted that species when
adult. Furthermore, the longer they had been exposed to a zebra
finch in the second period of exposure in early life the less likely
they were to court a Bengalese finch when adult. When the initial
period of exposure to a Bengalese finch was 28-32 days, and the
subsequent period of exposure to a zebra finch was 30-122 days, the
males were more likely to court the zebra finch than the Bengalese
finch. In other words the brief initial experience was outweighed by
the longer subsequent experience. It is clear from these results
that catch phrases like "primacy is more important than recency" are
misleading.
So far the analysis leaves unanswered the question of what keeps

the preference intact. When we have an example of a highly stable
preference, how is that preference protected from the effects of
subsequent experience? A behavioral defence, such as escape from, or
indifference to, novelty provides part of the answer, but even in the
case of filial imprinting not the whole solution. We shall need to
look into the nervous system for explanations but a prior question is
whether stable preferences can be reversed under any circumstances.
Here the evidence consists of little more than hints, but the answer
would seem to be "yes". I first started to think about this after
witnessing a change in the behavior of an adult female Soay sheep
which was part of a flock kept in the laboratory grounds of the
Sub-Department of Animal Behavior at Madingley near Cambridge. We
have a small flock inside a two hectare enclosure. The sheep are
timid and keep well clear of human beings. The female sheep in
question used to behave like all the others. Then, one Spring, she
had a particularly difficult time with a birth. It was necessary to
catch and anesthetize her and pull the lamb out. Ever afterwards,
until she died, this sheep remained attached to humans and would
follow people around as they moved about the enclosure.
One method of breaking-in adult horses involves drastic strangu-

lation of the horse with a rope round its neck. Even a wild horse
can be reduced to gentle submissiveness in as little as 15 minutes.
Similarly, I have been told that some unsocialized adult dogs can be
induced to form strong attachments to humans by means of traumatic
discipline. Clearly, one should not base a theory on somewhat
dubious anecdotes. Nevertheless, they set off a train of thought
about what may be the permissive conditions for such dramatic changes
in behavior in adults. One obvious candidate is stress or extreme
alarm. Here, I should like to consider the links between this possi-
bility and two very different bodies of knowledge. One is with a
colorful, but not uninteresting, area of "brain-washing". The other
is with the neurophysiology of plastic change in the nervous system.
ANXIETY AND ADULT PLASTICITY
Undoubtedly, the ability to manipulate adult minds excites

considerable military interest. How convenient it would be if
enemies could be made friends by having their beliefs changed. How
useful if certain well-placed people could be "turned" so that they
would operate against their own country. In the present context, the
examples of brain-washing - if they exist - would provide evidence
for plasticity of value systems that are commonly supposed to be
established early in life. A dramatic example of changes in behavior
was apparently provided by American prisoners in the Korean war.
About a third of the 7000 prisoners collaborated with the Chinese and
North Koreans and, when the war was over, 21 refused to return to
America. These "conversions" generated great shock and consternation
in the United States and were followed by intense examination of the
seemingly sinister techniques used. Many of the apparent conversions
turned out to have been little more than attempts to secure better
living conditions. Furthermore, the methods used by the Chinese were
neither subtle nor sophisticated (Watson, 1978). However, something
happened to some of the prisoners who were extremely frightened and
subject to intensive indoctrination.
In his book Battle for the Mind, Sargant (1957) drew on a wide
variety of examples ranging from military brain-washing and police
interrogation through to religious conversions and psychotherapy.
It was perhaps unfortunate that Sargant attempted to explain all of
these phenomena in terms of an unconvincing theory derived from
Pavlov. Critics were able to discredit the explanation and, by a
familiar academic trick, simultaneously to dispose of the evidence
(Watson, 1978). However, Sargant's less speculative points should,
I feel, be taken seriously and are relevant to the issue of adult
plasticity. He noted the importance of creating great fear and
excitement in the process of religious conversion. John Wesley, for
instance, would paint a terrifying picture of external damnation as
part of the softening-up preparatory to actual conversion. In modern
revivalist meetings in the American bible-belt, a state of hysteria
is sometimes enhanced by passing round extremely frightening objects
like live poisonous snakes. Once the state has been induced, Sargant
argued, humans are enormously suggestible.
64 P. BATESON
Sargant's method of helping shell-shocked soldiers in the Second

World War was interesting. He and his colleagues would arouse strong
emotions in the patients about events that had no direct connection
with trauma they had experienced. "Outbursts of fear or anger thus
deliberately induced, and stimulated to a crescendo by the therapist,
would frequently be followed by a sudden emotional collapse. The
patient would fall back inert on the couch - as a result of his
exhausting emotional discharge .•. It then often happened that he
reported a dramatic disappearance of may nervous symptoms. If,
however, little emotion had been released, and he had only had his
intellectual memory of the horrible episode refreshed, little benefit
could be expected". (Sargant, 1957 p xxi).
Later in his book Sargant argued for the importance of the

emotional "abreaction" in psychoanalysis. Patients are made anxious,
guilty, and even angry, by the analysts and, as a consequence, may
change their previous patterns of behavior. He quoted comments by
one of Freud's ex-patients as follows:
"For the first few months I was able to feel nothing but
increasing anxiety, humiliation and guilt. Nothing about
my past lift seemed satisfactory and more, and all my old
ideas about myself seemed to be contradicted. When I got
into a completely hopeless state, he (Freud) then seemed to
start to restore my confidence in myself, and piece every-
thing together in a new setting." (Sargant, 1957 p 57).
If Sargant is right about psychoanalysis, then the method has

something in common with the technique of "flooding" (Polin, 1959) in
which the patient is made extremely frightened in the presence of the
object towards which they have a strong phobia. Contrary to what
intuition might suggest, the patient's fear of the object is greatly
reduced in many cases. It may not be necessary to elicit fear with
the object itself, and experimental work with animals suggests that
an intense arousal of fear may be nonspecific in its beneficial
effects (Mineka, 1979).
The common element in the various military, political, religious

and therapeutic attempts to change the way adults think and behave,
is the combination of stress and suggestion. High levels of stress
are associated with rapid synthesis and turnover of noradrenalin
(norepinephrine) (see Ursin et al., 1978; Anisman, 1978). Strik-
ingly, noradrenalin is implicated as a factor by the neurophysio-
logical work on renewed brain plasticity. These studies are relevant
because they have been done on a form of neural plasticity that
characteristically occurs at a particular stage early in the life-
cycle.
NORADRENALIN AND ADULT NEURAL PLASTICITY
The development of human binocular vision is seriously affected

by squinting in the first three years of life. If it is not corrected
quickly by surgery at this stage, the child's binocular vision is
greatly impaired subsequently. If a squint develops at later stages,
binocular vision is not greatly affected (Banks et al., 1975; Hohmann
and Creutzfeldt, 1975). Similarly, the capacity of an eye to drive
neurones in the cat's visual cortex depends on whether that eye
received visual input from about 1 to 3 months after birth (e.g.
Hubel and Weisel, 1970; Rauschecker and Singer, 1981). If an eye is
visually deprived during this period it virtually loses its capacity
subsequently to excite cortical neurones. Once established, it is
exceedingly difficult, on the one hand, to reverse the dominance of
one eye over the other or, on the other hand, to impair binocular
vision in normally-reared subjects. These look like classic examples
of sensitive periods in development. Even so, Pettigrew and
Kasamatsu (1978) have found that infusion of noradrenalin into the
visual cortex of older cats can re-establish plasticity. If
normally-reared animals are monocularly deprived during the period of
noradrenalin infusion, binocular control of the neurones is lost in
the visual cortex of the hemisphere that was infused. No such change
occurs in the visual cortex of the other hemisphere. This result
firmly links at least some kinds of neural plasticity with noradrena-
lin. Much of the noradrenalin produced could arise from the locus
coeruleus (Redmond and Huang, 1979). However, noradrenergic ter-
minals have recently been found in the visual cortex of the cat
(Itakura et al., 1981).
The ways in which neural connections, once formed, can be pro-

tected from subsequent alteration is beginning to be understood (e.g.
Rauschecker and Singer, 1981). What is more, an understanding of the
links between neural plasticity and the behavior of the whole animals
are being established, particularly in the case of phenomena like
imprinting (see Horn, 1981). So it may soon be possible to under-
stand the internal mechanisms underlying the stability of preferences
established by imprinting and other examples of early learning. In
the current debate about sensitive periods, it is important that at
least one method has been discovered of reactivating plasticity both
in the nervous system and in behavior.
I can picture the wagging of fingers at what will be taken to be

such flagrant reductionism and over-simplification. So let me empha-
size my belief that the role of noradrenalin in preparing adult
brains for change is not the only way in which plasticity can be
facilitated. Nor need noradrenalin ever be necessary for some
changes. Furthermore, in those cases where stressful events do seem
to influence neural plasticity, by the permissive effects of nor-
adrenalin, the degree of stress may be very important. The relation
between stress and plasticity probably takes the form of an inverted
66 P. BATESON
U, as Yerkes and Dodson (1908) argued in another context. When the

level of stress is too great it may not be possible for subjects to
assimulate anything about their external conditions, or what is being
suggested to them. All that I accept. My major point is that under
certain conditions, stable adult behavior can be rendered labile once
again.
CONCLUSIONS
The evidence reviewed here both amplifies and qualifies a point

made by the Clarkes (1976) that children are able to recover from
virtually every kind of behavioral deficit, granted a radical change
of circumstances. It should be appreciated that the evidence for
rehabilitation leaves untouched the question of which forms of behav-
ior, once developed, are most strongly buffered against subsequent
change. It seems likely that cognitive processes are more easily
changed in adults than those underlying their emotions. We should
expect adaptations that protect certain well developed preferences
and habits from alteration. Fear of novelty, though general in its
effects, would serve precisely this function. Clearly we need to
look for and examine other forms of protection that could buffer
established systems in much more specific ways.
A positive point that emerges is that evidence for sensitive

periods in development can be readily reconciled with evidence for
subsequent changes in behavior. This is most clearly the case when
the form of treatment involves experience that would not normally be
encountered in later life. Once the mechanisms protecting behavior
from change are stripped away by suitable treatment, change resulting
from renewed plasticity is once again possible. I hope that this
reconciliation of the opposed views about the effects of childhood
and adult experience will lead to a more detailed and more open-
minded study of changes in sensitivity with age than has been the
rule in work on child development. If changes in sensitivity are
found, no particular mechanism is implied. The search for what might
generate a sensitive period in development is a separate enterprise.
In clinical circles dislike of talk about sensitive periods may

have sprung from the implied pessimism that once a child had missed
the bus, nothing could be done for it. Even if that pessimism were
justified, it would hardly be a creditable reason for averting our
gaze, however much we might want to avoid upsetting patients with
seemingly irreversible deficits. If the phenomena are to be under-
stood, they must surely be studied. In any event, the evidence I
have discussed here suggests that the grounds for optimism are con-
siderable. Furthermore, studies of sensitive periods, while they do
not provide general principles or common mechanisms, are offering
concrete examples of how developmental processes can work. This is
finally bringing to an end the grotesque search for single causes in
behavioral development. Also, coherent accounts of the interplay

between internal and external factors are a welcome relief from the
obscurantism of the view that in development everything matters all
the time.
SUMMARY
1. A sensitive period is a phase in development when a given event

can exert is maximum influence on the subsequent characteristics of
an individual. This is a description of what can sometimes happen
and is not an explanation.
2. Different examples of sensitive periods are almost certainly

brought about in different ways. In the case of imprinting in birds
a sensitive period arises from internal changes in the animal's state
which then allows the development of a pre-emptive preference for
something in the external environment.
3. Imprinted preferences are protected in part from subsequent

change by escape from novel objects. A change in preference can
occur if escape has waned. However, if imprinting has been suf-
ficiently prolonged, both filial and sexual preferences are protected
internally.
4. The possibilities for changing stable, internally-protected

adult behavior are explored. A number of cases have been noticed in
which renewed plasticity is obtained after great stress. For a
change to occur stress must be accompanied or followed by exposure to
external conditions that are different from those that were experi-
enced in early life.
5. The development of binocular V1Sl0n occurs in a classic sensi-

tive period, but, nevertheless, the underlying neural plasticity can
be reactivated by the infusion of noradrenalin (norepinephrine) into
that part of the central nervous system in which changes in connec-
tivity first occurred. Noradrenalin serves a permissive role and is
not sufficient for the plasticity. The connection with the behav-
ioral studies is that synthesis and turnover of noradrenalin in-
creases during conditions of high stress.
6. Evidence for sensitive periods early in development can readily

be reconciled with evidence for rehabilitation later in development.
Analysis of the mechanisms normally protecting behavior from sub-
sequent change can provide valuable insights into the nature of
developmental processes.
ACKNOWLEDGEMENTS
I am grateful to Klaus Immelmann who allowed me to analyze and

refer to some of his unpublished data. I am also indebted to Giorgio
68 P. BATESON
Bignami, Ann Clarke, Robert Hinde, Gabriel Horn, Giovanni Jervis,

Paul Martin, Michael Rutter and Joan Stevenson-Hinde, all of whom
commented on an earlier version of the the manuscript.
REFERENCES
Anisman, H., 1978, Neurochemical changes elicited by stress:

behavioral correlates, pp 119-172 in: "Psychopharmacology of
Aversively Motivated Behavior," H.Anisman and G. Bignami,
eds., Plenum, New York.
Asdourian, D., 1967, Object attachment and the critical period,
Psychon.Sci. 7:235-236.
Banks, M. S., Aslin, R. N., and Letson, R. D., 1975, Sensitive period
for the development of human binocular vision, Science 190:
675-677 .
Bateson, P. P. G., 1964, Effect of similarity between rearing and
responses, J.Comp.Physiol.Psychol. 57:100-103.
Bateson, P. P. G., 1976a, Specificity and the origins of behavior,
Adv.Study of Behav. 6:1-20.
Bateson, P. P. G., 1976b, Rules and reciprocity in behavioral
development, pp 401-421 in: "Growing Points in Ethology,"
P.P.G. Bateson and R.A. Hinde, eds., Cambridge Univ. Press,
Cambridge.
Bateson, P., 1979, How do sensitive periods arise and what are they
for? Anim.Behav. 27:470-486.
Bateson, P., 1981, The control of sensitivity to the environment
during development, pp 432-453, in: "Behavioral Development,"
K. Immelmann, G. Barlow, L. Petrinovich and M. Main, eds.,
Cambridge Univ. Press, Cambridge.
Bateson, P. P. G., and A. A. P. Wainwright, 1972, Effects of prior
exposure to light on the imprinting process in domestic
chicks, Behavior 42:279-290.
Cherfas, J. J., and Scott, A., 1981, Impermanent reversal of filial
imprinting, Anim.Behav. 29:301.
Clarke, A. M., and Clarke, A. D. B., 1976, "Early Experience: Myth
and Evidence," Open Book, London.
Fischer, G. J., 1970, Arousal and impairment: Temperature effects on
following during imprinting, J.Com.Physiol.Psychol. 73:412-
420.
Freud, S., 1910, "Three Contributions to the Sexual Theory," J.
Nervous and Mental Diseases Publ. Co., New York.
Freud, S., 1949, "An Outline of Psycho-analysis," Hogarth Press,
London.
Guiton, P., 1959, Socialization and imprinting in Brown Leghorn
chicks, Anim.Behav. 7:26-34.
Hales, D. J., Lozoff, B., Sosa, R., and Kennell, J. H., 1977,
Defining the limits of the maternal sensitive period, Dev.Med.
Child Neurol. 19:454-461.
Hohmann, A., and Creutzfeldt, O. D., 1975, Squint and the development
of binocularity in humans, Nature 254:613-614.
Horn, G., 1981, Neural mechanisms of learning: an analysis of
imprinting in the domestic chick, Proc.Roy.Soc.B. in press.
Horn, G., Rose, S. P. R., and Bateson, P. P. G., 1973, Experience and
plasticity in the central nervous system, Science 181:506-514.
Hubel, D. H., and Wiesel, T. N., 1970, The period of susceptibility
to the physiological effects of unilateral eye closure in
kittens, J.Physiol. 206:419-436.
Immelmann, K., 1969, Uber den Einfluss Fruhkindlicher Erfahrungen auf
die geschlechtliche Objektfixierung bei Estrildiden. Z.
Tierpsychol. 26:677-691.
Immelmann, K., 1979, Genetical constrains on early learning: A
perspective from sexual imprinting in birds, pp 121-133 in:
"Theoretical Advances in Behavior Genetics," J.R. Royce and L.
Mos, eds., Sijthoff and Noordhoff, Alphen ann den Rijn,
Netherlands.
Immelmann, K., and Suomi, S. J., 1981, Sensitive phases in
development, pp 395-431 in: "Behavioral Development," K.
Immelmann, G.W. Barlow, ~ Petrinovich and M. Main, eds.,
Cambridge Univ. Press, New York, in press.
Itakura, T., Kasamatsu, T., and Pettigrew, J. D., 1981,
Norepinephrine-containing terminals in kitten visual cortex:
laminar distribution and ultrastructure, Neurosci. 6:159-175.
Kovach, J. K., 1970, Critical period or optimal arousal? Early
approach behavior as a function of stimulus, age, and breed
variables in chicks, Dev.Psychobiol. 3:73-77.
Landsberg, J-W., 1976, Posthatch age and developmental age as a
baseline for determination of the sensitive period for im-
printing, J.Comp.Physiol.Psychol. 90:47-52.
Landsberg, J-W., and Weiss, J., 1976, Stress and increase of the
corticosterone level prevent imprinting in ducklings, Behavior
57:173-189.
Lenneberg, E. H., 1967, "Biological Foundations of Language," Wiley,
New York.
MacDonald, G. E., 1968, Imprinting: drug-produced isolation and the
sensitive period, Nature 217:1158-1159.
Martin, J. T., 1975, Hormonal influences in the evolution and
ontogeny of imprinting behavior in the duck, pp 357-366 in:
"Hormones, Homeostasis and the Brain. Progress in Brain--
Research Vol. 42," W.H. Gispen, T.B. van Wimersma Greidanus,
B. Bohns and D. de Wied, eds., Elsevier, Amsterdam.
Martin, J. T., and Shutz, F., 1974, Arousal and temporal factors in
imprinting in Mallards, Dev.Psychobiol. 7:69-78.
Mineka, S., 1979, The role of fear in theories of avoidance learning,
flooding, and extinction, Psychol.Bull. 86:985-1010.
Moltz, H., and Stettner, L. J., 1961, The influence of patterned-
light deprivation on the critical period for imprinting,
J.Comp.Physiol.Psychol. 54:279-283.
70 P. BATESON
Oyama. S •• 1979. The concept of the sensitive period in developmental

studies. Merrill-Palmer Q. 25:83-103.
Paulson. G. W., 1965, Maturation of evoked responses in the duckling,
Exp.Neurol. 11:324-333.
Pettigrew, J. D•• and Kasamutsu. T•• 1978. Local perfusion of nor-
adrenaline maintains visual cortical plasticity, Nature 271:
761-763.
Polin. A. T •• 1959, The effects of flooding and physical suppression
as extinction techniques on an anxiety motivated avoidance
locomotor response, J.Psychol. 47:235-245.
Rajecki, D. W•• 1973. Imprinting in precocial birds: interpretation,
evidence and evaluation, Psychol.Bull. 79:48-58.
Ratner. A. M., and Hoffman. H. S., 1974. Evidence for a critical
period for imprinting in Khaki Campbell ducklings (Anas
platyrhynchos domesticus), Anim.Behav. 22:249-255. ----
Rauschecker, J. P., and Singer. W•• 1981, The effects of early visual
experience on the cat's visual cortex and their possible
explanation by Hebb synapses, J.Physiol. 310:215-239.
Redmond. D. E•• and Huang, Y. H., 1979. Current Concepts II. New
evidence for a locus coeruleus-norepinephrine connection with
anxiety. Life Sci. 25:2149-2162.
Rutter. M•• 1980. The long-term effects of early experience. Dev.Med.
Child Neurol. 22:800-815.
Salzen, E. A•• and Meyer, C. C•• 1968. Reversibility of imprinting,
J.Comp.Physiol.Psychol. 66:269-275.
Sargent, W., 1957. "Battle for the Mind." Heinemann, London.
Scott, J. P .• ed., 1978, "Critical Periods," Dowden, Hutchinson and
Ross, Stroudberg, Penn.
Sluckin, W., and Salzen, E. A., 1961, Imprinting and Perceptual
Learning, Q.J.Exp.Psychol. 13:65-77.
Smart, J. L., Byrne, E. A., and Dobbing, J., 1977, New thoughts on
catch-up growth, Proc.Nutr.Soc. 36:99A.
Smith, F. V., and Nott, K. H., 1970, The "critical period" in
relation to the strength of the stimulus, Z.Tierpsychol. 27:
108-115.
Ursin, H., Baade, E., and Levine, S •• eds., 1978, "Psychobiology of
Stress," Academic Press, New York.
Vidal, J-M., 1980, The relations between filial and sexual imprinting
in the domestic fowl: effects of age and social experience,
Anim.Behav. 28:880-891.
Watson, P •• 1978, "War on the Mind," Hutchinson, London.
Weiss, J .• Kohler, W•• and Landsberg, J-W •• 1977, Increase of the
corticosterone level in ducklings during the sensitive period
of the following response. Dev.Psychobiol. 10:59-64.
Yerkes, R. M., and Dodson, J. D., 1908, The relation of strength of
stimulus to rapidity of habit-formation, J.Comp.Neurol.
Psychol. 18:459-482.
SOCIAL DEVELOPMENT IN RHESUS MONKEYS:
CONSIDERATION OF INDIVIDUAL DIFFERENCES
Stephen J. Suomi
Department of Psychology and Primate Laboratory

University of Wisconsin-Madison
Madison, Wisconsin 53706 U.S.A.
INTRODUCTION
The development of social behavior by rhesus monkeys (Macaca

mulatta) has attracted the interest of numerous investigators over
the past 2 decades. Researchers have watched rhesus monkey infants
grow up in many different physical and social settings, including
feral environments within the Indian subcontinent (Lindburg, 1973;
Taylor et al., 1980), outdoor enclosures containing social groups
similar in composition to those found in the wild (Sade, 1967;
Berman, 1978), and a variety of laboratory environments in which
access to social stimuli is under rigorous experimental control
(Hansen, 1966; Hinde and Spencer-Booth, 1967; Dienske and Metz,
1977). In general, it has been found that if rhesus monkeys are
reared under conditions of severe social deprivation obvious psycho-
pathology will result, but if they are reared in social environments
that contain their mothers and access to peers they will most likely
develop behavioral repertoires highly similar to those displayed by
rhesus monkeys reared in natural habitats (Harlow and Harlow, 1969;
Suomi and Harlow, 1978). Indeed, monkeys reared in socially "ade-
quate" laboratory environments follow the same general ontogenic
schedule, in terms of the timing and sequence of emergence of specif-
ic patterns of behavior, as do rhesus monkeys who grow up in the wild
(Rosenblum 1971; Suomi, 1977).
Despite the general consistency of developmental changes in

social behavior displayed by rhesus monkeys reared in either field or
"good" laboratory environments, there are numerous individual differ-
ences in precisely how and when these developmental changes are
expressed. Individual differences in social ontogeny can be of con-
71
72 S. J. SUOMI
siderable significance for a variety of reasons. From a biological

perspective they are important to the degree that they are associated
with individual differences in reproductive success within a popula-
tion or group of monkeys. From a psychological perspective individu-
al differences in social ontogeny are of interest to the extent that
they can predict differences in personality or in social competence
during adulthood. Finally from a clinical perspective they can be of
great practical value if they permit identification of particular
individuals who are at high risk for subsequent development of ~
chopathology.
In this chapter I will discuss the nature and or~g~n of indi-

vidual differences in social development among rhesus monkeys. I
will begin by describing the general pattern and sequence of develop-
mental changes that are shared by virtually all monkeys who group up
in socially adequate environments, as well as some differences bet-
ween individuals that can emerge during development. I will then
consider some of the factors that clearly contribute to these onto-
genic differences. Two of those factors - the quality of maternal
care received and the nature of social stimulation provided by other
group members - have been thoroughly studied to date, and some of the
relevant results from this research will be briefly reviewed. A
third possible source of influence - inborn temperament differences
in fearfulness or anxiety - will be examined more extensively, and
new findings involving both physiological and behavioral data will
be presented. Finally, some implications of these findings for
future studies of both monkey and human social development will be
considered.
NORMATIVE PATTERNS OF RHESUS MONKEY SOCIAL DEVELOPMENT
Virtually every rhesus monkey infant spends most of its first

few weeks of life on or in close proximity to its mother. During
this time the infant is dependent on its mother not only for nourish-
ment but also for physical warmth and emotional security, or "contact
comfort" as Harlow (1958) has termed it. The mother also provides
the infant with protection from predators and other potential threats
to its survival.
Most rhesus monkey newborns are highly inquisitive and readily

explore almost anything within their physical reach. As their loco-
motive abilities rapidly expand during the second month of life these
infants begin to leave their mothers for brief periods in efforts to
extend their range of exploration. While some mothers may initially
restrict such activity by their infants, most mothers become increas-
ingly willing to permit their infants to explore nearby objects and
conspecifics as they grow older. The infants, in turn, continue to
use their mothers as a base for exploration and a source of security
as their excursions become more frequent and of longer duration in
SOCIAL DEVELOPMENT IN RHESUS MONKEYS 73
succeeding weeks. When away from their mothers, young rhesus monkeys
increasingly come into contact with other monkeys in their social
group, especially peers and older siblings. Social relationships
with these other monkeys develop rapidly, so that by 5 or 6 months of
age most infants spend more of their waking hours interacting with
peers than with their mothers (Suomi, 1979a).
Social play is the predominant behavior characterizing most peer

relationships developed by young rhesus monkeys. As they grow older
the quality and sophistication of their play interactions progres-
sively increase; bouts of play become longer in duration, involve
more extended sequences of mutual exchanges, and tend to include in-
creasing numbers of participants (Symonds, 1978; Suomi, 1979a).
During this time sex differences in the form, frequency, and choice
of partners in these play bouts also typically emerge. Males tend to
engage in more play interactions, and these interactions usually are
more physically oriented and more likely to involve male partners
than is characteristic of play bouts initiated by young rhesus monkey
females (Harlow and Lauersdorf, 1974). Although these sex differ-
ences are relative rather than absolute, with considerable overlap
between individual males and females, the differences generally
become more pronounced as the monkeys approach adolescence
(Ruppenthal et al., 1974).
While there is little question that social play is a prominent

social activity for rhesus monkeys from infancy to adolescence, there
has long been considerable controversy as to its functional signifi-
cance (Smith, 1981). However, it is clear that precursors of most
rhesus monkey adult behavior patterns, including the basic motor
patterns involved in copulation and those employed in aggressive en-
counters, can be readily identified in the social play of youngsters
(Harlow and Lauersdorf, 1974). Some investigators have suggested
that adult performance of these and other social activities is en-
hanced when individuals have had the opportunity to develop, prac-
tice, and perfect the behaviors within the context of social play
during childhood. Indeed. evidence from numerous laboratory studies
has demonstrated that rhesus monkeys prevented from playing while
growing up tend to be hyperaggressive and sexually incompetent as
adolescents and adults (Alexander and Harlow, 1965); Harlow and
Harlow, 1969; Suomi, 1979a).
Normally, the incidence of social play declines rapidly as

rhesus monkeys approach adolescence, and by the time they are adults
play has all but disappeared from their repertoires. Most other
interactions with peers also become less frequent once a rhesus
monkey has passed through puberty. Instead, both males and females
expand their range of social relationships during adolescence, al-
though they do so in markedly different fashions. Females tend to
spend more time interacting with older female siblings and their
offspring, remaining in the same social subgroup as their mothers.
74 S. J. SUOMI
In contrast, most males tend to leave their natal troop following

puberty, initially staying at the periphery of the troop, perhaps
joining an all male "gang" for 2 or 3 years, then eventually entering
a different troop (Lindburg, 1973; Sade, 1967). Thus, as adults,
most females reproduce within their natal troop, while most males
move out and spread their genes among conspecifics with whom they did
not grow up.
While the same general developmental route has been followed

from birth to maturity by countless generations of rhesus monkeys,
there are ample opportunities for anyone individual to take onto-
genic excursions along the way. No two rhesus monkeys develop social
repertoires in exactly the same fashion. Instead, they are likely to
differ from one another in any number of ways while growing up.
For example, rhesus monkey infants differ in the type of social

relationships they establish with their mothers in the first few
weeks of life. They also differ in how soon they begin to leave
their mothers to explore their immediate surroundings, as well as in
how frequent and extensive such exploratory forays turn out to be.
Young rhesus monkeys subsequently do not all establish social rela-
tionships with others in their social group at the same exact age or
in precisely the same manner, nor do they all spend the same amount
of time interacting with peers and other conspecifics. Moreover, not
all rhesus monkeys are afforded the same opportunities to expand
their social repertoires and sharpen their social skills through play
interactions. Finally, rhesus monkeys do not all share the same set
of experiences as adolescents, just as they do not as adults.
Thus, even though virtually all rhesus monkeys begin life in

close association with their mothers, develop additional social
relationships with peers and other troop members during childhood,
and undergo major social changes once they reach puberty, anyone
monkey's particular pattern of ontogeny is unlikely to be precisely
matched by that of any other monkey. The opportunities for individu-
al differences to emerge during development are clearly numerous, and
they are potentially available at virtually every stage of social
ontogeny. Furthermore, differences between individual monkeys early
in life are likely to become exaggerated, at least under some circum-
stances, if the individuals continue to accumulate different experi-
ences while growing up.
FACTORS CONTRIBUTING TO INDIVIDUAL DIFFERENCES IN DEVELOPMENT: THE

ROLE OF MOTHER
Numerous factors have been shown to influence the process of

social development in young rhesus monkeys. One of the most promin-
ent and most thoroughly studied of these factors concerns the quality
of the maternal care an infant receives. There is no question that
rhesus monkey mothers play a crucial role in the early social devel-
opment of their offspring. Not only do they provide nourishment and
protection in the earliest months of life, but also they provide a
source of warmth, comfort, and security, a base from which the in-
fants can begin to explore their physical and social environment. It
is no accident that a rhesus monkey infant's first sustained social
relationship is invariably with its own mother. While this relation-
ship is unique in many respects (Hinde and Spencer-Booth. 1967;
Suomi. 1979b). it also can provide a general blueprint or style for
the many additional social relationships the infant will establish
with other monkeys as it grows older (Sroufe and Waters, 1977).
Rhesus monkey mothers do not all rear their infants in identical

fashion, and the relationships that different mothers establish with
their respective infants can differ markedly from dyad to dyad. The
basis for such differences is often multifaceted. For example, not
all mothers provide their infants with the same amount of milk, and
some start weaning their infants to solid food earlier than do
others. Rhesus monkey mothers can differ in the relative frequency
and degree to which they restrain or restrict their infant's efforts
to explore the environment early in life, and they can also differ in
how often and intensely they punish their infant as it grows older.
Some mothers are always willing to intervene on behalf of their
infant in disputes it may have with peers or others in the social
group, while other mothers frequently reject their infant's attempts
to gain or maintain physical contact or access to a maternal nipple
(Rosenblum, 1971; Dienske and Metz, 1977). Many of these differences
in maternal care can lead to differences in the types of long-term
social relationships established between mothers and infants. Dif-
ferences in mother-infant relationships, in turn, can lead to differ-
ences in how readily and how rapidly infants begin to leave their
mothers to interact with others in their social group.
For example, a mother who is overly restrictive of her off-

spring's early attempts to explore will in all likelihood be reducing
the infant's exposure to others in the group. This, in turn, may put
it at a disadvantage relative to those peers whose exploration and
play are not restricted by their mothers (White and Hinde, 1975;
Suomi, 1979a). Alternatively, an infant whose mother is inconsistent
or unpredictable in her caretaking activity may develop and insecure
or "anxious" attachment relationship with her. As a result, the
infant may be reluctant to venture away from the mother and conse-
quently may be limited in its exposure to peers and others in the
social group (Hinde and Simpsom, 1975). Other studies have shown
that when a mother is unusually punitive or excessively rejects her
infant's efforts to maintain body or nipple contact, the offspring
typically becomes preoccupied with mother-directed activities and
correspondingly displays lower-than-normal levels of exploration and
peer interactions throughout early development (Arling and Harlow,
1967; Rosenblum, 1971). In each case, the eventual result is an
76 S. J. SUOMI
infant who is functionally deprived of opportunities to establish new

social relationships to expand its social repertoire and to improve
its social skills.
Differences between mothers in other respects not directly

related to their caretaking capacities can also be of consequence for
the social development of their offspring. For example, numerous
studies have revealed that the relative. status or position of a
mother in the dominance hierarchy of her social troop can be a major
factor in how her infant is treated by other group members
(Missakien, 1973; White and Hinde, 1975; Berman, 1980). Infants
whose mothers are high in the dominance hierarchy essentially have
the run of the troop. These infants are treated with considerable
deference by not only their peers but also all other group members,
presumably out of fear of possible retaliation by socially powerful
mothers. Indeed, other group members often appear to seek out
friendly interactions with offspring of high-ranking females in order
to enhance their own status (Sade, 1967; Spencer-Booth, 1968). Thus,
these infants are all but guaranteed a life rich in positive social
stimulation as they grow up. In contrast, offspring of low-ranking
mothers are treated with deference by few if any other monkeys in the
troop; indeed, they may serve as scapegoats. Because a low ranking
mother usually cannot effectively intervene on her infant's behalf
should it get into trouble with other group members, a common strate-
gy on her part is simply to restrain her infant, further limiting its
opportunities to interact with other monkeys (White and Hinde, 1975).
These examples serve to emphasize the point that the actions and
status of an infant's mother can have a major influence on its social
development within its natal troop. Mothers who differ in their
relationships with their infants, as well as in their relationships
with other group members, are likely to contribute substantially to
differences in how their respective infants grow up. Individual
differences among mothers may lead to ontogenic consequences that
continue long after the infants have become largely independent of
maternal care.
THE ROLE OF OTHERS IN SHAPING ONTOGENIC DIFFERENCES
Mothers are not the only individuals with whom young rhesus
monkeys form social relationships. Others in the social group play
increasingly important roles in the infants' social development as
they grow older and their mothers become involved with new offspring.
Because a young monkey typically forms different types of social
relationships with various others in its social group, e.g., peers,
older siblings, and nonrelated adolescents and adults (Suomi, 1979b),
the availability of these various others as partners for social
interactions can be an important factor in a given infant's pattern
of social development.
For example, it has consistently been found that young monkeys

generally prefer to play with age-mate peers, especially those of the
same sex, when such age-mates are available (e.g., Harlow, 1969;
Ruppenthal et al., 1974). Consequently, infants who grow up in
social groups that contain relatively few same-sex peers may spend
less time engaging in play interactions and their interactions may be
more restricted in scope and complexity than is the case for infants
who grow up in social groups where peers are plentiful. On the other
hand, if numerous peer playmates are available to a young rhesus
monkey, it may become so involved in interacting with these age-mates
that its development of social relationships with others in its
social group suffers. As described previously, relationships with
these others serve to broaden the young monkey's range of social
experiences and make its overall social repertoire more flexible.
Thus, individual monkeys that spend excessive amounts of time in peer
interactions may actually be limiting .their social experiences, just
as infants who are preoccupied with interactions with their mothers
may be retarding other aspects of their overall social development.
The potential complexity for differential effects of "demograph-

ic" influences on anyone individual's particular pattern of ontogeny
can be seen in studies of sibling relationships among young rhesus
monkeys. Both laboratory and field investigations have revealed that
the presence of an older sibling tends to accelerate the development
of independence by an infant from its mother (Suomi, 1977; Berman,
1978). However, there are sex differences: infants with older male
siblings generally leave the immediate presence of their mothers
earlier chronologically than do infants with older female siblings,
and this difference is usually greater when the infant itself is a
male rather than a female (Berman, 1978). Furthermore, the age gap
between the infant and its older sibling, but the less involved will
be the relationships with an older male sibling, especially if the
infant is a male (Suomi, 1981a). These findings all suggest than
even subtle differences between young monkeys in terms of available
siblings can contribute substantially to differences in their overall
social development.
Additional research has demonstrated similar complexities with

respect to individual differences in other types of social relation-
ships young rhesus monkeys routinely establish as they are growing
up. For example, an infant can establish a wide range of possible
social relationships with adult males in its social group, depending
in part on the sex of the youngster and on the availability, "person-
ality", age, and social status of the adult males, as well as their
biological relationship to the infant (Parke and Suomi, 1981; Snowdon
and Suomi, 1981). Clearly, in addition to the mother, many other
individuals in the social environment can differentially affect an
infant's social development.
Other aspects of a young rhesus monkey's rearing environment

involving more than simple group demographics can also have a consid-
78 S. J. SUOMI
erable influence on that individual's social development. In partic-

ular, factors that tend to disrupt ongoing activities within the
social group or to increase overall group tension or instability can
have deleterious consequences for an infant's budding behavioral
repertoire. Such factors include sharp changes in the dominance
hierarchy of the troop, the introduction of strangers within the
troop, intense competition from other monkey troops, troop fission,
and increased pressure from predators. A common consequence of each
factor is that mothers typically become more restrictive and less
willing to permit their infants to explore and play at will; addi-
tionally, potential play partners usually become less readily avail-
able under these circumstances. Often the end result is that infants
are deprived of many opportunities to expand social repertoires and
to develop social skills relative to infants who grow up in more
peaceful social settings.
Thus, the pattern and process of a rhesus monkey infant's social

ontogeny is sensitive to a wide variety of environmental influences
that are independent of its mother's caretaking efforts. Moreover,
each of these influences can interact with other factors, including
those involving maternal care, to produce unique effects on an in-
fant's development. For example, if one rhesus monkey infant grows
up in a troop that has been stable for years, while another infant is
reared in a troop that is in the process of splitting into several
fragments, the former infant is likely to have more opportunities to
interact with peers and adult males as it grows up than will the
latter. However, if the former infant's mother is highly restrictive
and/or punitive relative to the latter infant's mother, the end
result might be highly similar for both infants. On the other hand,
if the second infant's mother were more restrictive and/or punitive,
ontogenic differences between the two infants would likely be exag-
gerated.
In summary, many environmental factors have been shown to influ-

ence rhesus monkey social development. To the extent that individual
infants differ from one another with respect to any of these factors
or to their interactive effects, there will most likely be differ-
ences in the infants' respective patterns of social development.
INDIVIDUAL DIFFERENCES IN FEARFULNESS OR ANXIETY
Another important source of ontogenic variability among young

rhesus monkeys can be traced not to differences between mothers or
rearing environments but rather to inborn differences among the in-
fants themselves. Rhesus monkeys are not all born alike; soon after
birth there may be obvious differences between infants in terms of
physical, constitutional, and temperament factors. Foremost among
the latter characteristics, at least from the standpoint of social
development, are differences between infants with respect to inherent
fearfulness or anxiety.
Many developmental theorists and researchers, including those
studying human as well as nonhuman primate subjects, have recognized
the role fear or anxiety (timidity or wariness) can play in a pri-
mate's social development (Harlow and Zimmermann, 1959; Bowlby, 1969;
Bischof, 1975; Suomi and Harlow, 1976; Sroufe and Waters, 1977).
When an infant is frightened or anxious it invariably seeks out its
mother for protection and security, and all exploratory and play
activity stops until the infant has been sufficiently comforted and
reassured by its attachment object. Thus, frequently frightened,
chronically anxious, or constantly wary infants will very likely have
less time to explore and fewer opportunities to play than will in-
fants who are not. Such self-imposed restraints may serve to retard
or otherwise impair the social development of timid or insecure
infants if these tendencies are maintained throughout their childhood
years.
Differences between infants on this temperament dimension might

be expected to be most pronounced under conditions that are mildly
stressful for most individuals. Under such conditions the least
fearful or anxious infants might well continue ongoing exploratory or
play activity, eschewing the relative safety of maternal contact.
Moderately timid or anxious infants might well interrupt ongoing be-
havior to return to their mothers briefly for reassurance, then leave
their mothers and resume their previous activities. On the other
hand, highly fearful or wary infants might not leave their mother's
immediate proximity for some time after the stress subsides, perhaps
never going back to the activities interrupted by the appearance of
the stress.
Thus, under conditions of mild stress substantial differences

between infants who vary on this temperament dimension would be ex-
pected. In contrast, under conditions of severe stress all infants
would be expected to stay with their mothers until conditions return-
ed to normal, while in situations in which environmental stress was
minimal or absent few if any infants would be restricted in their
exploratory or play activity. Thus, differences in the amount of
stress to which anyone infant is exposed may produce differential
effects on its social development depending on its particular temper-
amental status.
Given these considerations, it follows that any differences bet-

ween infants in their inherent fearfulness (anxiety, timidity, or
wariness) could readily interact with a number of other factors,
including those pertaining to maternal care and rearing environment,
in shaping particular patterns of social ontogeny. More Specifical-
ly, factors that served to produce stressful situations or experi-
ences for developing young primates would likely have differential
consequences for infants who differed in their susceptibility or
responsiveness to stressful events. In statistical terms, there
would be interactive effects (synergistic consequences) between in-
80 S. J. SUOMI
fant temperament differences and differences in those maternal care

and rearing environment variables relevant to the induction of stress
in these subjects.
For example, consider the case of two rhesus monkey infants both
having mothers that reject them at unusually high rates, but who
differ considerably with respect to their relative tolerance for
stressful stimulation, including rejection by their mothers. The
infant that responds to mild stress with marked fearfulness and
wariness may experience a rise in anxiety whenever it is rejected,
and if its mother indeed rejects it at a high rate, it may grow up in
an almost chronic state of anxiety. In contrast, the infant with a
high threshold for response to stress may be relatively unaffected by
frequent rejection by its mother; for this infant the adverse conse-
quences of being reared by a high-rejecting mother would likely be
minimal. On the other hand, if both infants were reared by mothers
that almost never rejected or punished their offspring, any tempera-
ment differences they might have could well be masked and they would
likely have similar patterns of social development, assuming they had
otherwise similar experiences. Thus, the consequences of temperament
differences depend on what kind of mothers infant monkeys have, and
vice versa.
Along parallel lines, differences between infants in their

respective thresholds for reactions to stress can have quite varied
ontogenic consequences depending on the relative stability of the
rearing environment. In a relatively safe and stable social environ-
ment, with few dominance conflicts, group membership changes, or
predator pressures, infants with very different stress thresholds
might well show very similar patterns of development. In contrast,
if the infants' rearing environment were unstable and unpredictable,
temperament differences between the infants might serve to exaggerate
any ontogenic differences that might emerge. It should be pointed
out that young monkeys prone to fearfulness or anxiety might not
always be at a disadvantage in unstable social rearing environments -
especially if threats to the infants' survival were common. Under
such circumstances a propensity for wariness or fearfulness might
well turn out to be highly adaptive in the long run, even if social
development were somewhat retarded relative to what it might be in a
stress-free rearing environment.
These examples serve to illustrate some of the many ways in

which differences between young monkeys in relative fearfulness or
anxiety can contribute to major differences in their social develop-
ment. Inherent temperament differences can be largely masked and of
trivial long-term ontogenic consequence when infants are reared under
circumstances that are generally stress-free. However, the same
temperament differences can be an important source of ontogenic
variability when infants grow up under more stressful circumstances.
Moreover, it is not difficult to envision certain types of rearing
environments in which a propensity for timidity or wariness would be

highly adaptive. even though a similar propensity expressed in other
rearing environments might result in retarded social development.
AUTONOMIC INDICES OF TEMPERAMENT DIFFERENCES: ASSESSMENT AND DEVELOP-

MENTAL STABILITY
Although, as was argued above, individual differences between

young monkeys in inherent fearfulness, anxiety. timidity, and wari-
ness may serve as major sources of variability in social development
among these individuals, the empirical assessment of such temperament
differences has proven to be quite problematic to date. The most
obvious and straightforward approach to the measurement of tempera-
ment differences - direct observation and description of behavioral
expressions of temperament - is fraught with difficulty. First of
all, behavioral expressions of fearfulness, anxiety, timidity, and
wariness typically undergo substantial changes as young monkeys
grow older and expand their behavioral repertoires (Suomi et al.,
1981). Therefore, direct comparisons between such temperament
indices obtained from newborn monkeys and those obtained from older
infants, juveniles. or adolescents may be somewhat suspect. i.e •• it
would be akin to comparing young apples with older oranges. More-
over, behavioral assessment of "real" temperament differences
between young monkeys is greatly complicated by the fact that such
differences can clearly interact with differences in maternal care
and/or numerous characteristics of the social rearing environment, as
was previously discussed. Thus. expressions of fearfulness, anxiety,
timidity, or wariness will almost always be in part a function of
various maternal and rearing environmental factors that are largely
independent of intrinsic temperament differences ~~, and these
factors may act to obscure or exacerbate "true" or "pure" temperament
effects when assessed by behavioral measures. In fact, the only cir-
cumstances under which "pure" temperament differences between infants
could be directly assessed behaviorally would be cases in which all
of these factors were identical for each infant under comparison, an
unlikely occurrence except under highly controlled experimental
conditions.
One alternative approach to the assessment of temperament dif-

ferences between infant monkeys can be found in possible physiologi-
cal concomitants of fearfulness or anxiety in these subjects. Recog-
nition that expressions of such emotions have physiological as well
as behavioral outlets can be traced at least back to the 19th century
writings of William James (1891). Since then a number of investiga-
tors have argued that individual differences in sympathetic nervous
system reactivity are likely to parallel differences between the
subjects in their thresholds for fear or anxiety (Spence. 1964).
We have recently begun to look at measures of autonomic reac-

tivity as a means of assessing possible individual differences in
82 S. J. SUOMI
relative fearfulness or anxiety in our monkey subjects at Wisconsin.

Our first studies in this area involved the measurement of heart rate
changes in infants placed in a standardized conditioning paradigm.
Differences between infants on these psychophysiological indices were
then correlated with individual differences in levels of certain
behaviors displayed by the infants at various stages in their devel-
opment.
In the initial study 10 nursery-reared infants were each run

through a total of 80 conditioning trials over a 10-day period,
beginning when each infant was 28 days of age. On each trial a
10-second 70db tone preceded a 4-second burst of 105 db white noise,
and the subject's heartrate change scores were averaged over the 80
trials to yield a single mean heart rate change score (bHR) for each
subject. Subjects were then reared individually with surrogates for
the rest of their first year of life, and during this period their
home-cage behaviors were observed and recorded 3-4 times per week.
Each subject's scores for each behavioral category were summed over
3-month intervals, and these mean category scores were then correlat-
ed with the origin~l EHR scores recorded for each infant. Striking
findings emerged: ~HR scores correlated strongly with all behavioral
indices of fearfulness and anxiety during each subsequent 3-month
period (r's ranging between +.82 and +.92), but the same ~HR scores
failed to correlate significantly with other behavior categories
during the same 3-month periods (Baysinger et al., 1978).
Follow-up study of these 10 monkeys in a variety of situations

revealed that the early LHR scores continued to accurately predict
other behaviors - right up to puberty (the study was discontinued at
that point). Moreover, the early bHR measures showed high positive
correlations with several measures of CSF amine metabolites obtained
during the subjects' third year of like (Suomi et al., 1981). Taken
as a whole, the findings from this first study suggested that indi-
vidual differences in behavioral indices of fearfulness/anxiety were
relatively stable throughout development for subjects raised in the
same environment and that these individual differences could be
predicted from a psychophysiological measure of autonomic respon-
sivity tapped during the first month of life. A replication study,
carried out on subjects reared in a more socially stimulating envi-
ronment, produced essentially the same results (Suomi, 1981b).
More recent research at Wisconsin has focused on the relation-

ship of this bHR measure to other indices of autonomic reactivity in
developing young monkeys. One obvious measure of this type is that
of plasma cortisol, probably the most widely used index of adrenal
activity found in the vast literature on stress response in animals
(Natelson et al., 1976; Hennessy and Levine, 1979). Numerous studies
of cortisol response to a variety of social, environmental, and
pharmacological stressors have been carried out with rhesus monkey
subjects. In some of these studies cortisol levels have been direct-
ly compared with various behavioral and other physiological measures

of the subject's reactions to the stressors (Mason, 1975; Coe and
Levine, 1981). However, none of these studies have focused upon in-
dividual differences in terms of cortisol responsiveness, and no
study has traced such individual differences throughout development.
For these reasons, it seemed appropriate to look longitudinally at
cortisol levels in monkey infants for whom ~HR data and various be-
havioral measures were also available.
Twelve rhesus monkey infants were therefore separated from their

mothers at birth and reared in our laboratory nursery in incubators
for the first 21 days of life. On day 22 they were removed from
their incubators and placed in "regular" nursery cages; 2 hours after
this move a blood sample was drawn from each infant. Each sample was
then assayed for plasma cortisol content. Six days after blood sam-
pling, at 28 days of age, heartrate conditioning trials were begun
for each subject according to the previously described procedure.
Following heartrate conditioning trials, subjects were assembled into
3 peer groups of 4 infants; each group was housed in a separate pen.
Subjects remained in their respective peer groups for the next 17
months, except for the periodic peer separations described in the
next section.
At 18 months of age, each subject was removed from its peer

group for a 2-hour "activity test", then returned to its group. The
test was designed to be mildly stressful. During each 2-hour test,
the subject was placed alone in a standard-sized cage in a strange
room and its activity monitored by a device sensitive to air disturb-
ances caused by the subject's own movements (Scallet, 1981). A blood
sample was drawn just before the start of the activity test (basal
value), and a second sample was taken at the end of the 2-hour test
(2-hour stress value). The two blood samples for each subject were
then assayed for plasma cortisol levels, and the activity date for
the test session were summed to yield a single score for each sub-
ject.
Comparison of these activity test measures taken at 1 1/2 years

of age with ~HR and cortisol measures gathered from the same monkeys
Table 1. Correlations: Physiological Measures
t:.HR CortB CortPk Act

.59* ~ .56* -.48 Cort - 22d
.08 .70** -.68** t:.HR - 28d
.38 -.37 CortB - 18 mo.
-.68** CortPk - 18 mo.
*.E. < .05

**.E. < .01
84 S. J. SUOMI
when they were 1 month old yielded some striking findings in terms of
the stability of individual differences. These comparisons are sum-
marized in Table 1, which presents the intercorrelation matrix for
22-day cortisol, 28-day ~HR, 18-month basal cortisol, l8-month peak
cortisol (after the 2-hour activity test), and l8-month activity
scores for the 12 monkey subjects. As can_be seen from the table,
individual differences among subjects for AHR, 22-day cortisol, and
l8-month peak cortisol scores were strongly intercoErelated, while
activity scores were significantly correlated with ~HR and 18-month
peak cortisol scores, and the l8-month basal cortisol scores failed
to correlate significantly with any of the other measure. Thus, sub-
jects that displayed high levels of cortisol at 22 days of age when
they were moved out of incubators showed the greatest KHR scores
during subsequent conditioning sessions, and they also displayed the
highest cortisol levels 1 1/2 years later immediately following an
"activity test" but not immediately before. These findings suggest
that the tendency to exhibit extreme autonomic reactions to mildly
stressful events is highly stable throughout long periods of develop-
ment but may well be masked in the absence of environmental stress-
ors.
RELATIONSHIPS BETWEEN AUTONOMIC AND BEHAVIORAL INDICES OF FEARFULNESS

AND ANXIETY IN YOUNG MONKEYS
The same 12 monkeys that provided the physiological data summa-

rized in Table 1 were also observed and their behaviors recorded on
an almost daily basis throughout their first 18 months of life.
(These observations have continued to the present). For most of the
time between initial group formation (immediately after the condi-
tioning trials) and 18-month activity tests those monkeys lived
undisturbed within their respective peer groups. However, three
times during this period-at approximately 3, 6, and 9 months of age -
each subject was removed from its group and housed for a 7-day period
in an individual cage in another room in the laboratory. An enormous
body of pervious research has demonstrated that such group separa-
tions are almost certainly stressful for virtually all rhesus monkey
infants in this age range (e.g., Mineka and Suomi, 1978).
During every separation each of the 12 subjects was observed for

a total of eight 5-minute periods and its behaviors recorded accord-
ing to an exhaustive category scoring system (Sackett, 1978). For
every category, duration scores were summed over the 7-day separation
period for each subject. Category duration scores gleaned from the
7-day periods immediately preceding each separation (while subjects
were still in their respective social groups) were summed in like
fashion for each of the 12 subjects in order to provide presumably
nonstressful preseparation baseline date with which the separation
reactions could be compared for each subject. Baseline and separation
scores for each of the physiological measures and the activity mea-
Table 2. Preseparation Group Behaviors: Correlations With Other

Measures
Category Cort- HR- CortBs CortPk Act-

22d 28d -18 mo - 18mo 18 mo
Self-directed
disturbance 3 mo. .30 .65* -.19 .24 .07
6 mo. .46 .41 .25 -.15 .01
9 mo. -.61* .13 -.04 .04 -.17
Vocalization 3 mo. .32 -.12 .12 -.37 -.23

6 mo. -.16 .09 -.43 -.17 -.16
9 mo. .54* -.18 .27 -.39 -.19
Locomotion 3 mo. -.21 -.39 .38 -.49 -.12

6 mo. -.35 -.32 .37 -.65* -.05
9 mo. .48 -.61* .12 -.36 .15
Passive 3 mo. .03 .19 .23 .14 -.01

6 mo. .27 -.17 .61* -.28 -.15
9 mo. .49 .15 .08 .09 -.31
Exploration 3 mo. .34 .08 .31 .17 -.44

6 mo. -.06 .07 .08 .17 -.27
9 mo. .27 -.37 -.37 .11 -.31
Social contact 3 mo. -.07 .09 -.37 .37 -.40

6 mo. .13 .37 -.48 .48 -.36
9 mo. -.44 .05 .09 .59* -.69**
Social play 3 mo. .75** .07 .19 -.44 .29

6 mo. -.03 -.02 .35 -.79** .38
9 mo. .08 -.35 .07 -.03 .29
*.£. < .05
**.£. < .01
sure previously described for these subjects. Correlations between

the physiological measures and behavior scores during each of the
three separation periods are presented in Table 3.
Inspection of Table 2 reveals relatively few significant corre-

lations between any of the physiological measures (22-day cortisol,
28-day ~HR, 18-month baseline cortisol, and 18-month peak cortisol)
and 3-, 6-, or 9-month preseparation baseline behavioral levels. Of
the total 105 correlational values presented in Table 2, only 10 were
statistically significant at the p < .05 level, and these were essen-
tially randomly distributed across the various measures and times of
measurement.
86 S. J. SUOMI
In contrast, inspection of Table 3 reveals numerous significant

correlations between behavior category scores during separation
periods and some physiological measures. Moreover, there appears to
be a highly systematic pattern in terms of the significant correla-
tions, especially with respect to self-disturbance behavior, perhaps
the most valid behavioral index of fearfulness/anxiety/stress of all
the categories listed. As can be seen in Table 3, subjects' levels
of self-disturbance behavior during each of the three separation
periods (at 3, 6, and 9 months of age, respectively) were signifi-
cantly correlated with cortisol levels at 22 days of age, ~HR scores
at 28 days of age, and 2-hour peak cortisol levels at 18 months of
age; these correlations were all positive and accounted for as much
as 90% of all intersubject variance for the self-disturbance scores.
However, self-disturbance scores during separation were not signifi-
cantly correlated with 18-month baseline cortisol values~r these
subjects. Additionally, vocalization scores during each of the
separations were significantly negatively correlated with the 28-day
~HR measure, although they were not significantly correlated (posi-
tively or negatively) with any other physiological measures. Locomo-
tion scores during the last two separation periods were negatively
correlated with 22-day cortisol values. The few remaining signifi-
cant correlations between separation behaviors and the various physi-
ological measures were essentially randomly scattered over Table 3.
Taken as a whole, these results suggest that: (1) Different

measures of autonomic reactivity appear to correlate with each other
when subjects are exposed to stressful situations, but not under
baseline conditions. (2) Individual differences on these measures
appear to be quite stable during development, such that monkeys who
display extreme reactions early in life are also likely to display
extreme reactions as juveniles. (3) Young monkeys that display
extreme autonomic reactions to mild stressors also are prone to dis-
play extreme behavioral reactions involving fearfulness, anxiety,
wariness, and withdrawal when placed in stressful situations. (4)
Individual differences in these behavioral reactions to stress also
appear to be stable over time and across repeated experiences with
stressful events. (5) Finally, these individual differences in
expressions of fearful and anxious behavior are masked under stable
social-environmental conditions, such that monkeys at high risk for
extreme physiological and behavioral reactions to stress appear to be
totally "normal" in the absence of stress.
CONCLUSIONS AND IMPLICATIONS
In this chapter the species normative pattern of social develop-

ment for rhesus monkeys was outlined and some important sources of
individual differences in such development were described. Generally
speaking, monkey infants whose mothers are highly restrictive, puni-
tive, or rejecting are more likely to be retarded in various aspects
Table 3. Separation Behaviors: Correlations With Other Measures
Category Cort- CortBs CortPk Act-

22s HR-28d -18 mo -18 mo 18 mo
Self-directed
disturbance 3 mo. .67** .91*** -.24 .54* -.24
6 mo. .63* .70** .03 .55* -.35
9 mo. .54* .59* -.33 .58* -.50*
Vocalization 3 mo. -.01 -.53* -.18 .03 .48

6 mo. .33 -.56* .34 -.19 -.04
9 mo. .42 -.57* .11 -.35 .18
Locomotion 3 mo. -.15 .09 .01 .04 -.12

6 mo. -.76** .29 .37 -.16 .53*
9 mo. -.51* .67 -.13 -.01 .23
Passive 3 mo. .23 -.11 -.16 .55* .29

6 mo. -.21 -.12 -.32 .12 .11
9 mo. .28 -.64* .05 .16 .14
Exploration 3 mo. -.44 .01 .39 -.58* -.16

6 mo. .28 .47 .43 .35 -.37
9 mo. .16 .60* -.09 .17 -.24
*E. < .05

**E. < .01
***E. < .001
of social development than are infants raised by confident and com-

petent mothers. Young monkeys that grow up in sterile, unstable, or
chronically stressful social environments are more likely to display
developmental difficulties than are monkeys that grow up in social
environments which are stable, supportive, and stimulating. Finally,
early temperament differences between infants in fearfulness or
anxiety can have important developmental consequences because such
differences appear to be quite stable throughout ontogeny.
Although each of these factors appears to be important in its

own right for rhesus monkey social development, none operates in a
vacuum. Not all infants having competent mothers grow up in benign
and stable social environments, while not all infants with highly
restrictive mothers grow up in socially unstable environments.
Similarly, infants born with fearful or anxious temperaments will
most likely be at a developmental disadvantage, relative to infants
lacking such reactivity, if brought up by punitive mothers and/or in
88 S. J. SUOMI
unstable social environments. However, they may have no problems if

they are reared by competent and sensitive mothers in stable, sup-
portive social environments. Clearly, maternal, environmental, and
temperament factors are not totally independent, but rather are in-
teractive in their effects on rhesus monkey social development. In
some cases these factors might cancel out each other's relative
influence, while in other cases their combined influence might be
additive or synergistic in nature. In most cases the interactions
are likely to be complex.
Thus, analysis of the basis for ontogenic differences between

any two rhesus monkeys is clearly a difficult task. Nevertheless, it
is not necessarily an impossible one. Numerous previous investiga-
tions have demonstrated that it is possible to observe and describe
the nature and quality of maternal care an infant receives, and it is
possible to characterize the social environment in which it grows up,
especially in terms of the number and severity of stressors that
serve to alter the individual's particular course of social develop-
ment (Hinde, 1974). Additionally, it now appears possible to assess
a newborn's relative fearfulness and anxiety in terms of both physio-
logical and behavioral measures and it appears that such assessments
may well provide accurate predictions of relative responsiveness to
stress throughout much of development.
This last assessment capability has some interesting implicat-

ions tor future studies of primate social development. If an inves-
tigator can indeed determine a newborn's relative sensitivity to
stressful stimulation and is also able to predict the infant's sensi-
tivity to such stimulation in the future, then prospective experi-
ments with infants who differ in such stress sensitivity can be
carried out under conditions in which they type of ~terna1 care and
the nature of the social rearing environment are systematically ma-
nipulated. The outcome ot such experiments should enable the inves-
tigator to determine precisely how these various factors interact in
their contribution to ontogenic differences among young monkeys.
Actually, experimentation of this sort is currently underway at
Wisconsin.
Another implication of the relative stability of stress reac-

tivity throughout development for rhesus monkeys lies in possible
retrospective analysis and interpretation of an older monkey's previ-
ous social development. Suppose an investigator has knowledge of a
juvenile, an adolescent, or even an adult's social rearing environ-
ment and is able to characterize the type of maternal care the indi-
vidual received as an infant. Also suppose the investigator lacks
any temperament data for the individual, but is able to run the sub-
ject through the 2-hour activity test described on page 8. Under
these conditions the investigator could readily use the results of
the activity test (or comparable assessment tool) to reconstruct the
invididual's previous social history, especially in terms of its
probable responses to prior stressful experience. Such reconstruc-

tion might prove to be of considerable value in efforts to diagnose
and understand various developmental deficiencies or disorders and in
subsequent attempts to devise effective therapeutic procedures or
preventive strategies.
Finally, the results of the rhesus monkey studies described in

this paper carry some interesting implications for considerations of
human social development. The very same factors emphasized in the
above analyses of rhesus monkey social ontogeny - the quality of
maternal care, the nature of social rearing environments, and temper-
ament differences between infants - have long ben viewed as important
factors in human social development by numerous theorists (Thomas et
al., 1968; Bowlby, 1969; Maccoby, 1980; Rutter, 1981), although con-
ceptually the emphasis has usually been on single factors rather than
on possible interactions among them (Suomi, 1981b). Indeed, if any-
thing, it seems likely that the interactions of these various factors
would be even more complex for young humans than they apparently are
for young monkeys.
Nevertheless, it can be argued that the conceptual framework for

describing and understanding individual differences outlines for
monkey ontogeny could be readily applied to analysis of individual
differences in human social development. While human infants and
children are not usually appropriate or practical subjects for con-
trolled prospective longitudinal developmental research and it takes
much longer for them to grow up than it does for monkey infants, this
does not preclude all generalization of dvelopmental phenomena bet-
ween the two primate species. If, for example, the same types of
autonomic indices of fearfulness and anxiety are stable throughout
development for. human children, as they apparently are for monkey
youngsters, they could provide valuable assessment tools for clinical
investigators dealing with problems of human social development.
Thus, the study of individual differences in monkey ontogeny

carries with it some promise of extending our conceptual and practi-
cal knowledge of social development in human children. The degree to
which this promise is realized will ultimately depend not only on the
nature and outcome of future primate studies, but also on the degree
to which they are accepted and utilized by those researchers, educa-
tors, and clinicians who deal directly with the children themselves.
ACKNOWLEDGEMENTS
Some of the research described in this chapter was supported by

USPHS Grants No. MH-11894 and MH-28485 from the National Institute of
Mental Health and by Grant No. BNS77-06802 from the National Science
Foundation. Special thanks are in order to Helen A. LeRoy for her
editorial assistance and to Barbara Harlow for final preparation of
the manuscript.
90 S. J. SUOMI
REFERENCES
Alexander, B. K., and Harlow, H. F., 1965, Social behavior of

juvenile rhesus monkeys subjected to different rearing
conditions during the first 6 months of life, Zool.Jb.
Physiol., 71:489.
Arling, G. L., and Harlow, H. F., 1967, Effects of social deprivation
on maternal behavior of rhesus monkeys, J.omp.physiol.
Psychol., 64:371.
Baysinger, C. M., Suomi, S. J., Cronin, C., and Ohman, L. E., 1978,
Infant rhesus monkey heart rate changes predict behavioral
levels later in life, Abst.Amer.soc.Primatol., 1:2.
Berman, C. M., 1978, The analysis of mother-infant interaction in
groups: Possible influence of yearling siblings, in "Recent
advances in primatology, Vo. 1: Behavior, " D. Chivers and J.
Herbert, eds., Academic Press, London.
Berman, C. M., 1980, Early agonistic experience and rank acquisition
among free-ranging rhesus monkeys, Int.J.Primatol., 1:153.
Bischof, N., 1975, A systems approach toward the functional
connections of attachment and fear, Child Develop., 46:801.
Bowlby, J., 1969, "Attachment," Basic Books, New York.
Coe, C. L., and Levine, S., 1981, Normal responses to mother-infant
separation in nonhuman primates, in "Anxiety: New research and
changing concepts," D. F. Klein and J. G. Rabkin, eds, Raven
Press, New York.
Dienske, H., and Metz, J. A. J., 1977, Mother-infant body contact in
macaques: A time interval analysis, Bio •. Behav., 2:3.
Hansen, E. W., 1966, The development of maternal and infant behavior
in the rhesus monkey Behav., 27:107.
Harlow, H. F., 1958, The nature of love, Amer.Psychol., 13:673.
Harlow, H. F., 1969, Age-mate or peer affectional system, in "Ad-
vances in the study of behavior, Vol. 2," D. S. Lehrman, R. A.
Hinde, and E. Shaw, eds, Academic Press, New York.
Harlow, H. F., and Harlow, M. K., 1969, Effects of various mother-
infant relationships on rhesus monkey behavior, in "Determin-
ants of infant behavior. Vo. 4. B. M. Foss. ed •• Methuen.
London.
Harlow, H. F., and Lauersdorf, H. E., 1974, Sex differences in
passion and play, Perspect.Biol.Med., 17:348.
Hennessy, J. W., and Levine, S., 1979, Stress, arousal, and the
pituitary-adrenal system: A psychoendocrine hypothesis, in
"Progress in psychobiology and physiological psychology," J.
M. Srague and A. N. Epstein, eds., Academic Press, New York.
Hinde, R. A. 1974, "Biological basis of social behavior, Academic
Press, New York.
Hinde, R. A., and Simpson, M. J. A., 1975, Qualities of mother-infant
relationships in monkeys, in "The parent-infant relationship
Ciba Foundation Symposium 33 (new series), "Elsevier,
Amsterdam.
Hinde, R. A., and Spencer-Booth, Y., 1967, The behavior of socially
living rhesus monkeys in their first two and a half years
Anim.Behav., 15:169.
James, W., 1891, "The principles of psychology, Vol. 2," Holt, New
York.
Lindburg, D. G., 1973, The rhesus monkey in North India: An ecolog-
ical and behavioral study, in "Primate behavior, Vol. 2," L.
A. Rosenblum, ed., Academic Press, New York.
Maccoby, E. E. 1980, "Social development: Psychological growth and
the parent-child relationship," Harcourt, Brace, Jovanovich,
New York.
Mason, J. W., 1968, Organization of psychoendocrine mechanisms,
Psychosom.Medic. 30:2.
Mineka, S., and Suomi, S. J., 1978, Social separation in monkeys,
Psychol.Bull. 85:1376.
Missakian, E. A., 1972, Genealogical and cross-genealogical dominance
relations in a group of free-ranging rhesus monkeys (Macaca
mulatta) on Cayo Santiago, Primates, 13:169.
Natelson, B. J., Krasnegor, N., and Holaday, J. W., 1976, Relations
between behavioral arousal and plasma cortisol levels in
monkeys performing repeated free-operant avoidance sessions,
J.Comp.Physiol.Psychol., 90:598.
Parke, R. D., and Suomi, S. J., 1981, Adult male-infant relation-
ships: human and nonhuman primate evidence, in Behavioral de-
velopment," K. lmmelmann, G. W. Barlow, L. Petrinovich, and M.
Main, eds, Cambridge University Press, New York.
Rosenblum, L. A., 1971, The ontogeny of vertebrate behavior,"
Moltz, ed., Academic Press, New York.
Ruppenthal, G. C., Harlow, M. K., Eisele, C. D., Harlow, H. F., and
Suomi, S. J., 1974, Social development of infant monkeys
reared in a nuclear family environment, Child Develop., 45:
670.
Rutter, M., 1981, Stress, coping, and development: Some issues and
some questions, J. Child Psychol.Psychiat., 22:323.
Sackett, G. P., 1978, "Observing behavior, Vo. 2," University Park
Press Baltimore.
Sade, D. S., 1967, Determinants of dominance in a group of free-
ranging rhesus monkeys, in "Social communication among -
primates," S. Altmann, ed., University of Chicago Press,
Chicago.
Scallet, A. C., 1981, Adrenocortical, B-endorphin, and behavioral
responses to controlled stressful conditions: A comparative
approach in rhesus monkeys and rats. Unpublished doctoral
dissertation, University of Sisconsin-Madison.
Smith, P. K., 1981, Does play matter? Functional and evolutionary
aspects of animal and human play, Behav.Brain Sciences, in
press.
Snowdon, C. T., and Suomi, S. J., 1981 (in press), Paternal behavior
in primates, in "Child nurturance, Vo. 3, "H. E. Fitzgerald,
J. A. Mullins, and P. Gage, eds., Pleum Press, New York.
Spence, K. W., 1964, Anxiety (drive) level and performance in eyelid
conditioning, Psychol.Bull., 61:129.
Spencer-Booth, Y., 1968, The behavior of group companions toward
rhesus monkey infants, Anim.Behav., 16:541.
92 S. J. SUOMI
Sroufe, L. A., and Waters, E., 1977, Attachment as an organizational

construct, Child Develop. 48:1184.
Suomi, S. J., 1977, Development of attachment and other social
behaviors in rhesus monkeys, in "Advances in the study of
communication and affect, Vo1. 3: Attachment behavior," T.
Alloway, P. Pliner, and L. Krames, eds., Plenum Press, New
York.
Suomi, S. J., 1979a, Peers, play, and primary prevention in primates,
in "Primary prevention of psychopathology, Vo1.3 Social compe-
tence in children," M. Kent and J. Rolf, eds., University
Press of New England, hanover, N. H.
Suomi, S. J., 1979b, Differential development of various social
relationships by rhesus monkey infants, in "The child and its
family," M. Lewis and L. A. Rosenblum, eds., Plenum Press, New
York.
Suomi, S. J., 1981a, (in press), Sibling relationships in nonhuman
primates, in "Sibling relationships," M. E. Lamb and B.Sutton-
-Smith, eds., Erlbaum, Hillsdale, N. J.
Suomi, S. J., 1981b (in press), Genetic, maternal, and environmental
influences on social development in rhesus monkeys, in
"Primate behavior and sociobiology," A. B. Chiarelli and R. S.
Corruccini, eds., Springer-Verlag, Heidelberg.
Suomi, S. J., and Harlow, H. F., 1976, The facts and functions of
fear, in "Emotion and anxiety," M. Zuckerman and C. D.
Spielberger, eds., Erlbaum, Hillsdale, N.J.
Suomi, S. J., and Harlow, H. F., 1978, Early experience and social
development in rhesus monkeys, in "Socio-personality develop-
ment," M. E. Lamb, ed., Wiley, New York.
Suomi, S. J., Kraemer, G. W., Baysinger, C. M., and DeLizio, R. D.,
1981, Inherited and experimential factors associated with
individual differences in anxious behavior displayed by rhesus
monkeys, in "Anxiety: New research and changing concepts," D.
F. Klein and J. Rabkin, eds., Raven Press, New York.
Symonds, D., 1978, "Play and aggression: A study of rhesus monkeys,"
Columbia University Press, New York.
Taylor, H., Teas, J., Richie, T., Southwick, C., and Shrestha, R.,
1978, Social interactions between adult male and infant rhesus
monkeys in Nepal, Primates, 19:343.
Thomas, A., Chess, S., and Birch, H., 1968, "Temperament and behavior
disorders in children," New York University Press, New York.
White, L. E., and Hinde, R. A., 1975, Some factors affecting
mother-infant relations in rhesus monkeys, Anim.Behav., 23:
527.
AND WHAT OF FETAL AUDITION?
Marie-Claire Busnel and Carolyn Granier-Deferre
Laboratoire de Physiologie Acoustique

Institut National de la Recherche Agronomique
78350 Jouy-en-Josas, France
INTRODUCTION
The question of whether the fetus (or even for certain sensory
modes, newborn) sees, hears, tastes and feels, has been under dis-
cussion for many years, but only recently has actual experimentation
on the subject been carried out.
Even though we will be concerned with audition in this chapter,

it should not be forgotten that the fetus, as well as the newborn,
has already well-organized neurophysiological mechanisms and that no
sensory function can be either studied or considered without some
reference to the others, for there might be mutual enhancement, or,
on the contrary, exclusion of one sense by the others.
It is in birds that prenatal acoustical learning has first been

demonstrated. Studies in relation to the respective role of geneti-
cally programmed species specific song learning and of, in ovo,
imprinting, have been extensively performed with success. The value
of such prenatal learning in later behavioral fitness of young birds
to specie recognition has also been shown.
Yet these most fascinating results have not triggered similar

research on human fetus. This apparent lack of earlier interest on
the subject, might be due to methodological difficulties, or to the
fact that while early recognition of species specific signals (be it
visual or acoustic) has an obvious survival value of birds, no such
utility was recognized, at the time, for humans. Babies are born
with such an immature motor system, that they depend entirely on the
mother's willingness to care for them, and therefore do not, like
fowls, need to learn to follow her.
93
94 M.-C. BUSNEL AND C. GRANIER-DEFERRE
It is however now recognized that the newborn does need to be

emotionally secure within a known environment (be it acoustic,
tactil, olfactory or visual). The notion of early attachment
(Kennell, 1974; Klaus et al., 1972) generated, in the sixties and
there after, a new interest on early competence of the newborn, and
even of the fetus.
Even though, the link between such research on fetal and newborn
sensory development and a better knowledge of infant needs, is not
usually expressed, it undoubtedly underlies many research projects.
Such results will be of help in resolving a number of questions
concerning early perceptive and cognitive processes.
INTRAUTERINE ACOUSTIC ENVIRONMENT
Many years ago, the sea was considered as a "World of Silence"

(Cousteau). In the same way, the possibility that there might be
noises in the aqueous environment of the fetus was not a question
until recently. Many women realized that during the last months of
pregnancy their fetus was agitated and reacted by kicking when she
attended concerts where sound intensity was particularly high, but
this fact did not attract research until the nineteen thirties.
Not only is the fetus subjected to sounds coming from the out-
side, as we will see below, but there is also a noisy environment due
to the mother and to itself. Such sounds as heart beat, blood flow,
intestinal gurgling and the swish due to its own movements in the
amniotic fluid are constantly present. This has been measured, for
instance, by Walker, Grimwade and Wood (1971); Murooka et al. (1976).
Sound intensity inside the uterus, for a mother living in a

domestic environment, has been described as averaging at 90 dB SPL
and even reaching 95 dB (after the R wave component (E.C.G.) of
maternal heart beat, Walker et al., 1971). But we have always won-
dered at such high values. That the fetus lives in a constant noisy
environment is unquestionable, but an intensity of around 90 dB would
be deafening and damaging.
Recently, Querleu et al., 1981, with more precise techniques

(using octave band analysis) measured this intrauterine intensity
during labor and did indeed find 86 dBA, but only from 7 to 32 Hz.
At 65 Hz intensity level is already down to 60 dB and oscillates
between 55 to 60 dB from 125 to 1,000 Hz (Fig. 1).* The highest
noise level is in the very low frequencies where human auditory
sensitivity is almost non existent. Thus, while the fetus does
* At 50 dB and below, it is difficult to separate real noise in the

uterus from electrical ground noise of equipment.
AND WHAT OF FETAL AUDITION? 95
dB
90
80 mProbably ground noise

of equipment
70
60
150
Fig. 1. Redrawn from Querleu (1981).

Intrauterine noise level from 25 to 20,000 Hz (Octave band
analysis).
dB
90
2 0 200 2 000 Hz
Fig. 2. Busnel (unpublished).

Gliding frequency spectrum measured:
a) in air
b) in air with microphone covered by two condoms
filled with physiological saline.
c) intravaginally, same as b.
inhabit a noisy environment, it is not extreme in the audible range.
We personally think that, as this noise is always present for the
fetus, it becomes like the sound of waves for those living on the sea
shore, part of the environment which is missed when it stops but goes
unnoticed while it lasts. Although not proven, let us use this as an
hypothesis.
One of us (Busnel, 1979) and Querleu (1981) have recorded what

part of outside sounds can be perceived inside the body. Unfortu-
nately, none of these experiments are without technical drawbacks.
Busnel introduced an intravaginal microphone (in a bag filled with a
saline solution) rather than intrauterine, and Querley, like most
previous authors, made his recordings after rupture of the amniotic
sac. Neither of these conditions can be considered ideal. But they
do coincide with Armitage, Baldwin and Wince's (1980) recording in
the sheep, where the microphone was introduced in the full amniotic
sac of a pregnant ewe, as well as Busnel's (unpublished results) in
the same animal.
Fig. 2 shows the intravaginally measured attenuation of a glid-

ing frequency spectrum emitted at 90 dBL, 50cm from the abdominal
wall. It can be seen that the higher the frequency, the higher the
attenuation by the human body: up to 250 Hz attenuation is minor and
increases to 30dB at 2,000 Hz; beyond this, it is very high. But
even more interesting is Fig. 3 where it can be observed that the
maternal voice, which we will discuss later, recorded via an intra-
uterine microphone, emerges well above background noise level at low
frequencies (between 250 and 800 Hz).
Fig. 4 shows a sonagram of the word "Bonjour", previously re-

corded and emitted through a loud speaker 50cm above the abdomen:
(A): the microphone was placed just above the abdomen
(B): same arrangement with the microphone located intravaginally
(C): microphone in same position, subject vocalizes the word.
While the fundamental frequencies remain in all three sonagrams, most
harmonics in B, and all of them in C have disappeared. However, the
word stays intelligible in both cases.
Our intravaginal recordings of musical and verbal sounds, at

different intensities, show that, at 90 dBA or more, most words are
intelligible, at 80 dBA only those containing plosives can be under-
stood. Below this value, only the sentence's rhythm and particular
personal intonation are detectable. From time to time, a word stands
out and can be recognized, as we will see in the section on speech;
music is always quite audible if emitted above 75 dBA.
What signals the fetus ear can pick up brings us to the dis-
cussion of his prenatal acoustical capability. But if and when he
becomes capable of hearing, it is now sure that the sound of his
mother's voice, the sound of music and most loud noises from the
outside environment are present in the uterus to be heard.
dB
o Intrauterine noise
II EmerqinQ maternal voice
60
50
40
Fig. 3. Redrawn from Querleu (1981).

Octave band analysis of emerging maternal voice measured
in utero.
A B c
kHz
3
2
IC .,-'~I···~.;'It1Vll'l.rrn
.•- I' _1I.Ia.& II ., 1n
01234560123456 o "2
1 3 4 5 6-5-
Fig. 4. Busnel (unpublished).

Sonagram of the word "Bonjour":
A. played back and recorded above abdomen.
B. played back above abdomen and recorded intravaginally.
c. spoken by subject and recorded intravaginally.
HOW EARLY CAN A HUMAN FETUS HEAR?
Anatomical Development*
This aspect will not be developed here since it has recently

been reviewed by Ruben and Rapin (1980), Rubel (1978) and Pujol (1976
to 1980). But a few points which are pertinent in view of the other
parts of this article will be briefly stated, e.g. the fact that all
the elementary layers of embryonic tissues (ectoplasmic, mesoplasmic
and endoplasmic) are involved in the auditory system's formation.
This means that audition is ontogenetically related with many other
organs of the body. Whether this early common origin will involve
later functional relationships with those organs, as suggested for
instance by Tomatis (1978), does not appear to have been investigated
or even considered. We will therefore let it stand as a question.
External, middle and inner ears differ as much in the chronology

of their development as they do in their embryonic origin. Inner
ears' main structures are in place at 3 months gestational age
(Streeter, 1917), at 4 months cochlear receptors seem ready to func-
tion, at 6 months all of the inner ear are present, though not yet
completely developed (Nakai, 1970). Although the external and middle
ears will only mature at 7 months,** audition and subcortical inte-
gration of acoustical signals seem possible at 6 months, since the
different auditory relays appear to be ready to function at that time
(Bast and Anson, 1949; Vasiliu, 1969; Dayal et al., 1973).
Anatomical gross development is not a sufficient index of a

system's working capabilities; synaptic activity and bioelectric
functioning must also be demonstrated. In all mammals studied, there
is always a delay between anatomical maturation and the appearance of
the first functional sign of audition as measured by electrical
potentials. For instance, in the cat, where audition starts at
* Many authors do not state precisely whether they are writing about
postconceptional age, measured at supposed conception time or, as
obstetricians do, from the last menstrual period. There might
therefore be, at times a 2 weeks discrepancy in fetal age
notations.
** It has often been argued that the presence of embryonic mesenchyme

and other mucus in the fetal middle ear brought about a tympanic
rigidity and a reduction of ossicle movements, therefore a much
attenuated auditory competence. This is still often accepted even
though Keith (1975) and McLellan (1964) showed that neither were
true. Electroencephalograms and electrocardiograms in utero on
animals (sheep and guinea pigs) confirm that the fetus responds to
acoustical stimulations despite tissue and liquid in the auditory
canal.
birth, cochlear microphonic potentials which measure the functional

development of cochlear hair cells, appear two days before birth.
Then, 3 to 4 days later action potentials can be recorded, and after
24 hours, the evoked auditory potentials. These delays correspond
principally to the myelinization of nerve fibers, the formation of a
sufficient number of synapses and the onset of enzymatic activities.
In a recent study on the cat, Ehret and Romand (1981) show that onset
of cochlear function (measured by microphonic and nerve potential)
and audition (behavioral tests) confirm each other. This seems to be
true of most mammals. In human fetuses precise electrophysiologic
studies at 4 or 5 months gestational age and the evaluation of local-
ized enzymatic activity are unthinkable on the fetus, therefore
animal studies like that of Ehret and Romand are of great help.
Electrophysiological investigations in most mammals indicate that the
more immature the auditory system, the more limited its cochlear
tonal sensitivity (especially for the higher frequencies) and its
coding capacities. Conversely in this immature system, latency,
threshold, refractory period and fatiguability are greater. Also, in
the beginning, only intermediate frequencies are heard; then, the
range of the spectrum extends at both ends of the scale, starting
with the low frequencies, so that, at onset, audition is different in
its range from what it will be later.
Fetal Reactions In Utero (with References to Premature's Reactions)
We have seen that the fetus has anatomical competence to hear

between 4 and 5 months, and that noises of maternal and environmental
origin are present in the uterus. We will now investigate the first
signs of objective behavioral and physiological reactions to sound.
Frequent references will be made to prematures, although fetuses are
really our concern; for, on one hand, more extended work has been
done on the premature than on the fetus, on the other hand, despite
probable differences, the premature will help us understand the
ambiguity of some fetal reactions.
There are two main reponses detectable in utero: changes in

heart rate and movements, the latter being more difficult to quan-
tify, as measuring techniques in utero are still fairly primitive.*
Except during labor auditory evoked potentials are not reliably
recordable in the fetus. In 8 months prematures and full-term babies
they are relatively similar (Parmelee, 1975) but there are differ-
ences in motor and behavioral reactions.
* Ultrasonic scanning, of course, now allows very fine detections,

from eye blinks (Birnholz, 1981) to breathing motions (Wilds,
1978), and fetal movements (Adamson et al., 1980). But to measure
fetal reactions to a specific stimulus it is necessary to perform
numerous tests, on each fetus, and such techniques are still
difficult to use in a routine testing procedure.
When compared at 41 weeks, with full-term newborns, prematures
are more easily aroused, but also more rapidly unresponsive. Due to
possible respiratory problems, among others, and to extrauterine
feeding, prematures exhibit muscular tension which the fetus probably
lacks and which might mask motor reactions (Saint-Anne Dargassies,
1966, 1974); Parmelee and Schulte, 1969). Prematures having spent a
few weeks free to move have a wider and more varied motor repertoire,
but efforts are of shorter duration. Therefore, the study of fetal
stages should bring more useful information than that of prematures
since they have normally no functional problems. However, when
comparisons are made, it is probably more legitimate to compare
premature and fetal stages rather than premature and newborns or the
latter with fetuses.
Preyer (1885) considered that it was evident that fetuses could

not respond to sound, but later some scientists revising this view
demonstrated that reactions existed: Peiper (1925), Forbes and Forbes
(1927), Ray (1932), Sontag and Wallace (1935) and Spelt (1938-1948).
All these authors stimulated 8 months old fetuses, and therefore give
no insight into precocious audition, except Sontag and Wallace (1935-
1936) who started at 5 months but with a stimulus (120 Hz) directly
applied to the abdomen, at these low frequencies, responses could be
primarily somesthetic rather than auditory.
It is only in the 1960's and 1970's that acoustical techniques

became dependable. It would be too long to present the details of
all these studies, since experimental conditions are very diversified
(see table 1). However, various general conclusions can be drawn:
1. Cardiac responses of the fetus can be acoustically elicited

independently of maternal cardiac changes.
2. Most authors take seven months as a reliable starting point for
fetal reactions.
3. Cardiac reactions to sound are often accompanied by Limb move-
ments or change in position. Grimwade et al. (1971) found 83%
motor reaction in 38 to 42 weeks fetuses.
4. In most cases, the response is a heart rate acceleration averag-
ing 15 beats/min* with a short latency of no more than 5 sec.
But as we shall see now, both on the fetus and premature, the
picture is far from being as simple as it appears in this short
resume. Cardiac responses to sound are very intricate and depend
both on age and physiological state, as well as on state of arousal
of infants, physical characteristics of stimuli, and their relevance
to the subject.
* It is known that normal Fetal Heart Rate (F.H.R.) has an insta-

bility of 5-25 beats/min due to vagel tonus oscillations; changes
in F.H.R. must always be compared with lengthy control period, as
modifications due to noise are of the same order of magnitude.
We have seen that most authors found no objective responses to

sound in the fetus before seven months, although, anatomically, the
auditory system appears sufficiently mature to be functional by the
age of four months. Prematures are known to respond to sound at 28
weeks (6 months) (Aube des Sens, Titran, 1981) which seems an ade-
quate age for first response since it corresponds to full establish-
ment of nerve supply to the cochlea. Tanaka and Arayama (1969) did
test two 6 months old fetuses finding no response. On the contrary,
Wedenberg (1965) showed a reaction at 5~ months (3 kHz - 110 dB).
Lack of experimental data, both in young fetuses and prematures

(which are generally not viable before 6 months) and most of the
above parameters can explain this long lasting ambiguity, about the
exact date of onset of human audition which oscillates between 4 and
6 gestational months.
Let us remember, however, that all maturing sensory systems are

limited in their ability to treat information. The fetal ear is not
a microphone and what is picks up and integrates must be different
according to state of maturation. Besides, even if the fetal audi-
tory system were sensitive to acoustic stimulations at 4 or 5 months,
the fetus would also be limited in its ability to respond. By 6
months, a maturational step is reached, complex nervous connections
have become functional between the various subcortical structures
implicated in auditory signal integration, thus peripheral reactions
to sound start to be measurable.
Studying these responses to sound, one of the most difficult

criterium is, of course, to determine the alertness of the subject.
Considering the number of intermediate states between sleeping and
waking (Curzi-Dascalova et al., 1981; Dreyfus-Brissac, 1981), and the
difficulty of deciding in which stage of sleep an infant is, very
systematic research is needed to take all of the possible influences
into account. In the fetus, the determination of wakefulness being
even more difficult.
It turns out that, in most past experiments using acoustic

stimulations, insufficient attention was put on this factor. We will
see that state of arousal can explain most contradictory results
observed in the fetus, in particular, those concerning the type of
cardiac responses obtained. Indeed, authors studying F.H.R. re-
sponses to sound also observe cases of deceleration (for example,
Grimwade et al. found 6% of them), others find decelerations followed
by accelerations or the reverse (see table 1). One of the most
interesting points here might arise from an understanding of the
difference between the accelerative and decelerative cardiac re-
actions.
Until a few years ago, it was thought that, in the first few
months after birth, responses to simple stimuli changed from accel-
o
N
Table 1. Fetal Heart Rate (F.H.R.) Changes and Movements After an Acoustic Stimulation, in the Human
Fetus. (Studies published between 1955 and 1981).
Authors Fetuses tested Cardiac resEonse

Acoustic Motor
(years of N age Nature Mean Variation Latency
stimuli reaction
publication) range of F. H. R. (bpm)
FLEISCHER, K. 79 6-9 pure tones: Present

(1955 ) months 500 Hz 75% only
- 1000 Hz Not studied Not studied negli- if stimu-
- warn horn gible lus abrupt
115 phones quick habi-
(20-30cm of the tuation
abdominal wall) :s::
I
0
MURPHY, K. P. 290 30-40 15" pure F.H.R. accelera- '" 16 at 500 Hz negli- unspec.
t:l:I
SMYTH, C.N. weeks tones: tion observed in '" 11 at 4000 Hz gible c
(I)
500 Hz 235 fetuses. 60 z
t>1
- 4000 Hz subjects reacted t-<
100 dB (at to the 4000 Hz g;
the abdominal tone and 215 to CI
wall) the 500 Hz. 0
(0)
DWORNI CKA, B. 32 38-42 5" pure F.H.R. accelera- '" 7 at 1000 Hz negli- unspec.
JASIENSKA, A. weeks tones: tion in most '" 11 at 2000 Hz gible ~
H
SMOLARZ, W. - 1000 Hz cases, but 2 t>1
WAWRYK, R. - 2000 Hz fetuses reacted Mean duration: ::0
I
100 dB (at by deceleration. CI
(1963) '" 5-15 sec t>1
':I:j
the abdominal Quick habituation. t>1
wall)
~
JOHANSSON, B. 10 35-40 I" pure F.H.R. accelera- unspecified unspec. present S;
t:j
WEDENBERG, E. weeks tone: tion.
WESTIN, B. - 3000 Hz
(1964) 110 dB ~
(measured 0
I'1j
in utero) I'1j
t:r:J
1-3
WEDENBERG, E. un- 22 and I" pure F.H.R. accelera- unspecified unspec. unspec. ~
(1965) spec. 26 tone: tion at 26 weeks
weeks - 3000 Hz No response at ~
t:j
110 dB 22 weeks H
1-3
(measured H
in utero) ~
."
BENCH, R.J. 12 34-37 2,5,10 F.H.R. accelera- unspecified 5 sec. present
MITTLER, P.J. weeks and IS" tion, no response
SMYTH, C.N. pure observed with a
VASS, A. tones: 60 dB level.
(1967-1970) - 3000 Hz Habituation of
- 4000 Hz response has
60 dB been observed
- 500 Hz after stimulus
105 and repetition.
60 dB (at the
abdominal wall)
TANAKA, Y. 134 6-9 5" pure F.H.R. accelera- :::: 20-30 negli- either in
ARAYAMA, T. months tones: tion in 124 gible terruption
(1969) 500 Hz fetuses (nothing or enhance-
( 2 at 6 months) - 1000 Hz before 7 months): ment.
( 9 at 7 " ) - 2000 Hz 100% + at 500 Hz Nothing
( 23 at 8 " ) 90 dB (at 97% + at 1000 Hz before 7
(100 at 9 " ) the abdominal 86% + at 2000 Hz months. 0
w
wall) •
Table 1. (continued) 0
.po
Authors Fetuses tested Cardiac resEonse

Acoustic Motor
stimuli reaction
SONTAG, L.W. 17 37-42 a 10" musical Very small F.H.R. '" 4-5* neg li- present
(1969-1972) weeks sequence pre- decelerations gible but non-
fered by the followed by a gradu- signifi-
mother. ally increasing cant.
65-110 dB acceleration with a
peak after 2'.
GRIMWADE, J.C. 14 38-42 20" pure F.H.R. accelera- 5 sec. 83% of

WALKER, D.W. weeks tones between tion: 94% '" 27 F.H.R.
BARTLETT, M. 500 et (mean duration: accelera- 3:
GORDON, S. 1000 Hz 3.4 min) tion are I
WOOD, C. 80 dB F.H.R. deceleration: ac- (")
(1971) (measured 6% '" 17 companied t:J;:I

in utero) by move- c::::
en
ments. ~
t""
CALVET, J. unspec. 40-42 2" pure F.H.R. accelera- unspec. 5 sec. present ~
COLL, J. weeks tones: tion. t::I
LAREDO, C. - 1500 Hz (")
CAMILlERI, L. - 2000 Hz CO')

(1972) 100 dB (at the
abdominal wall) ~
1-1
t:r:I
~
GOODLIN, R.C. 50 35-42 5" pure F.H.R. accelera- '" 8* unspec. unspec. I
t::I
SCHMIDT, B.S. weeks tone: tion or decelera- t:r:I
"'.1
(1972) - 2000Hz tion. With re- t:r:I
120 dB (at peated stimuli, ~
the abdominal an initial deceler- ~
t;;
wall) ation could change
to acceleration.
~
BENCH, R.J. 14 37-42 2" 1/3 oc- F.H.R. accelera- 2,5 - 8" for unspec. 0
'z:I
MENTZ, D.L. weeks tave noise tion followed by the ac-
'z:I
(1975) band centered deceleration. celeration t:j
...,
at 400 Hz or phase
2000 Hz - 19" for ~
100 dB the de- ~
t;;
(measured celeration H
...,
in utero) phase. H
0
--------,-~------ ,----'---------,-,---,---~-------------
READ, J.A. during** 5" pure F.H.R. accelera-

.Z..,
39 '" 15 unspec. present
MILLER, F.C. labor tone: tion in 27
(1977) - 2000 Hz fetuses.
105,115 and
120 dB (at the
abdominal wall)
GOUPIL, F.l 69 33-42 low frequencies ......•.••.... Not studied ....•.•.• 70% positive
LEGRAND, H. (121 weeks 10" duration Habituation
BREART, G. tests) l' apart studied. Great
LE HOUZEC, R. 10 to 20 stimuli variability
SUREAU, C. on fetal head
(1975)
lSismographie et reactivite foetales. 5emes Journees Nationales de Medicine Perinatale.
O. DUBOIS et R. RENAUD, eds, Arnette, Paris, 1976.
o
V'1
Table 1. (continued) o
0'
Authors Fetuses tested Cardiac response

Acoustic Motor
stimuli reaction
PEREIRA LUZ, N. 151 during** 5 pulses of .F.H.R. accelera- :::: 10* negli- present in
PEREIRA LIMA, C. labor 2" pure tone tion: 98% (.initial gible 84% of the
HECKER LUZ, C. (1" interval): (mean duration= increase = fetuses:
LUCIA FELDENS, V. - 1500 Hz 224" 21) mild or
(1980) 125 dB (at .Very rare F.H.R. (.maximal intense,
the abdominal deceleration increase the latter
wall) beginning before 29) followed
acceleration by an in-
crease in
fetal
activity :.::
I
(')
QUERLEU, D. 27 23-40 5" noises: .F.H.R. accelera- :::: 15 negli- present t:J:j
RENARD, x. weeks - white noise tion gible or c::::
til
CREPIN, G. - narrow band duration: 15 to a few sec. Z
tz:!
(1981) noise 30 sec. I:"'
centered at: .Long term varia- S;
1000, 1500, bility of more t::I
2000, 3000 Hz than 5 bpm (')
100-110 dBA .White noise is G")

(at the most effective
abdominal and response ~
H
wall) inconstant before tz:!
::d
28 weeks.
~
In cases of clinical research, only reactions of healthy fetuses are reported. In all studies, ;]
except * mothers wore earphones to mask fetal stimulation.
All studies reported here were carried prior to unset of labor except ** as examples.
~
eration to deceleration. (See for instance: Hutt et al., 1968; Graham

and Jackson, 1970; Hatton et al., 1970; Berg et al., 1971; Calvet et
al., 1972). It seemed that there was a curvilinear relationship
between acceleration response and age, e.g. a slowly rising (75 dB -
1,000 Hz) stimulus, elicited no significant response in awake new-
borns; a high deceleration (more than 10 bpm) in awake 4 months old
and the same reaction but of only 1.73 bpm in awake adults (Hatton et
al., 1970). But H.R. acceleration after a brief decelerative phase
was shown to occur mostly during sleeping epochs and deceleration
during waking states. Considering what has lately been found it
might well be that most "age effect" was an artefact of state of
alertness. For instance, Nelson et al., 1976* showed on newborns
that H.R. acceleration or deceleration to sound was highly correlated
to the amount of time the infants stayed awake after the stimulus.
Decelerations were found if the infant (n = 51) stayed awake for more
than 5 min after the stimulus, while drowsy or sleeping infants
responded by H.R. accelerations.
It is highly probable that these observations could be general-

ized to the premature or the fetus depending on state of health and
physiological maturation. The question of age is still open, for the
first stages, since authors like Neal (1979) in prematures, observed
in response to the same stimuli, decelerations at 31 weeks (few tests
only) and accelerations followed by decelerations from 32 to 36
weeks. In 1970, Schulman was a precursor showing that, at 30 weeks,
H.R. response was mostly acceleration, but that at 36 weeks, deceler-
ations were associated with awake epochs and accelerations with
sleeping ones.
In addition to age and state of alertness, another explanation

for discrepancy in observed cardiac responses might be that, as
suggested by Bench and Mentz, 1975, if the fetus, like older babies,
reacts to short tones with an acceleration followed by a deceler-
ation, then either authors have not persued observations long enough
to see the decelerative phase or, as we will see now, it might also
be a consequence of the type of stimulation used. Among others, Berg
et al. (1971) found that, in fact, responses depend both on state of
alertness and on physical characteristics of stimulus. Intensity,
spectrum rise time of stimuli and duration have been shown to change
the reaction (not speaking of the meaningfulness of the stimuli which
will be developed below).
* Nelson, M.N., Clifton, R.K., Down, J.M., Appleton, T., and Little,
A., 1976, Heart rate and sucking responses to tones in neonates:
New state controls suggest a possible explanation for previous
failures to obtain orienting responses. Psychophysiol. 13(4):
161-162.
As known in the young infant,* artificial stimuli, such as pure

tones and white noises, tend to elicite mostly H.R. accelerations,
while more complex stimuli as pulsed tones or speech signals induce
deceleration (authors say: "at the same intensity," but this is
meaningless when comparing a continuous or a pulsed tone. Effective-
ness on a subject being due to differences in the temporal character-
istics of stimuli rather than to their comparative intensity. Such
differential reactions have been found by Graham et al. (1978) on an
anencephalic infant (brain weighing 39g instead of 350 in normal
newborns). At age 3 and 6 weeks, H.R. modifications where character-
istics of a much higher stage of maturation (like those of older
children and adults): e.g. white noise produced cardiac acceleration
while synthetic speech and pulsed tones elicited cardiac slowing,
with a form and latency which resembled that of older awake normal
infants; behavioral signs of orientation was also observed.
In young infants, correlations between H.R. modifications due to

sound and behavioral states have lead many authors to interprete H.R.
acceleration as a "defensive" response to a sudden or intense
stimuli, H.R. deceleration, on the contrary, is considered as a sign
of attention, the latter is often referred to as "cardiac orienting
response".
While interaction between cardiac slowing and alertness is high,

it cannot be generalized since, as we will see in the next chapter,
decelerations have been obtained during sleeping epochs with speech
stimuli; H.R. acceleration, on the other hand, can be elicited inde-
pendently of state of arousal.
To confuse the problem a little more, it seems that acceler-

ations are closely related in infants to motor actions (others than
orienting behaviors which are accompanied by decelerations) (Nelson
et al., 1976). This is also the case in the fetus. For example,
Timor-Tritsch et al. (1976, 1978) have shown that normal fetal move-
ments, occurring without any known stimulation, are accompanied by
F.H.R. accelerations in 99.8% of those lasting more than 3 sec:
- F.H.R. accelerations followed by deceleration occur at or near the
onset of 67% of fetal movements (F.M.)
- an acceleration, without subsequent deceleration, we observed in
31,5% of F .M.
* Considering-the variations of H.R. changes in reaction to sound, a

whole battery of tests must be used as controls. Up to 1976 an
excellent review on postnatal reactions can be found in Eisenberg.
The different parameters used by authors are of two kinds: 1)
Physiological: E.E.G., E.C.G., electromyography, electro-
oculography, skin resistance. 2) Behavioral: conditioning,
differential reinforcement, habituation, orienting response,
sucking.
- a deceleration, without acceleration, was noted to occur only with

F.M. of less than one second duration.
Since we saw above that most sound stimulations induce a motor

reaction, in the 28 or 42 weeks fetuses studied, it could be that
F.H.R. acceleration to sound are only a correlate of the fetal motor
reaction to the stimulus.
But is this the whole story? Bench and Mentz (1975) explaining
the cardiac decelerations obtained in 37 to 42 weeks fetuses, theor-
ize that newborns may be subjected to temporary inhibitions of a
number of nervous functions. Graham et ale (1978) conclude in the
same manner that, since lower brain structures are functionally
sufficient for differential responses according to stimulus charac-
teristics, cortical immaturity produces descending inhibitory effects
on subcortical activities. Although this hypothesis is enticing, it
would warrant further research as, it now appears evident that no
definite agreement can be attained until fetal reactions to sound are
correlated with type of stimulus, age of the fetus (and health con-
dition*), arousal state and the possible effect of fetal movements.
Insisting on type of stimulation is reinforced by a recent

animal study in kittens which points out the significant relevancy of
species specific signals or acoustic stimuli which have common fea-
tures with them. Olmstead and Cillablanca (1980), in a most remark-
able research, have shown that cats' natural vocalization triggers
electrophysiological responses, different from those of stimuli, such
as a hand clap, a 2 kHz tone, shaking keys and so on, kittens start
responding to these and to natural sounds around 5 or 6 days after
birth. But the mature form of reaction is present between 5.5 to 7.5
days for natural sounds and only from 14.5 and 21 days for artificial
* It is interesting to note that most infants show, in the presence

of specific acoustic signals, specific motor reactions, which can
be quantified (Neonatal Neurobehavioral Assessment Scale).
However, prematures and low birth weight full-term babies have
different scores than normal weight ones (Kurtzberg et al., 1979),
suggesting a reduced auditory response or general responsiveness.
Some, on the other hand, show a hypersensitivity. Reise (1980)
observed that all those who presented hypersensitivity to a bell
were born at term, while all those who were hypersensitive to a
rattle noise were born prematurely. Although this still is but a
remark it should be kept in mind that, if systematic differences in
types of reactions to different signal characteristics can be
discerned between normal, low weight full-term newborns and
prematures, it might be of help in understanding both acoustic
reaction mechanism and the general neurophysiological state of
prematures, the latter being a great help for diagnostic purposes.
ones (all emitted around 70-75 dB). While it is easier to correlate

in the kitten ear canal opening, electrophysiological and behavioral
data, this type of research must be done in human both in premature
and prenatal stages for it is important, to the comprehension of
central mechanism developments, to experiment on reception of "mean-
ingful" species specific stimuli, linguistic or other to which the
developing organism has been exposed.
IS PRENATAL LEARNING POSSIBLE?
Although this problem has been the object of numerous dis-

cussions and theoretical speculations for years, no reliable exper-
imental data can be found in the literature. Ray (1932), Spelt
(1948) and Feijoo's (1975-1981) seem to be the only published studies
showing on humans a postnatal retention of a prenatal stimulus.
However, experimental data acquired on premature's and neonate's
reactivity to sound stimulations offer indirect evidences which
suggest that simple prenatal learning might be possible.
a) Habituation is the most simple learning process which has

been mentioned in the fetus. A progressive unresponsiveness, or a
modification of the nature of a cardiac response to repetitive acous-
tic stimuli has been described (Bench and Mittler, 1967; Smyth and
Bench, 1967; Goodlin and Schmidt, 1972) in fetuses older than 34
weeks.
These few observations would not be sufficient to trigger atten-

tion if they were not supported by animal experimentations, the most
interesting, in our opinion, being that of Vince (1979). She stimu-
lated female guinea pigs every day, during the two weeks of pregnancy
which followed auditory maturation of the embryo, with a feeding call
of Game bantam hens. This call has a consistent effect on guinea
pigs: startle, flight and/or freezing and a slowing of the H.R. With
repetition, these reactions disappear. Two hours after birth, the
newborn guinea pigs were tested with the hen call they had heard
prenatally. The stimulus which is mildly aversive to unstimulated
controls appeared to have lost most of its effectiveness. This
indicates an intrauterine habituation to a specific sound, for, when
both groups (prenatally and postnatally exposed) were tested with a
guinea pig call, the temporal modifications of heart beat rates were
analogous.
Considering the paucity of data on human fetus, it is difficult

to determine whether observed habituations are attributable to a
progressive disappearance of a defense or orientation reaction or to
the early fatiguability of the immature acoustic receptor. It is one
of the goals of our present research, to answer this question.
AND WHAT OF FETAL AUDITION? III
More interesting than habituation are trials to demonstrate b)

associative learning capacities in the human fetus.
The earliest conditioning experiments (Ray, 1932; Spelt, 1948),

though controversial, described classical conditioning, with extinc-
tion and reappearance of the conditioned response (a motor reaction)
in utero, in fetuses 8 and 9 months old. The conditioned stimulus
was vibrational, the unconditioned one was a loud noise. The fetus
"remembered" the association for at least 3 weeks.
It is now important to seek if such a fetal conditioning is

indeed possible using true auditory stimuli.
Feijoo (1975-1981) made a preliminary attempt in these direc-

tions by testing fetuses down to 6 months. He has associated a state
of great relaxation of the mother (sophronisation), with a twelve
seconds musical stimulus.* This stimulus was given three times
during each relaxation session which occurred twice a week during
four weeks, either during the 6th, 7th or 8th conceptional month.
(Unfortunately, only 23 women were tested up to now). Feijoo's
hypothesis is that the relaxation of the maternal abdominal muscles,
a supposedly pleasant experience for the fetus, would be associated
later on with the sound.
Tests were then performed either at 30 to 37 weeks in utero or

after birth. Due to the mother's lying position, fetal movements
occurred at every session with a latency of 6 to 10 min but, on
hearing the stimuli, reaction occurred between 7 and 49 sec (mean: 18
sec). Less than 6 min after birth, the newborns were stimulated with
the same musical sample, for the same duration: only those stimu-
lated from 22-36 weeks reacted. It was shown on 14 infants that,
those crying before stimulation (9) stopped crying, those that had
closed eyes (9) opened them, and most having clonic movements (10)
relaxed immediately after hearing the musical stimulus. None of
these effects were observed when subjected to other musical samples
or to the same one played backwards. The reaction is therefore
specific, and this "memory" seems to remain for a few months.
Referring once more to research on prematures, it is worth while

describing Tuber et al. most interesting study (1980): they tested a
2 months prematurely born female hydranencephalic twin and her normal
brother (approx. 32 weeks gestational age) with the "stimulus expect-
ancy procedure." The hydranencephalic female had virtually no cer-
ebral hemispheres, grossly abnormal basal ganglia and dorsal thalami.
* The stimulus was mostly composed of frequencies below 2,000 Hz.

When filtered to pass only frequencies above 3,500 Hz, no results
were obtained.
The infants' learning capability was evaluated by testing the

development of a conditioned association between two stimuli, one
visual, the other acoustic: 162 paired acoustic and visual stimuli
were given over a period of 4 sessions at 40 to 62 days after birth.
When the conditioned association is acquired, omission of the second
stimulus brings about measurable changes in H.B. rate and eventually
an orienting response, which are interpreted as an expectancy re-
action. Both the hydranencephalic and normal twin reacted thus with
a notably long latency cardiac acceleration which did not occur in
either twin when both stimuli were presented together. This is all
the more noticeable that the acoustic stimulus alone, before pairing,
produced a negligible effect on the normal infant and a deceleratory
one in the hydranencephalic.
This experiment demonstrates an association process independent

of the cerebral hemispheres. Therefore, subcortical networks, as
known in animals, seem capable of mediating complex behavioral pro-
cesses in the young infant.
c) Postnatal effects of intrauterine noise. Even without direct

experimentations, simple observations of newborn reactions to stimu-
lations by recorded uterine sound environment, should give useful
informations about this early learning process. The stimuli used
have been: heart beat alone or associated with recorded intrauterine
sounds and human voices.
Murooka et al. (1976) showed that intrauterine noise (80 phones)

given during the first 15 days of life (100 newborns) stopped, 86% of
those babies who cried, in 20 to 28 sec. Light sleep was induced in
30% of the 40 babies tested, with a mean latency of 46 sec, while
controls took 132 sec. R.E.M. sleep occurred in 16 min in those
babies given the recorded intrauterine sound and in 26 min in con-
trols. Six other noises, at the same intensity, did not give similar
results except the pulsed doppler ultrasonic signal of the femoral
artery* and pulsed low frequency noise (320 to 350 Hz). These two
sounds have common features with the intrauterine noises: low fre-
quencies and rhythmicity.
Another well known experiment, in this field, is of course that

of Salk (1960-1973) who showed that a heart beat stimulation, in the
nursery, soothes the newborns. This work has been followed - by that
of Roberts and Campbell (1967) with similar results Tullock et al.
(1964), Takemoto (1964) and Brackbill (1973) who found this stimulus
either ineffective or no more effective than any other long duration
sound.
* It is not the ultrasonic component of the signal which is reacted

to, but the low frequency output of the apparatus.
Few experiments have raised so many controversies, probably due

to the ethical implications of finding a postnatal effect of prenatal
stimuli. Salk (1960, 1962) showed that there was a 40g weight gain
during the first 4 days in 70% of newborns exposed to a heart beat
sound given day and night in the nursery (72 paired beats/min at 85
dB). Only 30% of the controls grained any weight at all (mean =
minus 20g). Stimulated babies cried 38.6% of the time, while the
controls did so for 60% of the time. As quantity of ingested food
was identical in both groups it can be inferred that weight gain was
acquired through less crying and more sleep. An accelerated heart
beat (128/min), on the contrary, produced enhanced crying and less
sleeping time.
Salk's results on sleep induction are similar, percentage-wise,

to those of Murooka (1976) who finds, that babies hearing the heart
beat sound fall asleep in half the time needed by those hearing no
sounds or lullabies. These sleep tests were done on 16 to 37 months
infants. This is worth noting, although such results should still be
confirmed, since Feijoo (1981) also suggested a lasting "memory" of
sounds heard during pregnancy.
Considering these behavioral effects of the prenatal acoustic

environment, it was natural to think of stimulating premature babies
too. Schmidt et al. (1980) induced modifications in the length of
the different sleeping phases, by emitting heart beat sound (80 dB).
They also analyzed H.B. influence according to the premature's state
of alertness. For instance, while preterms have a first sleep epoch
nearly twice as long as that of the full-term, it was reduced with
the H.B. sounds to nearly normal length (around 17 - 19 min).
The temptation was, of course, irresistible to use such exper-

imentally observed effects to pacify babies and put them to sleep.
Records and tapes of intrauterine sounds are sold in many countries
and parents seem to find them very effective and use them exten-
sively. The psychological effect of reexposing a newborn to its
intrauterine acoustic environment has not. to our knowledge, been
studied. It would, however. be worth while to do so before this
method becomes too popular. Indeed, while it is most probably ben-
eficial for pre term babies to be given a prenatal sound environment
during a transitional period, for full-term babies the question
remains open. It has been considered as "reassuring," but it could
also be argued that, bringing a newborn constantly back to its
uterine environment, is deterrent to its psychological development
or/and to his natural capacities for falling asleep.
Of all sounds reaching the uterus, those of speech are uniquely

human. We have seen (Fig 4) that some of the acoustical character-
istics of words and the prosody of sentences can be heard in utero.
Can the Fetus be "Sensitized" to them?
Malloy (1975) stimulated 180 to 230 days old infants (6 to 7~

months), in their incubators, either with their mother's or to
another feminine voice. Stimuli were given 6 times a day for 5 min.
Differences in developmental scales were investigated. These could
be expected if the newborn, hearing components of its prenatal
environment, was thus made to feel more secure and as a consequence
better able to cope with outside aggressions. But no significant
results were found except a certain weight gain during the first few
days. (It is by now accepted that the mother's presence in premature
wards is beneficial to the baby's growth and general health con-
ditions, but it is probably not due to the maternal voice alone, but
to her smell and touch as well).
IS LEARNING OF SOME ACOUSTICAL FEATURES OF HUMAN LANGUAGE POSSIBLE

IN UTERO?
Number of authors have worked on the hypothesis that prepro-

gramed specific detectors for language existed in human beings. It
is theorized that either, only those detectors being validated by the
linguistic environment will become functional or that these per-
ceptive capacities will be tuned in according to the specificities
of this environment. It can be compared to the process of refinement
of sensory acuity already observed in birds. It might also be that
these detectors are simply part of more general acoustic detectors.
Whatever, the issue of this actual debate, very early phonetic and
prosodic discriminations have been demonstrated in the infant thus,
these processes of validation, specification and adjustment are very
precocious. How early is the question? And does it apply to the
fetus?
Since we have shown that outside noises, of a sufficient level

are perfectly audible and provoke reactions from the fetus, the voice
of the mother and of other humans, speaking around her, which are
also a normal component of fetal acoustic environment, could be
learned, at least in some of their prosodic and phonetic structures.
No data have been published on such a possible fetal sensitiz-

ation to human speech. In birds, on the other hand, it has been
known for many years that chicks, in the egg, near hatching, are
imprinted by the voice of their species. Gottlieb et al. (1971,
1978) prevented isolated duck embryos from hearing in ovo (even their
own vocalizations through embryonic devocalization) and showed that
it takes them, after hatching, 24 h to discriminate the maternal call
of their species while normally, chicks can do it right at birth.
In the last few years, a number of papers have shown that chicks even
differentiate their own mother's calls from those of another hen
(Guyomarc'h, 1974; Gottlieb et al., 1966-1981). If given a choice
AND WHAT OF FETAL AUDITION? lIS
between the call of an ur.~:nown hen and either their own mother's call
or a hen call heard while still in ovo, they choose one of the two
latter, but not the unheard one.
It is without doubt a prenatal learning process, which organizes

perceptive preferences of the young bird. If devocalized ducks are
given a choice, right after hatching, between a hen call and a
mallard call, they do not show any preference, while they do it,
before being isolated and muted, they are given as little as 24 h to
hear their own vocalization.
Gottieb considers that prenatal experience constitutes the "fine

tuning" of perceptual preferences. What part of species specific and
individual recognition is due to this fine tuning through prenatal
learning and what part is due to genetic programming remains to be
shown in most animal species.
In humans as we have seen above, voices of outside speakers are

quite audible and some are understandable (Querleu's recording), but
it is not certain, since the amniotic sac was broken, that trans-
mission was similar to ordinary conditions. On the other hand, in
Busnel's experiments, although all precautions were taken against
direct transmission, the abdomen's distention and therefore the
quantity of tissue between the outside world and the microphone was
not similar to that of a women between 5 and 9 months of pregnancy.
The real level of attenuation will probably be found to lie in be-
tween those of Querleu and Busnel. For Busnel, language intelligi-
bility of a recorded spoken text (90 dBA at 50cm from the abdomen)
is poor, although words can be understood here and there and the
general prosody of sentences recognized. On the other hand, when
words are pronounced individually, many are understood. Those con-
taining fricative consonants [F, V, e, y, S, Z] less successfully
than vowels.
However, it is rare for anyone to talk at a 90 dB level. At 40

- 50 dB, the intensity ot the normally spoken voice, attenuation is
much greater and only the general prosodic characteristics of speech
may be recognized. A loud voice, on the other hand, is much better
received since its intensity is sufficient to be perceived inside
{e.g. as films or TV speakers, singers, etc.) so singing mothers
should be better perceived by the fetus than simple talking mothers.
Some traditional, so called "primitive" cultures, knew this better
than us since it is said among the Gaboneses: "a man should never get
angry at his wife while she is pregnant or say vulgar words, for this
raised voice turns seven times in her vagina and reaches the child to
be, thus feeding him bad concepts" (L'Aude des Sens, Maziere, 1981).
The mother's own voice travels both through the body and, as
someone else's, through aerial channels. Fig. 3 shows that the
maternal voice emerges by 12,5 dB from background noise at 200 Hz,
which corresponds to the fundamental frequency of human voice. It

is distorted as it travels through the body mass to reach the uterus.
Fig. 4C shows, by intravaginal recording of words spoken by the
subject, that all but the fundamental frequency have disappeared.
Therefore, the maternal voice in utero sounds very different from
what the baby will hear after birth although specificities of each
voice, either in rhythm, intonation or speed of delivery, can be
recognized; and one of the problems we presently study is how the
newborn adapts to this difference.
The reactions of newborns to speech stimuli are the only data

available on this hypothesis. We will now review evidence of a
possible prenatal "learning."
Condon and Sander (1974) have shown that infants, 12 hours to 2

days old, have limb movements which synchronize with parts of speech.
These results were obtained through film analysis. For instance, the
baby's arm and leg movements terminated at the same time as each
phonetic structures of the sentence. This publication has raised
much controversy, not solved as yet, and we will not take position
until new data is brought forth.
With a different approach, Eisenberg et al. (1974, 1976) ana-

lyzing the responses of newborns to speech structures, observed
different heart rate changes upon hearing a vowel than when exposed
to other noises. On hearing vowels, the newborn's cardiac response
decelerates and he presents a behavioral orientation. These deceler-
ations can be observed even during sleep. This can be remarked for
all other cases of decelerations in newborns have always been ob-
tained during alert states only. The structure of the electro-
encephalographic response, occurring as early as 12 h after birth,
is also different to verbal stimuli than to pure tones or other non
significant sounds. These seem to be definite specific reactions to
verbal stimuli.
The tend is now towards behavioral rather than physiological

measures of reactions.
Thus, with the non nutritive sucking technique, Mehler et al.

(1976, 1978, 1979), Bertoncini et al. (1980, 1981) (now working with
one or two day old babies and prematures) found, as Mills and
Melhuish (1974) that 3 weeks old infants were capable of discrimi-
nating their mother's voice. As of now, one of Mehler's conclusions
is that this infant's capacity is based primarily on rhythms and
intonation contours of sentences. When she reads a text from right
to left, or up and down (therefore with an abnormal prosody), the
baby does not distinguish her voice from another feminine one. This
could strengthen an intrauterine learning hypothesis, since rhythm
and intonation are particularly recognizable features in the intra-
uterine recordings (Busnel, 1979; Querleu et al., 1981).
Recently, De Casper and Fifer (1980) demonstrated that newborns,

younger than three days of age, but having spent no more than 12
hours with their mother, recognize her voice from another feminine
one: they will work more to earn the production of the former than
the latter. This study has, to our knowledge, dealt with the
earliest stage after birth. In the future, work on babies of anes-
thetized mothers and tested after birth, before being reunited to
them, should be the best population for demonstrating an eventual
prenatal learning.
The most fascinating studies of Eimas (1971), and Eimas et al.

(1974, 1975) deal with infants at least one month old; their analysis
of phonetic discriminations at this early age are most interesting
and served as models for many research on this subject, and we hope
it will also be of help for more precocious observations. Let us
mention the work of Streeter (1976). Although two months old babies
were tested, what was shown has, we believe, a bearing on the very
early determination of some language pattern recognition. She inves-
tigated the discriminative capacities of infants reared in a non
english environment and compared Eimas' results with those of infants
born of Bantu parents, and speaking Kikuyu. These infants, at two
months, were able to make the same discrimination as american ones
exposed to the voiced/voiceless contrast in their own linguistic
environment. But they were also capable of discriminating a pre-
voiced [b], in which the voicing precedes the stop release burst by
-30 ms, from a voiced [b] in which these two components are simul-
taneous. American infants, who are not in contact in their linguis-
tic environment with prevoiced labial stops, are not capable of
recognizing them (except if the voiced onset time is up to -70 ms).
Thus, the voiced/voiceless contrast is recognizable in both cultures,
which suggests a genetic origin of this capacity, but the prevo iced/
voiced contrast, not found universally, seems to stem from a very
early learning or adjustment process on the part of the Bantu chil-
dren.
This cross cultural study of reactions to phonetic categories

are most interesting and should be expanded and completed with new-
borns. We personally think that two chronologically different pro-
cesses might be involved. First a process of refinement in the
perceptive acuity of acoustic speech features at the auditory level.
Second, at central levels, and after a certain maturation has been
attained, prococious learning might take place.
Since many of the phonetic or syllabic categories differentiated

by the newborn depend for a good part on voice onset time, and since
this is the most affected factor by transmission to the uterus, it is
probable that the early process of speech recognition do not involve
words but certain physical characteristics of the voice which are
recognizable in utero, such as most vowels, the general prosody of
speech and the person's specific acoustical "signature."
lIB M.-C. BUSNEL AND C. GRANIER-DEFERRE
CONCLUSIVE REMARKS
This chapter began with the question: can the fetus hear in the
uterus? It ends by asking: does he discriminate some phonetic
features? The gap between these two questions indicates both the
amount of knowledge acquired in the last 20 to 25 years and the
amount still to acquire.
There is a danger that after having considered the fetus as a

mere larva (and the baby as a simple digestive tube) one now tries to
prove that at 6 months gestational age he knows it all! Preliminary
questions such as the nature of the intrauterine acoustical environ-
ment (remembering that background noise, although of a high level,
is not in the frequencies of its sensitive auditory areal), and what
kind of sound stimuli can elicite responses from 7 to 9 months old
fetuses, have been answered, but most are still under discussion
like: when does human auditory system become functional? Or, in
correlation with the maturation of C.N.S. structures involved, what
can the fetal ear actually pick up and integrate? To what degree
does its acoustic surroundings affect its developing perceptive
habilities?* What is the range of its responding and learning
capacities?
In human, the role of prenatal learning and genetic programming

is very difficult to determine. Therefore, most of the research have
to be conducted on animals which can be isolated, as it has been
described on hand raised birds whose perceptive environment can be
fully controlled.
As the anatomical structures mature, sensory perceptions do to,

and the fetus receives stimulations of all sorts. These represent a
preview of what he will, after birth, discover, with a greater inten-
sity and with sharper transitions. In utero, he does react to
acoustic stimulations as well as tactile, gustatory (given a sweet
injection in the amniotic fluid the sheeps' embryo will swallow more
often) and perhaps, to a lesser extent visual. Researchers have a
tendency to stimulate only one sensory channel, oblivious of the
others. Yet in this period of maturation, we can hypothesize that
stimulation of one sense could suppress input into the others or, on
the contrary, that it might so awaken the general responsiveness of
the fetus, that all sensory systems would benefit from a generalized
alterness.
An analogy to this can be inferred from young children who,

having suffered from cerebral anoxia or slight brain damage, are in
* For lack of space, we have not dealt with the question of

plasticity of the acoustic system subjected to very early sound
stimulation. This would need a chapter to itself.
need of reeducation; there is often an extinction of imperfectly

acquired sensory functions. In such cases, the process of reedu-
cation of one sense or motor behavior may obliterate whatever knowl-
edge there was of the others. For instance, while relearning the
difficult process of walking, the child becomes deaf and dumb, only
to have his hearing improve as soon as he recovers walking processes,
and his speech, as soon as he has recuperated audition. While the
study of the fetus as a "feeling being" must be accomplished, it is,
therefore, important to approach each sense separately, then, to
integrate all of them and to see how they interact.
Thus, after more or less twenty years of research and obser-

vations on the influence of acoustic stimuli on fetuses and infants,
and despite many interesting results, all of which have an intrinsic
value, it still is difficult to have a clear view, so numerous are
the involved parameters.
Since we have seen that verbal stimuli are reacted to in a

different manner than non verbal ones, it seems that future research
should be oriented towards:
1. Showing that fetus and preterm infant's reactions to neutral

and meaningful stimuli such as species specific signals (vocaliz-
ation) are different, in nature or in intensity, from non-species
specific signals, according to the level of maturity of the respond-
ing organism.
2, Proving an after-birth retention of prenatal auditory stimuli

and its temporal range (with special attention to vocal ones); corre-
lating the complete range of physical, physiological and chronologi-
cal characteristics should bring worth-while results. This kind of
research, on the effect of different types of fetal stimuli and their
possible memorization, is the present orientation of our group. As
well as determining the usefulness, as a diagnostic tool, of certain
acoustic stimulations in determining fetal state of health indepen-
dently of state of arousal.
The main conclusions of the review seem to be that sensory

physiology alone will not be able to give the final answer. We think
that ethological data will be able to sort out the complexity of
present data, and bring the means for reuniting apparent ambiguity
through a comprehension of the fetus as a complex entity in inter-
action with its environment.
These types of studies should be undertaken in the future, for,

if pregnancy is to be considered as a period during which the embryo
"learns" about its future perceptive environment, or attitude towards
the gestational period should be quite different. Only recently has
it become apparent that mother-infant communication is not unilat-
eral, but that the baby responds, and even triggers communicative
bouts, if and when the mother recognizes the signs of demand (facial
mimicry, eye contact, movements and so on). But one must be aware of
their existence to perceive them. And what does the fetus do? He
reacts, every mother knows it, by kicking and/or, moving about to
unpleasant, or simply, to strong stimulations. If future mothers
were to pay attention to these reactions, and change the acoustic
environment when the baby kicks, instead of simply remarking on it,
we think that the same type of relationships that establishes itself
between mother and infant by mutual attention (after birth) could
also occur between fetuses and mothers-to-be.
REFERENCES
Adamson, G. D., Cousin, A. J., and Gare, D. J., 1980, Rythmic fetal
movements, Am.J.Obstet.Gynecol., 136(2):239-242.
Ando, Y. and Hattori, H., 1970, Effects of intense noise during fetal
life upon postnatal adaptability, J.Am.Soc.Ac., 47:1128-1130.
Ando, Y. and Hattori, H., 1977, Effects of noise on sleep of babies,
J.Acoust.Soc.Am., 62(1):199-204.
Armitage, S. E., Baldwin, B. A. and Vince, M. A., 1980, The fetal
sound environment of sheep, Science, 208:1173-1174.
Bast, T. H. and Anson, B. J., 1949, The temporal bone and the ear,
Springfield, Ill., Thomas, ed.
Bench, R. J., 1968, Sound transmission to the human fetus through the
maternal abdominal wall, J.Gen.Psychol., 113:85-87.
Bench, R. J., Mittler, P. J. and Smyth, C. N., 1967, Changes of heart
rate in response to auditory stimulation in the human fetus
(abstr.), Bull.Brit.Psychol.Soc., 20, 14A.
Bench, R. J., Anderson, J. H. and Hoare, M., 1970, Measurement system
for fetal audiometry, J.Acoust.Soc.Am., 47:1602-1606.
Bench, R. J. and Vass, A., 1970, Fetal audiometry, Lancet, 1:91-92.
Bench, R. J. and Mentz, D. L., 1975, On the measurement of human
fetal auditory responses, in "Sound Reception in Mammals",
R.J. Bench, A. Pye and J.D-.-Pye, eds., Acad. Press, New York,
23-40.
Berg, K. M., Berg, W. K. and Graham, F. K., 1971, Infant heart rate
response as a function of stimuli and state, Psychophysiol.,
8(1):30-44.
Bertoncini, J. and Mehler, J., 1980, La perception du langage chez Ie
nourrisson : quelques observations, Reprod.Nutr.Develop.,
20,3B, 859-869.
Bertoncini, J. and Mehler, J., 1981, Quelques remarques a propos de
la perception chez Ie nouveau-n~, Rev. Praticien , Paris,
Foetologie, 31(5):387-396.
Birnholtz, J. C., 1981, The development of human fetal eye movement
patterns, Science, 213(4508):679-681.
Brackbill, Y., 1973, Continuous stimulation reduces arousal level:
stability of the effect over time, Child Develop., 44:43-46.
Brackbill, Y. and Fitzgerland, H. E., 1969, Development of the
sensory analysers during infancy, in "Advances in Child
Development and Behavior ll , L.P. Lipsitt and H. Reese, eds.,

Acad. Press, Inc., New York, 4:173-208.
Brown, C. J., 1979, Reaction of infants to their parents' voice,
Infant Behav.Develop., 2(4):295-300.
Busnel, M. C., 1979, Mesures intra-vaginales du niveau et des
distorsions acoustiques des bruits maternels, Electro
Diagnostic Therapie, 16(3):142.
Calvet, J., ColI, J., Laredo, Ch. and Camillieri, L., 1972, Les
r~actions auditives chez de nouveau-n~ et Ie foetus,
Folia Phoniat., 24:427-430.
Condon, W. S. and Sander, L. W., 1974, Neonate movement is
synchronized with adult speech, interactional participation
and language acquisition, Science, 183(4120):99-101.
Curzi-Dascalova, L., Monod, N., Guidasci, S. and Korn, G., 1981,
Transition veille-sommeil chez Ie nouveau-n~ et Ie nourrisson
avent l'&ge de 3 mois, Revue EEG Neurophysiol., in press.
Dayal, V. S., Farkashioy, J. and Kokshanian, A., 1973, Embryology of
the ear, Can.J.Oto-Laryngol., 2:136-142.
DeCasper, A. J. and Fifer, W. P., 1980, Of human bonding: newborns
prefer their mothers' voices, Science, 208:1175-1176.
Dreyfus-Brissac, S., 1981, Veille et sommeil au cours des premi~res
semaines de vie, in IIBiologie du D~velopmentll, A. Minkowski,
ed., Flamarion, Paris, 152-176.
Dwornicka, B., Jasienska, A., Smolarz, W. and Wawryk, R., 1964,
Attempt of determining the fetal reaction to acoustic
stimulation, Acta-Oto-Laryngol., ~7:571-574.
Ehret, G. and Romand, R., 1981, Postnatal development of absolute
auditory thresholds in kittens, J.Comp.Physiol.Psychol.,
95 (2) ,304-311.
Eimas, P. D., 1974, Infant heart rate changes to a synthetic speech
sound, J.Aud.Res., 14:21-28.
Eimas, P. D., 1975, Developmental studies in speech perception, in
IIInfant Perception ll , L.B. Cohan and P. Salapatek, eds., Acad.
Press, Inc., New York, 2:193.
Eimas, P. D., Siqueland, E. R., Jusczyk, P. and Vigorito, J., 1971,
Speech perception in infants, Science, 171:303-306.
Eisenberg, R. B., 1976, Auditory competence in early life, in liThe
roots of communicative behavior ll , University Park Press,
Baltimore.
Eisenberg, R. B., Marmarou, A. and Giovachino, P., 1974, E.E.G.
changes to a synthetic speech sound: a preliminary report,
J.Aud.Res., 14:29-43.
Eisenberg, R. B., Marmarou, A. and Giovachino, P., 1974, Infant heart
rate changes to a synthetic speech sound, J.Aud.Res.,
14:20-28
Elliot, G. B. and Elliot, K. A., 1964, Some pathological,
radiological and clinical implications of the precocious
development of the human ear. Laryngoscope, 79:1160-1171.
Feijoo, J., 1975, Ut Conscientia Noscatue, Cahier de Sophrologie,
(13): 14-20
Feijoo, J., 1981, Le Foetus Pierre et Ie Loup ••• ou une approche

originale de l'audition prenatale humaine, in "L'aube des
Sens", E. Herbinet and M.C. Busnel, eds., Stock, Paris.
Field, T., 1980, Supplemental stimulation of preterm neonates, Early
Human Develop., 3/4:301-314.
File, S. E. and Goodall, E. M., 1976, Prenatal influence on the
responsivity of neonate rats, Behav.Biol., 18:433-439.
Fleischer, K., 1955, Untersuchungen zur Entwicklung der
Innenohrfunktion (Intra-uterine Kinderbewegungen nach
Schallreizen). Z.Laryngol.Thinol., 34:733.
Forbes, H. S. and Forbes, H. B., 1927, Fetal sense reaction: hearing,
J.Comp.Physiol.Psychol., 7:353-355.
Goodlin, R. C. and Schmidt, W., 19/2, Human fetal arousal levels as
indicated by heart rate recordings, Am.J.Obstet.Gynecol.,
114 (5): 613-621.
Gottlieb, G., 1966, Species identification by avian neonates:
contributory effect of perinatal auditory stimulation,
Anim.Behav., 14:282-290.
Gottlieb, G., 1971, Ontogenesis of sensory function in birds and
mammals, in "The Biopsychology of Development", E. Tobach,
L.R. Aronson and E. Shaw, eds., Acad. Press, New York,
67-128.
Gottlieb, G., 1971, Development of species identification in birds.
An inquiry into the prenatal determinants of perception,
University of Chicago Press.
Gottlieb, G., 1978, Development of species identification in
ducklings: IV. Change in species specific perception caused
by auditory deprivation, J.Comp.Physiol.Psychol., 92:375-387.
ducklings: V. Perceptual differenciation in the embryo,
J.Comp.Physiol.Psychol., 93:831-854.
ducklings: VI. Specific embryonic experience required to
maintain species specific perception in Peking ducklings,
J.Comp.Physiol.Psychol., in press.
Graham, F. K., Leavitt, L. A., Strock, B. D. and Brown, J. W., 1978,
Precocious cardiac orienting in a human anencephalic infant,
Science, 199(4326):322-324.
Granier-Deferre, C. and Busnel, M. C., 1981, L'audition prenatale, in
"L'aube des Sens", E. Herbinet and M.C. Busnel, eds., Stock-:-
Paris.
Grimwade, J. C., Walker, D. W., Bartlett, M., Gordon, S. and Wood,
C., 1971, Human fetal heart rate change and movement in
response to sound and vibration, Am.J.Obstet.Gynecol.,
109(1):86-90.
Guyomarc'h, J. C., 1974, L'empreinte auditive prenatale chez Ie
Poussin domestique, Rev.Comp.Anim., 8:3-6.
Hatton, H. M., Berg, W. K. and Graham, F. K., 1970, Effects of
acoustic rise time on heart rate response, Psychon.Sci.,
19(2):101-103.
Hazlewood, V., 1977, The role of auditory stimuli in crying

inhibition in the neonate. J.Aud.Res •• 17:225-240.
Hutt. C•• Bernuth. H. v •• Lenard. H.• Hutt. S. J. and Prechtl. H. F.
R., 1968. Habituation in relation to state in the human
neonate, Nature, 220:618-620.
Hutt. S. J., Hutt, C., Lenard, H. G., Bernuth, H. v. and Muntjewerff.
W. J., 1968, Auditory responsivity in the human neonate.
Nature. 218:888-890.
Hutt. C., Hutt. S. J., 1970, The neonatal evoked heart rate response
and the law of initial value, Psychophysiology. 6:661-668.
Hutt. S. J., Lenard, H. G. and Prechtl. H. F. R., 1973. Influence of
"state" upon responsivity to stimulation, in "Early Human
Development", S.J. Hutt and C. Hutt, eds.,Oxford University
Press. Oxford, 150-160.
Johansson. B•• Wedenberg. E. and Westin, B., 1964, Measurement of
tone response by the human fetus. A preliminary report. Acta
Oto-Laryngol., 57:188-192.
Keith. R. W•• 1975. Middle ear function in neonates. Arch.Oto-
Laryngol., 101:376-379.
Kennell, J. K•• Jerauld. R•• Wolie. H., Chener. D•• Kreger, N••
McAlpine. W., Staffer. M. and Klaus. M. H•• 1974. Maternal
behaviour one year after early and extended postpartum
contact. Dev.Med.Child Neurol., 16:172-179.
Klaus, M. H. and Kennell, J. K•• 1970, Mothers separated from their
newborn infants, Pediatr.Clin.N.Am •• 17.1015-1037.
Klaus, M. H., Jerauld, R., Kreger, N•• McAlpine. W•• Steffa, M. and
Kennell J. K., 1972, Maternal attachment - importance of the
first postpartum days, New Engl.J.Med •• 286:460-463.
Kurtzberg, D., Vaughan, H. G., Daum, C., Grellong. B. A•• Albin. S.
and Rotkin. L.• 1979. Neurobehavioral performance of low
birth weight infants at 40 weeks conceptional age.
Comparison with normal full-term infants, Dev.Med.Child
Neurol., 21:590-607.
Leboyer, F., 1975. Pour une naissance sans violence. Le Seuil. ed ••
Paris.
Malloy. G. B•• 1975. The relationship between maternal and musical
auditory stimulation and the developmental behavior of
premature infants, Diss.Abstr.Int., 36(4):1-146.
Mehler, J., Barriere. M. and Jassik-Gerschenfeld, D., 1976, La
reconnaissance de la voix maternelle par Ie nourrisson,
La Recherche, 70:786-788.
Mehler, J., Bertoncini, J .• Barriere. M. and Jassik-Gerschenfeld. D.,
1978. Infant recognition of mother's voice. Perception,
7:491-497.
Mehler, J. and Bertoncini. J., 1979. Infant's perception of speech
and other acoustic stimuli. in "Psycholinguistics. Series II.
J. Morton and J.C. Marshall. eds .• Elek Scientific Books.
67-105.
McLellan, M. S •• Brown, J. R.• Rondeau. H., Shoughro. E., Johnson, R.
A. and Hale, A. R., 1964. Embryonal connective tissue and
exudate in ear, Am.J.Dis.Child •• 108:164-170.
Mills, M. and Melhuish, E., 1974, Recognition of mother's voice in

early infancy, Nature, 252:123-124.
Murooka, H., Koie, Y. and Suda, N., 1976, Analyse des sons
intra-uterins et leurs effets tranquillisants sur Ie
nouveau-ne, J.Gynecol.Obstet.Biol.Repr., 5:367-376.
Murphy, K. P. and Smyth, C. N., 1962, Response of fetus to auditory
stimulation, Lancet, 1:972-973.
Nakai, Y., 1970, An electron microscopic study of the human fetus
cochlea, Pract.Oto-Thino-Laryngol., 32:257-267.
Neal, M. V., 1979, Organizational behavior of the premature infant,
Birth Defects, 15(7):43-60.
Olmstead, C. E. amd Villablanca, J. R., 1980, Development of
behavioral audition in the kitten, Physiol.Behav.,
24:705-712.
Papousek, H. and Bernstein, P., 1969, The function of conditioning
stimulation in human neonate and infants, in "Stimulation in
Early Infancy", A. Ambrose, ed., Acad. Press, London,
229-252.
Parmelee, A. H., 1975, Neurophysiological and behavioral organization
of premature infants in the first month of life,
Biol.Psychol., 10(5), 501-512.
Parmelee, A. H., Schulte, F. J., Akiyama, Y., Wenner, W. H., Schultz,
H. R. and Stern, E., 1968, Maturation of E.E.G. activity
during sleep in premature infants, Electroencephalog.
Clin.Neurophysiol., 24:319-329.
Peiper, A., 1925, Sinnesempfindungen des Kindes vor seiner Geburt,
Mschr.Kinderheilk., 29:236-241.
Pereira Luz, N., Pereira Lima, C., Hecker Luz, S. and Feldens, V. L.,
1980, Auditory evoked responses of the human fetus, Acta
Obstet.Gynecol.Scand. 59:395-404.
Preyer, W., 1885, Specielle Physiologie des Embryo, Leipzig: Griebens
Verlag.
Pujol, R., 1976, Maturation du systeme auditif, Rev.Laryngol., 97,
Suppl.:551-562.
Pujol, R. and Marty, R., 1970, Postnatal maturation in the cochlear
of the cat. J.Comp.Neurol., 139:115-126.
Pujol, R. and Hilding, D. A., 1973, Anatomy and physiology of the
onset of auditory function, Acta Oto-Laryngol., 76:1-10.
Pujol, R., Carlier, E. and Lenoir, M., 1980, Ontogenetic approach to
inner and outer hair cell function, Hearing Res., 2:423-430.
Querleu, D. and Renard, X., 1981, Les perception auditives du foetus
humain, Med.Hyg., 39:2102-2110.
Querleu, D., Renard, X., Crepin. G., 1981, Bruit intra-uterin,
perception auditive et reactivite foetale aux stimulations
sonores, Gynecol.Obstet.Biol.Repr. (in press).
Ray, W. S., 1932, A preliminary study of fetal conditioning,
Child Dev., 3:173-177.
Read, J. A. and Miller, F. C., 1977, Fetal heart rate acceleration in
response to acoustic stimulation as a measure of fetal
well-being, Am.J.Obstet.Gynecol., 129(5):512-517.
Riese, M. L., 1980, Hypecsensitivity to auditory stimulation during

administration ot the neonatal neurobehavioral Assessment
Scale, Dev.Med.Child.Neurol., 22:404-405.
Roberts, B. and Campbell, D., 1967, Activity in newborns and the
sound of the human heart, Psychom.Sci., 9:339-340.
Romand, R., 1979, Development of auditory nerve activity in kittens,
Br.Res., 173:554-556.
Rubel, E. W., 1978, Ontogeny of structures and functions in the
vertebrate auditory system, in "Handbook of Sensory
Physiology", IX. Development-of sensory systems, M. Jacobson,
ed., Springer-Verlag, Berlin.
Ruben, R. J. and Rapin, I., 1980, Plasticity of the developing
auditory system, Ann.Oto-Rhino-Laryngol., 89(4):303-311.
Saint-Anne Dargassies, S., 1966, Neurological maturation of the
premature infants of 28 to 41 weeks gestational age, in
"Human Development", F. Falkner, ed., Saunders, Philadelphia,
p.306.
Saint-Anne Dargassies, S., 1974, Le developpement neurologique du
nouveau-n~ ~ terme et du pr~matur~, Masson, ed., Paris.
Salk, L., 1960, The effects ot the normal heartbeat sound on the
behavior of the newborn infant: implications for mental
health, World Mental Health, 12(4):1-8.
Salk, L., 1962, Mothers' heartbeat as an imprinting stimulus,
Trans.N.Y.Acad.Sci., 24:753-763.
Schulman, C. A., 1970, Effects of auditory stimulation on heart rate
in premature intants, Develop.Psychobiol., 2:172-183.
Schmidt, K., Rose, S. A. and Bridger, W. H., 1980, Effects of
heartbeat sound on the cardiac and behavioral responsiveness
to tactual stimulation in sleeping preterm infants, Dev.
Psychobiol., 16(3):175-184.
Smyth, C. N. and Bench, R. J., 1967, Fetal response to audiogenic
stimulation as an indication of neurological function, in
"Digest of 7th International Conference on Medical and
Biological Engineering", B. Jacobson, ed., Stockholm:
Organizing Corom. 7th Int.Conf.Roy.Acad.Eng.Sci., 137-499.
Sontag, L. W. and Wallace, R. F., 1935, The movement response of the
human fetus to sound stimuli, Child Dev., 6:253-258.
Sontag, L. W. and Wallace, R. F., 1936, Changes in the rate of the
human fetal heart in response to vibratory stimuli, Am.J.
Dis. Child, 51: 583-589. --
Sontag, L. W., Steele, W. G. and Lewis, M., 1969, The fetal and
maternal cardiac response to environmental stress, Human
Dev., 12:1-9. -----
Spelt, D. K., 1938, Conditioned responses in the human fetus in
utero, Psychol.Bull., 35:712-713.
Spelt, D. K., 1948, The conditioning of the fetus in utero, J.Exp.
Psychol., 38:338-346.
Streeter, G. L., 1917, The development of the Scala tympani, Scala
vestibuli and perioticular cystern in the human embryo,
Am.J.Anat., 21:299-320.
Streeter, L. A., 1976, Language perception of 2-months-old infants

shows effects of both innate mechanisms and experience,
Nature, 259:39-41.
Suga, N., 1978, Specialization of the auditory system for reception
and processing of species specific sounds, Fed.Proc.,
37:2342-2353.
Taketomo, Y., 1964, Sleep induction by heartbeat rhythm, Folia
Psychiatr.Neurol.Jpn., Suppl.7:347-351.
Tanaka, Y. and Arayama, T., 1969, Fetal responses to acoustic
stimuli, Pract.Oto-Thino-Laryngol., 31:269-273.
Timor-Tritsch, I. E., Dierker, L. R., Zador, I., Hertz, R. H. and
Rosen, M. G., 1978, Fetal movements associated with fetal
heart rate accelerations and decelerations, Am.J.Obstet.
Gynecol., 131(3):276-280.
Timor-Tritsch, I., Zador, I., Hertz, R. H. and Rosen, M. G., 1976,
Classification of fetal movements, Am.J.Obstet.Gynecol.,
126:70.
Tomatis, A., 1978, L'oreille et Ie langage, Le Seuil, Ed., Paris,
50-58.
Tuber, D. S., Berntson, G. G., Bachman, D. S. and Allen, N. J., 1980,
Associative learning in premature hydranencephalic and normal
twins, Science, 210:1035-1037.
Tulloch, J. D., Brown, B. S., Jacobs, H. L., Prugh, D. G. and Greene,
W. A., 1964, Normal heartbeat sound and the behavior of new-
born infants. A replication Study, Psychom.Med.Heartbeat
Behav., 26:661-669.
Vasiliu,~., 1969, Contributions to the morphological study of the
auditory apparatus, Rev.Roum.Physiol., 6:159-167.
Vince, M. A., 1979, Postnatal effects of prenatal sound stimulation
in the guinea pig, Anim.Behav., 27(3):908-918.
Walker, D. W., Grimwade, J. C. and Wood, C., 1971, Intrauterine
noise: a component of the fetal environment, Am.J.Obstet.
Gynecol., 109:91-95.
Wedenberg, E., 1965, Prenatal test of hearing, Acta Oto-Laryngol.,
Suppl.206:27-32.
Wilds, P. r., 1978, Observations of intrauterine fetal breathing
movements: a review, Am.J.Obstet.Gynecol., 131(3):315-338.
Wolff, P. H. and Ferber, R., 1979, The development of behavior in
human infants, premature and newborn, Ann.Rev.Neurosci.,
2:291-307.
L'Aube des Sens, Les Cahiers du Nouveau-ne nO 5, E. Herbinet and M.C.

Busnel, eds., Stock, Paris, 1981.
Note: Since the American scientific community is more familiar with
American publications than with European ones whenever there were
similar works done both in America and Europe, we have favoured the
European ones, thinking this procedure would be more useful.
SOME PECULIARITIES OF ELECTRICAL BRAIN ACTIVITY CORRELATED
WITH BEHAVIORAL STATES IN INFANCY: A REVIEW
Carmine Faienza
Consiglio Nazionale delle Ricerche - Rome, Italy

Program of Preventive Medicine (Project Perinatal Med.)
Child Neuropsychiatric Unit - University of Parma, Italy
The most important capacity of neural structures is to mediate

information; this capacity is a function of the precise stages of
ontogenetic development and can be investigated by recording from the
scalp the spontaneous electrical activity or the evoked electrical
responses to various sensorial stimulation.
Our proposal of limiting to the first year of life the dis-

cussion on the use of spontaneous or evoked bioelectrical brain
activity recorded from the scalp, in the study of some developmental
aspects of human behavior, should not be considered in a restrictive
sense, but rather, as a responsible attempt of considering it in
depth and in a systematic way, as one of the periods of greater
sensitivity in human life.
The only fact of emphasizing the extreme behavioral differences

shown by the pre term and full term neonate justifies our wish to
concentrate attention on this short but complex ontogenetic period.
On the other hand it is important to stress the fact that

although mammal new-born behavioral repertory is determined by the
degree of maturation reached by its C.N.S.; the more we rise in the
evolutionary scale, the greater the dependence of the new-born on the
adults of its own species, particularly the mother.
Since the human being is the most dependent on adults for its
survival such dependence, which is almost complete at the beginning
of its life, brought us to believe that its behavior should scarcely
be considered organized at birth.
127
128 C. FAIENZA
This trend of thought (now out of date) is in contrast with the

results of the most recent researches in neuropsychology of the
developmental age: it is sufficient to think of the well-structured
organization and the complexity of the neuro-behavioral patterns that
underline the capacity of breast-feeding from the very first hours of
life, and how rapidly this activity becomes specialized.
We must also emphasize the close relationship existing between

psychic and somatic development; in fact it is extensively demon-
strated that the basis of the behavior of an individual depends on
the maturation of his nervous structures (which are the fundamental
organic basis determining behavior) as well as on the normal growth
of other organs and apparatus, particularly those of the skeletal and
muscular.
It is not my duty to re-propose the dilemma whether the psychic

development is to be interpreted as a phenomenon strictly connected
to the maturation of innate processes or mechanisms, (even of a
chemophysical kind), or if it is the environment that not only moulds
such inborn processes, but even determines the acquisition of totally
new mechanisms. Anyhow, from an eclectic outlook we can pass over
the disputes between nativists and empirists and we can surely main-
tain that the neonate builds up its behavioral patterns by adapting
a genetically determined and passed on inheritance on the basis of
continuous exchanges with its environment.
Starting from these preliminary considerations we shall try to

outline what kind of contribution the neurophysiological study of the
newborn baby can give us to understand in which peculiar way it
interacts with environment in the first months of its life.
The newborn (as observed in its usual environment) shows a wide

set of specific behavioral patterns characterized by a monotonous
repetition and temporal steadiness, although a great interindividual
variability must be admitted.
It is quite absurd to describe all the newborn's behavioral

repertory; this can only be done if we consider some variables, which
are to be kept in mind for the entire list of the behavioral patterns
we give.
For the purposes of our study we shall limit our attention to

the bioelectrical study of the brain in relation to the evaluation of
behavioral states and their development. As behavioral states we
shall define, (as Prechtl has done) a convenient categorization of
many conditions which are relatively stable over time and which can
be easily recognized if (or when) they occur (Prechtl, 1977).
The study of the behavioral states of the newborn infant and

their bioelectrical implications, in our opinion, is one of the most
PECULIARITIES OF ELECTRICAL BRAIN ACTIVITY 129
objective methods to assess early infant behavior and its development

in a sufficiently precise way.
Prechtl has in fact confirmed again and again the op~n~on that
such states must not only be considered as a descriptive behavior
classification, but as a distinct mode of brain activity (Prechtl,
1974).
In this sense, looking for the specific bioelectrical peculi-

arities of every state, (if they exist), and being able to relate
them to specific brain structures or mechanisms, may appear a promis-
ing method of studying the infant's early behavior.
In the neonatal period such research meets with two main ob-
stacles:
1. the weight of gestational age on the EEG pattern;
2. a remarkable interindividual variability.
If the first obstacle can easily be overcome by estimating the

real gestational age precisely enough, with a careful anamnesis of
gestation and by adopting standardized criteria in order to allow
precise assessment of gestational age, the problems relative to the
second point appear to be more complex.
In fact such individual variations may result from various

factors, first the genetic ones and those related to mother-infant
interaction (Sander et al. 1970).
Dittrichova has emphasized that the differences among infants

may be stable and last for periods even longer than six months
(Dittrichova and Paul, 1975).
Touwen (1978) stresses that a wide variability within the indi-

viduals, considered as the norm, shouldn't be underestimated, whereas
on the contrary a rigid stereotype should be considered an indicator
of pathology.
First of all it is appropriate to see whether there are any

anatomical or functional reasons that can justify some of the
peculiar ways of reacting in the first stages of life. We shall
obviously refer to the full term neonate and to the first months of
extrauterine list; the subject would become much more complex if we
had to consider the preterm neonate and the lowest gestational age,
still we must make a few notes about these conditions.
The chronological stages of some of the most important phenomena

related to the maturation of the C.N.S. can be outlined.
It clearly appears from Fig. 1, (drawn from Herschkowitz, 1975)

that cell differentiation (particularly of the glia) , cell migration
and myelinization are still very active at birth.
130 C. FAIENZA
a D ,
I
I
,
b Di
c
f
~ ____________~\t~____~
C B 2 3 9 10 yoera
Fig. 1. Timing of some phenomena in brain development.

C - Conception; B - Birth; a - proliferation of neurons;
b - migration of neurons; c- proliferation of glia;
d - differentiation of neurons; e - development of
connections; f - myelinization.
Particular emphasis should be given to the phenomenon of the

development of connections. In fact Purpura (1975) has demonstrated
that the cytoarchitectural features and details of neural geometry
that characterize the visual cortex of the full term newborn infant
are already well established by the 8th month of gestation. We can
affirm that the calcarine cortex of the 8 month-old preterm is
morphophysiologically similar and equivalent to that of the full term
neonate,~. However, although not denying the importance of these
elements it is likely that the single most important event in the
final stages of maturation of visual cortex is dendritic differen-
tiation, which includes dendritic spine development and axospino-
dendritic synaptogenesis. It is reasonable to think that the same
explanation can b e reported to the other cortical zones that have an
analytical function. As a consequence of this, the peculiarities of
the genesis of brain electrical activity during perception in the
first months of life can be partly referred to this developing
phenomenon, as it is shown especially by the EP's. Purpura's hypoth-
esis that the long latency of an early negative component observed in
the VER (visual evoked response) of a preterm under 30 weeks is
connected with the absence of dendritic spine, seems rather exciting.
The phenomenon of cellular migration, particularly for Netz

cells, is more complicated to analyze. The analysis would be easier
with regards to the process of cell myelinization. Although
Langworthy, when studying neonate marsupials in 1928, had already
demonstrated that myelinogenesis could not be considered as an indi-
cator of the beginning of nervous conduction, nevertheless nobody has
so far disproved the hypothesis that myelinogenesis indicates a

greater precision (if not a greater speed) in nervous conduction and
therefore in neurosensorial and neuromotor patterns.
For instance, with regard to the myelinization of the visual

system, thalamic radiation begins to show the presence of myelin just
before term, but this process is completed within the fifth month of
life. On the other hand, with regard to the acoustic system, these
pathways can be considered totally myelinized only towards school-
age.
An analysis of the visual afferent sensorial pathway allows us

to establish the possibility of the coexistence and use of a second-
ary and philogenetically older visual system, which van integrate the
main one in the first months of life; because only after the second
month the possibility of a full use of the primary visual system
arises (Bronson, 1974).
The existence of a secondary acoustic system has been well

documented.
An interesting outlook on the early development of sight and

hearing derives from this; in fact rather than considering postnatal
changes as being due only to a general maturation of a system, insuf-
ficiently structured initially, it appears to be more appropriate to
assume the emergency of a series of new capacities, corresponding to
the progressive development of more sophisticated structures. See
Purpura's hypothesis on the growth of dendritic spine.
Such new emergencies in substitution of more primitive systems

can be explained by the transient neural function hypothesis (Prechtl
1980).
We emphasize the fact, Bower (1974) with regard to visual and

acoustic perception, recalls the existence of some differences in
dimensions and distances, and therefore in anatomic structures
between eyes and outer ears in babies and adults.
Having emphasized these anatomo-functional basis we can make a

deeper examination of behavioral states in infancy.
After the first fundamental works by Wolff, Prechtl, Parmelee,

Stermann, Anders, there is not much we can add to what has already
been extensively documented.
However, there is no general agreement on the classification of

behavioral state in neonatal age and infancy.
But this disagreement is only in relation to the criteria chosen

to identify a behavioral state. If the number of selected criteria
132 C. FAIENZA
is too small the discrimination may be lost; if the number is too

large many conditions will be found which don't satisfy the proper-
ties of the state and we are often forced to use the term "indeter-
minate state" (Anders et al., 1971).
In full term newborns, as done by Prechtl (1977), five different

states can be recognized, which are characterized by the following
criteria:
State 1: eyes closed, regular respiration, no movements (quiet

sleep, n-REM).
State 2: eyes closed, irregular respiration, small movements (active
sleep, REM).
State 3: eyes open, no movements (quiet awake).
State 4: eyes open, gross movements (active awake).
State 5: eyes open or closed, crying.
These criteria are not strictly objective and are based on a

combination of heterogeneous variables (respiration, motor activity,
closing or opening of the eyelids), but with them, the assessment of
these behavioral states can easily be done when we combine methods
based both to direct observation and to poligraphic records (~rechtl
and Beintema, 1964; Prechtl et al., 1968).
For the poligraphic records, in our Laboratory, we use a Van

Gogh Poligraphic recorder with 16 channels, an FM Magnetic tape
recorder AMPEX FR 1300A to store all analogical data and a MINC - 11
Digital, to analyze the data.
The poligraphic recordings are loaded on tapes; allowing the

possibility of off-line analysis.
THE DEVELOPMENT OF BEHAVIORAL STATES AND THEIR RELATED

ELECTRICAL DATA
The alternance, the duration and the distribution of a single

behavioral state over 24 hrs, is a function of the ontogenetic stage
of development of each individual of a species.
In human premature babies, although we are often forced to use

the expression "indeterminate state", systematic studies have shown a
high frequency of active sleep in lower gestational ages, in com-
pliance with that observed in all mammals. A concept, which has to
be rejected, is to consider active sleep as "a primitive anarchic
state and quiet sleep as a more mature highly controlled state"
(Parmelee and Stern, 1972).
Still another peculiarity of low gestational ages up to the full

term neonate is the fact that the transition from waking to sleeping
state takes place directly through an active sleep phase (REM). This
modality is maintained in the first weeks after birth only; towards
the end of the first month of life, suddenly the baby passes from
waking state on to quiet sleep.
These features find an explanation on the basis of different

developmental levels of the various kinds of sleep. It has been
widely proved, that active sleep originates from mesencephalic struc-
tures, indeed hierarchically archaic. (Jouvet stressed the role of
the nucleus reticularis pontis oralis et caudalis, Jouvet 1965).
Whereas quiet sleep requires an advanced development of cortical
structures. It has been infact demonstrated that a decorticated cat
shows no evidence of quiet sleep (Jouvet, 1965).
In one case of hydroanencephaly studied by us no stable quiet

sleep phases could be singled out.
However it is important to underline that, only in the ontogen-

etic sense, active sleep can be considered as a "primitive" state.
The cyclical alternance of behavioral states is typical of a

specie, it is a direct function of age (and therefore of develop-
mental stage) and is only slightly affected by external influence.
See results of the studies on sleep deprivation (Dement, 1972).
Salzarulo et al. (1980) for instance, have recently studied some

infants under continuous parenteral or enteral feeding from birth.
In almost all these infants, ranging from 1 to 8 months, the absence
of feeding rhythms didn't appear to greatly modify sleep organization
and maturation.
I shall now try to summarize the important changes both in the

distribution of the single behavioral states and in the sleep wake-
fulness relationship, which appear in the first months of life, and
particularly the modifications of spontaneous electrical brain
activity and evoked responses to sensorial stimulations.
EEG CHANGES AND BEHAVIORAL STATES IN INFANCY
It is sufficiently confirmed that up to 26 weeks of gestational

age it is impossible to identify a definite behavioral state with the
observation or looking at EEG patterns.
The earliest records of electrical brain activity in the human

was recorded by Bergstrom in a fetus at 70 days of gestational age
(GA) , with some electrodes implanted in the pontine brain stem
(Bergstrom, 1969).
134 C. FAIENZA
However, one of the first EEG recordings from the scalp in a

non-viable fetus of 19 weeks of gestational age is reported by R.
Engel (Engel, 1975). Brain activity was characterized at the begin-
ning of the record by a polymorphic activity of 9-10 Hz; with about
25~V in amplitude, and occasional peaks of 45~V, flattening more and
more as the heart rate drops to 50-40 pulse frequencies.
A) - In a preterm at 24-27 weeks of GA EEG activity (Fig. 2) consists

of high voltage discontinuous polymorphic patterns (Dreyfus-Brisac,
1962, 1967, 1968) with frequencies up to 15 Hz, but with dominance of
delta frequencies (Ellingson, 1979).
This activity of high amplitude occurs in bursts lasting 3-20

sec. (Dreyfus-Brisac et al., 1975). Spikes of high amplitude (200-
300~V) may be mixed with the irregular theta and delta waves of the
burst periods (Engel, 1975). Ellingson codes this pattern as pattern
A (Ellingson, 1979). Sometimes a more continuous EEG activity may
occur, up to 1-2 min., contemporaneously with crying and body move-
ments (Dreyfus-Brisac, 1979). At this age an assessment of behav-
ioral states and a differentiation between wakefulness and the sleep
state is impossible (Monod et al., 1977). Although Sterman and
Hoppenbrouwers (1971) affirm the existence of a brain rest activity
cycle (BRAC) in fetus, recording some movements of the fetus in
utero, at the moment we haven't sufficient data to support the exist-
ence of BRAG in prematures under 27 weeks of gestational age. Jouvet
and Schade (1965) have stressed that the differentiation of sleep
patterns is possible only at a relatively advanced stage of matu-
ration.
# 4574 9 concepllonol age 24 weeks 2 days old welghl 480g

________ ______ ______ ____ ______________
F.-C.~~ ___________ ________________----__________

. ~. ~~--
C, - o, ........._~......
C. - O2 ________--'"
--------------------------------~-------
0 , - T, _ - ----...Jo-
O2 - r4 _ _ _ _ _ t-----._________________ ~ ____ -------
F.- 02~~---_---- . . .--"------'---_______--------'-

Fig. 2. Premature infant. EEG tracing poorly organized. One burst
of high amplitude between long inactive phases. (From Engel,
1975).
B) - Between 28 and 32 weeks of GA, the EEG pattern becomes more

continuous, although a tendency toward intermittent bursts of theta
activity with voltage around 100~V remains, often separated by long
quiescent periods. (Fig. 3).
At the beginning, this theta activity shows a hemispheric iso-

synchronism, which disappears after 29 weeks of gestation (Monod et
al., 1977; Dreyfus-Brisac, 1979).
This pattern is coded as B by Ellingson (Ellingson, 1979) and in

similar in sleep and wakefulness, so it is impossible to assess the
behavioral states from EEG patterns. Even by observation, at this
age, it is not easy to establish clearly the awake state nor the
various sleep states (Monod and Garma, 1971), although some charac-
teristics of active sleep and quiet sleep, found in older infants,
are often observed at this period in life. Rapid eye movements,
regular and irregular respiration, clonic discharges, or startles may
occur without strict correlation to specific states; almost all of
sleep time is described as "indeterminate".
C) - The most important finding from 32 to 36 weeks of GA is the

onset of the difference between EEG patterns in active sleep and
quiet sleep. At this age, the pattern, is characterized by slow
waves (4-6 Hz) with superimposed rapid rhythms (8-15 Hz) and, is seen
in the occipital, temporal and central areas; asynchrony is the rule,
(Fig. 4A).
This pattern is continuous during wakefulness, as well as during

active sleep. During quiet sleep EEG activity becomes discontinuous
because of the intermittent sequence of waves of delta activity, on
which bursts of faster activity are superimposed. (Fig. 4B).
RESP
EKG .1 .1 • f
f .4
f 1, ,d ' "
f , d
4 , .I d ' , ,
! , I+ .J
! , I I J"f I I • , , I , J f • J • I
LEOG __~~~~----~------~~~~~~~
REOG __~__~~~---r'-~__--
EMG -, " ..
eye,cimed jaw jerks
F1C3 '-~~~~~'-~-v~~----~~
C301 __~~--~--~~~~~~
F1T3
T301
F2 C4 ~-r-"'\j 4' - _ , . , - . . . . , , -_ _
C402 ~-A~~~~
F2 T4
T402
C3 CZ _~,"",r- _______","","-'""'-~---'~r--..-----"""..
CZC4
Fig. 3. Normal infant. 28 weeks conceptional age. (From Werner et
al., 1977) .
136 C. FAIENZA
Lombroso (1975) calls these complexes "Spindle-delta-bursts".
This activity is interrupted by periods of flattening of vari-

able duration. Ellingson identifies this pattern as pattern C
(Ellingson, 1979).
D) - But EEG patterns, which allow a differentiation between wakeful-

ness, active sleep and quiet sleep, are clearly seen only after the
conceptional age of 36 weeks, when three different EEG patterns are
identified:
a) during wakefulness the EEG consists of a diffuse slow irregu-
lar wave activity (4-5 Hz) with low voltage. (Fig. SA).
This pattern is similar to that of full term newborn infants,

and has been called "act ivite moyenne" by Samson-Dolfuss (1955). b)
During active sleep the dominant activity is a continuous slow wave
pattern (4-7 Hz) with superimposed low voltage rapid rhythms (10-14
Hz). (Fig. 5B).
c) Quiet sleep is characterized by a discontinuous pattern

consisting of bursts of variable morphology and duration, often at
the beginning of the burst the faster activity described in the
spindle-delta burst appears (brushes by Lombroso, 1975, or ripples by
Engel, 1975) . (Fig. 6A).
Fig. 4. Newborn of 32 weeks C.A. - A (Left) Slow waves, (4-5 Hz)

with a superimposed rapid rhythm. - B (Right) Discontinuous
tracing. Intermittent sequence of delta with faster
activity superimposed: the spindle-delta-bursts.
fOI'l\419'
!f-.:;1W)"y
I ,.c.. •. 14~9
Fig. 5. Newborn of 36 weeks C.A. - A (Left) Slow irregulat wave

activity. "Activite moyenne". B (Right) The continuous
slow wave pattern has a superimposed low voltage rapid
rhythm.
> , I
R,ft ,tI .2U J I
Fig. 6. Newborn of 36 weeks. C.A. - A (Left) The bursts are more

synchronized. See brushes at the beginning of burst. -B
(Right) Newborn at term. Pattern with low theta activity.
The LVI of Anders.
138 c. FAIENZA
E) - Only in full time neonates the distinction between wakefulness

and the two sleep states is easy, when we combine the observation
with the poligraphic data.
a) The newborn infant when awake shows a diffuse low voltage

pattern, which differs little from the pattern seen in awake 8 month
premature. This pattern is a theta activity of 4-7 Hz with low
voltage (25-50~V): the low voltage irregular (LVI) of Anders et al.,
1971. Often this activity is mixed with a slower activity (1-4 Hz)
of higher voltage (50-100~V). (Fig. 6B).
b) In active sleep the same pattern appears but it is more

rhythmic than in the waking state; the mixed (M) pattern of Anders et
a1. (1971). (Fig. 7A).
c) A very peculiar and specific pattern is seen in quiet sleep

"trace alternant" (TA of Anders et a1.) characterized by bursts of
slow waves of high voltage (1-3 Hz; 50-100~V) bilaterally synchron-
ous, with interburst periods of relative inactivity or similar to the
low voltage pattern, seen in wakefulness and REM sleep, lasting 3 to
10 seconds. (Fig. 7B). Sometimes, at the beginning or at the end of
quiet sleep a continuous high voltage slow wave pattern (1-3 Hz;
50-100~V) appears; the high voltage (HV) pattern of Anders et al. We
don't agree with that illustrated by Anders et al. in their manual
for scoring behavioral states in newborn infants, regarding the
definition of a state analogous to stage 1 in adult and specified as
D (drowsiness).
, I
~_ ' 1"--1" -+-+-+-f--+-+-~-"--~'--t-+-
'· r 'IJ'.,
~ . · ,~t: , .- .,
i"t.. LI
' .
I
"~ OI
, I I
..po ...,
Fig. 7. A (Left) Newborn at term. Low voltage theta activity mixed

with some higher activity. Pattern M of Anders. - B (Right)
Newborn at term. "Trace alternant".
At term, the transition between the awake state and sleep is

abrupt into active sleep. Neither do we agree with the significance
of pattern M. We use the Ander's scoring method but we don't use a
binary score for the EEG: the low-voltage irregular (LVI) is scored
0, the mixed pattern (M) is scored 1, and the high voltage slow
pattern (HVS) and trace alternant (TA) are scored 2. In this manner
the total score 0-2 allows us to identify active sleep, score 4-6
quiet sleep and only score 3 the "indeterminate state".
F) - During the first months of life EEG changes are less rapid than
in the premature baby. We can summarize these changes in four points:
a) The most important is the disappearance of the "trace alter-

nant" in quiet sleep, at the end of the first month. However Nolte
(1978), describes a pattern (with the code number 447) characterized
by some bursts of slow waves (1-2 Hz) lasting 1.5-2.5 sec. with
faster activity superimposed, interrupting a slow wave pattern (3-6
Hz) of low voltage. This pattern is seen at 44 weeks of GA.
b) The second is the appearance in the second month of well

organized central sleep spindles, which are brief bursts of rela-
tively fast rhythmic activity, distinguishable from the slower back-
ground of the EEG in quiet sleep (Metcalf, 1970).
I think that the problem of EEG sleep spindle ontogenesis is

much more complex than has been thought, up to now. We must take
into particular consideration the relation between the faster ac-
tivity superimposed on the bursts, "the brushes", the rapid component
of the trace alternant, pattern 447 of Nolte and the sleep spindles
seen after the first month of life. In my opinion the motivations to
eliminate these relationships are not sufficient. The frequency
range, and topographical distribution are, certainly quite different,
but the spindles' rhythmic presence only in quiet sleep and, after,
in the second stage of quiet sleep is sufficient to reintroduce the
problem. I think that a deeper analysis of the frequencies (power
spectra, autocorrelation and cross-correlation) can help us to solve
it. A study which we are now doing.
c) Around the 3rd month, a well defined rhythmic activity

appears, in the occipital area, reacting to eye opening; being the
start of the blocking reaction. The frequency is nearer and nearer
to alpha.
d) From the 6th month during the first stage of sleep (we can
now use the term drowsiness) a high amplitude theta activity (4 Hz,
100-200~V), termed hypnagogic hypersynchrony, appears firstly
described by Gibbs and Gibbs (1950).
Some other changes occur later but they are very slight and slow
in comparison to those in the first year of life, and not so import-
ant.
140 C. FAIENZA
Now, let's consider some relevant notes on the development of

circadian rhythms of behavioral states.
The Parmelee group in Los Angeles accurately investigated the

development of alternance of sleep and waking states in infancy
(Parmelee et al., 1972).
It has been widely demonstrated that the most important changes

in the first months of life concern the relationship between wakeful-
ness and sleep states, being considered as two contrasting states of
consciousness, which occur in a cyclic manner in the course of 24
hrs.
These changes are not expressed so much in terms of overall

sleeping time, since this passes from 16.7 hours at birth to 13-14
hours at 6 to 8 months.
The most evident changes are in duration and distribution of

single sleep periods during 24 hrs. At birth each sleep period is
about 3-4 hrs.; by 6 weeks infants begin to sustain long 5-6 hr sleep
periods, not necessarily at night. Gradually each period becoming
longer; from 12 to 16 weeks the longest period reached being 8-9 hrs.
Parmelee demonstrated that a gradual shift to a diurnal pattern

starts soon after birth; at three months, sleep during daytime pre-
sents a tendency to consolidate into well-defined naps.
In comparison to sleep patterns, waking states change much less.

At birth infants awake about every 3-4 hrs. and stay awake for 1-2
hrs. At 16 weeks the longest sustained period of wakefulness passes
to 3-4 hrs. Regarding the waking states, infants seem to be most
attentive during state 3 (quiet-awake), which double in length during
the first month.
Parmelee underlines that the development of attentive behavior

proceeds simultaneously with the development of quiet sleep and
sustained sleep periods.
Up to now, the development of spontaneous electrical brain

activity in infancy has been discussed and a similar approach could
be made regarding the cerebral evoked potentials to sensory stimu-
lation.
We refer to the rather numerous articles on this subject, in

which the close correlation between ontogenetic stages of S.N.C. and
the behavioral states in determining the characteristics of the
evocated potentials to the sensorial stimuli are widely emphasized
(Ellingson, 1958; Engel et al., 1968; Watanabe et al., 1972, 1973;
Weitzman et al., 1965; Weitzman, Graziani, 1968; Graziani et al.,
1968; Akiyama et al., 1969; Engel, Young, 1969; Engel, 1971; Desmedt
et al., 1967, 1970; Hrbek et al., 1968, 1969).
REFERENCES
Anders, T., Emde, R., and Parmelee, A., 1971, A manual of standard-
1zed terminology, techniques and criteria for scoring of
states of sleep and wakefulness in newborn infants, UCLA Brain
Information Service, Los Angeles.
Akiyama, Y., Schulte, F. J., Schultz, M. A., and Parmelee, A. H., Jr.
1969, Acoustically evoked responses in premature and full term
newborn infants, Electroenceph.Clin.Neurophysiol. 26:371-380.
Bernet, A. B., Friedman, S. L., Weiss, I. P., Ohlrich, E. S., Shanks,
B., and Lodge, A., 1980, Vep development in infancy and early
childhood, A longitudinal study, Electroenceph.Clin.Neuro-
physiol. 49:476-489.
Bergstrom, R. M., 1969, Electrical parameters of the brain during
ontogeny, in: "Brain and Early Behavior," R.J. Robinson, ed.
pp.15-36, Academic Press, London.
Bower, T. G. R., 1974, "Development in Infancy," W.H. Freeman & Co.,
San Francisco.
Bronson, G., 1974, The postnatal growth of visual capacity, Child
Develop. 45:873-890.
Dement, W. C., 1972, Sleep deprivation and the organization of the
behavioral states, in: "Sleep and the Maturing Nervous
System," C.D. Clements, D.P. Purpura, F.E. Mayer, eds.,
Academic Press, New York.
Desmedt, J. E., and Manil, J., 1970, Somatosensory EPs of the normal
human neonate in REM sleep, in slow wave sleep and in waking,
Electroenceph.Clin.Neurophysiol. 29:113-126.
Desmedt, J. E., Manil, J., Chorazyna, H., and Debecker, J., 1967,
Potential evoque cerebral et conduction corticipete pour une
olee d'influx somesthesique chez le nouveau-ne normal,
C.R.Soc.Bioi. (Paris), 161:205-223.
Dittrichova, J., and Paul, K., 1975, Stability of individual
differences during paradoxical sleep in infants, Act.Nerv.
Super. 17:49.
Dreyfus-Brisac, C., 1966, The bioelectrical development of the
central nervous system during early life, in: "Human Develop-
ment," F. Falkner, ed., pp. 286-305, Saunders, London.
Dreyfus-Brisac, C., 1967, Ontogenese de sommeil chez Ie premature
humain: etudes polygraphiques a partir de 24 semaines d'age
conceptional, in: "Regional Maturation of the Brain in Early
Life," A.Minkowski, ed. pp. 437-4':J7, Blackwell, Oxford.
Dreyfus-Brisac, C., 1968, Sleep ontogenesis in early human
prematurity from 24 to 27 weeks of conceptional age, Dev.
Psychobiol. 1: 162-169. --
Dreyfus-Brisac, C., Curzi Dascalova, L., 1975, The EEG during the
first year of life, in: "Handbook of EEG and Clinical Neuro-
physiology," vol. 6 ""B,"" pp. 6-23, Elsevier, Amsterdam.
Dreyfus-Brisac, C., 1979, Ontogenesis of brain bioelectrical
activity and sleep organization in neonates and infants, in:
"Human Growth - 3" Neurobiology and Nutrition," F. Falknerand
J.M. Tanner, eds., pp. 157-182, Bailliere Tindall, London.
142 C. FAIENZA
Dreyfus-Brisac, C., 1962, The electroencephalogram of the premature

infant, World Neuro1. 3:5-15.
Ellingson, R. J., 1958, Electroencephalograms of normal, full term
newborns immediately after birth with observations on arousal
and visual evoked responses, E1ectroencep.C1in.Neurophysio1.
10:31-50.
Ellingson, R. J., 1975, Ontogenesis of sleep in the human, in:
"Experimental study of human sleep: methodological problems,"
G.C. Lairy, P. Sa1zaru10, eds., Elsevier, Amsterdam.
Engel, R., Crowell, D., and Nishijima, S., 1968, Visual and auditory
response latencies in neonates, in: "In Honour of C.C. De
Silva," Kularatne & Co., Cey1on.-
Engel, R., 1969, Calibrated pure tone audiograms in normal neonates
based on evoked electroencephalographic responses,
Neuropadiatrie, 1:149-160.
Engel, R., 1971, Early waves of the e1ectroencepha1ic auditory
response in neonates, Neuropadiatrie, 3:147-154.
Engel, R. C. H., 1975, Abnormal electroencephalograms in the neonatal
period, C. Thomas Springfield, Ill.
Gibbs, F. A., and Gibbs, E. L., 1950, "Atlas of Electroencephalo-
graphy," p. 324, Addison-Wesley, Reading, Mass.
Graziani, L., Weitzman, E. D., and Velasco, M. S. A., 1968,
Neurologic maturation and auditory evoked responses in low
birth weight infants, Pediatrics, 41:483-494.
Hrbek, A., Hrbkova, M., and Lenard, H. G., 1968, Somatosensory evoked
responses in newborn infants, E1ectroenceph.C1in.Neurophysio1.
25:443-448.
Hrbek, A., Hrbkova, M., and Lenard, H. G., 1969, Somatosensory,
auditory and visual evoked responses in newborn infants during
sleep and wakefulness, E1ectroenceph.C1in.Neurophysio1. 26:
597-603.
Herschkowitz, N., 1975, Influenza de11'a1imentazione su1 metabo1ismo
cerebrale, Simposio Nestle, in: "Svi1uppo Enzimatico e
A1imentazione Postnata1e," H-:R. Mii11er, ed., Milano.
Jouvet, M., 1965, Paradoxical sleep - a study of its nature and
mechanisms, in: "Progress in Brain Research," vol. 18, Sleep
mechanisms K-.-Akert, C. Bally and J.P. Schade, eds., pp.
20-62, Elsevier, Amsterdam.
Langworthy, O. R., 1928, The behavior of pouch young opossums
correlated with myelinization of tracts. J.Comp.Neuro1. 46:
201-240.
Lombroso, C. T., 1975, Neurophysiological observations in diseased
newborns, Bio1.Psychiatry 10:527-558.
Metcalf, D. R., 1970, EEG sleep spindle ontogenesis, Neuropadiatrie
1:428-433.
Monod, N., and Garma, L., 1971, Auditory responsivity in the human
premature, Bio1.Neonat. 17:292-316.
Monod, N., and Tharp, B., 1977, Activite e1ectroencepha1ographique
normale du nouveau-ne et du premature au cours des etats de
vei11e et de sommei1, Rev.EEG Neurophysio1. 3:302-345.
Parmelee, A. H., and Stern, E., 1972, Development of states in

infants, in: "Sleep and the Maturing Nervous System," C.D.
Clemente,'D.P. Purpura, and F.E. Mayer, eds., Academic Press,
London.
Prechtl, H. F. R., 1974, The behavioral states of the newborn infant
(a review), Brain Res. 76:185-212.
Prechtl, H. F. R., 1977, Assessment and significance of behavioral
states, in: "Brain Damage in Infancy and Childhood," S.R.
Berenber~ ed., Martinus Nijhoff Publ., The Hague.
Prechtl, H. F. R., 1980, Regressions and transformations during
neurological development, in: "Regressions in Development:
Basic Phenomena and Theoretical Alternatives," T. Bever, ed.,
Erlbaum, New York.
Prechtl, H. F. R., Akiyama, Y., Zinkin, P., and Grant, D. K., 1968,
Polygraphic studies of the full term newborn. I: Technical
aspects and quantitative analysis, in: "Studies in Infancy,"
M. Bax, and R.C. MacKeith, eds., Clinics in Developmental
Medicine, vol. 27, pp. 1-21, W. Heinemann, London.
Prechtl, H., and Beintema, D., 1964, The neurological examination of
the full term newborn infant, Clinics in Developmental Medi-
cine, vol. 12, W. Heinemann, London.
Purpura, D. P., 1975, Morphogenesis of visual cortex in the preterm
infant, in: "Growth and Development of the Brain: Nutritional,
Genetic and Environmental Factors," M.A.B. Brazier, ed., Raven
Press, New York.
Salzarulo, P., Fagioli, I., Salomon, F., Ricour, C., Raimbault, G.,
Ambrosi, S., Cicchi, 0., Duhame, J. F., and Rigoard, M. T.,
1980, Sleep patterns in infants under continuous feeding from
birth, Electroenceph.Clin.Neurophysiol. 49:330-336.
Samson-Dolfuss, D., 1955, L'EEG du premature jusqu'a l'age de 3 mois
et du nouveau-ne a terme, Thesis Med., Foulon, Paris.
Sander, L. W., Stechler, G., Burns, P., and Julia, H., 1970, Early
mother-infant interaction and 24 hour patterns of activity and
sleep, J.Am.Acad.Child Psychiatry 9:103-123.
Schade, J. P., Corner, M. A., and Peters, J. J., 1965, Some aspects
of the elctro-ontogenesis of sleep patterns, in: "Progress in
Brain Research," vol. 18, Sleep Mechanisms, K-:-Akert, C.
Bally, and J. P. Schade, eds., pp. 20-80, Elsevier, Amsterdam.
Sterman, M. B., and Hoppenbrouwers, T., 1971, The development of
sleep-waking and rest-activity patterns from fetus to adult in
man, in: "Brain Development and Behavior," M.B. Sterman, D.J.
McGinty, and A.M. Adinolfi, eds., pp. 203-227, Academic Press,
New York.
Touwen, B. C. L., 1978, Variability and sterotipy in normal and
deviant development, in: "Care of the Handicapped Child," J.
Apley, ed., Clinics in Developmental Medicine N. 67, W.
Heinemann, London.
Watanabe, K., Iwase, K., and Hara, K., 1972, Maturation of visual
evoked responses in low-birthweight infants, Dev.Med.Child
Neurology 14:425-435.
144 C. FAIENZA
Watanabe, K., Iwase, K., and Hara, K., 1973, Visual evoked responses
during different phases of quiet sleep in preterm infants,
Neuropadiatrie 4:427-433.
Weitzman, E. D., Fishnein, W., and Graziani, L. J., 1965, Auditory
evoked responses obtained from the scalp electroencephalograms
of the full term human neonate during sleep, Pediatrics 35:
458-462.
Weitzman, E. D., and Graziani, L. J., 1968, Maturation and topography
of the auditory-evoked response of the prematurely born
infant, Developmental Psychobiology 1:79-89.
Werner, S. S., Stockard, J. E., and Bickford, R. G., 1977, "Atlas of
Neonatal Electroencephalography," Raven Press, New York.
Wolff, P. H., 1959, Observations on newborn infants,
Psychosomatic Medicine 21:110-118.
INTERPERSONAL ABILITIES OF INFANTS AS GENERATORS
FOR TRANSMISSION OF LANGUAGE AND CULTURE
Colwyn Trevarthen
Department of Psychology
University of Edinburgh
ABSTRACT
There have been great advances in our knowledge of communicative

abilities of infants in the past decade.
A two-month-old may transmit emotional messages by facial ex-

pression, vocalization and gesture and engage in an affectional
exchange with the mother by sight and sound alone. Microanalysis
shows the interactions to be regulated by cognitive and motivational
processes specific for interpersonal engagement. Disturbance of the
maternal response leads to strong expressions of distress.
Communication develops rapidly as the infant expresses more

autonomy of motives in interactions governed by humour and teasing
and increasing interest in manipulation of objects. Maternal behav-
ior changes accordingly, expanding the range of emotional color while
taking up the infant's exploratory and performatory interests.
Towards the end of the first year, game playing, which mothers
ritualize in action songs and chants, is changed by the baby showing
active interest in the mother's directives and referential actions.
Coventional uses of artifacts are acquired simultaneously with aware-
ness of messages in speech.
We conclude that innate interpersonal abilities regulate and

drive forward the growth of cooperative awareness and that first
steps in language acquisition rest on mutual confidence. Further
developments in learning retain a foundation in interpersonal skills
by which interests, intentions and feelings are transmitted in
infancy.
145
146 C. TREVARTHEN
INTRODUCTION
The natural abilities of infants for interpersonal understanding

are now receiving more systematic attention by psychological science.
This reflects an important change of viewpoint on human nature.
For most of this century the dominant theory has been that
infants, at least those under six months of age, are neither aware of
other persons as beings like themselves nor capable of having the
emotions which regulate interpersonal communication. The social
signals of babies have been thought to be ruled by organic needs and
their encounters with caretakers limited to management of a physio-
logical dependence. There has been a kind of tabu on the idea that
infants could have complex interpersonal responses. Indeed the
prevailing philosopy, upheld by both Freud and Piaget, has thought
young infants to be incapable of representing anything in the outside
world separate from their bodies*.
The first revision of this conservative or reduced theory of the

infant mind follows from experimental demonstration that infants have
complex cognitive processes to represent the motion, size and posi-
tion of objects long before they can grasp and manipulate them
(Bower, 1974; Trevarthen, Murray and Hubley, 1981). The data has
come in the past 15 years by a new approach to examination of
cognitive processes. This observes infants' spontaneous exploratory
or orienting behaviors to determine their recognitions and prefer-
ences. The technique, which also uses operant conditioning prin-
*Nineteenth century physiology, with very limited knowledge of the

nervous system, generated a false belief that the inherent nerve
pathways of humans must be reflex or sensory-motor. The brain was
thought incapable of forming a mental image of an object distant
from the sensory receptors and linking all the modalities in a
common field of perception. Scientific psychology, which aimed to
base itself on an objective physiology, automatically concluded that
a newborn could not perceive external objects as separate from the
body and its 'sensations'. All experience in early infancy was
assumed to be both immediate and fragmented in an incoherent con-
glomeration of sensations, without geography in space or purpose in
time. A coherent set of faculties of a single self, knowing the
activities, locations and endurance of objects and formulating
intentions to explore and use them, was supposed to arise entirely
from experience, which formed conditioned associations between
reflexes. If an infant cannot represent and object separate from
himself, it follows that he cannot be conscious of another person as
a complementary being or a partner in communication.
Contemporary knowledge of the state of the human brain at birth and
how nerve networks are formed removes doubts that infants could be
born with elaborate foundations for mental activity of all kinds
(Trevarthen, 1979a, 1980a).
INTERPERSONAL ABILITIES OF INFANTS 147
cip1es, is built upon Piaget's 'clinical' method for exam1n1ng how

the 'object concept' comes about. Piaget (1953, 1970) demonstrated
that infants can carry the image of an object when it has been tem-
porarily concealed. They do this soon after they begin reaching and
grasping for objects and after they have had the experience of ex-
ploring them with many senses while handling them. Piaget stressed
that handling objects coordinates the sensory modalities while
collecting evidence about properties that belong to objects. The
more recent studies have used visual inspection and tracking move-
ments and sucking to show that much younger infants focus on objects
near them, discriminate many of their features, forming preferences,
and situate them in space remote from their bodies. Infants appear
to act in a single space-time frame in which sensory modalities are
coordinated by an inborn network. Piaget showed that the basic
functions of object perception develop independently of language and
kinds of thinking that use language to represent experiences. The
new findings show that the object concept is founded on intrinsic
cerebral structures that exist before object manipulation begins.
In spite of this major advance in knowledge of infant percep-

tions, cognitive psychology still evades the hypothesis that infants
perceive persons as agents with feelings like their own. Most exper-
iments on infants' perception of social signals (principally eye
contact, facial movements and vocalizations) discuss their findings
in exactly the same terms as are used for the psychophysics of object
detection. However, it is increasingly evident that in the first
three months, the perceptual abilities of infants are predominantly
tuned to detect the actions of persons and to interpret their expres-
sions as having emotional value (Trevarthen, Murray and Hubley,
1981). This is the kind of mental activity that young infants are
best equipped to perform.
After a lifetime of interest in the question, Darwin concluded

that human emotions are adaptive and largely innate. About 150 years
ago he began to collect detailed evidence on the facial and vocal
expressions of infants and to make inferences about interior states
that could motivate these expressions. After 40 years he published
his conclusions on evolutionary origins of human expressions of
emotion (Darwin, 1872). Modern descriptive and experimental studies
of infant behavior increasingly support Darwin's theory. For example,
smiling, even in newborns, has been shown to be related to perception
of another person who is behaving affectionately. It soon is a
response to a familiar caretaker and it is used effectively in con-
trol of interpersonal exchanges of feelings by infants less than two
months of age. Likewise, expressions of sadness or anger appear in
relation not only to identifiable physiological needs of the infant,
but also to the feelings and attentions adults direct towards the
infant. The infant resonates to emotions with expressions of
feeling.
148 C. TREVARTHEN
A smile is a form of behavior that can have no influence on the
physical or impersonal world. The movement of a smile has no sig-
nificant effect on the smiling person, even though the state of mind
which produces smiling is at the heart of self-awareness. Smiling
exists to cause an affective response in another person. Adults per-
ceive the expressions of others, such as smiles, as immediate indi-
cators of feeling which they relate to their own feelings or actions.
The human ego is as much concerned with its relations to other
persons as with relations to impersonal objects which have no
emotions. All this leads us to ask a plain question: Can a young
infant perceive human feelings directly, and can complementary feel-
ings be expressed by the infant to regulate an interpersonal engage-
ment with an adult?
My interest in the interpersonal abilities was aroused in the

late 1960s when I started film studies of mother-infant communi-
cation. A longitudinal study of five subjects over the first six
months, carried out with Jerome Bruner, Berry Brazelton and Martin
Richards at the Center for Cognitive Studies, Harvard University,
taught me three sets of facts that convinced me that humans are born
with a capacity for interpersonal communication (Trevarthen, 1974a,
1980b). I saw this endowment to be adapted from the start to joint
participation in tasks and the use of language, both of which become
effective components of behavior months later.
I list these basic findings here to provide a basis for an

outline of our current ideas of how interpersonal skills develop in
the first two years.
1. By two months an infant is strongly attracted to a mother when

she approaches, seeks eye contact and speaks in a gentle affec-
tionate way. The infant inspects the mother's face and ex-
presses pleasure with smiles and small vocalizations when she
responds appropriately. This behavior is adaptive only to
interpersonal contact. It is sustained, in the situation I
used, by seeing and hearing alone. A different pattern of
behavior is addressed to an inanimate object suspended near the
infant. The interpersonal responses develop before those suited
to manipulative mastery of things.
2. The engagement between mother and infant develops a conver-

sation-like pattern. Coordinated expressive behaviors create
episodes with beginning, climax and ending. The actions of the
partners are partly synchronized and partly alternating. Both
control the pattern. Among the behaviors of the infant to which
mothers attend closely, as if they were messages, are mouth and
tongue movements and hand gestures which appear to be rudimen-
tary efforts to speak and make hand signs.
3. Before five weeks infants rarely sustain face-to-face communi-

cation. After 12 weeks interest in face-to-face communication
is less than at 6-8 weeks and the infant is more attracted to

inspect the surrounding physical environment, especially what it
affords for manipulation. I concluded that interpersonal re-
sponses undergo systematic or programmed development under
constraint from growing brain structures (Trevarthen, 1982a).
Interpersonal functions seem to compete with functions for
solitary cognition of objects that develop in the third and
fourth month after birth.
The subsequent research in my laboratory has been aimed to

clarify aspects of the above behaviors, and we have extended our
studies throughout infancy into the time when the child really can
speak. This has given us material for a theory of the role of inter-
personal functions in the early development of language and thought.
RESPONSES OF THE NEONATE TO THE MOTHER'S PRESENCE
The unpredictable phases of spontaneous movement of newborns and

their shadowy, defensive responses to any stimuli arising from events
distant from their bodies seem to justify doubts about inherent
social consciousness. However, close inspection of how a baby may
react to the mother immediately after birth reveals that they possess
a paradoxical sensitivity to emotions.
A newborn will react to sensitive stimulation that is accurately

contingent and appropriate in intensity for the baby's interior state
and the activity it generates. The state of 'arousal' is shown in
movements of tension and distress or of relaxation and contentment;
in amount of limb movement and motor tonus, reactivity to stimuli,
facial movements, vocalizations and hand movements. By responding to
these with holding, cuddling, stro~ing, patting, rocking, or speaking
softly, as well as by feeding or removing physical causes of pain or
discomfort, a mother may regulate the infant's state (Tronick, Als
and Brazelton, 1979). Social communication of this kind may even
occur between a premature infant in an isolette and a responsive
mother (Marton, Minde and Ogilvie, 1981). It is claimed that new-
borns may synchronise limb movements with the beat of adult speech
(Condon and Sander, 1974). Sensitivity to human action both engages
the infant's self-regulatory mechanisms to the mother's care, train-
ing her how to administer effectively, and generates a powerful
maternal feeling of affection. There is increasing evidence that
experience of this intense communication of motivational state around
birth has value for both infant and mother by contributing to the
learning of skills for communication of affect in both of them.
Sleeping and feeding of a young infant and later development of
face-to-face communication and play all may be affected if the mother
fails to form a positive feeling to her infant soon after birth.
The affectionate care contributes to the welfare of the baby at an
emotional level.
150 C. TREVARTHEN
The above findings raise questions about what happens when
mother and infant have to be separated in the course of an assisted
birth or to achieve medical treatment of a newborn at risk. Prema-
turity or defective development of the infant may cause the maternal
response to fail because the infant cannot respond normally (Klaus
and Kennell, 1976). Treatment of infants that must be isolated from
their mothers is increasingly directed towards providing some substi-
tute for the responsive stimulation which the mother normally
affords.
Experiments show that a newborn may orient to the human voice

immediately after birth, seeking as if to see a face (Alegria and
Noirot, 1978). Newborns have been shown to prefer the mother's
voice, but not the father's, even if he were present at birth.
Evidently they identify features of the mother's voice learned ante-
natally (Spence and DeCasper, 1982).
An alert but relatively quiet newborn may be visually responsive

to the environment, scanning with saccades, fixating large features
and tracking moving objects. The baby may fixate the mother's face
and the sound of her voice may sustain the interest. However, new-
borns also orient away from face-to-face contact and they close their
eyes tight, bunch up and fret to reject social contact in favor of
'holding'. Thus, while affective mirroring occurs between mother and
infant immediately after birth, social avoiding is at least as strong
as seeking in the earliest contacts with the mother by sight and
sound. The ability to avoid person-to-person contact by withdrawal
of gaze remains evident at later stages of development in human
communication (Sylvester-Bradley, 1981).
Spontaneous facial movements of newborns are complex and irregu-

lar, but they may be organized momentarily into distinct expressions
(Oster, 1981). Smiling occurs spontaneously as well as in response
to gentle maternal attentions, but the social value of the smile is
reduced because it has low probability of occuring in response to the
mother's signals. Newborns sometimes imitate mouth and hand move-
ments seen. It is difficult to verify this because the same move-
ments occur spontaneously in the great variety of activity of
fingers, mouth and tongue, eyes and facial muscles. However, the
timing of some matching movements is such as to confirm that true
imitation, relying on perception of the movement seen as equivalent
to one that may be produced, is possible in the first weeks after
birth (Maratos, 1973; Meltzoff and Moore, 1977).
Newborn communicative responses must be viewed in relation to

known features of the growth of the sensory projection pathways.
Large changes in the anatomy and function of the cortical visual area
of humans occur just before full term gestation and continue in the
first post-natal weeks (Trevarthen, 1979a; Trevarthen, Murray and
Hubley, 1981). Comparable developments occur in the auditory path-
ways (Parmelee, 1981). Behavior tests show that significant changes

in visual acuity and visual focal ising movements occur in the second
month. The infant gains a capacity to focus on details within a
figure. Before this, visual exploration is cut down by closing of
the eyes and turning away. It appears that prenatally wired in
systems for recognising persons at a distance, as well as those for
perceiving objects suitable for prehension, are weakly expressed in
newborns because their basic perceptual apparatus is undergoing rapid
self-differentiation under the influence of a diet of stimulation
that is severely rationed by motor mechanisms. We should regard the
newborn as a period in which many problems of morphogenesis in pri-
mary sensory and motor structures must be solved. Central motive
structures for awareness of persons and objects are therefore diffi-
cult to evaluate at this stage.
PRIMARY INTERPERSONAL ENGAGEMENTS IN THE SECOND MONTH
Because two month olds actively seek face-to-face interactions

with their mothers for the first time as a reliable part of their
behavior and then exchange vocal, facial and gestural signals in well
regulated patterns, I have described these engagements as primary
interpersonal or intersubjective communication (Trevarthen, 1979b).
We have charted developments in a number of infants from the begin-
ning of the second month. There is invariably a marked increase in
the intensity and constancy of attention to the mother's face and
voice at about 5-6 weeks after a full-term birth and an increase of
smiling and cooling (Figure 1). The mother is excited by the in-
fant's orientation to her and she makes finely regulated attempts to
elicit further communication.
If the above kind of interaction does not occur, that is suf-

ficient to lead one to suspect that the mother's attachment to her
infant or the infant's perceptual functions are abnormal. Thera-
peutic intervention when the mother is profoundly distressed emotion-
ally and cannot face her baby can lead to dramatic improvement in the
quality of interaction between mothers and infants and the mother's
awareness of the infant's response assists her recovery (Fraiberg et
al., 1980).
Mothers react to positive eye-contact and smiling of two month

olds by increasing their output of speech and by turning of their
expression of affect so that it comes to reinforce what the infant
does. The responsive maternal echo which was seen to the newborn
combined with intimate questioning speech becomes more active as the
baby shows definite recognition of the mother's face and smiles in
response. The mother shows facial expressions of interest, surprise,
concern or affectionate smiling. She moves her head gently in
synchrony with her undulating sing-song speech. The vocal expression
(voice quality) is soft, breathy and lax (Marwick and Trevarthen,
U1
N
("")
>-3
fg
Fig. 1. Above: Full-term infants, Scotland. Left, intent regard of mother, 30 days; Right,
watching face, smile, vocalization and gesticulation, 35 days. Below: Dutch infant, 2
months, intent regard, smiling, gesticulations, vocalization, tonguing. (Photographs,
Saskia van Rees). z
~
1982). In return the infant becomes calm and attentive, focussing

intently as shown by a staring "knit-brow" expression with dropped
jaw (Oster, 1978, see Figure 1). Periodically the infant breaks
concentration to move with the mother or to emit brief (2 to 4
seconds) bursts of vocalization and gestural movements of the hands.
The tonguing movements which I have called 'prespeech', because they
resemble rudimentary articulatory appositions of tongue and/or lips
(Trevarthen, 1979b), have been shown by Sylvester-Bradley to be
coupled to gesture-like hand movements in which the hand is moved
high in front of the body (Sylvester-Bradley, 1980).
Mother's describe these utterance-like outbursts of infants as

'saying' or 'telling' and they make exclamatory or confirmatory
replies in their speech. They play with the effects of their imi-
tations of the infant's expressions and vocalizations and try to find
reasons for the infant refusing to communicate or turning away.
Well-sustained interactions are accurately described as 'conver-
sation-like' because the mother and infant exchange expressive ac-
tivity in brief alternating bursts, the mother speaking when the
infant pauses and the infant becoming expressive after attention to
the mother's speech.
The complexity of this behavior is illustrated in Figure 2 which

shows photographs taken from video screens in the course of an en-
gagement between a two-month old and mother that was entirely me-
diated by television (Trevarthen, Murray and Hubley, 1981). The
technique, devised by Lynne Murray to enable her to control presen-
tation of images of mother and infant, uses a partial mirror through
which a television camera observes the face of each subject while
this person sees a reflected image of a screen showing a full-size
color image of the other subject (Figure 2). We obtained good com-
munication in this double TV intercom apparatus which permits contact
between the persons by visual and auditory channels only. In fact,
the mother and infant shown were in separate rooms.
Murray's experiments test the affective regulation of the en-

gagement between mother and infant (Murray, 1980). She recorded the
behavior of both partners and then replayed samples of good positive
communication. When the mother's baby talk was replayed to the baby,
the latter started to react with smiles and positive vocalizations,
but within a few seconds became distressed and withdrawn, making
grimaces, avoiding gaze, wringing and sucking hands and ceasing
entirely to smile or coo (Figure 2). This proves that the contingent
responsiveness of the mother's behavior is essential to the mainten-
ance of a positive emotional state in the infant. When the infant
was replayed to the mother, without her knowledge, she perceived
something to be 'wrong' but did not identify what it was. She attri-
buted her failure to obtain responsive behavior to some defect of
interest or feeling in the baby, but felt to blame for this.
154 c. TREVARTHEN
,~J
.,
a CLOTH
SCRE EN
Fig. 2 Double-video communication, 2-month-old and mother. Video

images seen natural size and in colour. A. Normal, happy
interaction, smiling, cooing, tonguing and gesticulating
while turning away. !. Distressed grimace. wringing hands
with avoiding of eye contact, pout, when infant views a
replay of the mother's affectionate communication.
Murray also showed that a two-month-01d becomes distressed when

the mother who was communicating normally follows instructions to
immob1ize her face and simply look at her infant. As before, the
infant ceases to smile, avoids gaze while making brief 'paranoid'
glances to check the mother's expression, grimaces and makes more
self-touching movements with hands and mouth. If the mother is
simply interrupted by another adult speaking to her and engaging her
in conversation so she looks away from the baby, this causes the baby
to cease smiling and to make vocalizations as if to solicit her
attention, but the baby does not exhibit signs of distress.
It is clear from the new data on mother-infant interaction, most

of which has profited from microanalyses of film or video records,
that infants of two months or older can perceive mothers as providing
emotional support, directly. There is no reason to see the rapid
improvement in communication at a distance (that is by sight and
sound) at the close of the neonate period as a learned association of
the mother's expressive behavior with her feeding and other body
maintenance activities. Mothers see infants as beginning to express
affectionate feelings to them and as attempting to begin a speech-
-like behavior animated, as adult conversation is, by changing inten-
sity and quality of interpersonal feelings. These feelings are
expressed in vocal tone, vigor and tempo of body movement, hand
gestures and facial movements. The two month old reacts most inti-
mately and most positively to the mother, if she is the normal care-
taker. At this stage of development the relationship between infant
and mother is clearly the strongest one, except where a substitute
mother has developed the same kind of closeness and constancy of
interpersonal contact animated by a feeling of love. It is also
important to note that at two months the complexity of behaviors used
by infants to control face-to-face interactions with persons is far
greater than those they use to inspect inanimate objects. They do
not attempt to reach and grasp objects at this age.
DEVELOPMENT OF SELF-ACTIVATED AWARENESS OF OBJECTS AND OF GAMES WITH

THE MOTHER
After the third month, an infant is less willing than at two

months to sustain orientation to the mother's face when she places
herself close in front of her baby. This decline of face-inspection
and an increase in curiosity about the physical environment develop
at the same time as the infant starts to reach and grasp effectively
for objects (Figure 3).
Experiments on the tracking and operant responses of infants and

on their spontaneous perceptual preferences, indicate that there are
rapid changes at this age in the cognitive processes governing both
exploratory and performatory behaviors. Interesting results have been
obtained when infants are put into the control circuit of a servo-
156 c. TREVARTHEN
100r------------------,
A
100 r - - - - - - - - - - - - - - - - , C
E/ P
Vl
50
z
Q
Vl
Vl ,;_ _ _ _ _ J'
w
'" ..-
'"0
100
w
~ B
;:: r ,,
I R ,
0 I
,
, I
I
w I \ I
\)
~
50
.......:r. .\ / ,
\
I
I
Z
w
F
~
w
c..
ACE-
16 WEEKS 20 WEEKS
Fig. 3. Infant behaviours over the first year and mothers' responses,
from a longitudinal study, Edinburgh. A. Infants look at
mother's face (F) or hands (H) and look-away to explore or
manipulate (E/P) when the mother attempts face-to-face play.
Fig. 4. Mothers tease 36- to 41-week-olds with the ball. Top: Infant
smiles at reflection in camera window.
mechanism. Operant conditioning procedures require the subject to

generate a reward or punishment by executing a particular response.
Infants over two months rapidly learn to use limb and body movements
or sucking to control the occurrence of visual changes. In studies
of head turning Papousek (1969) found that three-or four-month-olds
will make many searching responses in an effort to control displays
of lights and that they often neglect the mild reward to watch for
the visual stimuli. Moreover, the success or failure of their pre-
dictions was reflected in facial expressions of positive or negative
affect (Papousek, 1967, 1969). Following a suggestion by Hunt (1965)
Fig. 3. (continued)
B. Looking at the mother's face (F), tracking (T) or reaching
(R) when the mother presents a ball. C. Mother's playfulness
with infant, face-to-face (Pch) and with suspended ball (Pb)
and mother's spontaneous presentation of nursery games (G).
Below: Girl at 16 weeks and 20 weeks avoiding mother to
explore the room, and reaching for a ball.
158 C. TREVARTHEN
that one could study motivation of infants by making their body

movements create stimulating effects, Watson (1977) observed the
behaviors of infants who were caused to switch on a motor-driven
mobile by movement of their head or limbs. Two-to three-month old
infants learned to regulate the feedback of 'activity' in the mobile,
and they expressed themselves pleased and excited with the effect by
smiling, cooing and waving their limbs about. Watson enunciated a
theory which intended to explain the development of all social ex-
changes in physical terms. He proposed that social partners auto-
matically trigger affective reactions which reward them by exciting a
mechanism in infants that is preset to any contingent reaction in the
environment. Any motion within a short time interval (of the order
of a quarter to a half second) of one's movement, is normally a
reliable signal of the response of another animate being to that
movement.
Watson's Contingency Theory cannot account for the emotional

signals of interpersonal communication which use a code of ex-
pressions to signal affect. Why should a smile signal happiness? As
we have seen, emotional signalling operates with the youngest
infants. Indeed, the experiments of Watson, like those of Papousek,
demonstrate how an infant with selective interest in an event that
responds to his own actions may become playful, expressing feelings
of enjoyment about the success of attempts to gain control of that
event, as if to communicate with the human agent behind it (cf.
Papousek, 1969).
In normal play between mother and infant, the increased autonomy

and independence of a three-to-four-month old that accompanies wider
interest in surroundings leads to a large transformation in the
mother's behavior. She becomes less soft or solicitous and more
vigorously playful. She enters into the infant's changed motives by
creating repetitions and marked reactions to infant expressions in
teasing games, and by carefully regulating her presentation of ob-
jects to trigger laughter while attracting interest.
When the mother presents herself to the baby for face-to-face

play, seeking eye-contact and smiling and talking, the infant over
four months of age increasingly manifests disinterested, avoiding or
even aggressive forms of behavior. The infant's affectionate smiling
and laughter in response to playful teasing is accompanied by evading
eye-contact with the mother, inattention to her quieter forms of
speech and withdrawing from her touch. This avoiding leads the
mother to use a more exciting, surprising or arousing way of speak-
ing, including many questions about what the baby is looking at or
listening to and appeals for interest in herself (Sylvester-Bradley
and Trevarthen, 1978). Negative behavior in the baby may cause the
mother to withdraw communication and just watch her infant, or she
may switch to a caretaking form of behavior to which the infant has
learned submission.
In games the mother tracks the accommodative effort and explor-

atory aim of her infant's behavior as she tries to present herself or
an object she holds in her hand in an interesting way. She seizes on
any sign of attention to her movements and especially responds to
expressions of pleasure by making further effort to gain mutual
attention. Again, active avoidance and expressions of irritation
give the infant powerful means of correcting any tendency the mother
may have to over-guidance or interference. (Sylvester-Bradley, 1981).
Although different mother-infant pairs vary widely in the bal-

ance of initiative and the sharing of experience and pleasure with
infants of this age, all tend to use ritual games of vocalizing and
moving that are repeated over and over again because they amuse the
baby. Musical or dance-like play appears to engage inherent affect-
ive and expressive motives in infants. It excites the infant to seek
mastery of both hearing and seeing rhythmically marked and repeating
patterns of signalling movement. We find that infants strongly
appreciate singing and hand dancing from three-to-four months onwards
and most mothers start to use this kind of play then (Hubley and
Trevarthen, 1979; Trevarthen, Murray and Hubley, 1981). The games
they play are discussed below (Figure 5).
Playful behavior becomes richer as the infant gains efficient

control of reaching and grasping and handling of objects in the fifth
month. At 10 weeks an object presented by the mother excites intent
visual and auditory interest and tracking. The infant may make
strenuous but futile attempts to grasp hold of the object and mouth
it. After the development of efficient reaching and grasping at 16
to 20 weeks, seizing an object which the mother is holding opens up a
versatile new channel of communication through which the mother can
either assist or playfully frustrate infant motives in a game (Fig-
ure 4).
When able to reach and grasp, the baby may grab the mother's
body, pulling or pinching her nose, mouth or hair and the act may be
gentle, accompanied by smiling and laughter or be forceful and ag-
gressive with a 'hard' expression (frown and forward set jaw).
Infant play behavior often combines positive affection and aggressive
attack as does play of young carnivores or monkeys (Aldis, 1975).
Both mother and infant use eye contact and 'smiling' to invite the
other to take part in what becomes a dynamic balance of approach and
avoidance. Happy play appears to reinforce the affectionate re-
lationship between the mother and her infant, while permitting var-
iety in practice of complying with or resisting initiatives.
We find enduring differences in the affective quality of play

between mother and infant, as well as differences in willingness of
the mother to allow the infant to explore objects by themselves and
differences in the way she presents objects. Interviews with mothers
reveal different attitudes, but all but very distressed mothers
0\
+- + +
+-.-.-. +- + .+- o
, ~ b ~ ~ ,tJ'"
.- E g "'fJ 0::' ~ ;; . , ." 0
0:" .~ ."
o o
~
oC"~Q)
0 _ I) _~ 1..0
.. ..,
0, J: J:
+_.L .+_ . L + + l. l .. L_ +
A Jet. _
~luuLA."""" MICROPHONE
<:
~ I
"l> I "
"l> .. 0.
.) ~ , ." 0 C .. o Q. ~.s .,
..,c ;;"
~ " ." .) " ."
. 0
...." e }! .f:1 .- <:"l> 0
. ..,
o " ..c 0 ,-0 0:; _ .... 0'" .<:
,: I .)
co ,0
~ J: CJ
"'" '"
>-3
2 3 4 5 6 7 8 9 10 11 12 13 14 15 sec gg
Fig. 5. Girl, 20 weeks, playing with mother. A. Mother strokes right hand of infant, 'walks' up ~
arm and tickles to a traditional rhyme~ Long vocal sounds (dash) with stress (arrow), ~
gj
and short connecting sounds (dot) in regular temporal pattern. Infant's reaction shown z
in photograph. ~. Mother chants while infant moves fingers over mother's open palm.
acknowledge the wilfulness and humour of their infants' behaviors.

They regard them as autonomous individuals. When infants develop a
strong appetite for putting objects in the mouth and explore with
lips and tongue, this may become a bone of contention with the mother
and a stimulus to many prohibitives in her speech. Mothers differ
considerably in their permissiveness and correspondingly in the
frequency with which they use opposive actions, expressions and
speech in interactions with their infants while the latter handle
objects. We have evidence for social class differences in the way
British mothers apply control, and differences between British and
Nigerian mothers. We are making a detailed study of these differ-
ences and attempting to relate these to accepted ways of negotiating
cooperation and play in the mother's society.
From the third month the infant gains more marked and more
varied facial expressions as well as a richer variety of vocaliz-
ations. Positive vocalizations develop into babbling as motor skills
for articulation of well-voiced utterances mature. At the same time
variation from moment to moment in the configuration of the vocal
apparatus of larynx and mouth cavity is controlled with increasing
reliability to express interpersonal feelings. There is, as yet, no
systematic description of varieties of voice expression in infant
utterances that accompany play. A variety of communicative motives,
or feelings about actions, are expressed in systematic changes of
pitch contour, loudness and voice quality by six months.
The mother's speech to her infant reflects the changes we have

described in her play. Whereas maternal talk to a newborn or two-
-month old is gentle and sympathetic with relaxed voicing and with
content 'mirroring' the baby's feelings, that of an older infant is
more vigorous, with moments of high tension or intensity. There is a
much wider range of voicing features and these are expressive of
stronger more marked and more rapidly changing interpersonal feelings
(Marwick and Trevarthen, 1982). The utterances become more complex
in linguistic form as well as more staccato in delivery. They in-
volve use of exclamation to stimulate, surprise or recall excitement
while they use variation of pitch, loudness and quality to convey
emotional effects of a demonstrative or theatrical kind.
The interest of the infant in often repeated rituals of the

mother's presentation of herself or of objects she is holding, with
fine tuning of movements to follow the infant's reactions and rep-
etition of sounds in crescendo to a sudden change of emphasis aimed
to excite amusement, is reflected in the use of a certain type of
nursery rhyme after the infant is three months of age (Figure 5).
Dance-like movements (e.g., bouncing the baby or the hands), nonsense
chanting (ah boo, ah boo, ah boo boo boo) and singing of action songs
(Round and round the garden like a teddy bear, Hickory-dickory-dock,
the mouse ran up the clock, Clappa clappa handies, Hoppe, Hoppe,
Reiter) begin at this period. Infants may imitate both dance-like
162 C. TREVARTHEN
movements and song-like vocalizations from at least as early as six
months.
In attempting to explain these universal forms of communication

by mothers with infants of a particular age we are led to the con-
clusion that they must be based on innate characteristics of motiv-
ation in the baby that are becoming apparent to mothers then. We
recall that behavior of infants is strongly rhythmic or pulsing as if
under control of an internal 'clock' (Trevarthen, 1974b; Trevarthen,
Murray and Hubley, 1981). Apparently main cadences in motor coor-
dination (particularly in the range 2-4/second) are inherently set at
a level that corresponds with common beats in music. The same fre-
quencies are strongly and clearly marked int he songs mothers sing to
their babies. Infants characteristically move in bursts of a few
vigorously alternating limb displacements. Furthermore, infants of
this playful age will spontaneously vary the excitement in their
vocalizations. They play with covalization like they play with touch
and visual effects caused by hand movements, or explore banging,
rattling or scraping objects in the hands - activities which Piaget
called 'Secondary Circular Reactions' (Piaget, 1953). The songs and
chants mothers sing reflect all these features of the spontaneous
play of infants. Thus, in a sense, mothers teach schemata for play
that the infants may borrow for their enjoyment over and over again.
We observe that six month olds show an increasing interest in

the mother's hands and they will often reach to handle an object just
touched by the mother (Hubley and Trevarthen, 1979). It appears that
awareness of their own hands acting on objects gives them also an
awareness of other's hands as organs that perform voluntary acts.
Such an awareness of the equivalence of 'self' and 'other' for hands
would be analogous to the perception of equivalence between actions
of another's face and the infant's own expressive face movements.
From six months, deliberate imitation of face expressions,
vocalizations and hand movements may be seen.
THE RELATION OF GAME PLAYING IN THE FAMILY TO WARINESS WITH STRANGERS
The above account of spontaneous play is based on preliminary

findings of a longitudinal study of 16 mother-infant pairs in
Edinburgh. Comparative observations of 21 subjects pairs in Lagos,
Nigeria have been made in collaboration with Professor A. C. Mundy-
Castle. Our main conclusion is that infants over three months of age
characteristically learn to engage closely with the excitement and
action of games which develop in the next few months as part of ha-
bitual communication in a close affectionate companionship with the
mother. Scottish and Nigerian subjects were essentially the same
though Nigerian mothers used more vigorous and rhythmical movements
which excited more face regard with infants over four months of age.
Our subjects were also observed to play in a similar way with other
familiar persons who liked to play with the baby. Fathers, siblings,
uncles and aunts, grandparents or family friends could replace the
mother though their play could be different. During this period most
of the infants we studied showed increasing mistrust of a stranger
who sat down in front of them and attempted to talk to them in a
friendly way for a few minutes. A friendly stranger may succeed to
play with a six month old and keep the baby happy, but the game is
not so certain as those that develop with a familiar person. Often
the infant withdraws or cries (Figure 6).
The reaction of infants to strangers has been regarded as a

consequence of learning of schemas for perceptual recognition of
familiar persons, and the development of an 'object concept' and a
'self image'. The fear behavior is taken as a measure of the kind of
attachment between infant and mother, reflecting the style of "-
mothering". Our longitudinal observations and comparisons between
different mother-infant pairs in a variety of situations have brought
out evidence that many infants become more fearful when left alone
with a stranger and less willing to play with them at the same time
as they enter upon a more subtle and more intimate form of dependence
on the mother's games. Even secure, hitherto sociable infants,
showing every sign of healthy development in both cognitive and
affective areas, may be frightened by a friendly stranger as soon as
Fig. 6. Left: Fear and crying with stranger; boy above, girl below,
40 weeks. Right: Girl, 41 weeks, expresses suspicion with a
stranger, then cries angrily when her mother returns.
164 c. TREVARTHEN
they are left with him or her. The child's reaction is one of watch-
ful doubt or sadness, with insecure frowning, avoidance of gaze and
self-directed or nervous behaviors (e.g., handling own clothes,
scratching at surfaces, placing hands on head or in front of the
face). (Figure 6). After confronting a stranger with fear, infants
may greet the mother with angry distress on her return.
The two-to-five-month olds in our sample were more likely to

smile at a stranger and show little fear, at least at the beginning
of their meetings. Most showed increased fearfulness between six
months and one year, though the eight-month-olds we filmed avoided
negative emotions to a considerable degree by transferring their
interest to the room and to nearby objects. There were some remark-
able spontaneous attempts to engate strangers in games that had been
practised with parents, as if the child was trying to perceive the
stranger as a friend who would know how to play. These play attempts
were usually insecure and incomplete. Sometimes they appeared to be
in the nature of 'displacement activities' (Tinbergen, 1952).
The age at which suspicion of strangers appears in relation to

the development of game playing with the mother leads us to conclude
that the stranger is feared primarily because he does not understand
'familiar' rituals and ways of joking. He threatens the infant's
newly found confidence in performances that can be shared. I con-
sider the evidence to favor the view that strangers are immediately
perceived as threatening whatever they do. The one-year-old infant
lacks a universally useful common code or lexicon for communicating
about himself and about familiar objects to anyone. With the family
he can communicate by means of mutually recognized family-specific
expressions and actions. Video tapes made in the homes of subjects
revealed that fathers, aunts and uncles, siblings or grandparents
were often contributing significantly to this intimate form of com-
munication with favorite games that are often repeated.
When the whole of the first year of an infant's development is

observed several changes to less confident, more temperamental
periods and then recovery to cheerful self-confidence at a higher
functional level may be detected (Trevarthen, 1982b). They suggest
that infants pass through phases when their 'ego' structure and
personal self, as well as their dependence on affective support from
familiar others, is more fragile. Infant psychiatrists dealing with
hospitalized or bereaved infants, and pediatricians who face many
babies of different ages as strangers, report such changes, a period
of insecurity being noted to be common between six and twelve months.
We believe that this 'critical phase' is related to a major positive
development in cooperative awareness which takes place in mother-
-infant communication after nine months. Infants show other signs
that they are developing greater self-awareness at this stage.
DEVELOPMENT OF SELF-CONSCIOUSNESS
The participation of a six-month-old infant in a learned game

ritual which we have described involves mother and infant in mutual
awareness of many kinds of behavior. Purposes or feelings behind
movements of different parts of the mother's body have to be per-
ceived by the infant, presentations and witholdings of objects have
to be anticipated, and the significance of complex changes of ex-
pression in face and voice has to be deciphered. Infants show elab-
orate feelings and intentions clearly at this age. Out of the mixing
of attentions and intentions to objects on the one hand, and to
persons on the other, babies appear to gain an ability to create
teasing, self-consciously artificial, even deceitful, mannerisms.
They frequently make 'performances' aimed away from the mother, but
exciting her amusement and affection and responding to her. These
performances often appear to originate in mimicry, but it may be
difficult to know if the exaggerated expressive behaviors (e.g.,
scowling, wrinkling the nose, closing the eyes tight, blowing ras-
berries, making exaggerated vocalizations or strange gestures) were
originated first by the mother or by the infant, because the mothers
often imitate comical acts of their infants.
The self-consciousness or awareness of an observed self in these

kinds of playful display or 'joking' is revealed when they appear
spontaneously in the situation where the mother obeys instructions to
withold reactions and to sit still looking at her infant. When an
infant acts up with elaborate postures, gestures, facial display and
vocalizations into this 'communication vacuum', while looking away
from the mother (Figure 7) then looks at her as if to see the effect,
this is a self-presenting 'performance'. The effect on the mother is
often to cause her to laugh, in spite of her attempts not to do so.
Explorations by infants of their own image in the mirror appear to
begin about the same time. Amsterdam (1972) reports infants to show
self-conscious behavior in front of a mirror at nine months.
Such playful expressiveness in games is in marked contrast to

the serious manner of the same infant concentrating on looking about
or handling an object. Exploratory attending is usually linked with
looking away from the mother's face and possibly with deliberate
non-compliance in requests to share experience or to make a joint
performance. Mothers may interfere to break the infant's involvement
with object exploration, usually giving some moral or protective
reason, e.g., that the child should not put an object in its mouth,
or should attend when spoken to. There may be an aggressive con-
frontation in which the child shows anger (Figure 8).
If the mother tries to fit in with the baby's awareness and

actions on an object, she may steer the performance in a particular
direction, but before about 40 weeks the infant complies only by
accommodating to the mother's actions. There is rarely any sign that
166 C. TREVARTHEN
Fig. 7. Teasing and joking. Top line: Comical face and smile while
watching own reflection; mother required to keep her face
immobile. Nine months. Second line: Comical face to
reflection and to mother while playing with a toy. Nine
months. Third line: Touching mother's tongue and laughing at
her. Twelve months. Bottom line: Joining in a 'dance' and
peering at own reflection. Twelve months.
Fig. 8. Mother attempts to stop boy of 36 weeks putting wooden doll

in his mouth. Later he responds to same interference with
growl and severe stare which intimidates his mother.
the infant has voluntarily grasped her purpose and attempted to add a
matching or complementary act (Hubley and Trevarthen, 1979). Again,
a six-month-old will reach and grasp for a preferred object or one
placed on a surface in front of it. But the baby will not hand over
an object to the mother in compliance with her 'asking' and holding
out her hand. For this to occur a new form of awareness which re-
presents the mother as a partner in use of objects must develop.
THE BEGINNING OF COOPERATION IN TASKS AND OF UTTERANCES AND GESTURES

TO COMMUNICATE ABOUT THE PHYSICAL SITUATION
Hubley (Hubley and Trevarthen, 1979) has shown that the reluct-
ance or inability to comply with instructions concerning object use
described above changes at about 40 weeks after birth at which age
the infant develops a positive interest or willingness to take part
in the task which the mother is presenting. We confirm Hubley's
findings (Figure 9) and we observe that this age-related change has a
marked effect on the way the mother speaks to her child.
Mothers of infants whose infants are beginning to comply with

instructions about object use tend to greatly increase instructions
or directives delivered in a matter of fact tone of voice (Figure 9)
and to decrease their questioning, commenting and exclaiming about
the infant's play. This change in the distribution of functions in
the mother's speech towards the end of the first year appears to be
an adaptation to changing communicative imagination and motivation in
the child (Marwick and Trevarthen, 1982). It is comparable with
changing adaptations of 'baby talk' which Sylvester-Bradley and
Trevarthen (1978) described for younger infants who are developing
exploratory and manipulative interests and gaining a sense of game
playing. Both these changes occur in a majority of cases when the
infant is at a particular age. Therefore, the change is conditional
168 C. TREVARTHEN
upon some development in the infant that causes the mother to change
her behavior. The change in the mother's attitude evidently facili-
tates development of cooperative awareness, but it does not cause it.
Awareness of communication in infants over nine months of age is

shown not only in a greatly increased receptivity to maternal direc-
tives, but also in the infant's production of vocalizations to com-
municate about a change in awareness or to express a particular
purpose. These vocalizations are made like comments and they are
often incorporated in a conversational exchange by the mother. There
is a clear increase at one year in speech-like utterances that are
supported by appropriate facial expressions and gestures. These,
according to Halliday (1974) constitute 'acts of meaning' in 'proto-
language'.
The utterances in our recordings are made by infants to signal

interest, state of mind, or intention for the mother's attention or
to direct her intentions in a particular way. Different communi-
cation functions have different prosody or intonation. At the same
age imitations of marked forms of speech (e.g., counting, question-
ing, onomatopaeic sound play) show an increase in awareness of word-
-like sounds and the infant may begin to show comprehension of the
reference of a few words such as 'dada', 'plug', (of the bath),
'duck' or 'fish' (toys) and some personal names, all frequently
uttered by adults talking to the baby.
It would appear that the one-year-old infant has gained not only
some awareness of words, but a conception of sharing in a task and a
willingness to engage in exchange of language-like messages or in
constructive acts that have been chosen by the mother as part of a
task to be done. Awareness of her communicative potential has been
transformed in the infant, and this causes the change in her speech.
As with the behavior of mothers in game playing, individual

mothers may differ considerably in the way they adapt to the infant's
developing awareness of a joint task. Where infants develop cooper-
ative participation in a task late, mothers are late to adapt direc-
tive speech forms, continuing to question or comment on the infant's
self-directed behavior. We find indications that there are relation-
ships between a mother's instructive technique when her baby is
one-year-old and the constructs she uses to describe her personal
relationship in a Repertory Grid Test carried out a year later when
the infant was two (Marwick, Calam and Trevarthen, 1982). Further-
more, the personality of the mother shows relationship to the child's
development of language in the second year. We therefore conclude
that the mutual interpersonal adaptation between mother and infant,
while being changed by developments in the infant's communicative and
cognitive powers, is also affected by the mother's long term social
adaptations. The outcome will, of course, be affected further by
relationships to other persons in the life of both mother and infant,
but we have obtained little data on these other personal factors.
%
40
30
PERCENTAGE OF
ILLOCUTIONARY
ACTS OR
COMPLIANCE 20
.... ", J
••••••
... ....
; '-- ____ ATTRACT
10
•••••• STATEMENT
•••••• .. • .. OUESTION
16 24 32 40
AGE IN WEEKS
Fig. 9. When infants comply with instructions to put wooden dolls in

a truck, the mothers' speech changes. Questions and
attracting utterances decline, statements give way to
commands.
DEVELOPMENT OF CONVERSATION AROUND COOPERATIVE PLAY WITH

REPRESENTATIONAL OBJECTS IN THE SECOND AND THIRD YEARS
By one year an infant can follow a mother's directives in per-

forming a familiar task or in using an object. Understanding of
speech has begun and the infant makes utterances and gestures that
are coordinated with the attentions of the mother. In the second
year this communication of 'acts of meaning' to influence one
another's consciousness and intentions becomes both richer and more
efficient. The child's use of words to represent familiar shared
ideas is fitted into an already existing skill for signalling aware-
ness of a shared reality.
Television recordings we have made of our 16 Scottish infants at

play in the presence of the mothers at 19, 24 and 36 months of age
170 C. TREVARTHEN
show the development of awareness of conventional topics. We gave

our subjects a box of toys representing a person, an animal, a ve-
hicle and household tools (cot with mattress, cover and pillow, hair
brush, two cups, saucers, knives, plates, forks and spoons, a milk
jug, teapot, bath with sponge and towel, miniature baby bottle,
tip-up truck, female doll with removable clothes, fluffy dog) and
left mother and child to organize play for 10 minutes. The mother
was seated next to a low table in front of a concealed camera.
The 19-month-olds recognized many of the objects and performed

appropriate single acts spontaneously (Brushing hair of self, mother,
doll or dog with the brush, putting the doll in the chair or in the
bath). They also took suggestions from the mother, listening to her
and clearly understanding some words without looking at her face or
gestures. Sometimes they refused her suggestions, though appearing
to comprehend. They were at times self-absorbed and much of the play
was 'sensori-motor', i.e., using the objects to create some stimulat-
ing effect (e.g., sound making, accompanied with vocal action noises
having no relation to the 'proper' use of the object). However, the
ability to cooperate seen at one year with the same infants was much
stronger and the mother had more success in giving directives for
single acts. Objects were less frequently banged or mouthed. The
babies' play represented a disjointed, fussy succession of single
acts, suddenly dropped for another act, repeated with slight vari-
ation, occasionally irrelevant or without clear sense (using a baby
bottle as a 'tool' on the wheels of the truck).
When we compared this play with meaningful objects to that with

strange and unfamiliar objects, we found infants less enthusiastic
and happy with the latter and inclined to turn to the mother for
help. She showed and explained. With the meaningful objects mothers
joined in sound play and infants imitated their noises. This is a
continuation of nonsense chants and singing of the first year.
The infants' utterances were rarely clear words, but the proto-
language was fluent with well-controlled intonation, pitch contour,
loudness, prosody and quality variations to convey intended communi-
cations. Many gestures, attitudes and facial expressions were made
indicating the direction of interest, excitement, serious concen-
tration, amusement, imitation, etc. In this communication the
mother's familiar presence and her habitual forms of communication
were clearly important. The infant was incapable of this level of
inventiveness and enjoyment in the presence of another adult.
At two years the same infants were using, besides nonsense

sounds, many one or two word utterances, labelling objects shown to
the mother, labelling intentions, varifying or denying questions
asked by mother about what the child is doing and referring back to
objects previously played with. They behaved in a more systematic
way than six months previously, concentrating more and spending more
time on a given item. With the mother's help the child carried out
consecutive steps in a task (putting doll to bed, then feeding it,
taking clothes off doll to bath it, sitting the doll or dog in the
chair and brushing its hair). Often the child seeks approval from
the mother for his/her own ideas and listens well to the mother's
speech which is more elaborate and clearly very well comprehended. A
conversation may develop around a continuous sequence of actions with
the objects. Their interrogations concern the relation of the things
present to things known habitually. Thus the recognition of conven-
tional objects with meaning is enriched by the labelling of a more
comprehensive language with many verbal contributions from the child.
The mother tracks the child's intentions and recognitions,

sharing mastery of a conventional reality as one and a half years ago
she shared interest in the comings and goings of objects and in games
of expression and manipulation.
At three years, the child has made such strides in language that
genuine dialogue accompanies the play with toys. Many references are
made to absent persons, situations and experiences. There is richer
imagination about the intentions brought to life in speech and mean-
ingful actions. The efficiency of this communication is greatly
supported by the mother's comprehension of imperfectly pronounced
words, incomplete sentences, references to items of mutual habitual
knowledge. Some of the child's language is playful, inventive and
baffling to the mother. The mother may deliberately, and sometimes
facetiously, use language far above the child's comprehension, making
allusions for her own entertainment.
The cooperativeness of the play is greatly enhanced by dis-

cussions of what each will do. They negotiate roles and assign tasks
with rich invention, e.g., giving a meal to the dog.
Mother: Now where's this hot potato? (not present)

Child In the cooker (not present)
There is a much more lively awareness in the child of the poten-

tialities of the environment for 'story telling' and for jokes, with
highly cooperative use of invention, e.g.
Mother: Where is my coffee?

Child: We don't have coffee. We've got tea (not present)
Will you have coffee?
Mother: No, I'll have tea, thank you.
Discussions often digress:
Mother: Are you reading?

Child: No I can't read. Are you good at reading?
Mother: Yes, sort of.
172 c. TREVARTHEN
They talk about the taxi ride to the laboratory, father at work,
home, the other room.
In short, the three year old, while enjoying a versatile aware-

ness of the uses of the objects provided, and an inventive imagin-
ation, also has awareness of the mother's consciousness and individu-
ality of knowledge, intention and feeling. The child's self is
situated verbally with the familiar other and with situations they
share actually or habitually. The mother's speech relies on this
awareness of the child. It is rapid, conversational, with wide
vocabulary. She is clearly very confident of achieving immediate
comprehension of some abstract concepts and she easily corrects for
failure of the child's comprehension.
When we asked the mother to teach three new games ('Snap!' with
picture cards and 'Hide and Find', a red wooden top being hidden in
one hand while both hands were held behind the back) and to present a
simple Piagetian conservation of number task, the children joined
enthusiastically with the games the mother was trying to teach them
and showed much willingness to learn the 'rules' of behavior which
are appropriate. The conservation task, although still concentrated
upon, does not offer the same scope for mutual enjoyment. One child
managed the task perfectly, and the rest were seen to vary in per-
formance despite some ingenious presentations of the task by their
mothers. One infant summed up her position succinctly when during
the task she turned to her mother and said with revealing introspec-
tion, 'I can't do this; I'm too young to do this'.
The speaking child we have just described is fluently involved

not only in language, but also in the sharing of a highly contrived
world. The enthusiastic play we observe is carried on by the instan-
taneous recognition of meanings inherent in objects that can be made
to do things for the child and for the communication with the mother.
Finally, the child, as well as the mother, expects to be cooperating
and conversing about the experience.
There is much in this behavior in the children of 19 to 36

months that is absent form that of the one year old. Nevertheless,
there are also remarkable similarities. The non-verbal shape of
utterances, orientations, manipulative actions, mutual attentions,
expressions of feeling and of attitude to one another, negotiations
of intentions, sharing of interest and actions with respect to ob-
jects, these are all much the same. Furthermore both kinds of com-
munication share the same quality of intimacy. Just as a one year
old is wary of a stranger and awkward in play and quiet, if not
distressed, so a three year old is less inventive, less confident,
less talkative with an unknown person.
CONCLUSIONS
I have described significant changes in the communicative behav-

ior of infants and mothers through infancy to the toddler stage where
language and reasoning of the child are closely integrated with, and
to a large degree dependent on, the mental processes of the adult.
The facts support the claim that inherent abilities to perceive a
human presence and to reflect feelings and purposes exist in infants.
They seem to possess perceptual and motor structures that are pre-
adapted to engage with human expressive behavior at all levels,
including speech and gesture. Awareness of objects appears to develop
within a preestablished awareness of what others do with objects.
Thus infants are aware of the cultural value of things before they
can talk about them.
The relationship with the mother we have seen is built step by

step on a foundation of interpersonal awareness that becomes highly
active within a few weeks of birth and regulated by expressions of
emotions. A six or eight-week-old even shows rudimentary forms of
the speech and gesture with which the three year old makes his mental
processes highly specific in communication with the mother. The
joint or reflective interest in intentional impulses, orientation to
objects and self-other-presentation which becomes enriched in the
middle months of the first year with the guiding influence of the
sense of humour is still essential to negotiations in conversation.
Even the temporal organization of an affectionate teasing game played
by a mother with her six month old may be similar to that of typical
conversational play at three years, though the affective coloring may
be more subdued as the two share thoughts through the medium of
speech.
Obviously all these functions benefit from learning of specific

instances and specific, arbitrary signs. Nevertheless, the consist-
ent regulation of human interaction by emotional processes that
function only at an intimate interpersonal level, as well as the
age-related changes in use of communication, both indicate that the
human brain contains a built in person-recognizing component. Unfor-
tunately our knowledge of what this component could be like in ana-
tomical location or functional design is virtually non-existent.
ACKNOWLEDGEMENTS
Research on which this article is based has been funded by the

Social Science Research Council of the U.K. and by the Spencer Foun-
dation. The study of Lagos infants was made possible by the support
of the University of Lagos to my colleague, Professor A. C. Mundy-
Castle, and the Spencer Foundation.
174 C. TREVARTHEN
POSTCRIPT: A TRIBUTE TO COMENIUS
Comenius, John Amos Komensky, the first modern educator, de-

manded training for every human being, because he or she is a human
being gifted to be taught. He claimed that, from birth to adulthood,
laws of nature govern the growth of the mind as well as the body.
The natural playful enjoyment of the child should guide the educator
to the best course and speed of instruction. At the mother's breast,
at play with peers, exercising the senses to appreciate a real world
while speaking about it to others in the mother tongue and then, only
after the first decade, fit to enjoy such abstractions as the rules
of Latin grammar, the child's growing mind determines what is needed
from a teacher.
Over 300 years ago, in 'The School of the Mother's Breast'

(Schola Materni Gremii), he wrote: "My aim is to show, although this
is not generally attended to, that the roots of all sciences and arts
in every instance arise as early as in the tender age, and that on
these foundations it is neither impossible nor difficult for the
whole superstructure to be laid, provided always that we act reason-
ably with a reasonable creature."
The recent history of infant psychology would suggest that we

are still struggling to achieve some approximation to Comenius'
insightful view of the nature of human learning.
Quotations from works of Comenius after "Essays on Educational

Reformers" by R.H. Quick. Longmans Green & Co., London, 1910.
REFERENCES
Aldis, O. 1975, Play Fighting, New York: Academic Press.

Alegria, J. and Noirot, E. 1978, "Neonate orientation behavior
towards the human voice", International Journal of Behavior
Development, 1: 291-312.
Amsterdam, B. 1972, "mirror self-image reactions before age two".
Developmental Psychology, 5: 297-305.
Bower, T. G. R. 1974, Development in Infancy, Freeman, San Francisco.
Condon, W. S., and Sander, L. W. 1974, "Neonate movement is syn-
chronized with adult speech: interactional participation and
language acquisition". Science, 183: 99-101.
Darwin, C. 1872, The Expression of Emotions in Animals and Man.
Methuen, London.
Fraiberg, S. 1980, Clinical Studies in Infant Mental Health: The
First Year of Life. Tavistock, London.
Halliday, M. A. K. 1975, Learning How to Mean: Explorations in the
Development of Language. Arnold, London.
Hubley, P. and Trevarthen, C. 1979, "Sharing a task in infancy", in:

Social Interaction During Infancy, New Directions for Child
Development, I. Uzgiris, ed., 4: 57-80.
Hunt, J. McV. 1965, "Intrinsic motivation and its role in psycho-
logical development", in: Nebraska Symposium on Motivation,
D. Levine, ed., pp. 189-282. University of Nebraska Press,
Lincoln.
Klaus, M., and Kennell, J. 1976, Maternal Infant Bonding. Mosby, St
Louis.
Maratos, O. 1973, The Origins and Development of Imitation in the
First Six Months of Life. Ph.D. thesis, University of Geneva.
Marton, P., Minde, K. and Ogilvie, J. 1981. "Mother-infant inter-
actions and the preterm nursery: A sequential analysis". in:
Preterm Birth and Psychological Development, S. Friedman and
M. Sigman, eds., Academic Press, New York. pp. 179-205.
Marwick, H., Calam, R., and Trevarthen, C. 1982. Significant
dimensions of personality in mothers of two year olds. (In
preparation) .
Marwick, H. and Trevarthen, C. 1982, Adaptation of vocal expression
in mother's speech to infants. (In preparation).
Meltzoff, A. N., and Moore, M. H. 1977, "Imitation of facial and
manual gestures by human neonates". Science, 198: 75-78.
Murray, L. 1980. The Sensitivities and Expressive Capacities of
Young Infants in Communication with their Mothers. Ph.D.
thesis, University of Edinburgh.
Oster, H. 1978. "Facial expression and affect development". in: The
Development of Affect, M. Lewis and L. A. Rosenblum, eds.,
Plenum Press, New York. pp. 43-75.
Papousek, H. 1967, "Experimental studies of appetitional behavior in
human newborns and infants" in: Early Behavior Comparative and
Developmental Approaches, H. W. Stevenson, E. H. Hess and H.
R. Rheingold, eds., John Wiley and Sons, New York, pp. 249-
277.
Papousek, H. 1969, "Individual differences in learned responses in
human infants", in: Brain and Early Behavior, R. J. Robinson,
ed., Academic Press, London and New York, pp. 251-263.
Parmelee, A. H. 1981, "Auditory function and neurological maturation
in preterm infants", in: Preterm Birth and Psychological
Development, S. Freidman and M. Sigman, eds, Academic Press,
New York, pp. 127-150.
Piaget, J. 1953, The Origins of Intelligence in the Child, Routledge
and Kegan Paul, London.
Piaget, J. 1970, "Piaget's Theory", in: Carmichael's Manual of Child
Psychology, P. H. Mussen, ed.-,-John Wiley and Sons, New York.
pp. 703-732.
Spence, M. J. and DeCasper, A. J., 1982, "Human fetuses perceive
maternal speech" Paper delivered at the International Confer-
ence on Infant Studies, Austin, Texas, March 1982.
Sylvester-Bradley, B. 1980, A Study of Young Infants as Social
Beings. Ph.D. thesis, University of Edinburgh.
176 C. TREVARTHEN
Sylvester-Bradley, B. 1981. "Negativity in early infant-adult

exchanges and its developmental significance", in: Communi-
cation in Development, P. Robinson, ed., Academic Press,
London. pp. 1-37.
Sylvester-Bradley, B. and Trevarthen, C. 1978, "Baby talk as an
adaptation to the infant's communication", in: The Development
of Communication, N. Waterson and C. Snow ,-ed., John Wiley
and Sons, New York. pp. 75-92.
Tinbergen, N. 1952, '''Derived activities', their causation,
biological significance, origin and emancipation during evol-
ution". Quarterly Review of Biology, 27: 1-32.
Trevarthen, C. 1974a, "Conversations with a two-month-old". New
Scientist, 2 May, 230-235.
Trevarthen, C. 1974b, "The psychobiology of speech development", in:
Language and Brain: Developmental Aspects Neurosciences Re-
search Program Bulletin, E. H. Lenneberg, ed., Neurosciences
Research Program, Boston. 12: 570-585.
Trevarthen, C. 1979a, "Neuroembryology and the development of
perception", in: Human Growth: A Comprehensive Treatise, Vol.
III. F. Falkner and J. M. Tanner, eds, Plenum, New York.
Trevarthen, C. 1979b, "Communication and cooperation in early
infancy: A description of primary intersubjectivity", in:
Before Speech: The Beginnings of Human Communication,
M.Bullowa, ed., Cambridge University Press, London.
Trevarthen, C. 1980a, "Neurological development and the growth of
psychological functions". in: Developmental Psychology and
Society, J. Sants, ed., Macmillans, London.
Trevarthen, C. 1980b "The foundations of intersubjectivity:
development of interpersonal and cooperative understanding in
infants", in: The Social Foundations of Language and Thought:
Essays in Honor of J. S. Bruner. D. Olson, ed., W. W. Norton,
New York.
Trevarthen, C. 1982a, "Basic patterns of psychenetic change in
infancy", in: Dips in Learning. T. Bever, ed., N. J. Erlbaum,
Hillsdale.--(In press).
Trevarthen, C. 1982b "Primary motives for cooperative understanding",
in: Social Cognition: Studies in the Development of Under-
standing. G. Butterworth and P. Light, eds., Harvester Press,
London. pp. 77-109.
Trevarthen, C., Murray, L., and Hubley, P. 1981, "Psychology of
infants". in: Scientific Foundations of Clinical Paediatrics.
J. Davis and J. Dobbing, eds., William Heinemann Medical
Books, London. (second edition).
Tronick, E., Als, H., and Brazelton, T. B. 1979, Early development of
neonatal and infant behavior, in: Human Growth: A Comprehen-
sive Treatise, vol. III, F. Falkner and J.M. Tanner, eds.,
Plenum, New York.
Watson, J. S. 1977, "Perception of contingency as a determinant of
social responsiveness", in: Origins of the Infant's Social
Responsiveness. E. B. Thoman, ed., Erlbaum, Hillsdale, N.J.
PATTERNS OF PARENT-CHILD INTERACTION IN A
CROSS-CULTURAL PERSPECTIVE
Irenaus Eibl-Eibesfeldt
Max Plank Institute

Seewiesen
W. Germany
The patterns of parenting, in particular early mother-child

interaction, have been a focal point of interest for psychoanalysts,
anthropologists and psychologists, who all agree that early in child-
hood the foundation is laid for the development of personality
traits.
In particular the experiences in early childhood are of utmost

importance. However the extent to which experiences on the one hand,
and maturational processes on the other, determine the behavior of
the child is open to dispute. Much speculation exists. Thus it was
argued that birth is experienced by the baby as a trauma, influencing
later conduct. Others suggested that the baby's bond to his mother
resulted from simple conditioning. The child would learn that his
mother fulfilled his needs for food and comfort, extend his self love
to the love for the breasts, and finally generalize these feelings,
becoming bonded to his mother.
Parental dominance, toilet training, repression of children's

sexual behavior, and other features of an "authoritarian" education
were thought to be responsible for personality traits like greed
aggression and other egotistic behavior. As a consequence, the
monopoly of the family in early childhood education was considered
problematical, since it was believed to be one of the reasons for the
rift between private and public values. Reformers, therefore, pro-
moted models of collective education as alternatives to family
education. The child, in order to grow into a responsible member of
society was to be freed trom parental authority and repression by
communal rearing and education.
These propositions were based on the assumption that man's

nature was totally malleable, and that there was no reason to take
177
178 I. EIBL-EIBESFELDT
human nature into consideration, until Bowlby (1958, 1969) and Spitz
(1965) pointed out certain needs of the child which had to be ful-
filled if he was to develop a healthy personality. In particular a
reference person should be available to allow the child to bond with.
Only in such a relation, they argued, could the child develop the
basic trust which constitutes the cornerstone of any healthy person-
ality. They pointed to the fact that hospitalized children, who were
deprived of the opportunity to establish such an intimate personal
relationship, experienced serious distortions in the development of
their personality.
Bowlby (1969) and Ainsworth (1969, 1973) elaborated the thesis

that babies are born with a bias for discriminatory bonding, which
they named "monotropy". They argued that mother and child are bio-
logically fitted to form a dyad, by means of a phylogenetically
evolved signalling code, amongst other mechanisms. This "biological
attachment theory" has stimulated research, and, since then, many
students of human behavior have ventured into objective studies of
the mother-child relationship (Hassenstein 1973, Stern 1977, Papousek
and Papousek 1977, Trewarthen 1979 and Keller 1980). Comparatively
little recent work, however, has been done on a broader cross-
cultural basis. The previous studies (Mead 1930, Whiting 1963) are
strongly biased by cultural relativistic views. This often led to
hasty conclusions, such as when Mead argued using the Mundugumur as
an example, that deprivation of love and body contact breeds aggres-
sive traits (Mead 1939), whereas nursing at demand and ample body
contact creates peaceful friendly habits. The situation, however, is
certainly not as simple as that. The "fierce" Yanomami provide love
and body contact, feed their babies at demand, but nonetheless they
are aggressive and engage in warfare. The sam holds true for the
Masai and many other belligerent sheep-rearing tribes of Africa, as
well as for many of the neolithic horticulturalists of New Guinea.
In these cases we find that, through identification with the parent
model, the child readily accepts the cultural norms, regardless
whether or not they are pacifistic.
Thus two theories oppose each other, both serving as a basis for
educational experiments on a large scale. Environmentalists argue
that our form of family life is the result of economic developments,
involving the acquisition of property and accompanying rules of
inheritance. Prior life is assumed to have been structured on a
collective basis, representing the original state of man, which
accords to his nature. Children therefore should be liberated from
parental dominance in favor of collective education and grow up free
trom frustration. Guidelines for teaching in Hessian schools
recently went as far as to promote Wilhelm Reich's ideas on the need
for the sexual liberation of the child. Others consider these ideas
to be harmful and inadequate for the developmental stage of child-
hood. Furthermore they emphasize that there are also certain psycho-
logical needs of children and parents which must be taken into con-
sideration, in particular the fact that man is, by nature, a familial
being.
PATTERNS OF PARENT-CHILD INTERACTION 179
In the light of such a situation, we certainly need to take a

sober look at the parent-child relationship, to investigate whether
it is indeed flexible and open to unlimited environmental modifica-
tion, or to what extent phylogenetic adaptations, like those hypothe-
sized by Bowlby, make man predisposed to intimate parental bonds and
to age-specific strategies of education. Since cultures constitute
experiments in socialization practices, we should be able to find at
least some of the answers to these questions by examining cross-
cultural data.
My cross-cultural studies devote particular attention to the

patterns of parent-child interaction, and in the following pages, I
would like to present data relevant to the disputed issues of man's
familiality in contrast with his communality. How widespread is the
individualized mother-child bond? Is "Monotropy" fiction or fad? Do
universal patterns of mother-child interaction exist, which can be
considered as a shared phylogenetic heritage of Homo sapiens? In
this context I would like to elaborate on the question of whether
there are any needs of the children and parents which must be ful-
tilled, in order to avoid severe frustration and personality dis-
tortion.
A number of publications portray a child's life in tribal

society as very romantic, in contrast with that of a child in our own
society. Based on my data, I will endeavor to outline where their
intuition has guided them correctly, and where facts to do support
their views about "happy primitive childhood". Against the back-
ground of non-literate cultures we can indeed see that, with the
development of mass society, a number of changes have taken place,
which pose major, yet unsolved, problems.
My data are largely based upon an extensive film and sound

documentation of the Kalahari Bushmen (!ko, G/wi, !kung), the Eipo,
Biami, and Daribi, neolithic horticulturists of New Guinea, the
Yanomami of the upper Orinoko, the Himba, sheep-rearing tribes of the
Kaokoland, and the Balinese. In addition I have film samples from
the Walbiri and Pintubi (Australia), the Tasaday and several other
cultures.
THE MOTHER-CHILD BOND
Collective child rearing is occasionally reported to occur in

non-literate societies, and used to justify or even promote similar
practices in our society, with the aim to create citizens who are
loyal to society and lacking the family egotism so disturbing to the
minds of some political theoreticians. Margaret Mead (1939), amongst
others, emphasized that Samoan children were bonded to many people
and did not show a particularly strong emotional tie to their mother.
Yet while visiting the village of Saanapu on Upolo (Samoa), Derek
Freeman (1) read me the relevant passage in Mead's publication,
stating that there exists no strong emotional tie between mother and
child on Samoa, and, at the same time, he pointed at a crying toddler
who had to be held back from following his mother on her fishing
excursion. This separation protest is familiar to us in our society
and well-known to the Samoans as well. Thus, in Samoa too, the baby
singles out mother as the most favorite person, and indeed a strong
emotional tie exists between mother and child. Once Derek Freeman
had opened my eyes to the nontriviality of such a seemingly trivial
event, I kept them open and, so far, have encountered no culture in
which Bowlby's "monotropy" did not manifest itself. I might add that
the term monotropy is perhaps misleading, since a child can be bonded
to several reference persons in various degrees, especially his
father. But since the term is meant to describe the baby's unique
predisposition to bond primarily with his mother, it is adequate, as
long as one keeps in mind the fact that the baby bonds to other
people as well.
An observer in a "primitive" culture may indeed get the first

impression that a child is raised by the community and equally bonded
to all members, but this view will be corrected at closer scrutiny.
For example, I counted among the !ko Bushmen the number of contacts
tow babies had with persons different from their mother. The two
babies, who were approximately 8-10 months old, spent 47-49% of
day-time (morning until late afternoon) in bodily contact with the
mother. 26-30% of the time the babies played alone or slept alone,
and they spent the rest of the time (24%) with other persons. During
the total observation time (2) the baby No. 1 (a girl of approx-
imately 8 months) had 46 contacts with 29 persons other than her
mother and the baby No. 2 (a boy) had 98 contacts with 22 persons
other than his mother.
Children and adults of both sexes engaged in play with the

babies, carried them around and the babies seemed relaxed and happy.
However, as soon as a baby started whining, it was passed back to his
mother and certainly it sought its Mother's contact. In addition,
when a stranger approached, the mother was always the selected person
for retreat. Thus, among the !ko, despite the numerous relaxed
contacts with other group members, there exists a preferential
mother-child bond. Of all the cultures I know, the Bushmen come
closest to the idea of communal raising, yet a clear preference for
the mother as reference person was evident. She was the secure base
from which the child operated, and separation protest was an everyday
occurrence, whenever the mother went away and left the child with
others.
(1) Derek Freeman just informed me by letter that his book: "On
Coming of Age in Samo: The Nemesis of an Anthropolocical Myth", is
now in print at the Oxford University Press in New York.
(2) Baby No. 1 486 minutes, baby No. 2 542 minutes, both during
daylight hours.
Konner (1975) found that !kung babies, up to the age of 20

months spent a high percentage of their time in physical contact with
all persons including their mother, starting with about 80% of the
observation time at an age of 1-8 weeks, and gradually decreasing to
30-40%. On these contacts 70-80% were with their mother and 20-30%
with other persons. Of the latter, half were with children, and
girls, particularly siblings, had more contacts with babies than did
boys. Sisters showed great interest in baby siblings and were re-
sponsible for the majority of contacts a baby had with persons other
than their mother. Of the face-to-face contacts without physical
contact, 80% of all such contacts, during the flrst 13 weeks, were
with their mother, but this figure decreased to approximately 50% by
15-51 weeks, while face-to-face contacts with other persons, partic-
ularly with children, increased accordingly.
All the other non-literate cultures I studied were more family-

centered, with babies circulating less within the group, although
they too had many contacts with other selected members. A preferen-
tial mother-child bond was evident in all cultures studied by us so
far.
It is also interesting that experiments on communal child rear-

ing, like that in the kibbutz, take into consideration the child's
need to bond by encouraging long nursing by the mother and thus
ensuring extensive mother-child contact during the first year of life
(Liegle 1971, KohenRatz 1968). Only gradually, with the return of
the mothers to professional life during the second year, is the task
of child rearing transferred to the Metaplet, and mother-child
contact increasingly restricted to the play hours. This phase of
restricted periods of mother-child contact is a stressful experience
for both mother and child, particularly for the separation at night.
Even though in kibbutz the child finally has more contact with the
Metaplet than with its parents, the parent-child relation remains
emotionally distinct, as it can be observed from behavior at meeting
and separation time (Gewirtz u. Gewirtz 1965, 1968, Spiro 1966, Rabin
1965).
As we have seen above, then, the individualized bond between

mother and child seems to be of paramount importance in all societies
we have looked at so far, although it is embedded in a wide variety
of socialization practices. Let us now go on to examine which
mechanisms forming this bond exist cross-culturally and thus appear
to have a biological basis.
Mechanisms of bond formation
Interestingly enough, the mechanism of bond formation by mothers

has not been studied in detail. In fact we know more about what
triggers motherlove in sheep and goats than what triggers it in man.
For example, goats get individually attached to their newborn during

the five minute period immediately after birth. If the kid is left
with the mother for five minutes following birth and afterwards
separated, for one hour, the mother will accept it if the same kid is
returned, but she will reject any other. Should one however separate
the young immediately after birth and return it after one hour the
mother will not recognize it as her own, but will reject it as a
stranger. Evidently the mothers are sensitive to bond formation
during only a short period following birth. Thereafter they will not
accept any kid. Klopfer (1971) to who I refer, suggests a probable
mechanism for this sensitive period. When the young, during the
process of birthgiving, passes its mother's cervix, this triggers
oxytocine release. During the five minutes following birth this
hormone is broken down. Klopfer suggests that oxytocine induces the
readiness to bond with the newborn, a hypothesis which is supported
by the observation that the oxytocine reflex can be released in
virgin goats by mechanical extension of the cervix, and that this
results in readiness to accept any newborn presented during the
five-minute period following this experiment. This observation
however has been challenged recently.
Until recently clinical birth in Western societies did not allow

for intensive mother-child contact immediately after birth. The
mother, still under the influence of anaesthetics, is normally shown
the child, which is then taken away to a nursery for at least a few
hours. Only recently have doubts been raised as to whether this
procedure could afflict the mother-child bond, and, as consequence,
some studies have considered mother-child interaction immediately
after birthgiving (Klaus 1972). He and his coworkers have found that
if intensive contact is allowed, and provided that both mother and
child are not under the influence of any anaesthetics, intensive
interaction takes place, with the mothers taking the initiative.
(Klaus and Kennell 1970, 1976) (figure 1). If the mothers are given
the newborn immediately after birth, they respond with elated remarks
as if they thought the baby could understand. They caress and pat
the newborn and verbally invite it to look at them. "Look at me so
that I can see you love me" and utterances of similar content are
addressed to the baby, indicating the importance of eye contact for
the establishment of the bond. In turn, babies are programmed to
behave as if they can establish eyecontact.
Newborns are capable of turning their heads in the direction of

their mothers' voices and even though their vision is very poor at
this age, they behave as if they were looking, to their mothers'
great delight. Freedman (1964) demonstrated that even the blindborn
fixate on their speaking mother, evidently due to a centrally pro-
grammed fixation process, which constitutes part of the inherited
program evolved in the service of establishing contact with the
mother. Immediately after birth babies are quite active and in a
state of wakefulness. Their drive to suckle is very strong. Should
one deprive a baby of drinking, the next peak of equal sucking
strength will occur only 40 hours later!
Fig. 1. Immediately after birthgiving many mothers seem in an

elated mood addressing the baby verbally and responding to
the baby's reactions. The baby is quite active too, even
capable of pushing himself along by effective crawling
movements. This picture shows a mother interacting with
her newborn, which is still attached to the umbilical cord.
The afterbirth has not yet been discharged. The birth was
"natural" and occurred in Munich.
(From a 16mm film taken with 25 frames/so by Sigrid
Austen) .
Grossmann (1978) videotaped the behavior of 10 randomly selected

mothers during three feedings on three different days for half an
hour, each day during their postpartum stay in the hospital. When
the babies opened their eyes, a significant change in the behav.ior of
the mothers took place. In 92.5% of all cases, they showed more
lively facial expressions, spoke more to their baby, moved the infant
closer to their body. Vestibular stimulation of the baby dropped to
a lower level, which indicates that it serves to stimulate eye-
opening. In general, social behaviors of the mothers were twice as
intense after their babies' eyes opened as before.
If mother-child contact is allowed to occur immediately after

birth, the rate of touching and talking to the baby is significantly
higher during the following five days, than is the case in the frame-
work of the traditional hospital routine. But this effect wanes and
later no significant differences in the way mothers treat their
babies are found. Klaus and Kennell, who evidently expected cont-
inuing differences in the mother-child bond, sound a bit disappointed
as their results appear to support the opinion of those who consider
natural birth a romantic fad without real significance. However, I
think this is too hasty a conclusion and would promote the thesis
that mother-child contact immediately following natural birth has
promoted attachment in a critical phase of development in the past,
and thus might be still of great survival value, particularly for
children who were unwanted for socio-economic reasons. One could
investigate this matter among mothers who wish to give their babies
up for adoption, looking at what percentage of mothers, who deliver
by natural child birth with immediate mother-child contact after
birth, stick to their decision in comparison with mothers who deliver
according to the usual clinical routine. I would predict that more
of the former than the latter would change their minds. Although
bond formation is enhanced by immediate contact after natural child-
birth, the system appears to be flexible. The mere presence of a
baby will ensure the growth of strong maternal attachment even at a
much later stage and after prolonged mother-child separation. As is
the case with many biological systems in many other mammals, we have
a number of insurance mechanisms which back each other up in the
event of one failing. It is the initial acceptance of the child
which is assured by mother-child contact after birth. Should for
some clinical reasons such a contact not be possible, a strong bond
will nonetheless grow, but it will take more time to achieve equal
strength.
Little is known about mother-child interaction following birth

in tribal societies. SchiefenhBvel (personal communication) who has
documented nine cases of birth among the Eipo of Western New Guinea,
finds that contrary to our expectations, mothers show a bout of
affection only after the placenta is delivered. Then the umbilical
cord is severed and the baby raised to the breast. Before this time,
the baby may lie there for several minutes in front of the mother
who looks at it with comparatively few signs of emotion. This
delayed responsiveness might be a cultural adaptation to the practice
of infanticide, to which the Eipo resort for population control.
The delayed bonding lessens the conflict of the mother in case
infanticide must be practiced. (1).
Whereas the mother-child bond usually develops fast, the indi-

vidualized bond the child forms with his mother grows slowly during
the first months of life. The discrimination between mother and
others, however, occurs surprisingly early. One week old babies are
able to discriminate, by smell cloth impregnated with their mothers'
milk, from that of other mothers. In experiments they turn signifi-
(1) Mothers decide whether a child shall live or not. Healthy baby-
girls may be killed if the mother already has a girl. in such a case
she decides before birth. The baby then will be wrapped in fern
leaves and the parcel discarded in the bush. (see SchienfenhBvel, G.
and W. 1978).
cantly more often towards their mothers' smell (MacFarlane A. 1975),

Schaal in Coworrees, 1980). There are also indications of early
discrimination between their mothers' voices and those of others.
Visual discrimination, however, occurs much later. Still we can

say, that the child is programmed to form early individual attach-
ments. The longheld belief that the newborn is basically a
brainstem-being with a very limited potential for communication,
certainly needs to be revised, particularly in face of studies like
those of Trevarthen (1979).
Certainly the child is, from the start, programmed to communi-

cate and also to form early individual attachments (see also
Hassenstein 1973).
With the development of the individualized bond, the child

starts to discriminate in a very conspicuous way between mother and
strangers. This awareness of strangers, which often manifest itself
as "fear of strangers", is not al all an artifact of our culture.
We have found it to occur in all cultures studied so far (figure 2).
There are individual differences to be found, but certain ambivalence

between approach and withdrawal responses in the behavior of the
child is always evident. Furthermore it can be demonstrated that
negative experiences with strangers are not a prerequisite for the
fear response to occur, indicating that the responsiveness of the
baby to signals of a conspecific exists and matures as phylogenetic
adaptation, which conforms with observation on Rhesus monkeys
(Sackett 1966).
The mother-child bond is mutual. Both partners actively seek

proximity. Babies universally experience separation fears, as
indicated by crying, when left alone, and once they are capable of
locomotion, they seek their mothers whenever afraid. Furthermore
they defend their relationship to their mothers against rivals.
Sibling rivalry, for example, occurs in all societies even in those
such as the Bushmen and Yanomami (Eibl-Eibesfeldt 1974). Children
have to learn that bonds with their mother have to be shared with
siblings and they learn to share this bond less readily than they
learn to share objects. Since attachment is accompanied by strong
positive affection, threats to severe the bond can be used as a
weapon of defence in case of conflict. Babies are capable of using
cut off threats (figure 3) in case of conflict with their mother.
MOTOR PATTERNS OF AFFECTION AND CARETAKING; STRATEGIES OF MOTHER-

CHILD INTERACTION:
Patterns of Face-to-Face Interaction
I mentioned earlier that the newborn orients himself towards

the mother's voice, turning his face towards the source of sound and
a)
b)
Fig. 2. The response of stranger awareness in a G/wi baby girl

(Bushmen, Central Kalahari). In response to eye contact with
a stranger the baby shows pattern of contact readiness and
contact avoidance.
c)
d)
Fig. 2 (cont.) The patterns sometimes superimpose each other but also
alternation can be observed.
(From a film sequence taken with 25 frames/s by the
author).
visually fixating, even before he has good visual abilities. Reflec-
toric smiling also occurs in the newborn, and mothers respond to
these signals as if they were signs of affection, interpreting these
and many other utterances as acts of intended communication, comment-
ing and answering them and stimulating further utterances. Later in
the baby's life the mother will respond largely to vocal and finally
to verbal utterances. According to Stern, (1977) two types of inter-
action occur from the start, which he labelled coaction and alterna-
tion. During coaction both mother and children engage in the same
type of activity, while during alternation both take turns as in a
dialogue. Stern emphasizes that the latter does not derive from the
former, but rather that both patterns exist simultaneously from early
age. Coaction occurs when both mother and baby are having fun in
play and thus are strongly emotionally engaged. It demonstrates
unity and, in this respect, it appears also in adult rituals such as
love-duetting in opera, hymns, march music and other activities
(Stern 1977). Alternation is characteristic for situations in which
the mother instructs. I would add, however, that it can also be
another from of demonstrating unity comparable to the antiphonic
duetting which bonds birds.
When mothers start dialogues with their babies, they orient

their faces in such a way as to put themselves in the visual field of
the baby, which (at an early age) is approximately 25cm from the
baby's face (Papousek and Papousek 1979) and perform a very interest-
ing "greeting". Once face-to-face orientation is established, they
lift their heads with jerking movements, raise their eyebrows and
then lower their head towards the baby smiling and talking, often
with mock-expressions of naive surprise. The entire pattern is often
repeated in a rhythmic fashion. It occurs in many cultures as a
typical way in which mothers and fathers start interaction and keep
them going (figure 4,5). It occurs also cross-culturally - in greet-
ing situations among adults in the form of more rapid movements - the
headtoss and the eyebrowflash (Eibl-Eibesfeldt 1968, 1971). Movement
patterns for interaction with babies, while similar in form, are thus
slowed down and exaggerated, probably in response to babies' percep-
tive capacities. 1 have also observed that adults of other cultures
often address us with slowed-down and amplified signals, evidently in
attempts to make themselves better understood. In origin, the
pattern is a response of happy surprise upon seeing someone a person
likes.
When both mothers and fathers speak to their babies their voices
change and the intonation level becomes raised approximately one
octave (figure 6,7,8,9). Mothers talk higher, in a softer voice and
with simpler vocabulary than in ordinary speech: in other words, in
baby-talk. Ferguson (1964) found the same principal patterns of
baby talk in five European cultures. I can add that even in cultures
as remote from our own as the Eipo, Himba or Yanomami, mothers engage
in this sort of baby talk. The subject is presently being investi-
gated by R. Eggbrecht.
a)
b)
Fig. 3. Babies already employ early in life certain strategies of

social interaction.
(a) Here a Yanomami baby boy (upper Orinoco) appeals for
contact.
(b) He protests, since his mother does not pay attention
to him, and touches the mother but she refuses contact.
c)
d)
Fig. 3 (cont.) (c) When she finally shows readiness to accept him, he
responds with a clear cut off. Then he will continue to
protest and finally will allow his mother to take him.
(From a l6mm film taken by the author with 2S frames/s.)
Fig • 4. Young Eipo woman (West New Guinea) addressing a baby with
a smile and an eyebrow flash in typical face-to-face
orientation. This will be followed by verbalization and
face-to-face contact. (Film sequence taken by the author
with 25 frames/s.)
By tactile, visual, vestibular and acoustic stimulation -

lifting, shaking, tickling - mothers try to release eye contact vocal-
ization and smiling in their babies (figure 10). They perceive
smiling as a reward and try to get it. Smiling in response to eye-
contact is the strongest reward, and mothers of blind-born babies
experience initial trouble in coordinating their stimuli and babies'
responses, since smiling often fails to occur at the right moment.
As often the babies show initiative for contact (figure 11). Robson
(1967) pointed out the fact that the young child has little to give,
except for patterns like smile, which are the sole reward for the
mothers' investment. Smiling is a universal pattern and it serves
everywhere to appease and bond. It matures even in the deaf and
blind born (Eibl-Eibesfeldt 1973).
Several forms of face-to-face contact occur. (Examples in

Eibl-Eibesfeldt 1972, 1976). Mothers often press and rub their
foreheads against the foreheads of their babies. In addition forms
of nose-rubbing exist, which are probably derived from friendly
sniffing, since mother inhale during this process. People in some
cultures refer to nose-rubbing as "sniffing kiss".
Fig. 5. !Ko-Bushman addressing a toddler with eyebrow flash and

face-to-face contact.
(From a 16mm film of the author).
Touching babies' faces and bodies with the lips is a universal

practice. It may take the form of a blowkiss, during which the lips
are pressed against the baby's body, and air is blown out causing a
sensation of vibration which babies like. The blow kiss has to be
distinguished from the simple kiss, during which the lips, after
being pressed against the body of the baby, part with a smack. It
is highly probable that this latter pattern is derived from maternal
mouth to mouth feeding, since a sequence of intermediate patterns,
going from mouth-to-mouth feeding to kiss, can be found. This may
be illustrated by the following series of photographs, taken among
the !Ko Bushmen, the Himba and the Yanomami (figure 12, 13). It can
be seen from these sequences that one partner always acts as donor,
shoving morsels into his partner's mouth by tongue movements, while
his partner opens his mouth in a sort of gaping response. The
partners may take turns, and they demonstrate this donor-receiver
pattern even when no morsels are passed.
WA IKA : MAN--CH ILD

8T NS
• ~ '1 "". 2000 Hz
==- 1000 .....

--......~ 1.--
...... -
WAlKA : MAN--OOG
BT NS
- 2000
~ttI- IOOO
- 200 Hz
EIPO : CHILD- - BABY

BT NS
~~I
~tltl
- 2000
..;A, ~ ,',
t' I~ r--, - 1000 t",
,...
"".''''.
° Hz - - --
- ~ .,.
Fig. 6-8.Examples for baby talk (BT) and normal speaking (NS),
Top: Yanomami male (upper Orinoko) addressing a baby
(BT) and normal speech (NS).
Middle: Yanomami male addressing a dog (BT) and normal
speech (NS).
Bottom: Eipo (West Newguinea) child (girl) addressing a
baby (BS) and her normal speech (NS).
The sound spectrographs were made by R. Eggebrecht from
tapes taken by the author.
GERMANY CAMEROON NEW GUINEA

BRAZIL EIPO
KALAHAR I
OCTA
5
4
HALF-1 3
TONES 2
1
NS ----4 n.89 n=17 n=10 n=19 n=14
Fig. 9. The difference between normal speaking and baby talk in five
cultures. The sound level is raised by about one octave.
From a published work from R. Eggebrecht.
I may add that kissing and kiss feeding as expressions of

friendly affection are known to occur in chimpanzees, gorillas and
orang-utans (Lawick-Goodall 19/5, Blitz 1943). There are also cul-
tural differences in the way mothers fondle their babies. Fondling
of the babies' genitalia is widely practiced. Among the Yanomami,
for example, mothers and fathers alike blowkiss, lick or manually
rub the vaginal orifice of baby girls and stroke the scrotum of boys
or mouth his penis until the age of three. In the Kalahari Bushmen
and less often in the Eipo, I observed similar behavior. In many
parts of New Guinea a form of greeting is derived from this ex-
pression of affection. During affectionate greeting older women, but
sometimes also men caress the scrotal region of the greeted partner
with a gentle stroking movement of the hand (Eibl-Eibesfeldt 1977).
This follows the general principle that partners derived from parent-
ing are often used as a means of expressing affection among adults.
Hugging, Patting, Caressing
I know of no culture where mothers do not hug, pat and caress

their babies. During hugging, children are held and gently pressed
against their mothers' chests. This is frequently done to comfort a
baby in distress. In such a case, comforting verbal utterances will
accompany hugging, while the mother pats and strokes the baby. The
basic pattern of the adult embrace seems to have its roots in this
infant hugging. Hugging should not be confused with clasping, which
Fig. 10. In a great variety of ways mothers initiate interactions

with their babies. Here a Himba mother (Koakoland,
Namibia) initiates interactions by blowing at her baby's
face, with leads to playful interactions.
(From a 16mm film taken by the author with 25 frames/s).
is the response of the baby who seeks to hold his mother. The baby's
hands, in this case, seek a firm hold and grasp. It is a protection-
seeking response and occurs in man and non-human primates as self-
clasping during spells of lonely despair.
Fig. 11. Babies in turn often take the initiative in establishing

contact and again by a variety of means. Here a Tboli-Blit
baby (Mindanao Philippines) seeks the attention of the
father by biting him in his shoulder. A face-to-face
interaction with kiss follows. Typical is the babies
gaping response, which is adaptive during kiss-feeding.
(From a 16mm film taken by the author).
Fig. 12. Kiss feeding in the !Ko Bushmen: a young woman kiss feeding
her baby-halfsister to comfort her. The baby responds with
acceptive gaping, the woman pushes with her tongue a small
piece of melon in the babies mouth.
(From a 16mm film taken by the author with 50 frames/s).
Maternal Responses to Crying
Contrary to a widespread opinion, children and babies do cry

frequently in nonliterate societies in which mothers provide ample
body contact and nurse on demand. In these societies babies exper-
ience frustrations and afflictions as well. A child may fall, lose
a quarrel with a sibling, seek the attention of his or her occupied
mother, and depending on the situation, the child cries with despair,
pain or anger. The response of the mother varies culturally and
individually from simple irritation and anger to sympathy. Yanomami
mothers, when pestered by crying babies or toddlers, can get very
angry and slap the baby on its back with the palms of their hands,
with empty banana shells, or may even hit them with pieces of fire-
wood. These anger fits never last long, however, and the mother will
finally respond by taking the baby to the breast for comfort.
Crying triggers the milk flow reflex and elicits parental

response, whether it acts as a releaser arousing sympathy, or whether
it is simply so irritating that caretakers do their best to switch
the signal off, as has been recently discussed by Murray (1979), is
an open question. Both in fact happen. Newborn respond to tapes of
crying by crying, girls being more responsive than boys (Simmer 1971,
Sagi and Hoffmann 1976). The distress response to another's distress
Fig. 13. Yanomami girl kiss feeding her baby sister with saliva.
(From a film sequence taken by the author with 25 frames/s.)
occurs in babies who are only 34 hours old, and is probably innate.
It is in fact an expression of "sympathy" in its earliest manifesta-
tion. Individuals have a crying pattern which is universal. It is
composed of an expiratory sound of .6 - 1.4 seconds, followed by a
pause of .2 seconds, then an inspiratory whistle of .1 - .2 seconds
duration, a pause of .2 sec. and again an expiratory sound. The
fundamental frequency is 400 Hz beginning with 300-350 (.2 sec.)
rising to 500 for .2 sec. and dropping to 300 or 200 for .2 sec. The
utterance is loud, 80 decibels at 30cm from the mouth. Hunger, pain,
and birth cries are variations on a basic theme, signalling differ-
ences in experienced discomfort. A rising and falling melody was
found to be associated with hunger cries, any melody other than a
rising and falling one with a length of more than 1.5 sec. associated
with pain, and a similar one with shorter intervals with birth. The
basic pattern is recognizable in different cultures, but cultural
styles also occur. Caudill and Weinstein (1969) found pronounced
differences in the crying Japanese and American babies at the age of
Fig. 14. While drinking, babies manipulate the free breast with one
hand. Top: !Ko-Bushmen Bottom: Himba (Photographs by the
author).
three months. Experiments with Japanese and European mothers during

their postpartem stay in the hospital revealed that mothers are
capable of recognizing their babies individually (Morsbach 1980,
Morsbach and Bunting 1979). Mothers in different cultures respond
with different delay. In Western cultures the delay is 5-30 minutes
Fig. 15-16. The different ways of carrying a baby.

!Ko Bushwoman carrying her baby with support of
an antelope skin. Photographs by the author.
(Bernal 1972, Brazelton 1962) during the first 10 days of a baby's

life. To respond faster is considered bad since it is assumed that
it spoils the baby and teaches him to complain. Children in our
culture cry 1-2 3-4 hours per day. The bushmen in contrast respond
with little delay to a baby's crying and put it to their breast. The
same holds true for the Eipo, Himba and Yanomami. If the baby does.
not stop crying, mothers can show signs of irritation and even anger.
I observed Yanomami mothers slapping their crying babies, and leaving
them crying on the ground in distress for 15 minutes. Crying does
arouse a mixture of sympathy and irritation. Pathological forms of
crying like the "cri du chat" or the crying of premature children are
experienced as particularly irritating, and children with such defec-
tive signals including visual appearance, are more prone to be
victims of child abuse (Zeskind and Lester 1978, Frodi and Lamb 1978,
Frodi et al., 1978a, 1978b).
Fig. 17. Yanomami girl carrying two children. The younger

rests already in the sling, the older is held on
his arm over her shoulder. He will be carried by
help of the sling too. Photographs by the author.
Nursing and Weaning
In the Yanomami, Eipo, Himba and Bushmen nursing is done at

request, except when the mother is very occupied with a specific
task. If a person plays with a baby or carries him around and he
starts to get restless and whimpers, the person immediately passes
the baby over to his mother. The subsequent drinking spells are
often very short - a minute or even less - but frequent. Wguke
drinking, the child tends to grasp the free nipple with one hand
squeezing and caressing it (figure 14). When the opportunity is
provided, our children will do the same and it could be a way to keep
the free breast occupied, and thus prevent others from drinking.
Babies are indeed very defensive against any rivals attempting to
drink. Occasionally I saw a Yanomami or Bushmen mother, while baby-
sitting, offering the free breast to the guest. This worked when her
own baby slept at the breast, or when it was still quite young. In
older babies it released often violent responses from her own baby.
If the intervals between births are long, weaning is a gradual

process. The baby gets pr2masticated food in addition to breast milk
from about six months on. He will be allowed to drink, however,
until the next sibling is conceived or born, whether he be three,
four or five years old, and he will be allowed to find comfort at
his mother's breasts even when they are already dry. It is the
favorite form of comfort for small children in distress. When a
sibling is born and the older is still nursing, weaning occurs
abruptly and traumatic consequences. In such cases the older may
show clear signs of hostility towards his younger sibling. This
period of weaning is the time of highest child mortality. Often the
child is taken over by a relative.
Carrying, Handling, Grooming and Cleaning
In all societies we have studied, babies and toddlers are always

attended. If they are already able to crawl and walk, they may play
in the vicinity of the mother or some other relative. They will
often get picked up and carried around in an expression of affection.
A baby is thus a focus of attention of the small communities. When
mother goes on collecting or gardening excursions, they often carry
their babies with them. Occasionally they may leave them for one or
two hours to a babysitter, a grandparent, aunt or other close rela-
tive. There are numerous ways of carrying babies (figure. 15-17):
The Eipo carry babies in nets on their backs. Older babies, which
can sit up, ride on mothers' shoulders or on top of their backload.
A tuft of hair on the mother's otherwise shaven, head provides the
child a firm hold. Bushmen carry their babies in a leather-kaross
or sling on their back or hip. The Tasaday carry them on their hips
without any support. The Yanomami support their babies by a sling
of bark either on their back or front, supporting the baby with one
hand. When carried in front, the babies are generally placed on the
left side as mothers need their right hand free for work. Often
mothers carry their babies in some way while working in the house-
hold, either to keep their babies from interfering with their activi-
ties, or to protect them from getting hurt, for instance, by the
fire.
When observing mothers in other cultures, one is often struck

by the apparent roughness with which they handle them. Babies are
lifted by one arm and swung on the shoulder. While being carried in
a sling or leather bag on the mother's back, the head of small babies
is sometimes flopping in a way appalling to us, but without any
apparent harmful consequences for the child.
There is great variation in amount of carrying from culture to

culture. Among the bushmen babies are carried everywhere by their
mothers. This may contribute significantly to birth control, since

frequent regular sucking appears to be responsible for the persis-
tence of amenorrhea during lactation, due to a hormonal reflex system
(Konner 1980). The sucking stimulus causes prolactin secretion which
in turn suppresses ovulation. Indeed the mean birth interval in the
"kung Bushmen is 39,8 months, in contrast to the shorter birth inter-
val of Australian aboriginal women in Arnhem land, who leave their
children in camp with babysitters while out gathering in the field.
To compensate for these short intervals, infanticide rates higher.
!kung mothers, as Lee (1979) page 279, puts it, carry their contra-
ceptive on their hips!
In the gardens where mothers often put their babies to the

ground while working contact is kept by mutual vocalization.
Babies are often passed on from one person to the other to be

carried for a while, relieving the mothers. Upon being passed over,
the baby is first held in such a way that his face is oriented to the
receiver's face, and is greeted in a kind of ritual with a headtoss,
eyebrow-flash or nod accompanied by a smile, friendly words and often
a kiss. When it is passed back to the mother, the baby is kissed or
patted as a farewell.
Play Dialogues
Mother and baby engage in a number of games, which appear to be

universally enjoyed. One favorite game, which I have observed in all
cultures visited, is one of approach and withdrawal or "peek-a-booh"
games. The mother suddenly moves her face towards the baby as if
intending to bite. She may even also make a mock-attack with other
tactile stimulation, for example tickling. Babies show clear flight
reactions (withdrawal, hiding), but at the same time enjoy these
games immensely. In games which involve getting caught, they squeal
and laugh with pleasure. There seems to be a strong motivation for
flight in man, which finds its cathartic outlet in such games,
and, later in life, we use other adventures to get similar stimula-
tion.
Another type of game takes the form of playful dialogues. A

baby passes an object to its mother, the mother accepts it and then
holds it out to the baby to be taken again. This sequence is repeated
as a sort of playful ritual of bonding, during which the initiative
often comes from the baby. It is surprising to see the readiness
with which the baby parts from an object in interaction with a refer-
ence person. This is not as trivial as it may seem at first glance,
as in order to allow a smooth passage of objects in such a dialogue
to occur, both giver and receiver must be programmed for coordinated
action. The person giving must somehow "Know" that the partner will
receive, and he must let go of the object the moment the other has
Fig. 18 !Ko baby (Bushmen, Central Kalahari) offering a woman (not

her mother!)' a piece of bark and thus initiating contact.
She takes it, kisses the gift and starts a playful inter-
action. (Film taken by the author with 50 frames/s.)
taken hold. In order for the partner to let go, the receiver must
act in a way as to express respect for the norm of possession, that
is, he should not try to take the object away before it is released.
The majority of infrahuman primates is evidently not capable of
passing on objects with the hand. A baboon, who wants an object from
another baboon, will simply make a threat face and try to grab and
run away. Situations of giving in most mammals and birds are re-
stricted to very specific situations of parental feeding and court-
ship, although chimpanzees and gorillas can pass on objects in the
manner described above.
Babies enjoy giving and taking dialogues with objects of food,

that is, they enjoy mutual feeding carried out in a symbolic way,
during which the food is often not eaten, but rather passed forth and
back. The babies offer the object to their partner's mouth. This
suggests that one root may be ritualized feeding derived from paren-
tal behavior, as may be the sharing of large prey in chimpanzees and
man. I have discussed this subject more thoroughly elsewhere (Eibl-
Eibesfeldt 1979a, 1973).
Contact-Initiatives of the Child-Pointing, Showing and

Exploratory Aggression
In his wakeful state the child is full of initiative, actively

seeking dialogue with its mother, to the degree that it becomes a
nuisance even to the exceptionally patient mothers in tribal societ-
ies. One universal gesture, by which babies and toddlers invite
contact, is through pointing at an object and uttering vocalizations.
We even possess a special muscle for pointing: Musculus levator
indici. Nonhuman primates do not point as we do with the index
finger extended, although chimpanzees may extend their hand in the
direction of some object or event, apparently with the intent to
guide attention. Human babies do not only point, but they also
understand pointing, that is, they follow visually the extended
finger to the directed object. If mothers do not respond to point-
ing, the baby may slap the mother and point again, and if mothers
respond by pointing, a dialogue might develop or even a play with
the object. But more often the objects just served as a mediator
and the baby loses interest once it gets the mother's attention.
As mediators in social interactions, objects certainly playa

decisive role already very early in life. Babies and toddlers offer
objects, or just point at them as a shared object of reference to
start an interaction (figure 18). Both strategies can be observed
throughout life. Objects serve as gifts to bond, or as object of
reference to provide a neutral platform for meeting. The English
term "conversation piece" illustrates this point.
Babies and toddlers also initiate contact in aggressive ways,

for example by poking with the index finger hitting, throwing
objects, taking away objects, or other means of disturbing interfer-
ence (figure 19). Although one may be inclined to view such acts as
expressions of the child's general activity, they are, however, a
specific strategy which the child employs to explore his social
Fig. 19 Explor atory aggres sion: a bushman toddle r (!Ko) hittin g

his
father playfu lly with a stick. Observ e the expres sive
"playf ace" (relax ed open mouth displa y). At this age the
boy
is allowe d to act this way, actual ly the expres sion of
the
mother in the backgr ound indica tes her pleasu re. Later
how-
ever he will be admon ished and thus learn what is allowe
d
and what not. Photog raph by the author .
enviro nment. Explor atory aggres sion contin ues to be of

paramo unt
import ance throug h adulth ood. By aggres sive acts, the
child inquir es
how far it can go, and what is consid ered good and bad
behav ior. It
is an active proces s of inform ation seekin g and the child
expect s to
get answer s. If an answer is not provid ed, explor atory
aggres sion
tends to escala te (Eibl- Eibesf eldt 1978b) . It is one of
the greate st
misund erstand ing of permis sive educat ion not to have realiz
ed its
functi onal aspect . By explor atory aggres sion the child
learns the
values and norms of its specif ic cultur e and this knowle
dge provid es
securi ty, since it makes the behavi or of the other predic
table.
Explor atory aggres sion contin ues to serve this functi on
for the
juveni le and growin g adult. Here again it is often misund
erstood as
rebell ion, wherea s in realit y it is a form of inquir y,
of experi men-
tal testin g out how far one can go. This inquir y needs
to be an-
swered in time, otherw ise escala tion occurs . Answers provid
ed at the
right time need not be repres sive, since they fill the
desire s and
expec tation s of those questi oning. Explor atory aggres sion
is also
employ ed by govern ments of newly formed states , to find
out what is
permit ted and what is not in intern ationa l relatio ns.
Recent histor y
has provid ed numerous examp les of what happen s when an
answer is not
given at the right time.
Early Socialization - Punishment and Reward
In a recent publication I discussed this subject in more detail

(Eibl-Eibesfeldt 1979c), so I will only deal with it briefly here.
The way in which mothers respond to babies who misbehave varies from
culture to culture. Kalahari San mothers behave very tolerantly.
In one of my films documentating sibling in the !kung, one sees how a
mother patiently endeavors to distract aggressive brothers, who are
engaged in robbing each other of objects, scratching, kicking and
hitting. With one hand she forms a barrier to keep the opponents
apart while trying to distract them in various ways. So far I have
not seen any severe corporal punishment of a baby or toddler by a San
woman, an observation supported by Draper (1976). Occasionally an
irritated mother may scold or even slap a child upon impluse, but go
no farther. In contrast, enangered Yanomami mothers may club a baby
with a piece of firewood, or slap it etc. while punishing it as men-
tioned earlier. Thus, in contrast to the Bushmen who fear violence,
the Yanomami train for immediate retaliation for every offense, and
this training starts early in life. It should not misguide us,
however, into thinking that Yanomami are less loving mothers, as
Bushmen mothers frequently make bitter complaints about their child-
ren, while the children are present.
Deprivation of love in another punitive measure. It takes

various forms of expressive cutoffs, including the verbal threat that
the baby may be abandoned to a stranger. Toddlers may be rejected
this way, and left on their own for a few minutes up to a quarter of
an hour. Usually nursing, grooming or other comforting activities by
the mother follow. Reward for good manners is not explicitly pro-
vided, but rather in friendly interaction.
Toilet training is part of the normal educational routine, even

in tribal cultures. Once a child is able to walk, it is expected to
move outside the living-area. In the bushmen, Eipo and Yanomami
children learn this with ease, particularly since clothing is no
problem. If they fail to do this, they get scolded. Nothing can be
observed which would back the psychoanalytical speculations about
feces and possessions, and the development of possessive traits in
connections with the act of defecation and toilet training (1).
The Father in the Baby's World
For a long time fathers were a forgotten subject in psychology.

Possibly because the subject of father-child interaction is more
(1) The emphasis early psychoanalysis has put upon toilet training,
and its importance for the development of character traits of the
adult is expressed in their terminology. To characterize the phase
where a baby starts to acquire language, walks, explores his environ-
ment as the "anal phase" is, to put it mildly, grotesque.
difficult to investigate than that of mother-child interaction.

This is due to great variation in timing of onset of extensive
fatherchild contact, and intensiveness from culture to culture. as
the father must not fulfill such basic functions as nursing the child
during the first years.
Furthermore the role of the father for the early development of

the child was considered of little importance. Thus Margret Mead
once wrote " .... fathers are a biological necessity, but a social
accident".
In the meanwhile a number of publications served to correct this

view (Biller 1971, Lamb 1976, Konner 1979, Clarke-Stewart 1978, Klaus
and Kennell 1976, Parke 1979). In our Western culture fathers
involvement is less in regular caretaking (nursing, cleaning) than in
playing with their children instead. Pederson and Robson (1969) in
interviewing mothers of nine-month-old babies found that fathers were
available 26 hours per week of the babies' awake periods. Of these
they spent in the average 8 hours a week interacting playfully.
While mothers certainly spent more absolute time in playing with
their children, fathers spent a greater percentage of their time with
this type of interaction (Kotelchuck 1976). Boys are preferred to
girls by fathers in our culture, and sex typing and sexrole socializa-
tion start from early babyhood. Babies show differential attachment
to fathers and mothers. Mothers are less often frowed at (5.3%) by
two-month-old babies than fathers (7.8%) or strangers (28.2%) (Yogman
et.al., 1977). Under stressful situations, like in an unfamiliar
environment, mothers are preferred as the secure basis by the 12 to
18 months old. For two year old children both parents function alike
(Lamb 1976). At home, infants aged 7-8 months showed, in the
presence of a stranger, preference for the father over the mother, as
indicated by more frequent displays of affiliative behavior (smile,
look, laugh, vocalize), but no differences in attachment behavior
(fuss, proximity, reach) were evident. Fathers play an important
role in the cognitive development of the child, particularly in early
childhood (references in Parke 1979).
Participation of the father appears to vary greatly from society

to society, although, in all, the father indeed plays an important
role in the emotional development of the child. They express tender-
ness for their babies, regardless of sex. However, there are strik-
ing differences in the amount of time spent in friendly interaction
with babies between mothers and fathers among the Eipo, fathers pick
up their babies at the women's area and carry it to the men's area,
where the baby remains for half and hour or so, getting friendly
attention from other boys and men. While working in gardens, fathers
engage in short bouts of friendly contact with their babies, and do
so again in the evening, before retiring to the man's or family house
(figure 20). In the Yanomami, fathers take their babies into the
hammock in the morning and after, returning from gardening or hunt-
Fig. 20 Eipo father playing with his little son.

(From a 16mm film taken by the author).
ing. Bushmen behaved similarly, though less restricted to certain

times of the day. All in all men may spend up to an hour per day
with their babies, sometimes less (!kung), fathers have relatively
frequent contact with their babies, particularly with baby boys, and
of all types of contact, body as well as vocal, contacts with
fathers, up to the ages of 99 weeks, make up 13.7% of all contacts
(West and Konner 1976) .
It is often said, that distanced paternity is correlated with

the father's need to educate children to warriors (Whiting and
Whiting 1975, see also West and Konner 1969). This simple casual
relationship does not exist.
The Eipo, as well as the Himba and Yanomami demonstrate strong

paternal affection, as expressed by caressing, fondling, hugging and
kissing small babies, engaging with them in rough and tumble play and
the like. Even though the periods of interaction between father and
child are generally short; they are nonetheless of great importance
for the children, who prize them very much. Both baby boys and girls
show expressions of delight when with their fathers. Fathers engage
more in rough and tumble play with their children than do mothers,
although in other cases they exhibit a similar repertory of affec-
tionate behavior, as described above for mothers. Thus they are in
the possession of all the behavioral tools for affectionate interac-
tion. They seem however to occur less regularly and frequently.
This could reflect a genuine gender difference, which expresses
itself early in the difference among play activities of boys and
girls.
Spiro (1979) found that girls raised with boys, under a strict
egaliteran scheme in traditional Kibbutz communities, nonetheless
played differently from boys. Among other things, girls preferred
women as models, but of the many female models available, they only
mimicked the nurturant models. In nonliterate cultures children grow
up within an intricate network of individualized relations. Those
outside the family being of particular importance for the development
of social skills. Of particular importance are children's play
groups. Among the Bushmen children, from three to puberty, spend
most of the day in the company of other children, joining or with-
drawing from play group as they please. These groups are sometimes
composed of children of both sexes and all ages, and sometimes of a
few children all of the sam sex. In Bushman play groups there exists
a rank order with older children usually holding the higher rank
positions (Hold 1980). They organize games, comfort the younger
children in distress, scold boys who misbehave, encourage sharing,
interfere in aggressive encounters (Sbrzesny 1976). Adults rarely
interfere with their children's activities, but children rather work
out their problems on their own. Children in many societies have
their own children's culture with traditions being passed on from
older children to the younger ones. The older teach the rules of the
games, the riddles and rhymes - and thus make the children culture
continue.
This pattern was similar in our culture, prior to urbanization

and schooling. Today small children spend most of their time with
children of the same age, and thus their social experience is nar-
rower. Small children have little chance to learn from the older
ones, and the rich variety of children's games and skills are dying
out. Thus we must confront the question of whether our children

today are exposed to a rich enough social environment to allow them
to acquire the social skills, necessary to develop well-rounded
personality.
Adult reference persons of importance, besides the parents, are

uncles, in particular the parent's siblings, grandparents and others.
Sociobiologists have recently attached much importance to the pre-
valence of a strong bond with the mother's brother in many societies
(Alexander 1974). They argue that where paternity is uncertain, the
mother's brother invests much in his sister's children, since here he
is certain that they carry a substantial part of his genes. But how
sure can he be that his sister is really his full sister, if father-
hood is so doubtful? Furthermore, the mother's brother plays a
distinguished role also where adultery is not the rule. A simpler
explanation can be given. Some conventions for social security must
be invested. The brother provides the most obvious guardian for his
sister's offspring in case of emergency, because he is already bonded
to them and is of appropriate age.
In many cultures grandparents invest much time in young child-

ren, who have been recently weaned, to substitute for their mothers,
and later offer the child a relaxed non-formalized relationship
(joking relationship).
Polly Wiessner (personal communication), in a discussion, about

grandparents, mentioned a Tswana man who had told her that one of his
earliest impressions was of his grandmother who always loved him,
even when other people were angry at him and regardless of what he
did.
For children it is very important to have someone who admires

them during both their good and bad phases. Spoiling by grandparents
has its very positive sides. It promotes confidence in the children.
Although time does not permit me to go into relationship between

the child and other close relatives in more detail, I just want to
emphasize that the child in modern society lacks this rich variety of
social interaction.
Summary and Discussion
In summary, we have seen that there is great variation in early

socialization and educational practices between cultures. Nonethe-
less there exist a considerable number of behavioral patterns involv-
ing mother-child interaction, which are practically alike in all
cultures, including a strong tendency to form individualized bonds.
The biological attachment theory of Bowlby and Ainsworth is thus
supported on a wider cross-cultural basis. Mother and child indeed
form a biological unit and, may we add, together with the father a
biological triad. In all cultures studied by us, the mother also
provides the secure basis from which the child ventures to explore
his world, and to where it returns to find security. In all tribal
cultures babies grow up in a very protective environment. They enjoy
much body contact with the mother, sleep with their mother, and are
nursed for a long time. This is one of the most striking differences
with Western culture where babies sleep alone in their cribs. This
is often criticized as causing traumatic experiences, but we should
not be too hasty in condemning child rearing practices as "unnatural"
before having looked into the possibility that we are dealing with
culture-specific adaptations. Furthermore we should not simply
equate separation of mother and child during sleeping with love
deprivation. CHildren adapt to it in society, provided that contact
and love are otherwise provided. Of course there are signs indicat-
ing that sleeping alone is experienced difficult for children to
adapt to, and consequently special rituals for saying good night have
evolved in our cultures as coping strategies. In addition, children
accept substitute objects like pacifiers - a breast substitute - and
security blankets or dolls with which they huddle while sleeping.
Children become bonded to these objects emotionally, as if they were
social partners. In fact I know of a young lady and mother who is
still bonded to a green croccodile made of cloth, which served her as
a companion in childhood. She is passing this habit on to her son,
and interesting example of the build-up of family-specific tradi-
tions, which may give raise to a "croccodile clan".
Speculating about advantages of early partial mother-child

separation - and not of love deprivation! I hypothesize that it is a
culture-specific adaptation to the emotional distance which is crit-
ical to many interactions which take place in our European culture.
The child emancipates itself earlier, the child-rearing practices
foster its independence.
REFERENCES
Ainsworth, M. D. S., 1973, The development of Infant-Mother-

Attachment, in: "Child Development Research." Cladwell, B. M.
u. Ricciuti,lH. N., eds., The University of Chicage Press,
Chicago, 1-95.
Alexander, R. D., 1974, The Evolution of Social Behavior. Ann. Rev.
Ecol. Systematics, 5, 325-383.
Bernal, J., 1972, Crying during the first 10 days of life and
maternal responses. Developmental Medicine and Child Neuro-
~, 14, 362-372.
Biller, H. B., 1971, Father, child and sex role. Lexington Mass.
(Heath).
Biller H~ 1974, Paternal deprivation. Lexington, Mass. (Heath).
Bilz, R., 1943, Lebensgesetz der Liebe. (S. Hirzel) Leipzig.------
Bowlby, J., 1958, The nature of the child's tie to his mother. Int.J.
Psychoanalysis, 39, 350-373.
Bowlby, J. 1969, Attachment and loss. Vol. 1. Attachment. The Int.
Psyco-Analytical Library, Hogarth Press) 79 London.
Brazelton, T. (1962) Crying in infancy. Pediatrics, 29, 597-588.
Caudill, W., and Weinstein, H., 1969, Maternal care and infant
behavior in Japan and America. Psychiatry, 32, 12-43.
Clarke-Stewart, K. A., 1978, And Daddy makes Three: The Father's
impact on Mother and young child. Child Development, 49,
466-478.
Draper, P., 1972, !kung Bushman Childhood. Unpublished doctoral
dissertation, Harvard University.
Draper, P., 1976, Social and economic constraints on child life among
the ! kung , in:"Kalahari Hunter-Gatherers," R. B. Lee, & 1.
DeVore, eds~ (Harvard U. P.) Cambridge/Mass. & London,
199-217.
Eibl-Eibesfeldt, l., 1968, Zur Ethologie des menschlichen
Grussverhaltens. I. Zeitschr. Tierpsychol., 25, 727-744.
Eib1-Eibesfe1dt, I., 1971, Zur Etho1ogie des menschlichen Gruss-
verha1tens. II. Das Grussverha1ten und einige andere Muster
freund1icher Kontaktaufnahme der Waika (Yanoama). Zeitschr.
Tierpsycho1., 29, 196-213.
Eibl-Eibesfeldt, I., 1972, Die !Ko-Buschmanngese11schaft:
Aggressions-kontrolle und Gruppenbindung. Monographien z.
Humanethologie 1., Muncher (Piper).
Eibl-Eibesfeldt, I., 1973a, The expressive behaviour of the
deaf-and-blind-born, in: "Social Communication and Movement."
M.V. Cranach and T. Vine, eds., Academic Press, London,
163-194.
Eibl-Eibesfeldt,l., 1973b, Der vorprogrammierte Mensch. Das Ererbte
als bestimmender Faktor im mensch1ichen Verha1ten. Vienna
(Molden) dtv 4177 (1976).
Eibl-Eibesfeldt, l., 1974, !Kung-Busch1eute (Kungve1d, Sijdwestafrika)
- Geschwisterriva1itat, Mutter-Kind-lnteraktionen. Humane-
thol. Filmarchiv der Max-Planck-Gesellschaft HF 41.
Homo, 24: 252-260.
Eib1-Eibesfeldt, I., 1976, Menschenforschung auf neuen Wegen. Vienna
(Molden) .
Eibl-Eibesfeldt, l., 1977, Patterns of greeting in New Guinea, in:
"New Guinea Area, Languages and Language Studies 3, Language,
Culture, Society and the Modern World, Fascicle 1, Division 6,
Non-Verbal-Communication", S. A. Wurn, ed.,209-247. Pacific
Languages Series C-Nr. 40.
Eibl-Eibesfeldt, I., 1979a, Ritual and Ritualization from a
Biological Perspective, in: "Human Ethology: claims and limits
of a new discipline".M. ~ Cranach, K. Foppa, W. U. Lepenies,
D. Ploog, eds. Maison des Sciences de l'Homme & Cambridge U.
P., 3-93.
Eibl-Eibesfeldt, I., 1979b, The Biology of Peace and War. (Thames &
Hudson) Great Britain.
Eibl-Eibesfeldt, I., 1979c, Le comportement des enfants: cultures:

tko-San Yanomani, Himba et Eipo. in: "Les Enfants et les
Cultures." cultures vol. VI., No.4, Les Presse de L'UNESCO et
de la Baconniere, 25-38.
Ferguson, C. A., 1964, Baby talk in six languages, in: "The
Ethnography of Communication." J. Gumperz andD. Hymes, eds.
American Antrhopologist 66, 103-114.
Freedman, D. G., 1964, Smiling in blind infants and the issue innate
vs. acquired. J.Child Psycol.Psychiat., 5:171-184.
Frodi, A. M., and Lamb, M. E., 1978, Sex differences in
responsiveness to infants: A developmental study of psycho-
physiological and behavioral responses. Child Development,
49, 1182-1188.
Frodi, A. M., Lamb, M. E., Leavitt, L. A., and Donovan, W. L., 1978a,
Father's and Mother's responses to infant smiles and cries.
Infant Behavior and Development, 1, 187-198.
Frodi, A. M., Lamb, M. E., Leavitt, L. A., Donovan, W. L., Neff, C.,
and Sherry, D., 1978b, Father's and Mother's responses to the
faces and cries of normal and premature infants. Develop-
mental Psychology, 14, 490-499.
Gewirtz, J. L., 1965. The course of smiling by groups of Israeli
infants in the first 18 months of life, in: "Scripta
Hierosolymitana, Vol. 14, Abgedr." in: "Determinants of Infant
Behaviour, III." B. M. Foss, ed., London, 205-260.
Gewirtz, J. L. u., Gewirtz, H. B. 1965, Stimulus conditions, infants
behaviors and social learning in four Israeli child-rearing
environments: A preliminary report illustrating differences
in child, in: "Determinants of Infant Behaviour," III, B. M.
Foss ed., London, 161-184.
Gewirtz, H. B., and Gewirtz, J. L., 1968, Visiting and caretaking
patterns for kibbutz infants: age and sex trends. American J.
of Orthopsychiatry, 38, 427-443.
Grossman, K., 1978, Die Wirkung des Augenoffnens von Neugeborenen auf
das Verhalten ihrer MUtter. Geburtshilfe und Frauenheilkunde,
38, 629-635.
Hassenstein, B. 1973, Verhaltensbiologie des Kindes. Munchen (Piper).
Hold, B. 1980, Attention structure and behavior in G/wi San children.
Ethology and Sociobiology, 1, 275-290.
Keller, H. 1980a, Gaze and gaze aversion in the first months of life.
Institut F. Psychologie d. Technischen Hochschule Darmstadt,
Nr. 80/5.
Keller, H. 1980b, Beobachtung, Beschreibung und Interpretation von
Elter-Kind-Interaktionen im ersten Lebensjahr. B.
Beobachtungsmaterial f. die ersten 4 Lebensmonate. Institu F.
Psycologie d. Technischen Hochschule Darmstadt, Nr. 80/8.
Keller, H., Gauda, G. U. Miranda, D., 1980, Beobachtung, Beschreibung
und Interpretation von Eltern-Kind-Interaktionen im ersten
Lebensjahr. C. Skalen zur Beurteilung "Angemessenes
Elternverhalten". Institut f. Psychologie d. Technischen
Hochschule Darmstadt.
Klaus, M. et aI, 1972, Maternal Attachment: Importance of the first

post-partum days. New England Journal of Medicine, 286, 460.
Klaus, M., and Kennell, J. 1970, Mothers separated from their newborn
infants. Pedistric Clinics of North America, 17, 1015-1037.
Klaus, M., and Kennell, J. 1976, Parent-Infant Bonding. St. Louis
(Mosby).
Klopfer, P. H., and Gamble, J., 1966, Maternal "imprinting" in goats.
The role of Chemical senses. Z. Tierpsychol., 23, 588-592.
Klopfer, P. H., 1971, Mother love: What turns on it? American
Scientist, 59, 404-407.
Kohen-Raz, R. 1968, Mental and motor development of kibbutz,
institutionalized and home-reared infants in Israel, in "Child
Development," 489-504.
Konner, M. 1975. Relations among infants and juveniles in comparative
perspective, in: "Friendship and Peer Relations", Lewis/
Rosenblum eds:: John Wiley, New York, 99-129.
Konner, M. 1977a, Evolution of human behavior development, in:
"Culture and Infancy, Variations in the Human Experience."
(Academic Press), New Yoek, 69-109.
Konner, M., 1977b, Infancy among the Kalahari Desert San, in:
"Culture and Infancy, Variations in the Human Experience."
Academic Press, New York, 287-328.
Konner, M. J. U. Worthman, C., 1980, Nursing frequency, gonadal
function and birth spacing among !kung hunter-gatherers.
Science, 207:788-791.
Kotelchuck, M., 1976, The infant's relationship to the father:
Experimental evidence, in: "The Role of the Father in Child
Development." M. E. Lamb; ed., Wiley, New York, 329-344.
Lamb, M. E., 1976a, Interactions between eight-month-old children and
their fathers and mothers, in: "The Role of the Father in
Child Development." M. E. Lamb, ed. Wiley, New York.
Lamb, M. E., 1976b, Twelve-month-olds and their parents: Interaction
in a laboratory playroom. Developmental Psychology, 12,
237-244.
Lamb, M. E., 1976c, Effects of stress and cohort on mother - and
father - infant interaction. Developmental Psychology, 12,
435-443.
Lawick-Goodall, J. van 1975, The behaviour of the Chimpanzee, in:
"Hominisation und Verhalten," G. Kurth and 1. Eibl-Eibesfeldt,
eds., Fischer, Stuttgart, 56-104.
Lee, R. B., 1979, The !kung San. men, women and work in a foraging
ciety. Cambridge U. P., London/New York etc.
Liegle, L., 1971, Familie und Kollektiv im Kibbutz. Baltz Verlag,
Berlin.
Liegle, L., 1971b, Kollektive Erziehung im Kibbutz. Piper, Munchen.
MacFarlane, A. 1975, Olfaction in the development of social
preferances in the human neonate, in: "The Human Neonate in
Parent-Infant Interaction, " Ciba Found. Symp., 33, Amsterdam,
103-117.
Maxwell-West, M. U. Konner, M. J. 1976, The role of the father: An
Anthropological perspective, in: "The Role of the Father in
Child Development," M. E. Lamb, ed., John Wiley & Sons, New

York, 185-217.
Mead, M., 1930, Growing up in New Guinea. Morrow, New York.
Meves, C. H., 1971, Verhaltensstorungen bei Kindern. Piper, Munchen.
Morsbach, G., 1980, Maternal Recognition of Neonates' Cries in Japan.
Psychologia, 23, 63-69.
Morsbach, G., and Bunting, C., 1979, Maternal recognition of
neonates' cries. Develop.Med,Child.Neurol. 21, 178-185.
Mosley, W. H., 1977, The effects of nutrition on natural fertility.
Paper presented at Seminar on Natural Fertility, Institut
National d' Etudes Demographiques, Paris, March, 1977.
Murray, A. D., 1979, Infant crying as an elicitor of parental
behavior: An examination of two models. Psychological
Bulletin, 86, 191-215.
Papousek, H., and Papousek, M., 1979, Early ontogeny of human social
interaction; its biological roots and social dimensions, in:
"Human ethology: Claims and Limits of a New Discipline."-
Maison des Sciences de l'Homme and Cambridge University Press,
M. V. Cranach, K. Foppa, W. Lepenies, and D. Ploog, eds.,
456-490.
Parke, R. D., 1979, Interactional designs, in: "Social Interaction:
Methods, Analysis and Illustration,"-R. B. Cairns, ed.,
Lawrence Erlbaum, New York.
Pedersen, F. A., and Robson, K. S., 1969, Father participation in
infancy. American Journal of Orthopsychiatry, 39, 466-472.
Rabin, A. I., 1965, Growing up in the Kibbutz. Springer, New York.
Robson, K. S., 1967, The Role of eye-to-eye contact in
maternal-infant attachement. J.Child Psychol., 8, 13-25.
Sackett, G. P., 1966, Monkeys reared in isolation with pictures as
visual input. Evidence for an innate releasing mechanism.
Science, 154, 1468-1473.
Sagi, A., and Hoffman, M., 1976, Empathic distress in the newborn.
Developmental Psycology, 12, 175-176.
Sbrzesny, H., 1976, Die Spiele der !Ko-Buschleute unter besonderer
Berucksichtigung ihrer sozialisierenden und grup-
penhindenden Funktionen. Monographien z. Humanethologie, 2,
Piper Munchen.
Schiefenhovel, G., and Schiefenhovel, W., 1978, Eipo, Irian Jaya
(West-Neuguinea): Vorgange bei der Geburt eines Madchens und
1!..nderung der Infantizid-Absicht. Homo 29/2 121-138.
Simner, M. L., 1971, Newborn's response to the cry of another infant.
Developmental Psycology, 5, 136-150.
Spiro, M. E., 1956, Kibbutz, Venture in Utopia. Harvard University
Press, Cambridge, Mass.
Spiro, M. E., 1979, Gender and Culture: Kibbutz women revisited.
Durham (Duke U.P.).
Spitz, R. A., 1956, The first year of life. Int. Univ. Press, New
York.
Stern D., 1977, The First Relationship. Infant and Mother. Harvard
U.P. Cambridge/Mass.
Treverthen C. 1979, Instincts for human understanding and for
cultural cooperation: Their development in infancy, in:
"Human Ethology," M. V. Cranach, K. Floppa, W. U. Lepenies, D.
Ploog, eds., Cambridge U. P., Cambridge, London, 530-571.
Tyson, J. E., and Perez, A., 1978. The maintenance of infecundity in
post-partum women, in: "Nutrition and Human Reproduction," W.
H. Mosley, ed., Plenum Press, New York, 11-27.
West, M. M., and Konner, M. J., 1976, The role of the Father: An
antropological perspective, in: "The Role of the Father in
Child Development," M. E. Lamb, ed., John Wiley, New York,
185-216.
Whiting, B. B. (ed.), 1963, Six Cultures - Studies of Child Rearing,
Wiley, New York.
Whiting, B. B., and Whiting, J. W. M., 1975, Children of six
cultures: A psyco-cultural analysis. Harvard U.P. Cambridge/
Mass.
Yogman, M. J., Dixon, S., Tronkick, E. Als, H., and Brazelton, T. B.,
77, The goals and structure of face-to-face interaction bet-
ween infants and fathers. Paper presented at the biennial
meeting of the Society for Research in Child Development, New
Orleans.
Zeskind, Ph.S., and Lester, B. M., 1978, Acoustic Features and
Auditory Perception of the Cries of Newborns with Prenatal and
Preinatal Complications. Child Development, 49, 580-589.
THE PSYCHOBIOLOGY OF THE FIRST DIDACTIC PROGRAMS AND
TOYS IN HUMAN INFANTS
Hanus Papousek and Mechthild Papousek
Developmental Psychobiology
Max-Planck Institute for Psychiatry
Munich, F. R. Germany
INTRODUCTION
As a guest to the Comenius Society and like Comenius as a man

born in Moravia, I wish to take the liberty of recalling some of his
ideas and using them as departure points for our presentation at this
symposium.
Jan Amos Comenius was the bishop of the Moravian Brothers and
one of the leading personalities of the reformatory movement in
Central Europe during the Age of Reason in the XVIIth century. His
extensive education, devotion to noble humanistic principles, and
lively contacts with leading scholars in most European countries led
him to intensive engagements at the Royal Academies in both England
and France. John Harvard attempted to make Comenius the President of
his university in New England and could not succeed only because of
Comenius's obligations concerning the reformation of the educational
system in Sweden.
The necessity as a Protestant against the Catholic Church to

spend his most productive years in exile, and the cruel experience
which Comenius and his family had to undergo during the devastating
time to the Thirty-Year-War with recurrent epidemics in Europe,
hardened Comenius's will to propagate humanism, pacifism, and ratio-
nalism among nations. In doing so Comenius concentrated upon the ed-
ucation of children in particular. His works, "Opera Didactica
Omnia" above all, belong to the pillars of didactics (1657).
However, what was unique at Comenius's time and remained rare

through the following centuries was his belief (1) that educational
care should be started already during infancy and be based upon pa-
219
220 H. PAPOUSEK AND M. PAPOUSEK
rental care, and (2) that education, both preschool and scholastic,
should be carried out playfully. "Schola Ludus" (1657) was the title
of one of his works important in this regard, whereas "0r bis Pictus",
the first picture book for children offering a fundamental rational
knowledge and a vocabulary in Latin and in the main European lan-
guages, quickly became the first international educational bestsell-
er. The current revival of interest in playful activities for young
and old, and the enthusiasm for didactic programs for the first year
of life hopefully justify reminding the reader of recommendations
made two-and-a-half centuries ago.
Contemporary approaches have long complemented the former ratio-

nalistic deductions with ecological, psychobiological and sociobio-
logical aspects, to name at least some of the more recent trends.
And yet, surprisingly enough, on a much higher scientific level, they
have only stressed what Comenius already did at his time, e.g., in
the manual for the maternal school "Informatorium Scholae Maternae"
(1628): the roles of parenting, playfulness, musical communication,
and the competence of the very young child. Obviously, Comenius's
rational thinking was closely interrelated with his rich educational
empirical experience and with the intuitive insight of a loving
parent. I hope that I shall be able to explain sufficiently why I
stress the capacity of retaining an intuitive insight in matters of
early didactics in a man whose rational capacity simultaneously pro-
duced a highly abstracted vision of humanistic pansophia.
DIDACTIC PROGRAMS FOR EARLY INFANCY
Turning now our attention to the didactic programs for early

infancy, we do not want to increase the contemporary flood of recom-
mendations and educational toys motivated mainly by commercial inter-
ests. On the contrary, we doubt the justification and sense of this
flood. Too often, we find only adultmorphic and speculative extrapo-
lations behind the production of educational aids and too much commer-
cial exploitation in its motivation misusing important scientific
discoveries on the infant's learning and cognitive competencies.
During a time in which scientists cannot yet find out how to utilize
the infant's competencies adequately, it is easiest for the producer
of educational aids to extrapolate from the interests of older child-
ren or even from preferences of adults and supply the perplexed
parents with goods corresponding to their taste. However, it was due
to gaps in our knowledge and not due to the producer's point of view
that we turned our attention to the question of didactic programs for
infancy.
Since a perspective on early didactics may be related to a per-

spective on the nature-nurture controversy, it is interesting to know
how strongly Comenius believed in the importance of early environmen-
tal are for the development of mind in children. Naturally, his po-
PSYCHOBIOLOGY OF THE FIRST DIDACTIC PROGRAMS 221
sition was that of a religious dualistic philosopher, believing in

the existence of an immortal soul and assigning it the primary impor-
tance. Conversely, however, he repeatedly stressed the mutual inter-
relations between mind and body or, in didactic terms between the
care for the mind's needs and that for the body's health and growth.
At a time preceding neuroscientific interpretation of mind-body
interrelations, Comenius obviously deduced his principles from rich
experience in family consulting, tutoring, and organizing educational
systems, which soon brought him an international reputation.
Didactics is a scholarly discipline dealing with theories and

methods of conveying knowledge to those who want to learn that know-
ledge. Most typically, didactics concern the communication between
professional teachers and their pupils. The reader can, therefore,
ask whether we imply nonprofessionalism when calling didactic those
educational approaches concerned with infants and carried out by
parents in nonprofessional ways. Professions and scholarly disci-
plines, of course, often have predecessors in non-professional human
activities and, moreover, sometimes even in animal activities.
Therefore, we could also ask whether we know enough about biological
origins of didactics, and since at present the answer would be "No",
it may be legitimate to focus attention upon the ontogenetic and
phylogenetic roots of didactics, which might offer an excellent
opportunity for looking at interesting new aspects of parent-infant
interactions. In fact, didactic programs for infancy have already
been matters of professional efforts for one or two decades in coun-
tries providing substitutional care for infants in various day-care
facilities. This circumstance, however, has only revealed the need
for improved understanding of didactic predispositions concerning
infancy.
Whether we approach the question of didactic programs for infan-

cy from the side of biological origins of didactics or from that of
the evolution of human parenting, we enter a territory insufficiently
explored both by humanistic sciences and by comparative biology.
It is true that the literature on animal parenting is very rich

and includes systematic analyses of the regulation of parental behav-
iors in laboratory animals (Rosenblatt, 1975) as well as many field
observations documenting the variability, survival values or sex-
dependent sharing of the care for progeny (Ridley, 1978; Wilson,
1975). However, far less attention has been paid to the earliest
postnatal development of integrative capacities in the progeny and to
the parental contribution to this development.
The human studies, conversely, have already yielded abundant

evidence on the infant's learning and cognitive competence, and yet,
only very little information on such parental behaviors which might
be seen as pointers to the evolutionary past of human care promoting
the development of such a competence. This lack might have resulted
from the prevalence of retrospective approaches in the study of par-

enting such as in the initial studies of parental deprivation (Bach,
1946; Goldfarb, 1945; Lowrey, 1940; Sears, Pintler and Sears, 1946;
Stolz et al., 1954) and from the prevalence of questionnaire methods
in later approaches which necessarily cover merely the conscious par-
ental attitudes and behaviors, i.e., almost exclusively factors de-
pending much more on sociocultural than on biological determinants.
The same is true about observations made with the help of items pre-
selected a priori from other than psychobiological aspects of early
interventions (Dunn and Richards, 1977; Kaye, 1977; Klaus and
Kennell, 1976; Lewis and Lee-Painter, 1974; Schaffer, Collis and
Parsons, 1977; Stern et al., 1977; Thoman, 1975), irrespective of
their valuable contributions i relation to other aspects of'parent-
ing.
From analyzing parent-infant interactions with microanalytic

methods, we have reason to believe that parenting also necessarily
consists of reflexive, automated or ritualized behaviors allowing
fast responses within interactional sequencies in which there is
often not enough time left for conscious, rationally controlled
behaviors. Contradicting this assumption, the literature on human
parenting leaves an impression with the reader that, unlike in an-
imals, the entire process of human infant-rearing consists of con-
scious, socioculturally determined parental acts. This may be true
about parental behaviors providing the infant with nourishment, pro-
tection, and necessary bodily comfort. These behaviors have been
influenced by sociocultural institutions to such a degree that they
have become uninteresting from comparative biological views. Even
such potential relics of the once vital protection against cold like
the tendency to touch the infant with open palms, to give him maximum
bodil~ proximity, and to direct breath toward him (Papousek and
Papou~ek, 1979b) are nowadays more frequently interpreted as
emotional or communicative behaviors.
Being primarily interested in parental behaviors with potential

relevance for the development of integrative competence of the
progeny we first had to consider two very general theoretical aspects
of the problem: (1) the theoretical position of didactic capacities
in the repertoire of parental behaviors; and (2) the theoretical
position of integrative processes in the repertoire of infant
behaviors.
From the view of systems theory as we explained elsewhere in

greated detail (Papou~ek and Papou~ek in press), the parent-infant
interaction is one of the potential form of social interactions,
i.e., one of the interactions among members of the same species. As
any interaction between living systems with common genetic materials
and nervous systems, the parent-infant interaction contributes to the
development towards the state of increasing differentiation,
integration, and improbability in the interacting systems. Thus it

helps them to live as active and dynamic systems, to act spon-
taneously and to be capable of selfregulation as unitary systems even
under constant external conditions or in the absence of external
stimuli. In principle, therefore, the parent-infant interaction is a
dynamic interaction, Moreover, it bears dialectic features, for
instance, in the sense that interacting systems influence each other,
than any response on one side is a potential stimulus for the other,
and that each system represents a synthesis of open and closed
systems changing with time in dependence not only on the course of
interaction but also on biological aging (Bertalanffy v., 1968).
The appurtenance of interacting systems to the human species

grants the parent-infant interaction new dimensions the common denom-
inator of which is man's specifically well developed capacity for
abstraction and symbolism. This capacity has been involved in the
development of complex means of verbal communication and social orga-
nization and has allowed man exclusively to integrate experience
across ages as well as across the borders of cultures, continents or
even planets.
In addition to all interactional features introduced above, we

want to stress one more which is specific to the parent-infant inter-
action, namely, the critical difference between the two interactants
in the amount of integrated experience, knowledge, and social aware-
ness stored in the memory (Papousek and Papousek, 1978; 1981). This
difference grants the parent-infant interaction the character of a
didactic system in which one member has the potency to convey inform-
ation and knowledge to the other and to choose adequate forms for
this purpose, whereas the other member has the potency to learn from
the didactic act. In our analyses of human parent-infant interac-
tions, there are strong arguments for the assumption that both inter-
acting sides are not only capable of but also highly motivated, bio-
logically and socioculturally, for participation in such didactic
acts. The infant has the integrative competence and intrinsic moti-
vation for the acquisition of knowledge corresponding to his state of
development, and the parent has a biologically determined competence
and intrinsic motivation for conveying the infant adequate forms of
knowledge.
Is this didactic aspect of parent-infant interaction to be seen

as a species specific phenomenon? Insomuch as we consider the in-
volvement of verbal communication and conscious attitudes in these
interactions we deal, of course, with specific human levels of didac-
tic capacities. The human parent may be species specifically influ-
enced by information delivered in various verbal forms. She or he
certainly also does a lot to support the development of verbal commu-
nication in the progeny. Conversely, however, we have no reason for
rejecting the existence of fundamental didactic capacities in animal
parenting since even in man they do occur in nonverbal and non con-
scious forms. The only reason for such a denial would be the present
lack of evidence, which as usually, may again result from mere lack
of attention paid to this aspect in theoretical concepts.
According to the present evidence, animal parents, including

primates, show neither enough inventiveness in teaching the progeny
nor any particular pleasure with the progeny's cognitive progress.
For instance, in the Lawick-Goodall descriptions of situations in
which young chimpanzees obviously learned from parental skills,
parents merely carried out predictable behaviors without distinct
didactic motivation and tolerated the presence and inquisitiveness of
the young (Lawick-Goodall, 1967). Systematic analyses devoted spe-
cifically to the given problem would be necessary for assessment of
the degree to which we are dealing with a species specific phenome-
non.
Having explained how we conceptualize the general theoretical
position of didactic competence in the repertoire of parental capac-
ities, we still have to comment on the theoretical position of inte-
grative capacities in the repertoire of infantile behaviors before we
can pass on to empirical evidence in support of our argument.
Again, since we have explained the role of integrative capac-

ities more explicitly elsewhere (Papou~ek and Papousek, 1979a; in
press), we shall only summarize the main points here. In our attempt
to conceptualize the infant's fundamental regulation of behavior, we
attributed the primary role among different behavioral categories to
integrative nervous processes, in spite of the fact that the observer
has to direct access to them. However, according to all neuroscien-
tific evidence, the organism first has to activate various mechanisms
controlling informational input and processing, in order to respond
adaptively to any biologically relevant situation with specific re-
sponses, for instance, with grasping and feeding, with social commu-
nicating or with a simple avoiding movement. In observable behav-
iors, the activation of the fundamental integrative mechanisms can be
seen in orienting, approach or exploratory activities.
Other mechanisms apparently function in an opposite way and

reduce the intensity of informational input and processing, thus
enabling the organism to cope with situations connected with excess-
ive stimulation or stimulation too difficult to process. Looking
away or turning away may be observable indicators of these mechan-
isms. In problem situations difficult to cope with, it is not unusu-
al for infants below two months of age to respond with a sudden
change in their behavioral state resembling "playing possum" as if
some protective "biological fuse" (Papousek, 1969) switched off in-
formational input, with such an internal detachment helping to avoid
exhaustion. Older infants respond more frequently with a re-
distribution of attention and with an observable active detachment in
analogous situations.
The primary role of the fundamental integrative processes also

becomes evident in the infant's readiness from the earliest postpar-
tum age to activate individual integrative mechanisms almost in the
fashion of preprogrammed inborn responses to certain features in the
structure of environmental stimulation. It has been relatively easy
to demonstrate experimentally that a mere variation of spatial and
temporal properties of the same stimulation sets in operation ade-
quate forms of integrative processes. Already in the newborn, a
repetitious stimulation triggers orienting responses first and then
inhibitory habituation of them if the stimulation does not signal any
further relevant relations. Any new perceivable change in the repe-
titious stimulation, however, reactivates orienting responses as has
been repeatedly shown in dishabituation experiments (Bartoshuk,
1962; Bridger, 1961; Engen, Lipsitt and Kaye, 1963; Graham, Clifton
and Halton, 1968). In aversive responses, an analogous control was
shown to function even in sleeping newborns during quiet, non-REM
sleep (Martinius and Papousek, 1970). If the same stimulation regu-
larly accompanies another relevant event, it then functions as a
conditioning signal and sets associative conditioning in operation
(Janos, 1959). Still another and quite striking integrative activa-
tion is elicited if the infant finds out that he can control the
given stimulation by his own act as in the paradigm of instrumental
learning (Papousek, 1964; 1967; Siqueland and Lipsitt, 1966). The
infant's orienting increases, and a lot of effort is mobilized in
order to learn how to reach a satisfactory control of stimulation.
Similarly, we could exemplify the primary participation of more

complex integrative processes such as categorization and concept
formation. Instead, we will draw attention to the interrelation
between the fundamental primary integrative processes on one hand and
emotional and communicative behaviors on the other. In our experi-
mental studies, we have repeatedly observed that the course of inte-
grative processes as such is regularly accompanied with signs of
unpleasant experience before learning or problem solving becomes suc-
cessful, whereas a successful integration is connected with signs of
pleasure. The observable signs of these emotional feelings are at
the same time communicative messages not only for the observer in the
laboratory but obviously first and foremost for the caregiver. In
terms of the primary parental didactics, we find it unusually import-
ant for the parent as an intuitive teacher that a set of observable
behaviors is available in the infant to serve as potential feedback
information on the momentary course of integrative processes.
Once we assign the integrative processes such as important role

in the ontogeny of adaptive behaviors, it is only logical to assume
that evolution has favored the phylogeny of integrative processes in
predictable fashions, including a certain surplus of learning situa-
tions granted by biologically determined behavioral programs. Exact-
ly this assumption has give us the crucial reason for looking for the
primary biological models of didactic activities. Culture is too
young from the evolutionary point of view to serve as a reliable

guarantee for the development of biologically highly relevant capac-
ities. The existence of factors favoring integrative growth indepen-
dently of culture, for instance, in the form of intuitive parental
support, would not only complement the argument for the crucial re-
levance of integrative capacities but could also help to explain why
the infant reaches the milestones of cognitive development, including
the acquisition of language, almost independently of so very differ-
ent sociocultural backgrounds.
Thus, stated simply for the sake of clarity, we can summarize

some deductions from our concepts through the following conclusions
on the question of primary didactics:
(1) The integrative processes play the most fundamental role in

behavioral regulation and development, and have been favored
during human evolution.
(2) The infant is intrinsically motivated to learn, recognize, and
acquire knowledge and skills, in short, to integrate experience
as well as to communicate about the outcome of such integration.
(3) The parent is intrinsically motivated to share his knowledge,

particularly with his progeny, and has a biologically determined
capacity to modify the form of conveying knowledge to the infant
in accordance with the developmental state and momentary course
of the infant's integrative capacity.
Now, the third point which is of utmost relevance for the ques-
tion of parental didactic capacity has gone far beyond the scope of
the preceding set of theoretical arguments. Rather, it indicates
where we have to catch up in our analysis and gives us a chance to
augment our effort by considering empirical findings.
As good luck would have it, our theoretical concepts mentioned

above have developed simultaneously with an exceptional chance to
accumulate empirical evidence on both infantile and parental compe-
tencies. During the time of pioneering attempts to study learning
abilities in newborns and younger infants, and hence also to try to
teach them something, we were able to keep babies with heir mothers
at an indoor research unit for up to seven or eight months. Exposed
to considerable didactic difficulties ourselves, my co-workers and I
had good opportunities to ask or to watch how mothers coped with
similar problems.
Soon, we were struck by discrepancies between objective records

of mothers' routines and verbal interpretations of these routines by
the same mothers in interviews. It became obvious that mothers were
often not consciously aware of practical forms of parenting carried
out by them several times a day. For the sake of our learning exper-
iments, for instance, we intended to interrupt bottle feeding ten
times in a session and before doing so, asked mothers whether they
would allow us to do this and whether they would recommend how to do
it without discomforting babies. Although according to our own
observations these mothers used to interrupt breastfeeding themselves
several times without difficulties, they could not give us any recom-
mendations. Having rechecked their experience in this regard with
increased conscious attentiveness, they were able to confirm that it
was easy to interrupt breastfeeding. However, in most cases they
gave us misleading explanations as to how to prevent protests from
babies. We had to detect the simple principle ourselves: if the
mother pulls out the nipple from the infant's mouth during a pause
between bursts of sucking movements, the infant remains quiet; other-
wise, it is very difficult to pullout the nipple at all, certainly
not without protest.
We have been able to reconfirm this discrepancy in various fur-

ther observations. Thus, in a recent study, we analyzed parental
support of visual contact with newborns (Schoetzau and Papou§ek,
1977) and found again that both primiparous and mUltiparous mothers
choose an unusually short eye-to-eye distance (22.5cm) when talking
to newborns, actively seek fact-to-face positions, and regard the
newborn with vivid greeting behaviors for achieving eye-to-eye con-
tact. Mothers produced these responses without showing any conscious
awareness of these behaviors in postobservational interviews, often
to the contrary believing that newborns cannot yet see anything at
all. The same has appeared to be true for fathers in relation to
various forms of parental behaviors.
The richness and interactive entrainment of a whole set of

intuitive parental behaviors have become particularly evident since
we started studying them microanalytically with the help of film or
television techniques (Papousek and Papousek, 1979b). Our own didac-
tic experience resulting from the attempts to teach newborns and
younger infants has probably facilitated our search for corresponding
patterns in intuitive forms of parenting. From out studies on learn-
ing and cognitive abilities in infants. we know. for instance. that
teaching can only be successful if we fulfill several conditions
(Papousek and Papousek, 1979b; in press), i.e., (1) if the infant is
in the optimal state of waking and alterness; (2) if the structure of
provided stimulation is simple and slow enough to be perceived and
processed by the infant; (3) if the learning tasks are repeated fre-
quently enough; (4) if the capacities to be trained are gradually
ordered according to their development in the infant; (5) if the
didactic process can be facilitated with adequate regarding mechan-
isms and modified with respect to feedback signals indicating the
course of integration and the limits of tolerance. In general, we
have to act very much like a teacher at school who also has to know
how to gain the pupil's attention, adjust communication to the
pupil's level or convey the selected piece of knowledge in the corre-
sponding form and dosage. Unlike the teacher, however, we get no
verbal feedback from the infant on the didactic effect, and we have
less time for conscious rational control of any communication with
the infant.
Alone the correct evaluation of the momentary behavioral state

of young infants is very difficult to achieve. The span of their
attention is typically short and cannot be influenced with the help
of instructions; it can only be affected by fast adjustments of
applied stimulations. Our knowledge about the premises of successful
learning in infants is so recent that it is known only to a small
group of specialists, a state of affairs which possibly makes it even
more interesting to see how parents cope with difficulties related to
infant learning.
Perhaps the best example demonstrating that parents do

intuitively teach their babies and can overcome the difficulties
mentioned above can be give in the description of parental support
for the development of infantile vocal communication. The parent's
own description would again hardly satisfy us; it would be something
like, "I simply talk to my baby or have a lot of fun with him, and he
talks back". According to parents, it is premature to.pay any
systematic attention to the development of language before the first
words appear. Sometimes they add that they had been discouraged to
use baby talk since babies should only hear the correct language. An
objective analysis of parenting, however, reveals a very different
picture.
Before we describe this picture, it may be useful to design a

basic script for teaching a language to someone who has not yet
spoken any language at all, as in the case of the newborn. This
circumstance creates a very unusual didactic situation for which we
cannot even find a precedent in Comenius's progressive work on teach-
ing languages "Janua linguarum reserata" from 1630-31.
Being unable to communicate verbally or at least explain our in-

tentions to the newborn, we can only try to attract as much attention
as possible and then display many examples which may encourage imita-
tion. We have to make our own behavior understandable and predict-
able and eventually to overexaggerate the displays of the most cru-
cial messages, in order to make distinct their relation to vocal
utterances. The messages should elicit recognition that it is useful
to communicate vocally, especially in the advantageous form of turn-
taking in a dialogue. For this purpose, we may effectively regard
every, initially perhaps only incidental, attempt to enter into a
dialogue. It might be advisable to start with lessons on variations
in melody and intonation for which we need only one vowel sound, and
which alone helps to label and convey the most fundamental categories
of messages indicating questions and answers, warnings, alarm signals
in case of danger, signs of social help, invitations for mutual
amusement and play, lullabies, or expressions of disappointment,
sadness or anger. The next lessons may include training how to

produce sounds and phonemes characteristic of the language of the
given social environment, whereby we should help to mold individual
phonemes in the order in which they develop in the infant.
This is already enough to analyze for the first trimester of

parent-infant interactions. The amazing thing is to see how parents
systematically follow this script without consciously knowing. First
of all, they do use baby talk even if they sometimes try to avoid
doing so, and they show how smoothly and quickly they can switch from
narrative speech to baby talk and vice versa if alternatively speaking
to adults and to babies, although both forms of communication differ
in many aspects. The average fundamental frequency of baby talk is
(1) higher than that of narrative speech, (2) approaches that of
infant sounds (Ferguson, 1964), and (3) may well help the infant to
recognize when the caregiver vocalizes to him. The structure and
syntax of utterances are simple in baby talk, with individual segments
being distinctly abbreviated and repetitive in slow rhythm with pro-
longated intersegmental pauses (Garnica, 1977; Phillips, 1973; Snow,
1977). This helps the infants to detect regularities in the flow of
speech, to become familiar with their patterns, to associate these
regularities with corresponding contexts, and to predict and recog-
nize them the next time such opportunities arise (Papousek and
Papousek, 1981). Certain patterns of musical properties of baby talk
affect the infant's behavioral state, increase his alertness or
comfort and soothe him (Papousek and Papousek, 1977b).
With baby talk, parents utilize various opportunities for

distinct or even overexaggerated displays of the so-called "Prosodic
envelopes" distinguishing questions, answers, warnings and other
fundamental messages from one another as mentioned above. Among
them, the rising musical contours typical for questions particularly
affect the infant's attention and readiness to vocalize independent
of the presence of a real lexical question.
Didactically seen, it is interesting how parents support the

infant's imitative capacity, one of the important integrative pro-
cesses still escaping a detailed neurophysiological interpretation.
Parents are evidently the tirst to imitate the infant after his birth
and imitate facial and vocal expressions in particular (Papousek and
Papousek, 1977b). By doing so with baby talk, they give the infant the
earliest chance to compare the products of imitation with his own
original sounds. Such a comparison may play supportive roles not
only in the further development of imitative capacities but also that
of self-awareness (Papousek and Papousek, 1981).
Another didactically interesting phenomenon may be seen in the

signpost features of baby talk (Papousek and Papousek, 1981). The
parent namely not only adjusts baby talk to the infant's present state
and need, but takes the lead by exploiting every developmental
progression by offering models for the further improvement of every

newly emerging capacity. This aspect becomes particularly evident
when the infant is first able to produce distinct syllables. Whereal
prior to this time the parent has not attributed any referential
meaning to presyllabic vocalizations, now he uses every distinct
syllable as a potential core for a future word and teaches the infanl
to associate this protoword with the adequate object or situational
context. Similarly, the parent tends to start teaching the first
nursery songs as soon as the infant starts imitating simple melodies.
The lexical content ot the baby talk deserves our attention as

well. Particularly in the first tow months, it shows several
interesting features such as a surprisingly high proportion of
questions or a tendency to interpret facial and vocal expressions of
the infant as signs of thoughts. The parent asks questions and
answers them himself; however, in doing so he formulates the answers
in accordance with his interpretation of the momentary facial and
vocal behaviors of the infant. Thus, the parent allows us to learn
how he interprets infantile behaviors and in the same manner he
confirms the presence of a particular sensitivity for all potential
signs indicating the course of the infant's integrative processes.
Again, this aspect of parental behavior for the most part escapes thE
parent's conscious awareness. In general, baby talk can be elicited
with such certainty in the infant's presence, but it is hardly
possible to produce in his absence.
Similar to other behavioral categories of high adaptive rele-

vance, the intuitive character of baby talk corresponds to the assump-
tion of a prevailing biological determination. By that we do not
mean that language could not develop without the described parental
support. The crucial importance of this support for the acquisition
of language is predictable but not yet proved; and we know that evo-
lution may favor multiple paths with a sufficient universality and
surplus for the realization of important programs. After all, baby-
talk is not at all a matter exclusive to the maternal domain. It
develops early during ontogeny in both sexes, i.e., between two and
four years of age (Papousek and Papousek, 1981; Sachs and Devin,
1976; Weeks, 1971), and can be elicited from both aged women and men,
In spite of the narrow focussing upon the one example of par-

ental baby talk in this presentation, much more could be discussed
with respect to didactic programs for early infancy. We have intent-
tionally left untouched the aspect of playfulness; because of its
importance and also because it is theoretically difficult, we want t(
devote the next section of this paper to this aspect of didactic
programs.
THE FIRST DIDACTIC TOYS
In the preceding section of this presentation, we have discusse(

only one aspect of parenting, coval communication, and yet, hope-
fully, have shown that rich and interesting sources of supportive
stimulation are available to satisfy needs related to the infant's
integrative development. Snow (1977), for instance, reports that
mothers respond to 100% of all vocalizations from their three-
month-oldbabies. Generally, in comparison to the infant's relevant
interactions with the physical environment, his relevant interactions
with the social environment differ both in quality and in quantity.
Under normal conditions, the physical environment offers only a
minimum of stimulation whose structure can correspond to the state of
young infants' integrative capacity and activate manifold integrative
processes without the caregiver's mediation. Thus, even the best
educational toy may complement, but never adequately substitute
parenting.
Yet, it is commonly assumed that infants spend most of their

time playing and that parental involvement has a playful character.
However, the reader is surely aware of the difficulty connected with
defining and measuring play scientifically. Considering the variety
of activities associated with the self-explanatory word "play",
ranging from the infant's finger play to a pianist or a professional
actor, we acknowledge that play is a multifaceted phenomenon, and
therefore, cannot be captured by a single criterion or measured
according to one quantifiable parameter. Similarly, it is difficult
to draw a line between playful and other categories of activities,
for instance, between playing chess and solving professional problems
or between role-playing in children and in actors. It is noteworthy
that logicians distinguish disjunctive categories the difference
between which can be defined exactly from injunctive ones, the latter
which cannot be differentiated unless we suggest an appodictic art-
ificial criterion like between "white" and "grey". Ostensibly, the
advantage of appodictic reversal of injunctive categories like "work"
and "play" into disjunctive ones would be very doubtful.
Nevertheless, if we cannot define how many corns make up a heap,

it may still be interesting to find out the composition and the pur-
pose of the heap. Our own interest, mentioned in the preceding
section, has raised the question of the relation between play and the
development of integrative capacities in general. Such a relation
has been repeatedly assumed, an assumption based on intuition or on
empirical grounds. It is remarkable that Comenius, a rational think-
er par excellence, assigned playful methods such an important posi-
tion in the acquisition of knowledge in children. Rousseau,
Pestalozzi, Froebel or Montessori belong to his later outstanding
followers in this regard. Huizinga (1955) considered playas the
major determinant of human culture and suggested that man is Homo
ludens rather than Homo sapiens. Huizinga's argument stems from the
analysis of how artists contribute to civilizing trends in human
development, leaving unexplored the relation of play to early cogni-
tive development.
Among the theoreticians on play in developmental psychology,

epistemology and child psychiatry, several authors have made import-
ant empirical or clinical observations and elucidated different
aspects of the interrelations between play and some of the other
integrative processes. Vygotski, for instance, emphasized the role
of rule-detection, symoblic transformation, and exploration in var-
ious forms of play (Vygotski, 1962). Piaget (1951) analyzed the
'relative influences of accommodation and assimilation, two fundamen-
tal cognitive processes central among his theoretical concepts.
Unlike other authors such as Bruner, Piaget regarded playas a trans-
itional phenomenon of childhood giving way to logical development in
adulthood. Bruner (1972) was mainly interested in the expressions of
the child's problem-solving capacities, exploration and reasoning in
play. In this and related studies, play was defined within a situa-
tional context, focusing on the availability of toys, rather than
behavioral parameters.
Hutt (1966), has perhaps been the most systematic in the experi-
mental analysis of the play of preschool children; she elicited
various perceptual and cognitive functions with an artificial toy
displaying visual and auditory feedbacks in controlled combinations.
Directing much more attention to affective predispositions and diffi-
culties resulting in children from severe problem situations, play
was employed as both a diagnostic and a therapeutic tool by Winnicot
(1971), Erikson (1963) and others. In spite of their important
contributions, the above studies have not focussed upon the earlier
ontogenetic and phylogenetic developmental roots of play or its
counterpart in parenting.
Researchers of animal behavior have been more consistent in

pursuing the evolutionary adaptiveness of play, often for the price
of narrowing the criteria of play behavior. Some of them consider
play adaptive and functional, and demonstrate its role in interac-
tional analyses of monkey and primate behaviors (Bekoff, 1972;
Loizos, 1967; Poirier, 1972; Suomi and Harlow, 1971). Others object
and argue (1) that some primates exhibit very little play, for in-
stance orang-utans (MacKinnon, 1971) or gorillas (Schaller, 1963), or
(2) that explorative and playful behaviors increase mortality,
making, for instance, olive baboons (Berger, 1972) or chimpanzees
(Teleki, 1973) easier targets for predation.
Our attempts to synthesize present knowledge about play and to

identify its position in the system of integrative capacities have
resulted in the following concepts (Papousek and Papousek, 1977a;
1978). The acquisition of knowledge is seen as an intrinsic movement
from the "unknown" to the "known" directed by integrative processes
so as to avoid, on one hand, stress from novelty or the "unknown"
and, on the other hand, stress from boredom or the "trivially known".
Integrative processes function on two main levels. On the lower
level, they help to cope with incongruity between the existing state
of integrated experience and the exposure to a novel object or situa-
tion. For this purpose, the system tends as soon as possible to
accumulate information and integrate a closed unambiguous, although

perhaps simplified and dogmatically imposed, concept on the
"unknown".
In order to avoid boredom resulting from the prevalence of such

"first aid concepts" in one's knowledge structure, a higher level of
integration can be activated which leads to the re-opening of seem-
1ngly definite and unambiguous concepts, to take innovative and
nontraditional looks at the "known" which make it "unknown" again.
The combination of integrative processes functioning on this higher
level of integration represent playful, creative, or also scientific
actions. The difterence among these actions may be due to the devel-
opmental state of the system or to the complex situational context,
however, at the heart of all of them is the activation of the higher
level of integration. The predicates "lower" and "higher" are used
to indicate not only differences in the degree of differentiation and
complexity, but also in ontogenetic and phylogenetic advancement.
From this perspective, play can only start if an individual has

already formed at least a simple concept of a novel event and taken a
certain attitude with respect to it. In animals and very young human
infants, we can assume the simplest concepts resulting from familiar-
1zation or fundamental forms of learning as well as empathic atti-
tudes resulting from referential interactions with parents. Replac-
ing the simplest, superficial or supersitious concepts with more
comprehensive and creative ones may well be essential for contribu-
tions to human culture including play, humor, arts, and science in a
longterm perspective.
Under laboratory conditions in the absence of social partners,

we exposed four-to-five-month-old infants to problem situations in
which they could activate attractive visual rewards by making correct
head turns (Papousek and Bernstein, 1969). Whenever the infant had
achieved accurate control of the situation, we increased the diffi-
culty of the game rules. This gave us not only a chance to study the
capacity of rule-detection and the complexity of concepts necessary
for coping with the problem situation, but it also drew the infant
into a play situation. These observations confirmed a surprisingly
high level of integrative competence in the infant and also showed
individual variability in the degree of playfulness with which in-
fants were capable of discovering and testing new solutions. For
some of them, it seemed to be a pleasant playful experience, for
others an overly straining situation in which they tended to show
little exploration and to stick to "superstitious" solutions
(Papousek, 1979).
Let us now consider where the infant can find the first toys
that would support the development of integrative competence, and
moreover, toys that would be so universally available and so early
applicable so as to point to the path of the evolutionary past of
toys. At the research unit mentioned earlier in the presentation,

our attention to educational toys was kept at a high level and
empirically nourished by activities of our co-worker, the late
Jaros1av Koch, an authority on toys who owned a large collection of
infant toys. Nevertheless, on the basis of all our observations, we
come to the conclusion that there are two entities in the infants
world which are preferred over all others, particularly in terms of
the earliest and most universal availability: the infant's caregiver
and the infant's vocal apparatus.
To all that we have said about parental didactic programs in

this presentation we should only add here that parents also regularly
exhibit a strong tendency to repeat a stimulating event, thereby
familiarizing the infant with it, and vary it as soon as the infant's
attention wanes. This tendency, obvious in baby talk as well as in
many games between parents and infants, not only maintains the
infant's attention at a desired level, but also provides the infant
with abundant examples demonstrating that a certain balance between
familiarity and novelty is particularly pleasant to experience and
can be achieved playfully or creatively through modifications of
available skills. In the case of parental baby talk, this tendency
can be observed with objective methods using audio-taping, videotap-
ing, spectrographic and automated electronic structural analyses of
parental voice during interactions, as we reported elsewhere in
detail (Papousek and Papousek, 1981).
With the same methods, corresponding evidence on the infant can

be gathered in vocal utterances either during interactions with the
caregiver or, even better, during monologues in the absence of care-
givers. On one hand, we can analyze how far and in what steps the
infant processes and increasingly imitates parental vocalizations.
Un the other hand, we can observe the increasing duration and emo-
tional involvement as well a qualitative changes of the developing
monologues.
During the first trimester, the infant mainly explores new vocal
capacities and first has to learn how to modify and expand the length
of expirations, the pitch range, or the intensity of elementary
sounds. Only with the increasing integration of component functions
can a higher competence enable more complex variations or combina-
tions of previous elements in new patterns. Signs of pleasant expe-
rience more distinctly start simultaneously to accompany similar
vocal activities and give them a character of vocal play. The signs
of pleasure observable during infant monologues belie the presence of
either boredom or stress due to the "unknown", and thus permit the
assumption that the infant can already successfully avoid both kinds
of stressful states by operating on the higher level of integration,
including playful operations.
In a detailed single-case observation (Papousek and Papousek,
1981), we have shown that during the second trimester, the modifica-
tions of repetitive segments appeared and were followed by facial
signs of pleasure. Modifications involved melodic, temporal or
intensity features of musical elements in vocalizations, i.e., fea-
tures controlled by the lower coval tract, which is believed to have
functioned earlier during evolution than the upper vocal tract
(Myers, 1968). With the development of cortical control over the
upper vocal tract, which is necessary for syllabic articulation, the
repertoire of vocal play expands to new dimensions in the third tri-
mester. Syllabic sequences, among others, enable displays of new
patterns of rhythm and accent, and the emergence of new forms of
articulation, for instance, in connection with dentition, stimulates
increased vocal exploration.
Without the slightest intention of trying to discourage the

parental population from reading the growing amount of educational
recommendations on infant-rearing or of trying to deprive the present
population of babies of all those neat educational toys available on
the market, we still believe that it is time to share some of our
ideas with parents, at least with those parents who are becoming dis-
oriented and losing parental self-confidence. It might soothe them
and enhance their confidence in their own parental competence if they
realize that the best recommendations for amusing the baby and sup-
porting his integrative development have already been given to them
by Nature in the form of scripts of behaviors which are triggered by
the baby's behavior. All that parents have to do in order to give
their babies the best intellectual training and the best toy is to
find enough spare time and spend as much of it as possible in sponta-
neous dyadic interchange with the baby.
Without difficulty, parents will then display pleasant and

didactically useful combinations of stimulation in various modalities
and in optimal dosages. In order to train all individual capacities,
parents, without even being aware of it, will make themselves famil-
iar, predictable, and understandable to infants and will respond
contingently to infantile behaviors. The infant will enjoy such
playful lessons and learn how to control and understand parental
behaviors and communication, while at the same time, parents will
learn to read the infant's messages accurately. If such interchanges
start early enough and continue to occur regularly, they will soon
become a source of increasing pleasure for both interactants, that
is, for the infant the pleasure of learning and for the parent the
pleasure of teaching successfully or hearing how with increasing
mastery, the infant joyfully plays with his natural vocal toy. Com-
parable pleasure lies ahead as well for the observer who analyzes
such interactions, for they hold in store many more challenges to our
current scientific understanding.
ACKNOWLEDGEMENTS
Following foundations have kindly supported our research: Die

Deutsche Forschungsgemeinschaft, Der Fond der Deutschen Bank beim
Stifterverband fUr die Deutsche Wissenschaft, and Die Stiftung Volks-
wagenwerk. We owe special thanks to Peter L. Mangione, PhD, for
helpful comments and editorial assistance in the preparation of this
manuscript.
REFERENCES
Bach, G. R., 1946, Father-fantasies and father-typing in father-

separated children, Child Develop., 17:63-80.
Bartoshuk, A. K., 1962, Human neonatal cardiac acceleration to sound:
Habituation and dishabituation, Perceptual and Motor Skills,
15: 15-27.
Bekoff, M., 1972, The development of social interaction, play and
meta-communication in mammals: An antropological perspective,
Q. Rev.Biol., 47: 412-434.
Berger, M., 1972, Population structure of olive baboons (Papio
anubis, J. P. Fischer) in the Laikipia districts of Kenya.
E.Afr.Wildl., 10: 159-164.
Bertalanffy, L. von, 1968, "Organismic Psychology Theory," Clark
University Press with Barre Publishers, Barre, Mass.
Bridger, W. H., 1961, Sensory habituation and discrimination in the
human neonate, Am.J.of Psychiat.,117: 991-996.
Bruner, J. S., 1972, The nature and use of immaturity, Am.Psycho-
logist,27: 687-701.
Comenius, J. A., 1628, "Schola Materni Gremii," English translation
in Comenius, J. A., 1956, "The School of Infancy," Chapel
Hill, N. C.
Comenius, J. A., 1657, "Opera Didactica Omnia", Amsterdam.
Dunn, J. B., and Richards, M. P. M., 1977, Observations on the devel-
oping relationship between mother and baby in the neonatal
period, in: "Studies in Mother-Infant Interaction," H. R.
Schaffer, ed., Academic Press, London.
Engen, T., Lipsitt, L. P., and Kaye, H., 1963, Olfactory responses
and adaptation in the human neonate, J.Comp.Physiol.Psychol.,
56: 73-77.
Erikson, E. R., 1963, "Children and Society," Norton, New York.
Ferguson, C. A., 1964, Baby talk in six languages. Am.Anthropol.,
66:103-114.
Garnica, O. K., 1977, Some prosodic and paralinguistic features of
speech to young children, in: "Talking To Children: Language
Input and Acquisition," C.E. Snow, and C. A. Ferguson, eds,
Cambridge University Press, Cambridge.
Goldfarb, W., 1945, Effects of psychological deprivation in infancy
and subsequent stimulation, Am.J.Psychiat., 102: 18-33.
Graham, F. K., Clifton, R. K., and Hatton, H. M., 1968, Habituation
of heart rate responses to repeated auditory stimulation
during the first five days of life, Child Develop., 39: 35-52.
Huizinga, J., 1955, "Homo Ludens," Beacon Press, Boston.
Hutt, C., 1966, Exploration and play in children, Symp.Zool.Soc.
London, 18: 61-81.
Janos, 0., 1959, Development of higher nervous activity in premature
infants, Pavlov J. Higher Nerv.Activ., 9: 760-767.
Kaye, K., 1977, Toward the origin of dialogue, in: "Studies in
Mother-infant Interatcion," R. H. Schaffer, ed., Academic
Press, London.
Klaus, M. H., and Kennell, J. H., 1976, "Maternal-Infant Bonding,"
Mosby, Saint Louis.
Lawick-Goodall, J. van, 1967, "My friends the wild chimpanzees,"
National Geographic Society, Washington. D.C,
Lewis, M., and Lee-Painter, S., 1974, An interactional approach to
the mother-infant dyad, in: "The Effect of the Infant on Its
Caregiver," M. Lewis, andL. A. Rosenblum, eds., Wiley, New
York.
Loizos, C., 1967, Play behaviour in higher primates: A review, in:
"Primate Ethology," D. Morris, ed., Weidenfeld and Nicolson,
London.
MacKinnon, J., 1971, The orang-utan in Sabah today, Oryx, 11: 141-191
Martinius, J. W., and Papousek, H., 1970, Responses to optic
and exteroceptive stimuli in relation to state in the human
newborn: Habituation of the blink reflex, Neuropadiatrie, 1:
452-460.
Myers, R., 1968, Neurology of social communication in primates, Proc.
Second Internat.Congr.Primatol., 3: 1-9. -----
Papougek, H., 1964, Conditioned reflectory movements of the head in
the human newborn, Act.nerv.super., 6: 83-84.
Papousek, H., 1967, Experimental studies of appetitional behavior in
human newborns and infants, in: "Early Behavior: Compartive
and Developmental Approaches~ H.W. Stevenson, E. H. Hess, and
H. L. Rheingold, eds., Wiley, New York.
Papousek, H., 1969, Individual variability in learned responses in
human infants, in; "Brain and Early Behavior," R. J. Robinson,
ed., Academic Press, London.
Papousek, H., and Bernstein, P., 1969, The functions of conditioning
stimulation in human neonates and infants, in: "Stimulation in
Early Infancy," A. Ambrose, ed., Academic Press, London.
Papousek, H., and Papousek, M., 1977a, Das Spiel in der
Fruhentwicklung des Kindes, Supp.padiat.Praxis, 18: 17-32.
Papousek, H., and Papousek, M., 1977b, Mothering and cognitive
head-start: Psychobiological considerations, in: "Studies in
Mother-Infant Interaction," H. R. Schaffer, ed., Academic
Press, London.
Papousek, H., and Papousek, M., 1978, Interdisciplinary paralleles in
studies of early human behavior: From physical to cognitive
needs, from attachement to dyadic education, Internat.J.Behav.
Develop., 1: 37-49.
Papousek, H., and Papousek, M., 1979a, The infant's fundamental
adaptive response system in social interaction, in: "Origins
of The Infant's Social Responsiveness," E. B. thoman, ed.,
Erlbaum Ass., Hillsdale, N.J.
Papousek, H., and Papousek, M., 1979b, Early ontogeny of human social
interaction: Its biological roots and social dimensions, in:
"Human Ethology. Claims and Limits of a New Discipline,"M.
von Cranach, K. Foppa, W. Lepenies, and D. Ploog, eds.,
Cambridge University Press, Cambridge.
Papousek, H., and Papousek, M., 1981, Musical elements in the in-
fant's vocalization: Their significance for communication,
cognition and creativity, in: "Advances in Infancy Research,
vol. 1," 1. P. Lipsitt, ed-::- Ablex Publishing Corp., Norwood,
N.J.
Papousek, H., and Papousek, M., in press, Infant-adult social inter-
actions, their origins, dimensions, and failures, in: "Review
in Developmental Psychology," T. Field, ed., Wiley-:-New York.
Phillips, J., 1973, Syntax and vocabulary of mother's speech to young
children: Age and sex comparisons, Child Develop., 44: 182-
185.
Piaget, J., 1951, "Play, Dreams and Imitation in Children,"
Heinemann, London.
Poirier, F. E., 1972, Introduction, in: "Primate Socialization," F.
E. Poirier, ed., Random House, New York.
Ridley, M., 1978, Paternal care, Anim.Behav., 26: 904-932.
Rosenblatt, J. S., 1975, Prepartum and postpartum regulation of
maternal behavior in the rat, in: "Parent-Infant-Interaction,"
M. O'Connor, ed., Elsevier, Amsterdam.
Sachs, J., and Devin, J., 1976, Young children's use of age-
appropriate speech styles, J.Child Language., 3: 81-98.
Schaffer, H. R., Collis, G. M., and Parsons, G., 1977, Vocal
interchange and visual regard in verbal and pre-verbal child-
ren, in: "Studies in Mother-Infant Interaction," H. R.
Schaller, G. B., 1963, "The Mountain Gorilla: Ecology and Behavior,"
University of Chicage Press, Chicago.
Schoetzau, A., and Papousek, H., 1977, Miltterliches Verhalten bei der
Aufnahme von Blickkontakt mit dem Neugeborenen, Zeitschr.f.
Entwicklungspsychol.u.Padagog.Psychol., 9: 231-239.
Sears, R. R., Pintler, M. H., and Sears, P. S., 1946, The effect of
father separation on preschool children's doll play agression,
Child Develop., 17: 219-243.
Siqueland, E. R., and Lipsitt, L. P., 1966, Conditioned head turning
in human newborns, J.Exper.Child Psychol., 3: 356-376.
Snow, C. E., 1977, The development of conversation between mothers
and babies, J. Child Language, 4: 1-22.
Stern, D. N., Beebe, B., Jaffe, J., and Bennett, S. L., 1977, The
infant's stimulus world during social interaction: A study of
caregiver behaviours with particular reference to repetition
and timing, in: "Studies in Mother-Infant Interaction," H. R.
Stoltz, L. M., et a., 1954, "Father Relations of War-born Children,"
Stanford University Press, Stanford, Cal.
Suomi, S. J., and Harlow, H. F., 1971, Monkeys at play, Nat.Hist.,
Special Supp1.: 72-75.
Teleki, G., 1973, "The Predatory Behavior of Wild Chimpanzees,"
Bucknell University Press, Lewisberg, Pa.
Thoman, E. B., 1975, How a rejecting baby affects mother-infant
synchrony, in: "Parent-Infant Interaction," M. O'Connor, ed.,
Elsevier, Amsterdam.
Vygotski, L., 1962, "Thought and Language," MIT Press, Cambridge,
Mass.
Weeks, T. E., 1971, Speech registers in young children, Child
Develop., 42: 1119-1131.
Wilson, E. 0., 1975, "Sociobiology: The New Synthesis," Harvard
University Press, Cambridge, Mass.
Winnicot, D., 1971, "Playing and Reality," Basic Books, New York.
DEVELOPMENT OF SOCIAL AVOIDANCE IN
AUTISTIC CHILDREN
John Richer
Paediatrics Department
John Radcliffe Hospital
Oxford, England
INTRODUCTION: PROBLEMS IN STUDYING AUTISTIC CHILDREN'S

EARLY BEHAVIOUR
Numerous difficulties face anyone trying to study the early

development of autistic children. The main ones are as follows:-
Delay in diagnosis. Although early infantile autism has its

onset before a child is about 2! years old, it is rarely diagnosed
then. From the time parents first feel concerned about their child,
they often have to wait a further one or more years until a diagnosis
is made. Ornitz et al (1977) found that 50% of the families they
interviewed were concerned about their child by the time it was 14
months, but that the median age of referral for diagnosis was 46
months, a delay of over 2! years. Thus by the time the child is
diagnosed, not only is the early history inevitably in the past, but
if asked to recall early behaviour and events, the parent has to
remember much further back.
Unreliability of retrospective reports. Many researchers have

attempted retrospective studies (e.g. Wing, 1971; DeMyer et aI, 1971;
Ornitz et aI, 1977). But the unreliability of parental reports is
usually acknowledged and well documented (e.g. Wenar, 1963; Robbins,
1963; Hefner and Mednick, 1969). Retrospective reports are especially
unreliable when the parents' own behaviour and parent/infant inter-
action (e.g. DeMyer et aI, 1971) are reported, less unreliable when
infants' "milestones" (e.g. Ornitz et aI, 1977) are reported (Wenar,
1963; Mednick and Shaffer, 1963).
241
242 J. RICHER
"Guilt" factors. The majority of parents of handicapped children
feel guilty enough, where there is no clear "organic" cause, their
guilt is often increased. Some of the early autism literature further
compounded this guilt by seeming to "blame" maternal handling for a
child's condition (Bettelheim, 1967; Ferster, 1961). This may partly
account for why it often takes several months for some parents to
describe certain factors e.g. marital discord, surrounding their
child's early life. This adds to the unreliability of retrospective
data.
Unfeasability of prospective studies. Prospective studies of

infantile autism would be prohibitively expensive. Since the
prevalence is only between 2 and 4 per 10,000, about 70,000 children
would need to be followed up to achieve an autistic group of only
about 20. In addition, no clear risk factors common to the whole
group had been identified to reduce that number.
Simplistic views of development. Discussion of autistic

children's ontogeny have not been helped by simplistic attempts to
find the "primary cause" of autism or by asking whether the cause
is "organic" or "environmental". Worst of all, many researchers
have investigated children once they are autistic, sometimes once
they have been several years autistic, and having found a difference
between autistic and control group children, (the "deficit") ascribe
to that deficit primary causal significance (too many to mention but
e.g. Rutter, 1968; Wing, 1971; Ornitz, 1971). These arguments con-
fuse correlation and cause and forget the child's intervening develop-
ment.
Lack of precise behavioural descriptions. Plotting the develop-

mental history of anything requires, most obviously, good description
of what the history is of. The point of the endeavour is somewhat
lost without it. Yet, for autistic childrens's social behaviour, this
description is deficient or not agreed. Social behaviour is central
to the diagnosis of early infantile autism, but only impressionistic
clinical descriptions come close to be, agreed, and to my mind Kanner's
original descriptions (Kanner, 1943) have rarely been bettered for
clarity and imediacy. But a reasonably detailed, comprehensive and
non-impressionistic non-inferentional description of observable be-
haviour is not agreed. Instead, the children are still described as
"aloof", "withdrawn", "failing to distinguish self from others",
"failing to make sense of gesture, language", and so on, which are
hardly simple publicly observable aspects of behaviour. There are
many reasons for this lack of progress. One is that the subject is
surrounded by some emotion and controversy, so many have preferred
to concentrate on other areas of functioning, language, cognitive
function, rigidity of behaviour, learning, etc. Some people active
in this field still sadly suffer from the unthinking reaction that
anyone examining social behaviour of autistic children is ipso facto
"blaming" the mother for her child's condition (e.g. Howlin:-r9~
SOCIAL AVOIDANCE IN AUTISTIC CHILDREN 243
This is logically absurn. Another more interesting reason is that

social behaviour has, until recently, been an area where psychology
and psychiatry have been particularly weak. Researchers have often
relied on tapping the opinions of people close to autistic children
with such devices as rating scales and questionnaires (e.g. Wing and
Gould, 1978), whose applicability to children, who by definition are
difficult to communicate with and difficult to understand, is particu-
larly questionable.
To summarise, studying the early development of autistic children

is fraught with difficulties. The development in question has inevit-
ably occurred by the time diagnosis is made, that diagnosis is often
delayed by one or more years, retrospective reports are unreliable,
especially those concerning parent/child interaction and made more so
by the delay in diagnosis, guilt factors surrounding autism may well,
and understandably, affect recall, prospective studies are not feasible,
simplistic views of development have often been adopted, and finally,
a good description of autistic children's behaviour, especially their
social behaviour, has not been agreed, so exactly what it is that the
developmental history of which is being sought, is unclear.
In this paper, I shall put forward a description of autistic

children's social behaviour and of it ask three of Tinbergen's "four
whys" (Tinbergen, 1963) concerning firstly causation, secondly con-
sequences, and thirdly ontogeny the central question of this paper.
After that, I shall draw some implications from therapy and describe
preliminary results.
SAMPLE CHILDREN
The autistic children I observed numbered well over 50 and ranged

in age from 18 months to young adulthood, from being severely mentally
retarded to being of normal intelligence, and from being grossly dis-
turbed with frequent, highly stereotyped behaviour, no language, and
very little social interaction, to being only mildly disturbed with
only a few obsessional features to behaviour, adequate language for
many situations, and many more social interactions. All conformed
to Rutter's criteria (Rutter, 1978). These are:
1. Onset before 22 years

2. Failure to develop emotional relationships with people.
3. Ritualistic and compulsive phenomena.
4. Language peculiarities and retardation.
METHODOLOGY
Whilst individual problems must be approached in ways best suited

to those problems, and not be constrained by a particular method, the
244 J. RICHER
maJor approach in the following studies was ethological. Thus the

children in the autistic sample as well as numerous non-autistic
children were observed in their everyday environments, namely home,
school, hospital, etc. and a picture of their behaviour built up.
The precise details of quantitative observations and experiments as
well as the exact nature of samples involved are reported elsewhere.
In this paper I shall try and construct an overall story rather than
give precise methodological details.
AUTISTIC CHILDREN'S SOCIAL BEHAVIOUR
I shall make a somewhat crude distinction between social approach

and social avoidance behaviour. Social approach behaviour is behaviour
by which, or associated with which, social interactions are started
or continued. Social avoidance behaviour is behaviour by which, or
associated with which, social interactions are avoided or escaped from.
Examples from these two categories are given in the appendix. It will
be seen that the category of social avoidance is the same as that of
flight behaviour (Grant, 1965).
The major description of autistic children's social behaviour

is that they show much more avoidance and much less approach behaviour
than non autistic children. In motivational terms, they are predomin-
antly avoidance motivated (Currie and Brannigan, 1970; Richer and
Nicoll, 1971; Tinbergen and Tinbergen, 1972; Richer, 1974, 1976).
However, this is not to say that approach by avoidance behaviour such
that the child's behaviour evinces much intense motivational conflict.
It is this intense conflict between social approach and avoidance
with avoidance predominating much more than in non autistic children,
that characterises autistic children's social behaviour.
This conflict is manifested in many ways, all of which have been

frequently described in the ethological literature (e.g. Hinde, 1970).
Alternation. A child may move towards someone, then retreat;

or he may alternate orienting towards with orienting away.
Simultaneous. The most common manifestation of conflict in

autistic children is the simultaneous expression of approach and
avoidance behaviours. For example, a child may move towards someone
but with his head hung down, or he may move towards but backwards, or
he may sit on someone's lap but gaze avert and avoid further inter-
action (when the child holds on tight, this is often misleadingly
called "empty clinging"), or he may receive a proffered object (ap-
proach) but gaze avert and pull his chin in (avoidance) at the same
time.
Compromise. The most common example of compromise behaviour is

when a child stands side on to someone, neither orienting fully to-
wards nor away, when doing this the child can often be caught darting
swift glances out of the corner of his eye at the other person.
Displacement activities. Both Hutt and Hutt (1970) and myself

(Richer, 1974, 1979)have argued that displacement activities are func-
tionally equivalent to stereotypes, defined by Hutt and Hutt (1970)
as "the repetition in an invariant way of certain motor acts having
no observable goal". Certainly, stereotypes accompany other conflict
behaviour. For example, a child may approach an adult but with his
head hung down, and simultaneously grind his teeth. Displacement ac-
tivities also occur when a child is approached and performs an avoidance
behaviour, for example, when an adult may walk towards an autistic
child and as he does so, the child starts rocking. They also occur
when the child himself starts an overintense approach, for instance,
just before a child rushes towards an adult, he may jump up and down
and slap his sides.
Overintensity. Examples of this are where a child might rush up

to an adult and career into him hard, instead of approaching more
slowly, or may cling hard instead of holding more gently, or may shout
instead of speaking ordinarily. Overintensity in approach behaviour
is often seen in improving autistic children.
This then is the basic description of autistic children's social

behaviour. Following the simple structure of Tinbergen's four whys,
I shall consider causation, consequences and ontogeny in turn, omitting
evolution.
Causation
Three immediate causal factors tending to increase or decrease

the probability of avoidance behaviour will be considered. These are
the state of the child, the mutual activity, and the behaviour of
others.
State. State effects are particularly difficult to measure. It

seems~ autistic children are more likely to react with avoidance
if they have just been performing avoidance behaviour or if their
behaviour is more stereotyped. There may be diurnal rhythms too.
Autistic children are least likely to be avoiding late in the evening
and perhaps first thing in the morning, but that may be not so much a
function of time of day as of the situation, namely being a quiet
"secure" situation where adults are not very intrusive. These states
where approach is more likely may be roughly characterised as ones
of low stress. But also extremely high stress states such as illness,
injury (personal observation) starvation (Clancy and McBride, 1969),
and electric shock (Lovass et aI, 1965) produce approach behaviour.
246 J. RICHER
More accurately it is attachment that is seen, and it seems that it

simply needs greater stress in autistic children to produce this
behaviour than is the case with non autistic children, but the nature
of many of the stressors is the same.
Mutual activity. If an activity is difficult or uncertain for

an autistic child, then avoidance is more likely (Churchill, 1971;
Richer, 1974). This is true of non autistic children too, the dif-
ference lies in the threshold for triggering avoidance, in autistic
children is very low. The obverse of this is that autistic children
often approach adults for extremely simple and predictable activities.
With the more disturbed autistic children there are three main types
of activity, sitting or lying on a lap, vigorous physical play such
as tickling or being swung around, or thirdly, an attempt to get the
adult to do something specific by leading the adult sometimes by the
hand but often by holding other parts of the body (this is misleadingly
called "using the adult as an object", it is merely conflict behaviour).
The first two are extremely simple activities and typical of very young
normal children, the third is pursued by the child rigidly minimising
the uncertainty implicit in the activity, and in addition the goal is
usually not social unless for sitting on a lap or vigorous play, but
instead is concerned with getting food, a toy, going outside, etc.
Behaviour of others. Whilst threatening or violent behaviour

by others produces avoidance in both autistic and non autistic children,
avoidance in autistic children is also often preceded by non threaten-
ing approaches or others just coming near, whereas this is rarely the
case in non autistic children (Richer, 1976). This suggests a very
low threshold for avoidance in autistic children. From a number of
studies and numerous observations, it appears that avoidance is less
likely if the other person behaves in one of two ways which may be
roughly characterised as "high intrusion" and "low intrusion".
Firstly, high intrusion, the adult continually makes approaches

to a child until the child acquiesces. This usually takes two forms.
Either the adult simply holds the child (Zaslow and Breger, 1969) or
he insists the child does something which he knows the child can do.
In both situations the child shows strong avoidance for a long time,
often with screaming, back arching, stamping, etc. Finally, however,
the child's "rage" and avoidance attempts subside. If he was held,
he sometimes cries, and moulds to the adult's body, is relaxed, and
gaze fixates (Zaslow and Breger, 1969; Dyer, pers. corom., Welch, pers.
corom.). If the adult was insisting he did something, he will have
done it (the adult continues until he does). To achieve this end in
either case can take more than an hour. The relationship between the
child and adult seems considerably improved in that the child frequently
seeks out the adult subsequently and is more cooperative.
Secondly, low intrusion, the first point to be made is that

autistic children's threshold for avoidance is extremely low (Richer,
1976). Given this low threshold it has been shown that avoidance is
less likely and approach more likely when an autistic child is not
gazed at (Hutt and Ounsted, 1970; Richer and Coss, 1975) or not reacted
to with intense smiles, talking, and other strong social signals
(Richer and Richards, 1975). The situation is not quite as simple
as that for there are times when autistic children react with further
approach to being looked at, smiled at, and so on. This is often In
vigorous physical play or very quiet, slow, simple interactions.
The effect of the "intrusiveness" of the other person and the

uncertainty of the mutual actIvIty seem to interact. Both uncertainty
and intrusiveness tend to promote avoidance, but if the activity is
very predictable then the autistic child tolerates more intrusiveness
without avoidance than if the activity is more difficult. The effect
of these causal factors and their interaction is worth analysing
further, both to define better the nature of low intrusion and because
it is relevant to therapy. This is best done within the framework of
a discussion of communication in autistic children.
Communication
Concept of communication. In ethology two individuals are said

to have communicated if it can be demonstrated that the behaviour of
one has influenced the behaviour of the other (Cullen, 1972). In this
sense, the terms "communication" and "social behaviour" become virtu-
ally interchangeable (Blurton-Jones, 1976). Autistic children are
frequently described as non communicating, and some theorists have
even suggested that autistic children fail to make sense of all social
signals (Wing, 1978). Using the term communication in the way just
defined, it is clearly false that autistic children are non-communi-
cating, since their social behaviour is not random.
Directed communication. It is useful to distinguish a sub-class

of communication behaviour: directed communication. Its behavioural
criteria are pausing and attending after an act (after "sending a
message"). In humans, this often takes the form of pausing and looking
at the other person. The participants take turns. Kendon (1967)
describes this in adult conversations, and Richards (1974) and Bruner
(1975) note the existance of this behaviour pattern in the first year
of life. Their basic form is as follows: The first person A says
or does something, stops, and looks at B. B very often looks away
and then replies, and so on. We may say that the changeover point
is the point of maximum uncertainty for both participants, for A be-
cause he doesn't know what B is going to reply - so he looks, and for
B because the reply is not yet formulated - so he looks away (in order
not to overload channel capacity (Kendon, 1967).
It is these types of interaction that autistic children especially

avoid (Richer, 1978). One important way in which non-autistic individ-
uals negotiate shared understandings from infancy onwards (Newson and
248 J. RICHER
Newson, 1975) is in directed communication interaction such as these.

These meanings are often attached to symbols - words, signs, formal
gestures, and so on. The term "intersubjectivity" (Trevarthen, 1974;
Newson and Newson, 1975) generally refers to the fact and the process
of sharing meanings. It points to the fact that we see others like
ourselves - as subjective active agents - and treat them as such.
People find it difficult to see autistic children in this way and
refer to them as " living in a world of their own", "being impossible
to get through to", "difficult to communicate with", "difficult to
understand". The major reason why people get this impression, and
why autistic children fail to learn language and other symbolic systems
with shared meanings is that they tend to avoid the directed communi-
cation interactions in which these meanings are acquired and refined.
Why should autistic children especially avoid these interactions?

I suggest it is because a number of causal factors conspire to produce
avoidance in them. Let us suppose the autistic child is the first
person A in the schema just described. Having done some social be-
haviour, he ought then to pause and look at the other person. Unfor-
tunately in th~s interaction this is a point of maximum uncertainty,
also the other person is being reactive, two causal factors which
promote avoidance, and in fact the child avoids at that point (Richer,
1978). Let us put the autistic child in the position of the second
person B. Here someone has made an approach and has paused and is
looking at the child. Again, there are two causal factors conspiring
to promote avoidance, namely uncertainty and being looked at, the
child avoids (Richer, 1978). By avoiding in these situations the child
(as B) reduces the number of social behaviours he tries out; and should
he attempt one (as A) his attention to their feedback from the other
person is also diminished.
Let me place within this framework the inter-relationship between

uncertainty and "intrusiveness". It follows from the foregoing argu-
ments that the more uncertain is the child at the changeover point
when he is B and has to reply, the less intrusive can the other person
be if the child is not to avoid. Unfortunately a further mechanism
comes into play where the longer the child delays replying, the more
intense is the other person's attention to him, waiting for his reply.
In a study of teachers with autistic children, the main teacher's
behaviour which was significantly more frequent when they were with
autistic children compared to non autistic children was craning round
to look in the child's face, in other words, signalling intense at-
tention to the child's reply (Richer, 1978). (From the child's point
of view, we may argue that the more intense the adult's attention to
his reply, and the less likely the child is to give one, the more
that attention becomes a "demand" for one. Such a demand is met with
avoidance).
The dynamic nature of the low intrusion style is perhaps becoming

a little clearer in that intrusiveness is a function not only of the
adult's behaviour but of its t1m1ng, its relation to the child's

uncertainty about the activity and the child's state. I shall discuss
this further in the section on therapy.
An extreme case perhaps highlights a constraint on information

transfer and learning suffered by autistic children. Learning takes
place where there is information transfer, and this happens only when
there is uncertainty to be reduced. The interrelationship of un-
certainty and intrusiveness could hypothetically give rise to an ex-
treme situation in which an extremely disturbed autistic child will
only tolerate intrusiveness when there is no uncertainty in the situ-
ation, but will avoid when there is any uncertainty. In this extreme
case, the hypothetical autistic child will tolerate social interactions
only when there is nothing to be learnt, and avoid those where there
is. No child is like this, but some approach it and a constraint on
autistic children's learning from others is illustrated.
Consequences
There are many interesting consequences of avoidance, but I shall

consider just one, and that is its effect on the social approach be-
haviour of adults. In numerous situations, especially teaching or
attempted play or conversation, an autistic child's avoidance is
frequently followed by an adult's approach. In teaching situations,
where I first noticed it, the interactions proceed as follows. The
child is successfully performing a task, but then meets a difficulty
and quickly gives up and performs some avoidance and perhaps stereo-
typed behaviour. At that point the teacher intervenes - to help.
Unfortunately the teacher is approaching at a time when not only is
the child meeting difficulty but also he is in a state where avoidance
is more likely, having just performed an avoidance behaviour. The
child usually performs further avoidance. The teacher makes renewed
approaches and the interaction continues like this with classrooms
ringing to the tones of "sit down" or "look at it" until usually the
teacher gives up. The essential features are that the child's avoid-
ance is followed by the adult's approach. After that, autistic chil-
dren tend to show more avoidance behaviour in contrast to non autistic
children who usually show further approach behaviour thereby resuming
the interaction (Richer, 1974, 1978). Eventually the adult usually
gives up and the encounter ends with the child continuing to perform
avoidance.
This immediate consequence of avoidance and the way the inter-

action subsequently develops has further long term consequences.
The argument goes like this. Because an autistic child avoids when
the adult makes approaches, we may deduce that the adult's approaches
are aversive. Encounters with adults are characterised by repeated
approaches by them, when the child is avoiding. From the child's
point of view, we might say that the adult makes repeated approaches
250 J. RICHER
even though the child is avoiding. Therefore, these social encounters

are aversi~e. Therefore, the tendency to avoid such encounters is
maintained. Two things should be noted. Firstly, these sequences
of events would be much less likely if the child's threshold for avoid-
ance were not so low. After all, they occur much less often in non
autistic children. Secondly, it would be wrong to call the adult's
behaviour "abnormal". After all, that behaviour "works" with non
autistic children in the sense that the interaction of child and adult
mutual approaches resumes. So we may conclude that this is one mecha-
nism by which autistic children's social avoidance maintains itself
albeit via "normal" behaviour of the adult.
Other interesting longer term consequences of avoidance include

the severe constraints it places upon learning language and other
social skills, leaving autistic children particularly deficient in
these areas (Rutter, 1968; Wing, 1971; Richer, 1978). In general, we
can conclude that avoidance puts constraints on an autistic child's
acquisition of his culture (Richer, 1978).
Ontogeny
Earlier I have argued that many attempts to discover the aetiology

of autism were flawed in many ways, including researchers being unclear
about precisely what it was they were asking aetiology of. Here it is
clearer, we are examining the development of the predominating social
avoidance seen in autistic children. Two questions will be addressed.
Firstly, how is predominant avoidance maintained? Early infantile
autism has, it must be remembered, a very poor prognosis (Kanner, 1971)
Secondly, how do autistic children become predominantly avoidance moti-
vated?
The first question has already been given a partial answer. I

would argue that the behaviour that autistic children's avoidance
elicits from adults - mothers, teachers, nurses, etc. - only serves
to maintain that avoidance. The youngest autistic child I have ob-
served was 18 months old and his behaviour was characterised by the
same avoidance with the same causes and consequences as I have seen
in older children. In particular, his interaction with his mother
frequently took the same course as interactions observed between older
autistic children and their teachers, nurses, and other adults. The
boy showed strong avoidance, and if the mother was attending to him,
this usually elicited approach from her. Often the correlation was
striking and an intensification of the child's avoidance would immedi-
ately be followed by an approach behaviour from the mother, often
taking the form of calling the child's name. By chance this boy had
a twin sister who was not autistic. Interactions between her and her
mother were very different and "within normal limits". Thus, even
at this early age, one factor maintaining avoidance is the behaviour
which the child's avoidance elicits from his mother and other adults.
This is consistent with the little evidence that exists on paren-

tal attitudes and behaviour in the families of autistic children.
The general finding is that these parents do not differ significantly
or meaningfully from parents of other groups of children, usually dys-
phasic children (Kolvin et al 1971b; Cox et al 1975; Cantwell et al
1978; McAdoo and DeMyer, 1978). However, most data gathered in these
studies is somewhat gross and evaluative. These authors use this data
to contradict earlier suggestions that parents of autistic children
are cold, undemonstrative, formal, introverted and obsessive (e.g.
Kanner, 1949; Eisenberg, 1957) whose behaviour has contributed to the
production of the child's autism (Bettelheim, 1953; Ferster, 1961).
Since the latter authors collected their data on parents of children
already autistic, the former workers are correct in arguing that their
data contradicts the latter's data base. Neither group, however, can
properly claim to have data which looks directly and in detail at the
child's ontogeny before diagnosis.
This brings us to the second and more difficult of the two onto-
genetic questions posed earlier, namely how did the child develop to
become so predominantly avoidance motivated? First, let me summarise
the factors so far discovered which at least correlate with autism.
Genetic factors. The rate of mental illness in the families of

autistic children is no higher than the general population, the proba-
bility that siblings will be autistic if one is is about 2%, or 50
times, the general population rate (Folstein and Rutter, 1978). Cole-
man and Rimland (1976) found a higher percentage, 8%, when the exten-
ded families (via. at maximum 4th degree relatives) was considered.
In a twin study, Folstein and Rutter (1978) found a 36% concordance
rate for autism in monozygotic male twins, but no concordance in di-
zygotic twins. Their data suggested that this concordance could not
be accounted for by commonly experienced detectable pre- or perinatal
difficulties. Since virtually no autistic people have offspring, this
line of genetic investigation is closed. But this fact naturally poses
the question of why the problem should persist. One hypothesis comes
from Ounsted (1974) who suggests that autism is the result of the
"assortive mating between two parents, each carrying some of the gene,"
which added together "predispose affected children to developing, at
an early age, a pattern of behaviour which is like that of extreme
introversion". Without this additive effect, individuals are often
highly successful, parents of autistic children without evidence of
"cerebral dysfunction" come from higher socioeconomic classes and have
higher I.Qs than average (e.g. Kolvin et aI, 1971d; Lotter, 1967).
Pre- and perinatal problems. There is an increased rate of pre-

and perinatal problems. Pollack and Woerner (1966) single out tox-
aemia, vaginal bleeding and severe maternal illness as being relatively
common prenatally. Kolvin et al (197la) find that nearly half their
sample suffered pre- and perinatal problems (see also e.g. Lotter,
1967; Whittam et aI, 1966; Links et aI, 1980). Birthweight is not
252 J. RICHER
lower than average in the autistic group (Links et aI, 1980). Although
not found in earlier studies, more recent studies find that maternal
age is higher than average (Links, 1980).
Signs of "cerebral dysfunction'. In addition to the circumstan-

tial evidence from pre- and perinatal problems, more direct evidence
of "cerebral dysfunction" from neurological, epileptic and E.E.G. data,
is found in a large percentage of autistic children, over one third
in the sample of Kolvin et al (197lc). Kolvin et al (197ld) also
find that the children with evidence of "cerebral dysfunction" did
not show the usual socio-economic class bias towards social classes
1 and 2. Autism has also been seen in conjunction with a wide variety
of conditions such as retrolental fibroplasia (Keller, 1954), infantile
spasms (Creak, 1963; Taft and Cohen, 1971), cerebral lipoidosis (Creak
1963), phenylketonuria (Wing, 1966), Addison's disease (Money et aI,
1971), coeliac disease (Goodwin et aI, 1971) and congenital rubella
(Wing, 1969).
Minor physical anomalies. A raised incidence of minor physical

anomalies has been found in autistic children compared to normal con-
trols (Walker, 1977) but no clusterings indicative of delineated syn-
dromes were apparent. Minor physical anomalies increased with maternal
age but are not related to pre- and perinatal problems (Links et aI,
1980). Children with more minor physical anomalies have lower I.Q.s,
more hospitalisation in the first three years of life, but less family
psychopathology (Links et aI, 1980).
Delayed early development. As might be expected in a group charac-

terised by a high rate of mental retardation, autistic children's
early milestones in development are generally delayed, this if found
from both retrospective studies (Ornitz et aI, 1977) and from the un-
usual data base of home movies of babies before diagnosis (Rosenthal
et aI, 1980).
Early major stresses. Although parents often date deterioration

from some event like the birth of a sibling, illness, change of house,
the prevalence of extreme early stresses for the autistic group as a
whole, has not been found to be significantly greater than in dysphasic
control children (Cantwell et aI, 1978).
Family factors. Parents of autistic children differ as a group

in tending to be of higher socioeconomic class and slightly higher
intelligence. The child is also more likely to experience two languages
at home either because the parents first languages are different or
because the parents live abroad (Kolvin et aI, 1971a). Otherwise most
recent studies fail to find factors which significantly differentiate
the parents and families of autistic children from others (e.g. Cant-
well et aI, 1978), however, most used procedures such as personality
questionnaires, family interviews, or other gross measures or obser-
vations of parental or family functioning.
From these data it is clear that no simple single early factor

or combination of factors even correlates with all cases of autism
let alone has been shown to cause all cases. Even where it is clearly
shown that there is a raised prevalence of some factors in the autistic
group, no mechanism has been convincingly demonstrated whereby these
factors lead to autistic behaviour, in most studies the mechanism is
not even suggested. It may be concluded that these children seem to
come to autism via a variety of different developmental paths (Kolvin
et aI, 1971c). However, it can be claimed that when looking at the
aetiology of an individual case genetic, pre- and perinatal, neuro-
logical and biochemical and social factors should all be considered.
Where does this leave us? It seems that the approach comparing
static factors in groups of autistic children and control groups,
though useful, has not yielded a clear picture. An additional approach
is needed. The one I propose is simple and familiar in ethology.
I propose to examine the ontogenies of individuals and look for cornmon
processes. These processes may not be influenced by exactly the same
factors in different individuals although the effect on the process
may be similar. I shall start from the end point of the autistic
child's behaviour and try and work back to discover processes which
could lead to it (cf Clancy and McBride, 1969, 1975). Unfortunately
because of all the difficulties involved in this developmental question
and in particular because these processes are lost in the past of each
child, direct data is rarely possible to obtain. Two approaches will
be used. Firstly, there exist a number of reports of processes leading
to avoidance and other "autistic behaviour" and these will be described.
Secondly, data will be analysed from individual children's histories
and early home movies (Massie, 1978a) to see if any of these processes
seem relevant.
Processes leading to social avoidance and other autistic behaviour.

Studies chiefly on monkeys show that prolonged social isolation from
birth leads to behaviour very similar to that of autistic children
(Harlow and McKinney, 1971). However, because these studies are of
non humans, and because such drastic isolation is virtually unknown in
autism, I shall consider these further.
Two sets of results are relevant. The first comes from the work
of ~1ain (1975) carried out within the framework of attachment theory.
The findings of interest here are that there is a small percentage
of home reared, normal, one year old children who, after a couple of
brief separations of only a few minutes each from their mothers, show
for a short period strong avoidance behaviour of their mothers upon
their return which is very similar to the avoidance of autistic
children. Such avoidance is also seen in most children after prolonged
separation as the early studies of the Robertsons and Bowlby showed
(Bowlby, 1969). After reunion, this avoidance later gives way to much
clinging, crying, attention seeking and other intense attachment
behaviours. Main finds that her avoidance prone babies are also more
254 J. RICHER
likely to show stereotyped behaviour, odd movements, odd vocalisations

and a tendency to approach mothers tentatively and touch unusual body
parts. Their mothers tended to engage in less physical contact and
be less expressive than mothers of less avoiding children. These
children show behaviour typical of less autistic children but to a
very mild degree, and it did not persist in the way that autistic
children's behaviour does. However, it does show'that the security
threatening event of a brief separation can trigger strong avoidance
in some "normal" children. Such brief separations may not be unCOlmnon
in many infants lives, they would certainly not be picked up by the
measures of early stress events used, for instance, by Cantwell et al
(1978). Insofar as the children Main describes were insecure, at least
for the period after separation, we may call autistic children extremely
insecure children. Like young normal children suffering insecurity
due to separation, their exploration is reduced (Cox and Campbell,
1968; Ainsworth and Wittig, 1969).
The second source of process data comes from observations of early

mother/child interaction (Brazelton et al, 1974). They report that
babies behaviour cycles between social attending and non attending.
Some mothers cue into this and make approaches mainly in the socially
attentive phase; in such cases the infants' social attention phase
tends to increase in length. Other mothers however did not cue into
this rhythm and keep up a constant barrage of approaches, or try and
establish their own rhythm; these infants' social attention phase tends
to diminish and some even show downright avoidance to some of the
mother's approaches. Brazelton et al (1971) and Stern (1977) describe
the development of avoidance behaviour and lack of exploratoriness
in some infants who experience this type of handling, such that these
authors feared the children would become autistic. They did not, but
the description of the process remains valid. As before, we may con-
clude that the child is insecure, and is so as a result of mothering
characterised as "intensive" (Ainsworth et al, 1974). These authors
in fact describe one manifestation of insecure attachment as "prox-
imity avoiding behaviour that effectively blocked the activation of
attachment behaviour and resulted in a degree of independence that
seemed both premature and inappropriate" (Ainsworth et al, 1974).
It must be emphasised that insensitivity is a characteristic of the
mother-child relationship and not only of the mother, some children
are easier to mother sensitively (Bernal, 1974). It must be further
emphasised that none of these children became autistic so that such
mothering is unlikely to be a sufficient condition for the development
of autism, however the process remains relevant.
Data from autisitic children. Some background factors which may

increase a child's vulnerability to autism have been mentioned above,
but their direct connection with social behaviour is not immediately
clear. It is difficult to gather data on aspects of autistic child-
ren's early behaviour relevant to social interactions. Evidence is
scarce and mainly retrospective. From case histories, Clancy and

McBride (1969) suggest four features characteris,e children in the first
year of life. These are as follows:-
1. Lazy sucking associated with long and tiresome feeds.
2. Absence of smiling response.
3. Quiet, undemanding behaviour when left alone, but irritation

when disturbed, baby squirming to be put down.
4. Unresponsiveness to the human voice.
Individually, these behaviours are not specific to autism, but

autistic children differ in that the presence of all is reported
(Clancy and McBride, 1969). These authors argue that these behaviours
function to shape an abnormal mother-child bond, or express one.
An interesting source of a small amount of developmental data

comes from detailed analysis of home movies of children later diagnosed
as autistic, collected by Massie (1978a). Unfortunatly, autistic
children are grouped with children with childhood schizophrenia and
symbiotic psychosis, so Massie's group data (e.g. Massie, 1978b) may
not be relevant. However, he reports 10 individual cases, four of
whom receive a diagnosis of autism (Massiem 1978a). In three, the
baby is described as "lifeless" "placid" "less than normal activity"
"less vigorous" "lacking visual pursuit", the other was described as
more "irritable". Either style of behaviour suggests that these autis-
tic children were more difficult to mother sensitively. Massie's
observations from the home movies indeed suggest that mothering was
not very sensitive. One mother repeatedly avoided gaze fixating her
infant despite its strong attachment behaviour up to the age of six
months after when the child initiated less and became more self ab-
sorbed. Another mother was described as strikingly stiff and self
contained, did not initiate cuddling or show playfulness or mould
herself to the baby. By five months the baby was observed to struggle
away from being held by the mother, and in later films only briefly
to gaze fixate. Another mother was described as "physically brusque
and coercive and apparently insensitive to the children's moods or
wants". The "children" were identical twins, and interestingly the
one who developed normally was the more vigorous of the two. The
fourth mother, of the more irritable child, was described as "stiff,
self concious, always grooming herself". She fussily adjusted his
clothes without holding him close or touching him. Her face was tense
and fixed in an angry smile. Neither parent was observed facing the
child whilst playing with him and when playing, often stopped each
tiI]1e the child started to smile. Massie notes that the father too,
showed the "same tenseness and lack of recipocity with the baby and
lack of awareness of the boy's moods or rhythm".
256 J. RICHER
The contribution of parent and child to this relationship where

the adult's parenting is insensitive cannot be partialled out from
this data and from the point of view of the relationship, it is neces-
sary to do so.
To summarise, some security threatening experiences can lead to

insecurity and periods of predominant avoidance behaviour and other
autistic like behaviour. These include separation or insensitive
mothering. But the probability of producing avoidance differs between
children depending in part on the prior behaviour and relationship
(Main, 1975, see also Hinde and Spencer-Booth, 1971). The small clues
to the early behaviour and interactions of autistic children suggest
that many are likely to have been difficult to mother sensitively
through apathy and lack of vigour and/or irritability, both of which
make it difficult to "mesh" with the child in social interaction, and
make such interactions often unrewarding for the mother. Furthermore,
from the analysis of home movies, some mothers' behaviour was charac-
terised by lack of sensitivity in that relationship.
The final source of evidence comes from retrospectively plotting

the developmental histories of autistic children. My own contribution
to this work is still in progress, but its early results confirm pre-
vious findings (e.g. Kolvin et aI, 1971a). From the histories of some
autistic children it seems clear that children su~fer deterioration
after certain events. This deterioration usually takes the form of
increased social avoidance, increased stereotyped behaviour and halting
or regression of development, especially social and language develop-
ment. This deterioration is reported as sudden or occurring gradually
over a period of a few weeks or months. The events in question were
classically those which elicit attachment behaviour and insecurity
if that attachment behaviour is not satisfied. These include, as is
often reported, birth of a sibling, move of house, or illness, but
also separation from parents and injury, and sometimes it seems that
mother was depressed or there was marital discord (which is often only
admitted after the parents have been known for some time and trust
has been built up).
Two case histories will illustrate this.
Case I. An autistic boy of normal non-verbal intelligence at

three, came from a family where his maternal grandfather had gone
through an "autistic" period when younger, and maternal uncle had re-
ceived special schooling for his autistic behaviour. The parents were
young, and mother depressed after his birth. He was said to develop
normally until 20 months when his sister was born. Just before this,
the marriage was very poor and near breakup. His mother was again
depressed after his sister's birth and at that time the family also
moved house. His behaviour started to deteriorate. At 26 months a
boiled sweet got stuck down his throat and he almost suffocated, and
about that time he was scalded with boiling coffee. At 27 months
the family went on holiday to the seaside. After this his autistic
behaviour was well established and his language and social development
virtually stopped for over two years until he started school.
Case II. A severely retarded autistic boy was the first child
of his mother's second marriage, she having had four normal children
by her previous marriage. He was said to develop normally up to 11
months when he was taken ill one evening and rushed to hospital. The
nurse insisted mother leave immediately. The ward was dark. The boy
remained in hospital for the next week with only daily visits from
his parents. His behaviour started to deteriorate markedly. At 18
months the family moved from their previous home and stayed with the
maternal grandparents for two months before moving to their new house.
During this period the boy was in a road traffic accident and trapped
face down between the front and back seats of the car for some time.
During the period from 11 to 20 months his behaviour deteriorated
until he was severely autistic. However, a definite diagnosis was
not made until he was 41 months although the family had been receiving
help before that. At 48 months the child suffered some "blank spells"
and the possibility of seizures is currently being investigated.
Other case histories contain no reports of such major security

threatening events correlating wit~deterioration in the child's be-
haviour. Clancy and McBride (1969) argue that the child's behaviour
was often odd before these events and that in some cases the parents
over emphasise these events in order to understand better their child's
aetiology. However, the evidence seems fairly strong from a number
of testimonies like this and from such data as early snapshots of the
children that these events at least produced a significant deterio~
ration in the child's behaviour and this is all that needs to be shown
to support the process view put forward here, namely that increased
avoidance and insecurity have as one group of casual factors major
security threatening events. Other factors will include more subtle
aspects of mother-child interaction, and the child's own vulnerability.
Finally, a speculation on the nature of the child's vulnerability.

Whatever brain system is involved, it seems it has to be one which is
both affected by a wide variety of aetiological agents and whose own
effects pervade behaviour. The over arousibility hypothesis of Hutt
et al (1965) might fit this, or more recent hypotheses concerning the
overactivity of the dopaminergic reward system (Richer, 1979). From
animal studies it seems that this system's overactivity is associated
with cut-off behaviour, lack of exploration and stereotyped behaviour
(Crow and Gillbe, 1974). Perhaps the placidity and lack of vigour
of infants who later become autistic is an attempt to keep this system's
activity down, and their irritability when stimulated a function of
its over activation. If parents of autistic children have relatively
active dopaminergic systems they might have passed on a "double dose"
of this tendency to their children increasing the likelihood of zest
and overactivity. Interestingly, Crow (1976) has argued that dopamin-
ergic reward system activity mediates appetitive behaviour, so we may
258 J. RICHER
speculate that the parent's dopaminergic reward system activity is

high, but not too high, and that this might mediate their drive and
success, and be one factor accounting for the skew socioeconomic class
distribution.
THERAPY
The implications of this analysis for therapy have some novel

and some well accepted aspects. Firstly, the goals of therapy. These
are:
- To decrease social avoidance and increase social approach

behaviour.
- To increase social skills especially in turn taking communi-

cative interactions and to develop language skills.
- To improve security of attachment between the child and his

mother and other care givers.
How is this done?
It is widely agreed that early detection is of paramount impor-

tance, and here the main burden rests with G.Ps, health visitors.
Parents occupy a central place in delivering treatment to the

child. Once the child is diagnosed, an important first step is to
try and give the parents understanding of the child's extremely con-
fusing and distressing behaviour. I found that most parents find use-
ful a formulation based on the analysis I have presented. This is
partly because it asserts that these children in most aspects differ
only in degree from normal children, and also because it does not rely
on jargon, catch phrases or appeals to ill understood "deficits" and
the like.
Coupled with this attempt to increase understanding and meaning

of the child's behaviour are recipes for action. In outline these are
as follows.
Concerning the activities that parents should try and do with

the child, these should, as is widely accepted, be clear, predictable
and well structured. Often they will seem over simple to parents,
but the emphasis is on having successful interactions to reduce the
child's avoidance motivation. As to teaching particular skills, two
points are made. The first is that autistic children learn a con-
siderable amount by observation and covert practice. It is not un-
common to find a child avoiding attempts at a task for a long time
and seeming to learn nothing, only later, suddenly, to display complete
competence at the task. The second point accommodates these children's
low frustration tolerance. Skills often have to be taught using back-

ward chaining and similar techniques.
The main novel therapeutic suggestion lies at the heart of the

analysis of social behaviour, and it concerns the adult's social be-
haviour towards the child. As implied by the casual analysis, adults
should adopt either a low intrusion or a high intrusion approach. The
same adult can ad@pt 0ne in one situation and another in another situ-
ation. The important thing is to avoid the interactions of repeated
child avoidance and adult approach which I have argued help maintain
avoidance.
In the low intrusion approach, the adult chooses clear, simple,

predictable activities, to maximise the chances of success, but does
not engage in excessive gaze fixation, talking, smiling, or other
social signalling, and does not shower the child with praise in a way
beloved of behaviour modifiers, she tries to monitor the child's un-
certainty about the activity and the child's motivational state, and
adjust the intensity of her social approaches accordingly.
In the high intrusion approach, the adult maintains her approaches

to the child. This takes at least two forms. In one the adult finds
the child is not doing something that she feels he should do and knows
he can do. An example with older children might be the child refusing
to put on his coat. The adult firmly insists that he does this. ·This
firmness is met with increasingly intense avoidance, screams, etc.
Eventually the child acquiesces. The relationship is usually consider-
ably improved. However, this confrontation may well take more than
an hour and the adult needs to be free from interruptions during this
time. This is often difficult at home and even in school or other
institution. However, some accounts written by parents claiming success
with their child seem to be using the high intrusion method of firmness
(e.g. Copeland and Hodges, 1973).
A very successful variant of this high intrusion firmness is

found in Clancy and McBride's therapy (Clancy and McBride, 1969; 1975).
They bring mother and child into a clinic. They utilise the fact that
almost all children have food fads. With mother present they offer
the child only the food he usually refuses. He refuses it. This
continues meal after meal. The child receives fluids and his physical
condition is monitored. Eventually the child eats. This can be after
as many as 17 days. Towards the end, and especially after the child
"gives in" he is much less avoiding and more sociable. His mother,
too, shows increasing concern for her child, not surprisingly. All
through this and afterwards, the child is continually approached and
intruded upon. Some days after the child has eaten, the therapy is
transferred to home. Considerable success, with treated children
attending primary school, is reported for this therapy. It is concep-
tualised by Clancy and McBride (1969) in terms of attachment theory,
intense therapy being seen as a way of quickly facilitating strong
bonding between mother and child.
260 J. RICHER
Another high intrusion method is holding. Here the adult holds

the child, usually on her lap, firmly but allowing him some movement.
The child usually struggles to escape, he screams, back arches, and
performs many behaviours indicative of considerable distress. Eventu-
ally, after perhaps more than an hour, the child quietens, perhaps
cries, moulds to the adult's body, gaze fixates and may be clearly
felt to relax.
Holding has been used by a number of therapists (Zaslow and Breger,

1969; Dyer, pers. comm., Welch, pers. comm.). Two types of holding
and holder, need to be distinguished. In one, the child will be very
distressed already, perhaps having a tantrum, and being destructive.
He is held until he calms down and then released and ordinary activity
resumed. This may be done by parents or others such as teachers or
nurses etc. The implicit message to the child is that the preceding
behaviour was not acceptable but that he is still loved and wanted
and containable. The other type of holding need not be precipitated
by behaviour in need of containment, although it is often easier if
it is, the holding continues after the child calms down with much in-
timate touching, talking etc. This should be done only by parents,
as this type of holding I suggest is much more bonding and so inap-
propriate for teachers and other non-parents. Viewed in attachment
theory terms, the parent is showing intense retrieval behaviour to
compensate for the dearth of attachment behaviour by the child.
We may also see the high and low intrusion approaches in behaviour
therapy terms, they correspond to the two methods of treating phobias,
namely flooding and desensitisation. Here, however, the object or
situations avoided are not spiders or heights or being unaccompanied
out of the house, the situations being avoided are aspects of social
interactions.
It is interesting but not surprising that so few parents or others

adopt these techniques. In not adopting them, they are, in a sense,
behaving entirely normally. Everyday social behaviour, our ordinary
reactions, are usually more sociable than the low intrusion method
requires. On the other hand, few people are likely to be as insistent
as the high intrusion method requires. It is usually not practical
unless special provisions are made. It can feel cruel and without
support and guidance few teachers, parents, or others, will stick to
it. Adults' behaviour to autistic children almost always falls between
these two extremes. Avoidance behaviour is therefore not diminished
but instead maintained.
This leads to the final aspect of therapy that I shall discuss,

namely that of maintaining the delivery of therapy. This is often
where therapy fails because the social environment that autistic
children require for improvement is not an everyday one. The everyday
environment after all tends to maintain the avoidance. The prosthetic
environment requires considerable effort and support for its main-
tenance. Many parents and teachers find the high intrusion approach
difficult to do for several reasons. They cannot bring themselves

to do it. They feel cruel or are afraid of their own reactions, many,
especially mothers of older children, are physically not strong enough
to hold the child for a long period, many find that there is no oppor-
tunity during the day when they could be uninterrupted and so pursue
the high intrusion approach to a conclusion. The low intrusion ap-
proach, too, requires considerable sensitivity to the child's state
and considerable ability to choose and flexibly maintain appropriate
successful activities. In everyday living, such skills are not easily
come by or easily put into practice. The parents often feel caught
in an impasse. Most of their attempts to communicate with their child
are met with avoidance. On the other hand, without such attempts,
they feel there is no communication. Therefore, the most urgent prob-
lem we are currently encountering is the delivery of therapy.
A rigorous controlled treatment trial testing these approaches

has yet to be done. However, the progress of children treated in
ways consistent with these approaches is encouraging. In particular,
changes in a child's behaviour as he improves are in accordance with
the predictions of the theory. Like other insecurely attached children
an improvement in the security of attachment leads to a period of in-
tense attention seeking and clinging behaviour. In addition, such
behaviour is first seen in those situations where avoidance was less
probable and where the child, on other grounds, may be hypothesised
to be most secure.
REFERENCES
Ainsworth, M. D. S., and Wittig, B. A., 1969, Attachment and explor-

atory behaviour of one year olds in a strange situation, in:
"Determinants of Infant Behaviour", Vol. 4, B. Foss, ed.,
Methuen, London.
Ainsworth, M. D. S., Bell, S. M., and Stayton, D. J., 1974, Infant
mother attachment and social development, in: "The Integration
of a Chi ld wi th a Social World". M. P. M. Richards, ed.,
Cambridge University Press, London.
Bernal, J., 1974, Attachment. Some problems and possibilities, in:
"The Integration of a Child into a Social World". M. P. M.
Richards, ed., Cambridge University Press, London.
Bettelheim, B., 1967, The Empty Fortress - Infantile Autism and the
Birth of Self, The Free Press, Collier-Macmillan, New York.
Blurton-Jones, N. G., 1976, Ethology and the study of human communi-
cation, in: "Language and Communication in General Practice",
B. Tanner: ed., Unibooks, Hodder & Stoughton, London.
Bowlby, J., 1969, Attachment and Loss, Vol. 1, Attachment, Hogarth,
London.
Brazelton, T. B., Young, C. G., Bullowa, M., 1971, Inception and reso-
lution of early developmental pathology. A case history. J.
Am. Acad. Child Psychiat., 10, 124-135.
262 J. RICHER
Brazelton, T. B., Koslowski, B., and Main, M., 1974, The origins of
reciprocity, in: The Effect of the Infant on its Caregiver.
M. Lewis and ~ A. Rosenblum, ed., Wiley-Interscience. New York.
Bruner. J., 1975. From communication to language - a psychological
perspective. Cognition 3 (pt. 3), 259-287.
Cantwell. D. P., Baker. L .• Rutter, M•• 1978. Family factors. in:
"Autism: A Reappraisal of Concepts and Treatment". M. Rutter
and E. Schopler, ed •• Plenum Press. New York.
Churchill, D. W•• 1971. The effects of success and failure in psychotic
children. Arch. Gen. Psychiat. 25. 208-214.
Clancy. H., and McBride. G., 1969. The autistic process and its treat-
ment. J. Child Psychol. Psychiat. 10. 233-244.
Clancy. H., and McBride, G•• 1975, The isolation syndrome in child-
hood. Develop. Med. Child Neurol. 17, 198-219.
Coleman, M., and Rimland, B., 1976, Familial autism, in: "The Autistic
Syndromes", M. Coleman, ed •• North Holland, Amsterdam.
Copeland. J .• and Hodges. J .• 1973. For the Love of Ann. Arrow Books.
London.
Cox. A., Rutter. M., Newman. S .• and Bartak, L., 1975. A comparative
study of infantile autism and specific development receptive
language disorder: II Parental characteristics. Brit. J.
Psychiat. 126, 146-159.
Creak, E. M•• 1963. Childhood psychosis. Brit. J. Psychiat. 109.
84-89.
Crow. T. J •• 1976, Possible relationships between afferent pathways
and ascending catecholamine neurones. A theory of phylogenic
origins of reward mechanism. in: "Brain Stimulation Reward",
A. Wauquier and E. T. Rolls, ed. Elsevier-North Holland. Amster-
dam.
Crow. T. J. and Gillbe, C•• 1974. Brain and behaviour. A critical
analysis of the relationship between Dopamine antagonism and
therapeutic efficacy of neuroleptic drugs. J. Psychiat. Res.
11. 163-172.
Cullen, J. M., 1972, Some principles of animal communication. in:
"Non Verbal Communication", R. A. Hinde, ed. University Press.
London.
Currie, K. R., and Brannigan. C. R., 1970. Behavioural analysis and
modification with an autistic child. in: "Behaviour Studies in
Psychiatry", S. J. Hutt and C. Hutt. ed. Pergamon, Oxford.
DeMyer, M., 1971, Perceptual limitations in autistic children and their
relation to social and intellectual deficits, in: "Infantile
Autism: Concepts, Characteristics and Treatme~'. M. Rutter.
ed. Churchill Livingstone. London.
Eisenberg. L .• 1957, The fathers of autistic children. Am. J. Ortho-
psychiat. 27, 715-724.
Ferster. C. B., 1961. Positive reinforcement and behavioural deficits
of autistic children. Child Devel. 32. 437-456.
Folstein, S •• and Rutter. M.• 1978. A twin study of individuals with
infantile autism. in: "Autism: A Reappraisal of Concepts and
Treatment", M. Rutter and E. Schopler. ed. Plenum Press. New
York.
Goodwin, M., Cowen, M., and Goodwin, T., 1971, Malabsorption and
cerebral dysfunction: a multivariate and comparative study
of autistic children. J. Aut. Child Schizo 1, 148-162.
Grant, E. C., 1965, An ethological description of some schizophrenic
patterns of behaviour, in: Proc. Leeds Symp. on Behav. Disorders.
Harlow, H. F., and McKinney, W:-T., 1971, Non human primates and
psychoses. J. Aut. Child. Schizo 1, 368-375.
Hefner, L., and Mednick, S., 1969, Reliability of developmental
histories. Paed. Digest. 11, 28-39.
Hinde, R. A., 1970, Animal Behaviour. McGraw-Hill, New York.
Hinde, R. A., and Spencer-Booth, Y., 1971, Effects of brief separation
from mother on rhesus monkeys. Science. 173, 111-118.
Howlin, P., 1978, The assessment of social behaviour, in: "Autism:
A Reappraisal of Concepts and Treatment", M. Rutter and E.
Schopler, ed., Plenum Press, New York.
Hutt, C., Hutt, S. J., Lee, I, and Ounsted, C., 1965, A behavioural
and electroencephalographic study of autistic children. J.
Psychiat. Res. 3, 181-197.
Hutt, C., and Hutt, S. J., 1970, Stereotypies and their relationship
to autism, in: "Behaviour Studies in Psychiatry", S. J. Hutt
and C. Hutt:-ed., Pergamon, Oxford.
Hutt, C., and Ounsted, C., 1970, Gaze aversion and its significance
in childhood autism, in: "Behaviour Studies in Psychiatry",
S. J. Hutt, and C. Hutt, ed., Pergamon, Oxford.
Kanner, L., 1943, Autistic disturbances of effective contact. Nervous
Child. 2, 217-250.
Kanner,~1949, Problems of nosology and psychodynamics in early
infantile autism. Am. J. Orthopsychiat. 19, 412-426.
Kanner, L., 1971, Follow-up of 11 autistic children originally reported
in 1943. J. Aut. Child Schizo 1, 119-145.
Keller, W. R., 1958, Autistic patterns and defective communication
in blind children with retrolental fibroplasia, in: "Psycho-
pathology of Communication", P. H. Hoch and J. Zubin, ed.,
Grune and Stratton, New York.
Kendon, A., 1967, Some functions of gaze direction in social inter-
action. Acta Physiol. 26, 22-63.
Kolvin, I., Ounsted, C., Richardson, L. M., and Garside, R. F., 1971a,
III The family and social background in childhood psychoses.
Brit. J. Psychiat. 118, 396-402.
Kolvin, I., Garside, R. F., and Kidd, J. S. H., 1971b, IV Parental
personality and attitude and childhood psychoses. Brit. J.
Psychiat. 118, 403-406.
Kolvin, I., Ounsted, C., and Roth, M., 1971c, V Cerebral dysfunction
and childhood psychoses. Brit. J. Psychiat. 118, 407-414.
Kolvin, I., Humphrey, M., and McNay, A., (1971d) VI Cognitive factors
in childhood psychoses. Brit. J. Psychiat. 118, 415-419.
Links, P. S., 1980, Minor physical anomalies in childhood autism.
Part II. Their relationship to maternal age. J. Aut. Devel.
Disorders, 10, 287-292.
264 J. RICHER
Links, P. S., Stockwell, M., Abichandani, F., and Simeon, J., 1980,
Minor physical anomalies in childhood autism. Part I. Their
relationship to pre- and perinatal complications. J. Aut.
Deve1. Disorders, 10, 273-286.
Lotter, V., 1967, Epidemiology of autistic conditions in young children.
II Some characteristics of the parents and children. Social
Psychiatry. 1, 163-173.
Lovass, I. 0., Schaeffer, B., and Simmons, J. Q., 1965, Building social
behaviour in autistic children by the use of electric shock.
J. Exp. Res. Pers. 1, 99-109.
Main, M., 1975, Mother avoiding babies. Paper presented at the Human
Ethology Conference, Sheffield, July, 1975.
Massie, H. N., 197£a, The early natural history of childhood psychosis.
Ten cases studied by analysis of family home movies of the in-
fancies of the children. Am. Acad. Child Psychiat. 14, 29-45.
Massie, H. N., 1978b, Blind ratings of mother-infant interaction in
home movies of prepsychotic and normal infants. Am. J. Psychiat.
135, 1371-1374.
Mednick, S. A., and Shaffer, J. B. P., 1963, Mothers retrospective
reports in child rearing research. Am. J. Orthopsychiat. 33,
457-461.
McAdoo, W. G., and DeMyer, M., 1978, Personality characteristics of
parents, in: "Autism: A Reappraisal of Concepts and Treatment",
M. Rutter and E. Schopler, ed., Plenum Press, New York.
Money, J., Borrow, N. A., and Clarke, F. C., 1971, Autism and auto-
immune disease - a family study. J. Aut. Child Schizo 1, 146-
160.
Newson, J., and Newson, E., 1975, Intersubjectivity and the trans-
mission of culture; on the social origins of symbolic func-
tioning. Bull. Brit. Psychol. Soc. 28, 437-446.
Ornitz, E. M.• 1971. Childhood autism: a disorder of sensorimotor
integration, in: "Infantile Autism: Concep-s, Characteristics
and Treatment~ M. Rutter, ed., Churchill Livingstone, London.
Ornitz, E. M., Guthrie, D., and Farley, A. H., 1977, The early develop-
ment of autistic children. J. Aut. Child Schizo 7, 207-229.
Ounsted, C., 1974, A biological approach to autistic and hyperkinetic
syndromes, in: "Modern Trends in Paediatrics", J. Apley, ed.,
Butterworth~ London.
Pollack, M., and Woerner, M. G., 1966, Pre- and perinatal implication
and "childhood schizophrenia": a comparison of five controlled
studies. J. Child Psycho1. Psychiat. 7, 235-242.
Richards, M. P. M., 1974, First steps in becoming social, in: "The
Integration of a Child into a Social World", M. P. M. Richards,
ed., Cambridge University Press, London.
Richer, J. M., and Nicoll, S., 1971, A playroom for autistic children
and its companion therapy project. Brit. J. Ment. Subnorm.
17, 132-143.
Richer, J. M., 1974, The Social and Stereot~ed Behaviour of Autistic
Children. PhD thesis. Reading University.
Richer, J. M., and Richards, B., 1975, Reacting to autistic children -

the danger of trying too hard. Brit. J. Psychiat. 27, 526-529.
Richer, J. M., 1976, The social avoidance behaviour of autistic chil-
dren. Anim. Behaviour, 24, 898-906.
Richer, J. M., and Coss, R. G., 1976, Gaze aversion in autistic and
normal children. Acta Psychiat. Scand. 53, 193-210.
Richer, J. M., 1978, The partial non communication of culture to
autistic children, in: "Autism: A Reappraisal of Concepts
and Treatment", M. Rutter and E. Schopler, ed., Plenum Press,
New York.
Richer, J. M., 1979, Some mechanism underlying stereotyped behaviour.
Paper presented at Symposium on Neurological Bases of Disorders
of Learning and Development. Wakefield.
Rosenthal, J., Massie, H., and Wulff, K., 1980, A comparison of cog-
nitive development in normal and psychotic children in the first
two years of life from home movies. J. Aut. Devel. Dis. 10,
433-444.
Rutter, M., 1968, Concepts of autism: a review of research. J. Child
Psychol. Psychiat. 9, 1-25.
Rutter, M., 1978, Diagnosis and definition, in: "Autism A Reappraisal
of Concepts and Treatment", M. Rutter-and E. Schopler, ed.,
Plenum Press, New York.
Stern, D., 1977, The First Relationship. Infant and Mother. Fontana/
Open Books, London.
Taft, L. T., and Cohen, H. J., 1971, Hypsarrhythmia and infantile
autism: A clinical report. J. Aut. Child Schizo I, 327-330.
Tinbergen, N., 1963, On the aims and methods of ethology. Z. Tier-
psychol. 20, 410-433.
Tinbergen, E. A., and Tinbergen, N., 1972, Infantile autism - an
ethological approach. Adv. Ethol. 10, 1-53.
Trevarthen, C., 1974, Intersubjectivity and imitation in infants.
Paper read at British Psychological Society Annual Conference,
Bangor, Wales, April, 1974.
Walker, H. A., 1977, Incidence of minor physical anomalies in autism.
J. Aut. Child Schizo 7, 165-187.
Wenar, C., 1963, The reliability of developmental histories. Psychosom.
Med. 25, 505-509.
Whittam:-H., Simon, G. B., and Mittler, P. J., 1966, The early develop;
ment of psychotic children and their sibs. Devel. Med. Child
Neurol. 8, 552-560.
Wing, J. K., 1966, Diagnosis, epidemiology, aetiology, in: "Early
Childhood Autism", J. K. Wing, ed., Pergamon, Oxford.
Wing, L., 1969, The handicaps of autistic children - a comparative
study. J. Child Psychol. Psychiat. 10, 1-40.
Wing, L., 1971, Perceptual and language development in autistic chil-
dren: a comparative study, in: "Infantile Autism: Concepts,
Characteristics and Treatment", Churchill-Livingstone, London.
Wing, L., 1978, Social, behavioural and cognitive characteristics:
an epidemiological approach, in: "Autism: A Reappraisal of
Concepts and Treatment", M. Rutter and E. Schopler, ed.,
266 J. RICHER
Wing, L., and Gould, J., 1978, Systematic recording of behaviours and
skills of retarded and psychotic children. J. Aut. Child.
Schizo 8, 79-97.
Zaslow,~., and Breger, L., 1969, A theory and treatment of autism,
in: "Cognitive Clinical Psychology. Models and Integration",
~ Breger, ed., Prentice-Hall, Englewood Cliffs, N. J.
APPENDIX
Examples of Social Approach and Avoidance Behaviour
Social approach: Move towards, turn towards, gaze fixate, proffer,

receive, point, talk, smile, VOIce lowering in pitch at the end.
Social avoidance: Move away, turn away, gaze avert, hang head,
on periphery, face wall, relinquish, fear grin, voice rising in pitch
at the end, defensive postures e.g. arm over face or head, chin in,
hunch.
PARENTAL AFFILIATION AS A KEY REFERENCE IN THE TREATMENT OF
INFANTILE AUTISM
Michele Zappe11a
Department of Child Neurology and Psychiatry

Regional Hospital
via Mattioli n.10
Siena, Italy
INTRODUCTION: PARENTS AS THERAPISTS
In the last twenty years there has been an increased involvement

of parents in the treatment of children with infantile autism. This
trend, which is apparently becoming more and more common, involves
a number of different techniques, sometimes taking up several hours
in a parent's daytime. It has often been connected with treatments
which make little use of activities belonging to the usual sphere of
parent-child relationships. For example, strategies creating a new
type of behaviour at home such as those described by Lovaas (1979),
when the first response required is "for the child to sit in a chair
for 5 to 10 seconds" do not belong to the usual sphere of relationships
that parents establish with children. The same also can be said of
nonverbal imitation training, such as raising arms in imitation of
the therapist, followed by imitating the therapist touching his shoe,
then clapping hands, touching a table and so forth. Similar arguments
can be brought forward for other behviour therapies where parents are
requested to become therapists themselves (for adequate reviews of
the literature see Berkowitz and Graziano, 1972; Johnson and Katz,
1973; Baker and Heifetz, 1976). On different theoretical grounds
Delacato (1974) asks that parents should give special stimuli to their
affected children such as lights, rough objects to touch, etc.
The above therapeutic techniques, despite minor differences, seem

to share a linear approach to human behaviour and difficulties, i.e.
a pathological situation has a cause or a set of causes. This approach
belongs to a line of thought used to interpret CNS activities on the
concept of reflex from Descartes down to present day.
267
268 M. ZAP PELLA
Parents are also part of family therapy treatment, but in this

case the problem is considered to be more the family than the psychotic
child and the outlook on the problem is seen as "circular". By this
expression family therapists usually mean that their model of inter-
pretation is based on information and feed-back mechanisms (Selvini,
1881) and within this outlook they consider communication and behaviour
as synonims and assume the causes of behaviour to be of secondary
importance, while its effects would be of the greatest relevance for
personal interaction within a family (Watzlawick et a1. 1967). With
this theoretical framework therapists usually think (Dell, 1980) that
parents in most cases have a wrong, "linear" approach to their personal
and family problems, while the correct "circular" approach to reality
is the domain of therapists alone.
The assumption of superior knowledge on the part of therapists

seems in fact a common trait in all these different schools of thought.
Within this framework it is clear that parents may be either an appro-
priate therapist-substitute or their communication within the family
may change eventually to the advantage of the psychotic child, but
always under the control of the therapist. In no case is there a
parental quality related to their natural or cultural history which
may represent a definite basis for a valid treatment.
Results obtained with these techniques, however, seem to be very

poor and Rutter (1979), who has among others recently reviewed behav-
iour treatments, has a pessimistic outlook on the future of autistic
children. Family therapists on the other hand have been unable to
give clear evidence of systematic positive results (Selvini et al.
1975).
It may be that these poor results are related to an inadequate

use of knowledge. Prechtl (1980), for example, says that "by no means
is the nervous system an instrument which becomes only active by the
grace of stimuli, on the contrary it may seek for particular stimuli".
If this statement is valid on neurological grounds, it becomes more
valid if applied to a problem of "affective contact" and it becomes
difficult to understand how a method, based mainly on conditioned
reflexes, can be of any help in such a situation.
The possibility, however, must also be envisaged that this

scarcely efficient use of parents in the treatment of their autistic
children is related to a contemporary difficulty in dealing with
emotions and feelings, i.e. the "ability to be involved with" (accor-
ding to Heller's definition, 1981). It is perhaps worth noting that
historically the phenomenon of autism was first described in a decade
in which the western world was becoming interested in problems of
communication and involvement between human beings. Kanner's paper
appeared in 1943 while Camus's "L'etranger", which describes in great
detail the utter insensitivity of a young man confronted with the
death of his mother, had appeared the previous year and most of the
PARENTAL AFFILIATION: TREATMENT OF INFANTILE AUTISM 269
seminal works of existentialism also belong to that decade. In other

words the "Autistic Disturbance of Affective Contact", the title of
Kanner's first paper, was discovered in an historical period when
awareness of difficulties in affective contact among people in general
was apparently high and, though the "Zeitgeist" has been subsequently
evolving, there is little evidence that our culture has improved from
this point of view. Parallel to this one notes that most therapies
conducted with parents have discarded any eventual natural or cultural
ability belonging to the parental condition,
A THERAPY BASED ON "SUPERPARENTING"
In the last few years, however, a renewed interest in the discovery

of feelings has developed and it may well be that this recent trend
has been influential in favouring new therapeutic approaches to autism
where parental affiliation and the problem of affective contact between
parent and child has become the central issue. In any case the strat-
egy that I am going to put forward is the result of a number of per-
sonal observations as well as contributions from contemporary scien-
tific literature.
My therapeutic work with autistic children began about eight

years ago, but it is only in the last five years that the possibility
of making a central use of parental abilities has been developed.
This method is based at present on the following main assumptions:
1) a place for observation and therapy which shifts from an outpatients
clinic to the family's home,
2) the use of one and, if possible, two therapists, usually a man and
a woman,
3) an attitude of collaboration on behalf of therapists towards parents
which is based on the assumption that parents can, and if at all
possibly must, make active suggestions and contributions to the
therapy.
4) An attempt to interpret behaviour in terms of main functional ac-
tivities which presumably have a cause or a set of causes and an
effect. This latter point requires some explanation, i.e. approach
and avoidance have a cause or a set of causes and a clear effect,
but behaviour which leads to one or the other of these two possibil-
ities can be read also in more specific ways: for example, looking
a baby in the eyes frequently causes him to smile. This approach,
derived from Tinbergen's ethological work is both linear and
circular in that it looks to causes, effects and interactions.
5) Taking into account the patterns of reciprocal emotional behaviour
between parent and child as they develop normally.
6) From the last two points one is brought to the need of defining
if, apart from cultural variations, there are some basic ways of
behaviour or a synthesis of them which lead to general laws which
must be respected by parent and child. For example, a parent must
not kill or let hi~ child be killed and viceversa.
270 M. ZAPPELLA
A valid reference point on this subject stems from the Ancient Greeks
and their concept of "natural law". It is constantly defined in their
tragedies, imposing on parents protection of offspring, provision of
what is necessary for their growth and introduction to the social
world around them and its culture. "Natural law" mayor may not agree
with "ordinary law": Agamennon, for example, by ordinary law ought
to have put his daughter Iphigenia to death, but by doing this he vio-
lated "natural law". The result of his action was in fact the starting
point of a number of tragic events. An ultimate ethic, stating which
are the basic reciprocal rights and duties of parents and children,
is necessary in order to define the limits of their behaviour. This
is perhaps even more true in a culture like ours where values are often
confused. For example, an autistic child aged four drinks only milk:
is his mother entitled to force him to feed on solid food? Is it
violence or is it her duty?
HOW TO SUPPORT POSITIVE ATTACHMENT
In the majority of cases autistic children do avoid their parents

as well as other people. The purpose of treatment is to restore an
adequate attachment between the child and his parents, such as to
allow him security in exploring his surroundings and establishing new
social bonds. Multiple attachments are also encouraged and, if another
family relative represents a further positive attachment figure, this
trend is considered important for the child's progress and hence en-
couraged.
A common threat to attachment between the child and his parents

is often represented by family disunion: the therapists must therefore
often work in two directions. On the one hand they have to attempt
to dissolve elements of disunion in the family group either favouring
reciprocal support or at least trying to obtain a situation where the
attachment attempts of either parent are not hampered by the other or
by other family relatives, and viceversa. On the other hand they must
support either one or both parents in trying to establish new, powerful
and socially positive attachments in the most efficient way.
Reciprocity between therapists and parents is the basis for both

types of work in the sense that the therapist deals directly with the
child either in a dual relationship or at his parent's side or listens
to the results of his attempts to find new ways of communication with
him at home. This can help the parent considerably from an emotional
point of view and can also increase his sensitivity in his relationship
with the child. This attitude is helpful also when the therapist is
dealing with parents' feelings of guilt, which may be too oppressive
and together with reciprocal criticism may contribute to parental dis-
union in some cases.
For example, in the case of a child that I will call Antonino

the depressive, guilty feelings of the mother and to some extent of
the father were apparently overcome by prolonged discussions with
both parents on the subject of the beginnings of their marriage, on
their difficulties when the child was born and the following period.
In these meetings mutual confidence was established and I told them
of the similar difficulties that I had personally experienced when
my first son was born. This attitude, together with other arguments,
contributed to reduce and redimension guilt feelings in the parents
and to provide them with a more correct view of their past, where a
number of external circumstances had played a definite, negative role
in putting obstacles in front of the development of their parental
abilities.
In another case, where severe family disunion considerably ham-

pered any therapeutic attempt with the child, a paternal grandmother
had apparently great power in the home and a privileged relationship
with the child's father, while his mother was practically put on one
side. In that case there was an evident need to reinforce both the
bond between the parents to play puppets to their child while the
grandmother was sitting with me as an audient. On this occasion I
tried to convince the grandmother as far as these activities were con-
cerned, very effective because her nephew appeared to be happy and
spoke more directly, that it was better that they be left to the
"young people", i.e. the parents and I added: "I personally wouldn't
manoevre puppets and perhaps this should also be your case". In this
way I was trying to put myself in the position of an old man, somehow
closer to her and this attitude proved to be effective.
The efficient ways to establish a new, intense bond between the

child and one or both of his parents are somehow related also to his
actual intellectual ability and even more to the degree of his emo-
tional maturity.
Again the example can be reported of Antonino, the only child of

two young parents, seen at the age of six and a half. This child was
then able to speak mostly in the third person or in an echolagic form
and partly in an unintellible way. He showed occasional gaze avoidance
and remained most of the time apart from people. He had bouts of ex-
treme anxiety, especially when it was raining or during a thunder
storm or when he was hurt. He was able to draw very elongated, complex
tubes, but unable to draw human figures. He had had an apparently
normal development up to the age of two years, when he began to show
symptoms of autism.
In his case, in spite of the severity of his condition, he was

able to do some things, therefore revealing some degree of emotional
maturity and an even greater intellectual ability. Soon after the
beginning of the treatment his father showed an increased ability to
guide at the side of his son in various activities: playing together
272 M. ZAP PELLA
building wooden objects and subsequently helping him vigorously in

starting to read and write. His interest and dedication at his son's
side became increasingly greater and, being on friendly terms with
his teacher, he attended school with him for an hour or two every
day, supporting him in his school activities. When his son's conditions
definitely improved, he left him entirely in the hands of the school
teacher.
One year after the beginning of this treatment Antonino was

speaking normally, was able to read and write, had an adequate contact
with his parents and with other adults and, apart from a residual shy-
ness in his ability to relate to his peers, he was normal in most
respects. He has remained so until now, three years after the end
of the treatment.
In this successful case the father was apparently able to estab-

lish an attachment on the basis of a greater sensitivity to his son's
needs as well as on the basis of an ability to interact with him in-
tensely. He was also able to be the centre of a number of new relation-
ships and interests for the child, both at home and in the school,
and capable also of leaving space for others, when his presence was
no longer necessary, as in the example of the school. Antonino's
mother also contributed to some extent to this success though hers
was a minor role compared to that of her husband.
The case of George, a child also aged six when I first met him,
is rather different. He was affected by a congenital disease affec-
ting foveal vision only, but preserving peripheral vision as well as
most of the others eNS abilities. His development had been normal
up to the beginning of his second year of life when, already able to
walk and say his first words, he began to deteriorate, going so far
back as to lose his speech abilities and even autonomous walking.
When I first met him, he had a prevalent gaze and hearing aversion,
was not able to utter a word, standing most of the time apart, sitting
or lying down, involved with a number of stereotypes. He was there-
fore at that time on a much lower level of intellectual and emotional
maturity than Antonino.
In his case I asked his mother to hold him firmly in her arms
and to resist his attempts to run away from her. This suggestion,
which is the core of M. Welch's technique, was well accepted by her.
She kept holding her child for long periods of time in spite of his
complete resistance, screaming and biting. I asked her to continue
holding him every day at home which she did, but in spite of regular
meetings between this family and myself no relevent changes in the
child's conditions could be registered after three months. At that
point I visited their home and saw immediately that the mother's
schedule was devoted most of the time to cleaning and driving her
children to their various activities. Staying with them I was able
to allow several suggestions to come up about the different ways of
dealing with problems and finding means of letting the mother relax
more and have more time with her affected son.
The change came when, a few sessions later, the mother told me
that a few days before she had brought her son to a barber's shop
and the child had made as usual a great fuss: she had had an explosion
of anger and took his face very close to her face, asking him to be
quiet and to behave properly. He then suddenly behaved well and sub-
sequently, when she brought him home, she continued to order him
firmly, obtaining from him a type of behaviour activities that she
had never obtained before. I asked the mother to repeat this sequence
and then to involve herself with him with all her energy and spontan-
eity. She took him in her arms, put her face in frontof his, speaking
loudly, asking him to call her "mummy", because she had had enough of
his silence: then she put him underneath her and, while the child
was screaming, continued for several minutes her request until he
answered and, weeping, called her "mummy, mummy!" She then took him
again in her arms and was at times very sweet and at other times she
made fun of him: he began to laugh and repeated some of the words
that she was saying.
On that occasion the mother was excited by the fact that this
activity with her son had evolved essentially from her suggestions:
it was also, in her own words, a way to show the other members of the
family that she was able to master her son's greatest difficulties,
whereas until then she had felt somehow inhibited by the paternal
grandparents who were living with them. Afterwards she made herself
free to be able to be with her son for the whole afternoon (in the
morning he was at school) and he remained with her during those hours
almost constantly.
This example, dealing with a child who is still undergoing treat-

ment, is a good indication of the time and of the condition required
for the emotional growth on the part of a woman. She doesn't build
on nothing, but the technique suggested is an empty tool at first
while she regularly attends the doctor's outpatient clinic. The situ-
ation changes when the therapist goes to her home and gets closer to
the reality of her life. At this moment the situation rapidly matures,
she feels the challenge that her child's refusal gives her as a mother
and this is easily connected with an existing rivalry with paternal
grandparents. Her maternal passion arises out of this challenge and
allows her to go far beyond the "technique" and to invent a number
of increasingly exciting performances which break the silence of her
child.
If we then consider the child, we are inclined to think that

prior to his mother's intense affective intervention his emotional
maturity was extremely primitive. In his case things develop as though,
through the close, inevitable union with his mother, the external
suffering can be translated into an inner pain with a consequent
274 M. ZAPPELLA
request of help. "Munnny, munnny!" he cries and after that he is re-

lieved, he can laugh and repeat happily other words that she says
and sings. The way to the "feeling" is from this point of view similar
for both the child and the mother: also in her case the fact of being
somehow more clearly understood, and therefore of being closer to the
therapist apparently permits the second step, of suffering because
of her child's resistance and passes from here to the inner pain and
to an opposite state of help, i.e. I will help you with all the means
that I have at my disposal. In fact the sequence union, suffering,
pain, help is common to both and appears as the key for reciprocal
behaviour and mutual involvement.
It is also impressive to see how these mutual activities can

evoke spontaneous language in the child. It may be that in this way
mother-child patterns of language interaction become mediated by a
non-verbal connnunication system which allows the child to detect better
the meaning of his mother's utterances by non-verbal means and also
allows the mother to put herself at her child's real communication
level and, through this intense exchange of emotions, to induce in
him a powerful motivation to speak.
In other words from this example it seems clear that the mother
is encouraged to make an extensive use of visual, auditory and tactile
stimuli which are well known to promote attachment from small babies
onwards. However, in order to break the "autistic wall" their in-
tensity must be higher than in normal mother-child situations and
therefore they must also vary. In order to accomplish this her feel-
ings (defined as functional aspects of behaviour, according to Heller,
1981) are moved in the correct direction by evoking some central as-
pects of her personal experience and history as well as by her prox-
imity to the child and by a particular way of patterning perception.
In this case the sort of "peak experience" that I ha1\le described

between mother and child was able to become, at least for some months,
the starting point of an every government of the mother's feelings
towards her child which was new, intense, prolonged and apparently
very stimulating for him in the many hours that she devoted to him.
A positive contribution to this relationship was certainly given by
other members of the family such as the father and his parents, who
understood the positive efforts of the mother figure and were pleased
about the positive results which followed. The elementary school
also, where the child went every morning in a normal, ordinary first
grade with valid support on the part of the teacher and auxiliary
teacher and with the child's peers having a pleasant social attitude,
represented a further, positive contribution to the child's emotional
growth and help to the mother who could thus be relatively free for
part of the day.
It is therefore evident that any progress, though centred, as in

this case, on the mother, is multifactorially determined and in fact
a strong social tie between herself and her son was made possible
because this couple was related to a rich collaborative social net-
work. In this respect one could say that if some central aspects of
this mother-child relationship, such as the eye-to-eye, extensive
touching, etc., may have a biological, genetically determined, instinc-
tual basis and may therefore favour a more intense response, this can
hardly happen without an adequate cultural background, related to
feeling and to personal history both in the mother and in her sur-
roundings.
When these conditions were not operant, I was exposed to failure.

In two cases where family disunion was great and a considerable dis-
tance between these families, living in towns far from our outpatients'
clinic was a further difficulty for a regular treatment, mothers were
very good "holders", according to Welch's definition, but their child-
ren did not improve. In one of these cases it was the mother who
stopped holding after a couple of months, while in the other it was
the child who stopped saying the few words that he was able to say
in spite of the continuing, desperate efforts of his mother. In this
last case the social isolation of this family was remarkable and con-
sequently it was unable to create valid interests outside the home
for the child.
A note at this point must be made about M. Welch's technique,

which I knew of at the beginning of 1980. It, is somehow similar to
Zanslow's "rage reduction method" (reported in O'Gorman's "The Nature
of Childhood Autism", 1970), which consists in having the child held
by an adult and looking into his eyes for several sessions: but M.
Welch's approach is based on mothers and she wants them to be the
only persons to do this. In addition she gives a greater emphasis
to touching. More details are given in Tinbergen's book "New Hopes
for Autistic Children" (on print by Allen & Unwin).
In my experience this may be a useful tool if it is used in cases

similar to George's and it may be of help for cases of differing de-
grees of severity either in those children who are with no language
development as yet, or in children who are already able to speak, but
with the characteristic speech of autistic children. In point of fact,
in spite of different abilities, autistic children usually need an
opportunity to mature emotionally from the point of view of extensive
tactile and primitive eye-to-eye contact. But in my experience at
least they never seem to need this alone as I will explain subsequen-
tly and therefore this strategy with the caution already advanced in
the case of George, appears to be more a fragment of a composite mosaic
than something to be used predominantly. In some cases in fact it
must not be used at all, at least at the beginning of a treatment, as
in the case of a four year old child with a symbiotic form of autism,
searching constantly for his mother, who was unable to avoid an overtly
ambivalent attitude towards him, often accompanied by clear signs of
dissatisfaction at his proximity and with frequent bouts of anger and
276 M. ZAP PELLA
an aggressivity towards him. In this case a premise for a new and

emotionally richer relationship between mother and child was found
through having the father, who was until then almost an outsider in
relation to his family, start holding his affected child and thereby
establishing a new balance in the network of general family relation-
ships.
NEED FOR THE STABILITY OF MAIN ATTACHMENT FIGURES
Among the purposes of this treatment the possibility that another

relative may become an important and at times a prevalent attachment
figure must also be envisaged. This was the case of Olivia, a little
girl three years old at the first visit: her autism was severe and
she used to stay always apart with a sad expression, continually
banging her clenched fists one over the other. She showed gaze and
hearing avoidance and uttered an unintelligible sequence of sounds.
Treatment started with a number of practical suggestions such

as having her take a bath together with her mother, both parents and
other members of the family caressing her and talking kindly to her.
The importance of simple means of communication such as pat-a-cake,
hide-and-seek, playing with a ball and of a warm, smiling attitude
towards her were emphasised. After the first session the parents, who
were living in town, decided of their own accord to leave their own
house and to go back to live with the mother's parents in the country-
side. I therefore encouraged them to let Olivia play and be involved
with animals, if she liked them, which in fact she did. It was also
apparent that the little girl at times quickly took objects, if she
was not seen. The proposal was therefore made to put her at the table
beside her parents, but slightly behind them, in order to facilitate
her wish to hold of food not seen. The mother was encouraged to take
her into her bed and, while she was near her, to talk and to caress
her.
In a month she had become an apparently happy, frequently smiling

little girl. She would eat alone with her hands, go up and down the
stairs (which she previously did not do). In her mostly unintelligible
talk some definite, clear words began to stand out. But most of the
time she would still bang her clenched fists one over the other.
In that period the most effective therapeutic figure within the

family was apparently Olivia's grandfather, who had a sort of extra-
ordinary ability to make his face move, while keeping the rest of his
body almost immobile. He would suddenly glance and smile at her and
she would scream with joy and call him or he would start a sort of a
dance with the upper part of his body, while sitting on a chair, and
she would in response come near him and dance and scream' and call him
and smack him on the face as a joke, This rather elderly man was
emotionally very rich and had a singular personal history. When he
was younger he had been taken by the Nazis in a concentration camp,
where, he told me, he was able to survive with the help of a similar
efficient but subtle way of communication. He had to make a definite
and large number of utensils everyday if he wanted to receive his
meagre meal and the same was true for a young German girl who was
allowed to go back home at the end of the working day. She was unable
to accomplish all this work and he helped her by doing what she could
not manage to do, receiving some slices of bread and butter from her
in return, which allowed him to survive. This extra work and the con-
sequent communication were carried out near the Nazi officers, but
they never discovered it. When he came back home he was distressed
and became an alcoholic: but recently after the birth of his two
grandchildren (Olivia was the second), he has suddenly become the
sweet and generous man that I was able to meet. This short account
of his personal history indicates that he had learned through his
personal experience the correct strategies for difficult communications
and, moreover, had attained an emotional maturity passing through the
stages of union, suffering, pain and help.
In those first months of treatment after a few sessions I also

introduced Welch's holding technique with Olivia's mother, but this
seemed to change her behaviour very little and did not help her to
become an important attachment figure.
I then made a great mistake letting Olivia go to the sea-side

together with her mother, maternal grandmother and aunt. She stayed
there for a month and became very nervous, often screaming, calling
desperately for her grandfather who had stayed at home in the country:
there was a serious regression with respect to her previous progress.
It took us several months to help her overcome this regression and
the situation finally improved when I was able to act forcibly on the
mother's feelings, allowing her to act very much as George's mother
had done. Then with two important attachment figures at her side,
her mother and her grandfather, and with an affectionate attitude on
the part of the rest of the family, Olivia's progress was possible
again: now, a year after that "bad summer" she has definitely stopped
banging her fists, says several clear words and is beginning to play
with objects.
THE SENSE OF "THE MARVELLOUS"
Olivia's history is an indication of the importance of the stab-

ility of attachment figures and of the environment in the treatment
of such a condition. It may also help to show an aspect of the re-
lationship with the autistic child which I think is of considerable
importance on many occasions: giving the child the sense of the
"marvellous". When, for example, Olivia was already stepping out of
her autism, she would stop almost fascinated in front of a glass door
painted with pretty, coloured images. She would smile in front of
them, touch them and start a kind of a dance nearby. Similar facts
278 M. ZAPPELLA
can be observed in other cases of treatment of autistic children, for

example, in the case of Antonino, who liked to learn the letters of
the alphabet by joking with them and transforming them into animals
and other unusual objects.
This sort of artistic propensity of some autistic children usu-

ally appears when they begin to come out of their loneliness and can
perhaps be understood both from the point of view of perception and
cognition and from the point of view of emotional growth. As far as
the first aspect is concerned it may be worth while to quote the Russian
writer Sklowsky who says: "if we consider the general laws of percep-
tion, we notice that actions, becoming usual, become mechanic ... the
proceeding of art is the proceeding of extraniation (ostranenie) of
objects" for which objects and phenomena of the external world get
an unusual status. Dorfles (1980), commenting on these statements,
says that this procedure of extraniation is able to give life, origin-
ality and new possibility of information to an element otherwise devoid
of any interest, for if we take the coca-cola bottle out of Rauschem-
berg's painting it loses any value and returns to be an amorphous
object. These reasons may help to understand why so often autistic
children in the process of their improvement search for and apparently
are in need of experiences of an artistic kind, according to the
definition given above. This fact had already been noticed by
Bettelheim (1967), who took particular care in the esthetic appearance
of his institution where autistic children were treated for long
periods of time. On the other hand Heller (1981) states that there
cannot be control of feelings without previously experiencing inner
pain and the relative request of help for oneself or for others. This
may help us to understand why autistic children show an active interest
in "artistic" situations only when they are already moving out of their
isolation, i.e. when they have been able to accept help and feel pain.
Heller also adds that one must be able to understand the situation
as well as the emotional concept in an artistic experience and this
may be a valuable indication for the kind of "artistic" experiences
which can be useful for an autistic child in the different stages of
his development and emotional growth.
A need for the "marvellous" is connected in fact with other

everyday aspects of the autistic child's growth. This implies as in
normal children, elements for both an emotional and a cognitive-per-
formative growth, but this need is felt much more by autistic children.
When Olivia's therapist refuses to give her a piece of bun unless she
screams for her "mummy!", she not only indicates to her the basic
direction from which to ask for help but, starting from her already
established friendly relationship with the child, gives her a slight,
though definite external suffering. This causes an inner pain and
a request for help which becomes concrete in Olivia's screaming:
"mummy, sweet mummy!". With that phrase Olivia has gone further than
a stimulus-response and has been able to grow both from an emotional-
performative point of view.
FAVOURING EMOTIONAL GROWTH
The central aspect of the treatment of autistic children through

parental affiliation lies in favouring the emotional maturation of
the child and, to some extent, of his parents too. It includes and
is obviously also related to the need of growth also in cognitive and
performative aspects, but its first decisive moment is an emotional
one. It is only through an intense emotion that George's mother is
able to offer her child the correct perception (by holding him down
on a carpet, eye-to-eye, passionate requests, etc.), which obliges
him to suffer, to "feel" an inner pain, to ask for help. In point
of fact if autism is, as Kanner defined it in the title of his basic
article, a "disturbance of affective contact", then the logical con-
sequence may be that the first place for building it is within the
family, which represents historically the basic set for the child's
emotional growth.
This is by no means the only one and in all the:'cases that I

have been treating considerable help has come from the school, the
ordinary normal elementary school or nursery which these children
have attended regularly. It is outside the limits of this chapter
to describe the proper attitude that the school should take in these
situations. For more detailed descriptions I prefer to refer the
reader to my various works (Zappella, 1976, 1979), which also deal
with this aspect of the problem. I would only mention that it is in
my experience an essential prerequisite of this treatment.
A postscript must also be made on the qualities required on the

part of the therapist, which are not only cognitive but centred essen-
ially in an ability to rediscover within his personal history those
elements of inner pain related to deception and solitude and starting
from this "cognition of pain", establish the correct relationship
with the people involved.
The results of the above reported strategies have been described

elsewhere (Zappe11a, 1976, 1979): here I can only briefly state that
I have had only three cases where treatment was stopped more than three
years ago, where it was possible to establish a successful circulation
of emotions within the family circle: they have remained normal, as
they were at the end of their treatment and they have either success-
fully finished their elementary course or the last classes (the case
of Antonino is one of them).
In the last eighteen months I have been adding elements of Welch's

technique and I was able to treat eight children. Four of them have
at present no gross elements of autism, then there is a couple of twins
who have improved only partially, and then two cases (reported previ-
ously) who were both failures and ended the therapeutic relationship
in a few months.
280 M. ZAPPELLA
The relative speed of these positive results may be difficult

to understand to those psychiatrists adhering for emotional growth
to the secondary drive theories either based on a behaviouristic ap-
proach or on a psychoanalytic one. These facts, however, can be ex-
plained, as I have attempted to do so, through elements taken from
the primary drive hypothesis together with some of Tinbergen's etho-
logical studies on autism and with other contributions from various
aspects of contemporary culture.
SUMMARY
Parents of children affected by infantile autism may not only

recover their parental abilities with respect to their affected child,
but may be helped to increase the intensity and quality of their
relationship towards him and therefore become a central reference
point in the treatment of their children. In order to establish an
affective contact with people and reality autistic children need stable
and positive attachment figures: these are better obtained in the
context of their family either through holding eye-to-eye contact and
close speaking or through the promptness in catching his signals and
wishes and the consequent ability to maintain an intense relationship
with him. Various examples are brought which show that parents in
order to develop this passionate relationship with their affected son,
must apparently be able to go through a sequence of suffering-inner-
pain-giving help, while the child through a sequence of suffering-
inner-pain-asking help. Once the recovery process is already under
way these children seem often in need of "artistic" experiences which
further support the growth of their affective and cognitive abilities.
The main elements are described of this therapeutic strategy, which
implies a close support of the autistic child within the normal school
system.
REFERENCES
Baker, B.L. and Heifetz, L.J., 1976, The read project: Teaching manuals
for parents of retarded children, in "Early intervention with
high risk infants and young children", T. D. Tjossem, ed.,
Univ. Park Press, Baltimore.
Berkowitz, B. P. and Graziano, A. M., 1972, Training parents as
behaviour therapists: a review, Behav. Res. Ther., 10, 297.
Bettelheim, B., 1967, "The Empty Fortress", McMillan, New York.
Camus, A., 1942, "L'etranger", Gallimard, Paris.
Delacato, C. H., 1974, "The Ultimate Stranger", Doubleday, New York.
Dell, P. F., 1880, II terapista familiare Hopi e la famiglia aristo-
telica, Terap. Fam., 8, 55.
Dorfles, G., 1980, "L'intervallo perduto", Einaudi, Torino.
Heller, A., 1981, "Teoria dei Sentimenti", Ed. Riuniti, Roma.
Johnson, C. A. and Katz, R. C., 1973, Using parents as change agents

for their children. A review, J. Child Psychol. Psychiat.
14, 181.
Lovaas, O. 1., 1979, Parents as therapists, in "Autism. A Reappraisal
of Concepts and Treatment", M. Rutterand E. Schopler, ed.,
O'Gorman, G., 1970, "The Nature of Childhood Autism", Butterworth,
London.
Prechtl, H. F. R., 1880, Assessment Methods for the Newborn Infant.
A Critical Evaluation, in "Psychobiology of the Human Newborn",
P. Stratton, ed., J. Wiley & Sons, New York.
Rutter, M., 1979, Etiology and Treatment: Cause and Cure, in "Autism.
A Reappraisal of Concepts and Treatment", M. Rutterand E.
Schopler, ed .• Plenum Press, New York.
Selvini Palazzoli, M., Boscolo, L., Cecchin, G. G. e Prata, G., 1975,
"Paradosso e contro paradosso", Feltrinelli, Milano.
Selvini Palazzoli, M., 1981, "L'anoressia mentale", Feltrinelli, Milano.
Sklowsky, V. B., 1929, "0 teorii prozy", Moskva.
Tinbergen, E. and Tinbergen, N., 1972, Early Childhood Autism. An
Ethological Approach., Z. Tierps., Heft 10.
Tinbergen, E. and Tinbergen, N., "New Hopes for Autistic Children",
Allen and Unwin, on print.
Watzlawick, P., Beavin, J. H. and Jackson, D. D., 1967, "Pragmatic
of Human Connnunication", Norton, New York.
Zappella, M., 1976, "11 Pesce Bambino", Feltrinelli, Milano.
Zappella, M., 1979, "Tl Bambino nella Luna", Feltrinelli, Milano.
URBANIZATION AS A FACTOR
INFLUENCING CHILD BEHAVIOR
Claudio Stroppa
University of Pavia
THE CONCEPT OF SOCIALIZATION
The concept of socialization, with all the problems involved in

terms of social reality, is the result of interdisciplinary research
led by a team of social science scholars (sociology, psychology,
anthropology) during the period from 1930 to 1940. This inter-
disciplinarity is most significant both for the very broad support
provided in the theoretical and practical elaboration of this con-
cept, and, more simply, for the links existing between these disci-
plines and others that can better explain the contents of this essay
and its significance in the framework of human ethology.
Formerly, Freud and Durkheim had pointed out in many parts of

their research a personal interest in socialization problems but
only through the works of the U.S. sociologists Park and Dollars in
the "American Journal of Sociology" (1933), for the attention devoted
by Ogburn and Nimkoff in their handbook of sociology, with the con-
tribution given by the psychologist Kardiner in "Individual and
Society" (It.transl.1965), and with the publication of books by
Murphy "Experimental Social Psychology: An Interpretation of Re-
search on the Socialization of the Individual" (I937) and "Frustration
and Aggressiveness" prepared by the Yale neobehavioristic school,
(I939) a "modern" definition of socialization emerged.
Innnediately, it was related of the traditional term of "edu-

cation". But the transition from the term "education" to the one
of "socialization" is characterized by an important change of
perspective: while education essentially refers to the value of
objectives and techniques, socialization rather refers to their
working and effectiveness. In other words, it is no longer a matter
283
284 C. STROPPA
of discussing the quality of objectives and methods; but of describing

their differences and analyzing the processes by which educational
influences produce their effect. In practice, the reformulation of
educational problems in matters concerning socialization processes
has focused the emergence of a more significant role of society as
opposed to one of the individual; this has reopened old theoretical
arguments between disciplines in the frame of social sciences, and
between scholars within the same disciplines.
In various opinions, the term "socialization" itself had the

meaning of visualizing society as an active principle fixing the
objectives to which the individuals is subordinated with major or
minor success again, in other words, socialization is mainly intended
as something which submits or at least influences the individual,
and this logically brings us to consider the individual as no longer
the actor of his own life, but as a passive subject in front of
social influences.
Because of this view, undoubtedly distorted, most of the present

researches on socialization become disputable. It is in this very
context that the importance and the role of urbanization emerge
showing it as a factor of child socialization. In inter-relations
between the political and psychological meanings of the term
"socialization" many have considered that the psychological meaning
of the term was lacking in the programmatic connotations of the
political meaning, but this can be appreciated only if the phenomenon
is dealt with superficially.
In fact, early forms of socialization theory, which appeared,

for instance, American anthropology, were from a structural point of
view, not very different from marxism. Kardiner, the most represent-
ative author of this trend, like every other orthodox marxist,
stretches a clear difference between primary and secondary insti-
tutions of society. But, if both theories agree on the political
and cultural nature of secondary institutions, according to Kardiner,
only the primary institutions influence the education of the child.
By this approach, Kardiner shows a deeper conviction that Marx on
the "overstructural" character of secondary institutions, so that
these, being a product of primary institutions, cannot be radically
changed without changing the latter. This means a precise reference
to urbanism and therefore to the city as a primary social institution
of our era: when we want to formulate a certain plan of social
action involving a real transformation process, it is necessary to
examine in which structural areas and in which ways the methods of
child socialization may be worked out or changed.
Clearly, this immediately appears connected with the specific

social problems of immigrants in urban areas, but also corresponds
to the claim of Freud's theory on this phenomenon. Let's only
mention the acculturation difficulty of adult immigrants, often
URBANIZATION INFLUENCING CHILD BEHAVIOR 285
traceable in behavior patterns achieved during early childhood, and

in this regard, the role of speech.
Therefore, from the point of view of social policy, the child-

hood period becomes the centre of programs aimed at accelerating
the acculturation process.
Since the early researches on the relations between culture and

personality by Kardiner's disciples Mead and Gorer, the study of
socialization has progressively appeared as a sector of research
alien to concerns of public intervention: that is an independent
investigation area marked by its own theoretical system and conse-
quent empirical analysis. The process by which the individual,
whether a child or an adult, becomes an active member of society,
certainly represents a legitimate investigation area open to ob-
jective analysis and a valuable source of theoretical problems for
sociology psychology, anthropology and all the correlated disciplines,
whose purpose is to study the human being. It is to be kept in mind,
however, that this research field continues evidencing its historical
origins.
At a certain level, this can be seen in the present effort to

stress the constant molding capacity of human reactions, and to deny
the existence of irreversible structural changes in human develop-
ment. But, even deeper analyses of socialization tend to show the
influence of what today might be defined an "ideology" of the social
engineering. This thinking seems interesting and relevant to the
themes treated in this essay. When we review this series of re-
searches, we find it difficult to avoid the feeling that most of
them have been motivated more by the hope to find adequate answers
to the problems raised, than by the willingness to understand them.
The valence can be dual, particularly if recognisable in a line of
"city policy." Certainly, the problems to be investigated have
often been expressed in such way as to indicate that we are always
supposed to estimate specific interventions on childhood as having
definite, predictable consequences on his social development.
On the other hand, for the very "delicateness" of the subject

under discussion, we are often likely to lapse into "cultural ab-
strations" without answering to the questions which urbanism, in its
daily evolution puts forward in a polyvalent perspective.
THE CULTURAL AND SOCIAL CHANGE
Traditional researches on socialization have high-lighted the

importance, in this phenomenon, of the parent-child system and of
the formation of the personality within the family. The dynamic,
social and cultural change in a sequence of rises and falls of
interest, has often indicated how concerns, more or less evident,
286 C. STROPPA
involved with the parent-child and family system, which are certainly
deeper in those cities where their significance is in sharp decline.
Modernisation and large scale industrialization have caused a constant
growth of new socializing agents, such as for instance, red-tape
school and mass-media. And it was thanks to a research on extra-
familiar socializing agents led in order also to eliminate a series
of prejudices - bearing in mind the ineluctability of complex indus-
trial societies - that the influence of urbanesim contents on the
current modes of child socialization became more evident.
The urban phenomenon can be defined a "charge-explosion" pro-

cess of cities and/or similar social structures. Historically, the
urban texture becomes progressively thicker with great population
density; it can be described through the concept of echo-system, a
consistent unity created around one or more cities, ancient or modern;
a concept, on the other hand, applied not only to disciplines con-
cerning the urban, but also in biology and in ethology, and this
only mentions two disciplines involved with environment study. But
while morphology can arise interest, it is not enough to explain a
given "way of life," more or less intense or degraded, that is urban
society. From a social and cultural point of view, this reality
involves both objective and value systems, rural and urban, with a
whole range of tensions that become exasperated. We have already
discussed about complex systems, including a series of questions to
which it is difficult to find answers or solutions: here lies the
concept of "city-crisis," theoretical and practical crisis, real
and supposed phenomenon affecting the present and future child is
behavior, but for the fact that the child is one of the main users
of the urban system, protagonist or passive subject in the real sense
of the word, agent of change according to expressed or unexpressed
patterns of behavior. Urban life implies relationships, encounters,
confrontations on different ways of life, patterns which can coexist.
There is the widespread convinction that urban reality has

disappeared, on the contrary, it has only generalized: the whole
society becomes urban. Only this assumption can be comprehensive
of a new interest in childhood, adolescence, etc.
Child behavior can still be related to the old specific cate-

gories, but at this "category" level, the child is born urban,
whether he lives in the city or in the country. (Obviously, such
definition is more appropriate for industrialized cultures, but
various researches have found out that significant influencing
patterns exist also for the children living in traditional rural
areas, whether they live in the Old or New World, or in the so-called
developing countries.)
Henry Lefebvre writes in this regard: "The dialectic process

is the following: the city - its refusal on the part industrial-
ization - its reinstatement on a large scale: the one of the entire
society. This process cannot develop without the conflicts. Be-

coming progressively more serious the existing production relations
have expanded, widened, simultaneously integrating agriculture and
urban reality, but in this expansion process they have introduced
new conflicts. On the one hand, decisional centres are born provided
with still unknown powers - because they concentrate wealth, re-
pressive power, information. On the other hand, the explosion of
the ancient cities allows multiform isolation processes; the com-
ponents of society are pitilessly separated one from the other in
space; this causes a dissolution of social relations together with
a concentration of relations primarly connected with property re-
lations"l. Thus, an important concept becomes evident, that of
"urban explosion," and this gives rise to meditations and reconsid-
erations on the urban aspects, previously scarsely taken into account,
such as "centrality," space as place of encounters, segregation
processes, habitat contradictions, etc.
The urban dimension is a simultaneous form that brings together

very different elements; for instance, centrality has its own specific
dialectic movement, like, in the same way, the communication processes
taking place in the urban setting from the top to the bottom and
viceversa. Undoubtedly, these and other urban processes are going
to influence child behavior, either as individual or member of a
group or various groups, more or less extended, mainly in the two
principal components of urban structure: space and time.
The French sociologist George Balandier, in a teamwork which

is the result of a national symposium held by the French Sociology
Association, stretches the connections among behavior, development
and change and specially creates a global term: "la sociologie des
mutations. " This work includes an es.say by an urban sociologist,
Raymond Ledrut, who deals with this paper suggested by Balandier
with regard to urbanesim.
The French experience, which is not different from the Italian,

German or English one, only to mention some European realities,
clearly reveals that morphologic changes brought about by the typical
urbanesim of the present period, give rise in their turn to important
changes of collective, social and cultural kind.
The first and most important ones - since they produce other
ones - are connected with the radical changes affecting the role and
even the existence of local communities, and more generally, in the
long run, the connection between collective life and space. More
and more often, one only sees the negative angle of the change that
has affected local communities, the start point of which can be very
remote. Ledrut even states: today, the city is no longer existing.
Surely, this statement can be very strong and if related to the
problem of child behaviour, particularly in a period of "strong"
institutional socialization (from 6 to 13-14 y.o.) it may introduce
288 C. STROPPA
present and future modes that can be very different from what hap-
pened in the past, because of a trend of influence from the city,
of perception from the child, different were it not only for a
generation gap.
URBANESIM AND URBANIZATION
Urban autonomy, even though relative, is threatened at all

levels: economical, political and social. The city's collective
personality and individuality are deeply threatened: we must point
out - as confirmed by several researches - that particularly the old
types of local communities (traditional districts, medieval type
villages, etc.) are in danger.
Urbanesim and new modes of space population, with the typical

phenomenon of different population mobility, complete the action
that capitalism and national states have been exerting for over a
century. But, in addition to undermining the life and the individu-
ality of the traditional "local conununities," the new space organ-
ization reveals the outlines of a new collective structure. The
more urbanesim develops, the more the old mode of morphological and
sociological organization disappears.
This dissolution, the most negative feature of which were

particularly visible at the end of XIX century, today has entered a
phase where restructuration elements become evident.
What disappears is an integration form of collective life in

space; what arises, in connection with the network of hyerarchical
centres, are new collectivities which are not at all local conunun-
ities and which - typical symbol of a change and revolution, are
still not in direct relation with the political and administrative
institutions. As always in these cases, only minorities are aware
of this phenomenon and put it into effect with their own will un-
doubtedly. This process has occurred gradually and through the
years, but there is always a question which could be asked already
in the past - it was only a problem of collective conscience, almost
always absent - but which today, presents itself as more problematic
and disturbing how and to what extent will the new generations'
behavior be different from the past generations as far as urban life
is concerned? In other words, to what extent is, that phenomenon
which we define tout court urbanesim, affecting expectations,
disillusions, etc. In other words, the formation of a "city resi-
dent" - like behavior among the existing children and those who will
be born (in spite of a decreasing birth-rate?) The changes taking
place in space collective formations are closely tied to the changes
taking place in the social life of populations (individual life,
family life) living in residential areas. The habitat has always
been - or at least partly - associated to modes of social relation-
ships between population members who have integrated more or less

permanently. The XX century urbanesim, in its most particular form,
introduces new modes of social life with regard to the habitat, con-
sidering that, if a particular structure of population and local
communities extinguishes, the dwelling in constant evolution persists.
Space still plays a role in social connections.
What has been investigated becomes evident in its conceptual

value not only for the adult, but also for the child. The latter,
who is to be considered a "new" urban subject and therefore affected
by such "condition;" he might find himself to perceive feeling of
unaccomplishment, the characteristics of which are much more man-made
than natural. This reality somewhat artificious ends by providing
the child with a new way of "subjectively" representing the habitat,
a way in which the child plays the actor's role. In fact, the en-
vironment is not to be considered as a granted element present in
everybody's conscience, but rather as the result of a long gradual,
cognitive process including perceptions, experiences, history. The
objective universe, casually organized in the space, represents a
gradual achievement in the mental maturity. Jean Piaget and Barbel
Inhelder insisted on this phenomenon.
Firstly, the child builds up the space object, secondly, the

permanent one, thirdly, a magic vision followed by an animistic pre-
judicial, an artificialistic prejudicial and finally, an adult
"scientific" vision. Each one of these moments comes into effect
however, as a consequence of the previous one and is obviously af-
fected by the way and completeness in which each stage has been able
to evolve. Werner adds that the space experience by the child is
much more undifferentiated, sy~cretistic and much more tied to con-
crete interactions than to a stable, abstract system.
The transformations taking place in infant modes of conceptual

structure of the environment, do have repercussions on the style
and behavior according to which the child lives the city and, in
general, the so-called urbanesim.
THE NEW CONCEPT OF "URBANITY"
His life project (in cultural, genetical and biographical terms)

has to face, daily, an "unnatural" environmental situation - scarcely
organized, also taking into account his presence and needs - which,
however, sees him more like an element to be controlled than like
a protagonist to be offered opportunities of expressing himself.
Then the environmental culture so formed through the mediation of
socializing agents, appears in its whole evidence like a very stimu-
lating subject of investigation, particularly from the view-point of
transcultural research.
290 C. STROPPA
It is known that urban civilization and society have adopted

distinctive characteristics, in the same way as in the traditional
rural civilizations or in the old towns with stable and limited
population, closed in their habitat. Mobility and urban growth
have created the man of the big cities, as described by Oswald
Spengler or Louis Wirth: isolated in a wide complex of different
groups, where the primary groups are declining or dominating formal
organizations or impersonal relations. The district life, almost a
country life, grows weak. Obviously, this new type of social life
takes its strength in very particular situations only. The scarcely
industrialized small European town partly escapes the process. What
Spengler did not expect, and similarly Wirth, is the rising of a
new civilization in embryo from the obsolescence of old urban rural
cultures.
Some people regretting the small local communities of the past,

whether rural or urban, can only think of culture and social life
as an image of societies and cultures that have disappeared. So,
they either see the new forms in gestation, nor they perceive the
changes in progress. Whoever talks about changes, does not mean a
simple change, but a structural improvement. If we examine the town
situation in a socialist country, such as the Soviet Union, we may
observe phenomena that are much alike those taking place in capital-
istic countries. These are not at all connected with the capitalistic
system, but on the one hand with the technique and technique-bureau-
cratic evolution of the present civilization, on the other hand with
the reactions to this civilization.
The concerns about social space administration lead all those

in charge of urbanesim, in technicall~ advanced and greatly urbanized
societies, to pursue a main goal: the space administration in view
of the city inhabitant integration in a district where he may be
able to find various facilities. Things are made more difficult by
the capitalistic society because of the profit motivation. Such aim,
however, although rational, today is being discussed by the city
residents.
Segregation is rejected by all those who cannot accept their

horizon limited to the district where they live. Today's great
urban change is the concentration of the signs and symbols of in-
habitants of every district or village want to take advantage freely.
The man of the small town used to lead a restricted social and
cultural life, then, in the big towns, the man has become a district
dweller.
Today, however, the man of the lonely crowd increasingly tries

to invent other communities to make use of space within his own
horizon, in a fewer, more creative and less limited manner. The
big city has started to create its own culture, not only its own
civilization, but a new form of social life particularly in the
last thirty years, and this "soul" has created new urban modes which
we could define, according to their own humanistic will, urbanity.
This does not mean at all that more typical, degraded forms of the
past, that have affected the social life, have completely disappeared.
We just want to emphasize, like in other sectors, the search for a
new social and cultural life style: the appropriation of space by
men in connnunities is c.alled upon to take new characteristic. The
old local integrations and ancient, social and cultural mediations
are dead or survive in a limited form, as well as types or urban
civilization connected with these realities.
A new integration system with its own space form will be con-
stituted. Certainly, this will influence the institutional social-
ization processes of childhood and consequently, its urban behavior.
In what way? In this regard, researches are scarce and often have
limited goals, just bec.ause they are functional to the solution of
the most urgent problems. More often, there is the need to find a
solution to the problems of urban alienation, typical psychologic
reality of the "urban transition" period.
SOME INDICATIONS EMERGED FROM A FIELD RESEARCH
A three years' research on this problem, carried out in Milan

by a team of psycologists who studied 2000 cases selected in less
privileged urban areas, has shown that the boys were constantly
talking about food. They were so harassed by the thought of it that
even at school, when a general problem had been tackled, such as the
difference between North and South of Italy, innnediately the image
that Southern people eat in a different way emerged. And "hearty
meals" are the only way to celebrate. Isolation, excess of indi-
vidual responsability, inability to overcome old prejudices or to
fight against new ones, forced the parents to search for individual
solutions within the family; the parents would give up food, the
children were conditioned by being excessively grateful to those
who, literally would "take the bread out of their mouth" to feed
them. The mother protracts breast-feeding, thus favouring an
exaggerated, typically Italian motherly care, meals are empoverished,
children are often beaten up "if they steal" more food, people turn
to grand-parents, uncles and the "big family" for help. On the
other hand, what can society offer? The family is only provided
with assistance if "the case" is considered an "emergency". This
assistance is mostly given with contempt, humiliating or punishing
the family and the child by taking the latter away.
It is easy to understand that by doing so, society confirms

the concept according to which is a virtue and a merit. Not is it
difficult to understand how, together with minor pathologies, these
values which are incompatible with the reality experienced by the
child, can lead to self-destruction: prostitution, alcoholism,
292 C. STROPPA
doping; or crime: smuggling, robbery, hold-ups. To become conscious

of this, at an early stage, is most important to understand that
every child has the right to be fed and every adult has the duty to
feed him, since the child is not the parents' property but a member
of society. While food is for children a natural need and is always
seen as a good thing and only so at least by smaller children, home
is seen since the beginning with a feeling of hatred mixed with love.
Children want a home, a place where they feel safe, a place where
they find their own roots and identity; but they want as well to go
out, be independent and have no ties. School is never concerned in
learning how children satisfy their need for shelter and protection.
It seems untouched by the problem. It has also been noted that only
occasionally a school member visited the children's home: over three
years, for a total of 4000 children this has happened about twenty
times. Usually, the teacher is not the person visiting the childrenTs
home: this task is left to the health officer, a member of the
parents committee, or to the school attendant, who takes the child
home when he has been naughty. The visit has never the purpose to
give support to the family or to back a request for a more comfort-
able house. The house is never considered a social service; more-
over, it is never connected with more general problems: job, health,
school. For the less privileged classes, on the contrary, to own a
decent house, maybe a "property" house, is something like a prize,
the aim of a whole lifetime.
Therefore, having a house means having a shelter when it rains

or when the sun is too hot, a place to go back to when the world
outside becomes boring. All these advantages, however, have a re-
versed side: if you want a shelter you must go home; but at home
you cannot relax or stay on your own because the family is disturb-
ing, you have not enough room for yourself: the house, in fact, is
almost never harmoniously linked to the outside environment, a
starting point to the world, but a place separating the private life
from the public life and precluding new experiences. An ideal way
of living should make one find a right balance between the natural
need for new experiences, adventures, change. More often, the
house becomes a place of repression where the child must control
himself in the name of everbody's peace. The adult, however, has
less restrictions than the child, because the house is his: he
does'nt want children having too much freedom of movement within
the house: for instance, those mothers who prefer their children's
happiness than a tidy home are severely criticized by neighbours.
The house must never be untidy, it must be spick and span,

brilliant; it must show that the dweller is efficient and doing well.
Then the basic conflict (house-shelter as opposed to house-prison)
is intensified by other unfavorable aspects (at home I can do what
I like provided I don't disturb my neighbours.) According to adults,
children living in big metropolitan areas enjoy themselves by
collecting post-cards, by moulding clay or playing in the streets,
in the basket ground or at the parish. Certainly, all these pastimes

seem to children less boring than sitting in front of television or
reading comic-strip magazines. Therefore they do it with pleasure,
but in these things they almost never find a way of really expressing
themselves: through these activities, artifically induced, which
are not the consequence or the expression of needs, thoughts, per-
sonal feelings, children do not grow up; they do not learn to know
themselves and by the time they are thirteen, fourteen y.o., their
personality is already distorted, dull, alienated. Only a minority
is not tempted by consumerism or mannered anti-consumerism. These
teenagers have accepted as their own a value proposed by adults:
faith for those going to church social organization, political power
for those actively participating in political activity; love of
nature for those practicing sports activities; culture for those
devoting themselves to study or art. "Power" is heavily exerted on
the child within the family, at school, within the organizations,
hampering their longing for freedom and independence.
Within the family, the decision power is usually left to the

father; at school, "conflicts" are made stronger. This type of
apparently democratic organization does not permit a real autonomy
to children, but it maintains the characteristic of the most archaic,
negative authoritarianism. The result of these behaviors, and other
similar ones, (for example, the convincement of male superiority,
inconsistency of women's participation in social life, etc.) is, on
the one hand a deprivation of responsibility for the child, who soon
realizes that he has been deceived by the illusion of a democratic
school; on the other hand, his failed liberation: racial prejudices,
competitivity, aggressiveness are maintained and made stronger.
We have talked about "urbanity." It may be an utopia; however,

it is always worth proposing it. This way of living is not a guaran-
tee against alienation, but what has been reported about the re-
search conducted in the Milan area, is rather symbolic: it is not
possible to create tout court a completely new reality for children
and therefore find a positive solution to the specific urban con-
flicts. But every effort made at political, social and cultural
level will enable us to take a step toward an ideal form of society
"in which everyone would have his own rights recognized, would be
able to reach maximum development according to his own physical and
moral faculties, and take advantage of them without the need of
being humble in front of a fellow creature or dominant; in conclusion,
a society where freedom would not affect equality; where every man's
feeling would be in accordance with reason, and where nobody would
be forced to operate against the dictates of this one, or stifle
the impulses of that one. In this case, man would be able to fully
manifest life and coulc1 be called perfect,,2.
294 C. STROPPA
REFERENCES
1. H. Lefebvre, II diritto alIa citta, Marsilio, Padova (1970).

2. C. Pisacane, Essay on Revolution, Feltrinelli, Milano (1944).
INDEX
Abilities, interpersonal, infants Amphetamine, effect on locomotor

see Interpersonal activity and behavior, 34
abilities of infants Anxiety
Acoustic and adult plasticity, 63-64
perception at birth, 131 abreaction, 64
stimuli, to fetus. heart rate brain-washing, 63
changes and movements, , flooding', 64
99-110, 118-120 noradrenalin, 64
conclusions, 119-120 revivalist hysteria, 63
tables, 102-106 shell-shock, 64
system, secondary, 131 individual differences, rhesus
Action potentials, earliest monkey, 78-81
recordings intrauterine, autonomic indices, 81-84
99 and behavioral relationships,
auditory, 99-100 84-86
and prematurity, 99, 100 heart rate, 82-84
Adoption of young, infant Audition, fetal, 93-127
signals, 2-11 (see also Hearing, fetal)
age, influence, 4 Auditory system, fetal,
age versus size, 8 responses, 99-110
brood parasitism, 10 tables, 102-106
cannibalistic behavior, 11 Aunts, role in child's upbringing
interspecific, mouse/hamster, 201-211
3-5 Autistic children
mechanism, 3 delay in diagnosis, 241
motility, 10 development of social
olfactory signals, 10 avoidance, 241-266
plumage pattern, 9 methodology, 243-244
pup inside/outside nest, 4 samples in study, 243
sound signals, 10-11 'guilt factors, 242
by virgin hamsters, 3 lack of precise behavioral
Adults, effects on development. descriptions, 242-243
rhesus monkeys, 77 simplistic views of develop-
Aggression, babies and toddlers, ment, 242
205-207 social behavior (avoidance),
Amniotic fluid, effect on 244-258
suckling, rat pup, 48-49 alternation, 244
295
296 INDEX
Autistic children (continued) Baby

social behavior (avoidance) face, 'ideal', 13-14
(continued) 'schema', 1, 9
attachment theory, 253-254 Baby talk , 188, 193, 194
case histories, 256-258 in didactic programs, 229-230
causation, 245-247 Beak flirting, 12
characteristic features, 255 Behavioral
communication, 247-249 assessment, rhesus monkeys,
compromise, 245 individual differences,
consequences, 249-250 81-84
displacement activities, 245 autonomic/behavioral
effect of, behavior of relationships, 84-86
others, 246-247 conclusions, 86-89
mother/child interaction, 254 heart rate, 82-84
ontogeny, 250-258 preseparation group
overintensity, 245 behaviors, 85-86
processes leading to, 253-258 separation behaviors, 86, 87
simultaneous approach and development, comparative
avoidance, 244 approach, 21-38
therapy, 258-261 encephalization levels, 24
therapy, 258-261, 267-281 evolutionary viewpoint, 22-24
parental affiliation, 267-281 genetic approach, 24-30
attachment figures, need and maturational pattern,
for stability, 276-277 23-24
failure, 275-276 neurochemical systems, 34-35
family disunion, 271, 275 and recovery after limbic
flavoring emotional growth, lesions, 27
279-280 circadian rhythmicity,
parental problems, 271 28-30
persistence, 272-274 specialist and generalist
prognosis, 268-269 animal, 22
sense of the 'marvellous', distinction between, 22-23
277-278 teratogeny, 30-33
success, 272 usefulness, 21
super parenting, 269-270 states and electrical brain
supporting positive attach- activity, 127-144
ment, 270-276 (see atso Electrical brain
prognosis, 268 activity: Electroencepha-
parental involvement, lographic changes)
268-269 Biting, 196
unfeasibility of prospective Bond formation see
studies, 242 Mother-infant bond
unreliability of retrospective Brain
reports, 241 activity, electrical, and
Autonomic indices of temperament behavioral states,
differences, rhesus infancy, 127-144
monkeys, 81-84 growth, effect of malnutrition,
and behavioral, relationships, 31-33
84-86 , -washing', 63
heart rate, 82-84
INDEX 297
Cannibalistic behavior, mice, 11 Cross-cultural perspective,

Cardiac response to acoustic parent-child interaction
stimuli, fetal, 99-101, patterns, 177-217
107-110 mother-child bond, 179-185
tabZes, 102-106 and communal (collective)
Caressing, 194-196 rearing, 179-181
Carrying babies, 202-203 mechanism of bond formation,
supports used, 202 181-185
Catecholaminergic processes, period immediately after
effect of amphetamine, 34 birth, 182-185
Categorization in didactic motor patterns of affection,
programs, 225 185-211
Cell differentiation, migration strategies, infant, 185,
and myelinization at 189-190
birth, 129-131 theories, 177-179
Cerebral dysfunction and autistic Crying, maternal response,
children, 252 196-200
Circadian different cultures, 197,
energy-deployment processes, 198-200
and paleoencephalic triggering milk flow, 197
activities, 28 Cultural
rhythmicity in mouse strains, patterns see Cross-cultural
28-30 perspective and social
Communal (collective) rearing of change, and urban-
children and mother bond, ization, 285-288
179-195
Communication Didactic programs, psychobiology,
in autistic children, 247 219-239
(see also Autistic children) categorization, 225
in didactic programs, 221 communication, teacher/pupil,
in infants, development, 221
167-169 concept formation, 225
in games, 159-162, 169-172 early infancy, 220-230
mother-infant reaction, environment, 220-221
153-155 feeding habits, 226-227
self-activated awareness, first toy, 230-235
155-164 fundamental integrative
(see also Interpersonal processes, 225. 226
abilities of infants) human studies, 221-222
Concept formation in didactic laboratory studies, 233
programs, 225 optimal conditions, 227
Contact-initiatives, 205-206 parent/infant interaction,
Contraception, during nursing 222-224, 234
period, 202 play, 230-235
Conversation, 2-3 year old child, measuring, 231
169-172 problem situations, 224
Cortisol, plasma, in conditioning relation to play, 232-234
trials, rhesus monkeys, studies over first 8 months,
82-84 227-230
preseparation group behaviors, teaching language to newborns,
85-86 117
298 INDEX
Domestication, avian, mammal Eye (and eyebrow flash) contact

species, 12-13 with baby, 188, 191, 192
(see also Face-to-face
Education communication)
and socialization,
differentiation, 283-284 Face-to-face communication,
through play see Didactic infancy, 148-149, 151,
programs 152, 188, 191-192
Electrical brain activity and sustaining, 148-149
behavioral states, Facial movements, newborn, 150
infancy, 127-144 Father in baby's world, 207-211
development, 132-133 cultural variation, 208
EEG changes, 133-140 distanced, 208-210
full-term newborns, 132 playing, 208
specific bioelectrical Fatty acid deprivation, effects
peculiarities, 129-133 on brain growth, 33
timing of phenomena in brain Fearfulness, individual
development, 129-131 differences, rhesus
visual states, 132 monkey, 78-81
(see also Electroencephalo- autonomic indices, 81-84
graphic changes) Fetal audition, 93-127
Electroencephalographic changes (see also Hearing, fetal)
and behavioral states, 'Flooding', 64
infancy, 133-140 Food
during active sleep, 136, 138 begging, 12
during first months, 139-140 in concept of urbanization
during wakefulness, 136, 138 research, 291-292
fetus, 19 weeks, 134 pellets, introduction after
24-27 weeks, 134 suckling, rat, 43-45
28-32 weeks, 135 in play dialogues,
32-36 weeks, 135-136 203-205
quiet sleep, 136, 138 in play dialogues, 203-205
transition between sleep and therapy and autistic children,
awake state, 139 259-260
Environment
acoustic, intrauterine, 94-97 Games, mother and infant,
factors related to behavioral 159-162, 169-172
rigidity or plasticity, Generalist animal, 22-23
29-30 distinction from generalist,
importance in didactic 22
programs, 220-221 Genetic
influences on rhesus monkey approach to behavioral
development, 76-78 development, 24-30
conclusions, 86-89 factors in autistic children,
Essential fatty acid deprivation, 251
effects, 33 Grandparents, role in child's up-
Evoked auditory potentials, bringing, 210-211
earliest recordings, Guilt factors, and critism, 242
intrauterine, 99
Handling babies, cross-cultural,
202-203
INDEX 299
Head toss in contact with infant, Initiatives, infant, 205-206

188-203 Interpersonal abilities of
Hearing, fetal, 93-127 infants, 145-176
conclusions, 118-120 cognitive processes, new
earliest signs, 98-110 theories, 146-147
anatomical development, 98-99 fact-to-face communication,
mesenchyme, effects, 98 148-149, 151, 152
intrauterine acoustic environ- facial movements, 150
ment, 94-97 infant's responses to
language, acoustical features, mother's presence, 149
learning, 114-117 mother-infant communications,
and prenatal learning, 110-113, 148-149
118 'prespeech', 153
reactions, fetal, 99-110 smiling, 147-148, 151, 152,
heart rate and movements, 99. 158
100 conversation development,
tables, 102-106 169-172
Heart cooperation in communication,
beat stimulation, effect on 167-169
newborns, 112-113 first year, 155-164
rate change scores, during games with mother, 159-162
conditioning trials, relation to wariness with
individual differences, strangers, 162-164
rhesus monkeys, 82-84 mother-infant reaction, 153-155
and movements, fetal, 99-110 negative behavior in infant,
tables, 102-106 158
Holding therapy and autistic normal play, 158
children, 260-272, 275 reaching and grasping, 159
House/home aspects of urban- second month, 151-155
ization and behavior, self-activated awareness of
292-293 objects and games with
Hugging, 194-196 mother, 155-164
Hysteria, revivalist, 63 self-consciousness, develop-
ment, 165-167
Imprinting, 59-60 television experiments,
'arousal', 59 153-155, 169-170
change in behavior, 62 third month, 155
filial, 61-62 Intrauterine
first, second and third acoustic environment, 94-97
objects, 61-62 postnatal effects of noise,
hormonal events, 59 112-113
internal control, 60 sound intensity, 94-97
novel objects, 60, 61 recordings, 96
preferences, internal
protection, 61 Kissing, and kiss feeding, 194,
sexual, 60, 61-62 198
visual experience, 59
Infantilisms, 11-12 Language
in man, 14 acoustical features, learning
Infantilization, 13 in utero, 114-117
300 INDEX
Language (continued) Milk, suckling

acoustical features, learning developing analysis, rat, 39-55
in utero (continued) effects of gastric preloads,
in birds, 114-115 42-44, 46
in humans, 113, 114, 11S-117 nutritional factors, 41-45
newborns, recognition of and termination, 46-47
mother's voice, 117 oral stimulation, 50
prenatal, evidence, 116-117, regulation of intake, 45-48
118 electromyography, 47
teaching to newborns, 227-230 intake during, regulation rat,
Learning, prenatal, 110-113 45-48
associative learning procedures for testing, 45
capacities, 111-112 Monkeys, rhesus see Rhesus
tests, 111-112 monkeys
habituation, 110 Monotropy, 178, 180
language features, 114-117 Mother-infant
postnatal effects of bond, 179-185
intrauterine noise, and communal (collective)
112-113 rearing, 179-181
heart beat stimulation, mechanism of bond formation,
112-113 181-185
sensitization, 114 period immediately after
sleep induction, 113 birth, 182-185
Lesions, limbic system, recovery communications, 148-149
after, mice, 27 reaction in communication,
Locomotor activity, effect of 153-155, 167-169
malnutrition, 32 conversation, 2-3 year olds,
Love, deprivation, as punitive 169-172
measure, 207 games, 159-162
and self-activated awareness,
Malnutrition 155-164
caloric/protein/lipidic, damage self-consciousness, infant,
by, 31 165-167
effect on brain growth during techniques by mothers,
pregnancy, 31 168-169
during suckling period, mice, (see also Parent/infant)
32 Mother's
essential fatty acid presence, neonate's responses,
deprivation, 33 149-151
locomotor activity, 32 separation from mother, 150
Maternal behavior role in social development,
and infant signals, 2-11 rhesus monkeys, 74-76
in virgin hamsters, 3 differences in individuals,
Maturational pattern and behav- 75-76
ioral development, 23-24 effects, 75-76
Maturity at birth, mammal, and Motor reaction to acoustic
evolution, 26 stimuli, fetal, 99-100
Methysergide, effect on suckling, tables, 102-106
51, 52 Mouse strains and genetic
effect on weaning, 52 studies, 24-30
INDEX 301
Neoencephalic and paleoencephalic Parent/infant interaction

mechanisms, 24 (continued)
Neural plasticity, adult, and patterns, cross-cultural
noradrenalin, 65-66 perspective, 177-217
binocular vision, 65 (see aZso Cross-cultural
Neurochemical systems, perspective)
development, and behavior Parents in treatment of autistic
patterns, 34-35 children, 258-261,
Neurophysiological study, 267-281
newborn, and behavior Patting, 194-196
states, 128-140 Peers, as playmates, rhesus
EEG changes, 133-140 monkeys, 77
Newborn Perinatal problems and autistic
separation from mother, 150 children, 251-252
visual states, 132 Physiological factors in
Noradrenalin and stress, 64 temperament differences,
and adult neural plasticity, rhesus monkeys, 81-82
65-66 autonomic/behavioral relation-
Nursing, 200-201 ships, 84-86
Nutritional factors in suckling, conclusions, 86-87
rat, 41-44 heart rate under conditioning
trials, 82-84
Odor conditioning and suckling, and preseparation group
rat, 49-50 behaviors, 85-86
Olfactory separation behaviors, 86, 87
signals, 10 Plasticity, adult
stimulus for suckling, rat, 48 and anxiety, 63-64
Ontogenic factors in autism and neural, and noradrenalin, 65-66
social avoidance, 250-258 binocular vision, 65
Opiate receptors, maturation, 35 Play in infancy, 159-162, 169-172
Oral stimulation, suckling, rat, dialogues with babies, 203-205
42-44, 50-51 didactic programs, 230-235
Oxytocin-stimulated glandular comparative studies, 232
system, rat, 48 measuring, 231
relation to integrative
Paleoencephalic capacities, 231, 232-233
activities, and circadian father's role, 208
energy deployment general aspects, 210
processes, 28 Plumage pattern as signal, 10
and neoencephalic mechanisms, Postnatal effects of intrauterine
24 noise, 112-113
Parental care Prematurity
acceptance of young, 2 and auditory evoked potentials,
male/female, 14 99, 100
Parent/infant interaction EEG changes, 134
biological attachment theory and prenatal learning, 111-112
and environmentalist Prenatal
theory, 178-179 learning see Learning, prenatal
in didactic programs, 222-224, problems and autistic
234 children, 251-252
302 INDEX
Preseparation group behaviors, Sensitive periods (continued)

rhesus monkeys, 85 rehabilitation and early
Punishment and reward, 206-207 experience, 66-67
vulnerable periods, 58
Quipazine, effect on suckling, 51 Sensory control of suckling, rat,
48-51
Reaching and grasping, infants, Separation behaviors, rhesus
159 monkeys, 86,87
Reflex activities, development, Shell-shock, treatment, 64
effect of malnutrition, Siblings, male, effect on young
32 rhesus monkeys, 77
Rehabilitation and early exper- Signals, infant, 1-19
ience, 66-67 in adoption of young, 2-11
Reward, and punishment, 206-207 (see also Adoption of young)
Rhesus monkeys, social develop- in adult and social behavior,
ment, 71-92 11-12
individual differences, 74-89 domestication, 12-13
anxiety, 78-81 sensitivity of man, 12-14
autonomic, indices, 81-84 Sleep
and behavioral, relation- and EEG changes, fetus and
ship, 84-86 newborn, 133-140
conclusions, 86-89 (see also Electroencephalo-
fearfulness, 78-81 graphic changes)
ontogenic differences, 76-78 induction and heart beat
preseparation group stimulation, 113
behaviors, 85 Smiling, in infants, 147-148,
role of mother, 74-76 151, 152, 158
role of others, 76-78 Snout denervation, effect on
normative patterns, 72-74 suckling, rat pup, 49
early stages, 72-73 Social
male/female differences, avoidance in autistic children,
73-74 241-266
social play, 73 (see also Autistic children)
and cultural change, and
Self-activated awareness, of urbanization, 285-288
objects and games, relationships, rhesus monkeys,
development, infant with 71-92
mother, 155-164 (see also Rhesus monkeys)
Self-consciousness, development, Socialization, concept, 283-285
in infancy, 165-167 definition, 284
Sensitive periods, differentiation from education,
interpretation, 57-70 284
anxiety and adult plasticity, early, 206-207
63-64 Sounds
definition of term, 57-58 intensity, intrauterine, 94-97
early experience, 58 recordings, 96
explanation, 58-59 outside, affecting fetus, 94-97
imprinting, 59-63 (see also Acoustic stimuli)
internal protection of signals, 10-11
preferences, 61-63
INDEX 303
Specialist animal, 22-23 Suckling (continued)

distinction from generalist, developmental analysis, rat
22-23 (continued)
Speech snout denervation, 49
in infancy, 170-172 tactile stimulus, 49
intrauterine, effect, 113 transition from suckling to
in birds, 114-115 weaning, 44-45
human, 113, 114, 115-117
postnatal sensitization, 114 Tactile
recognition of mother's contact, 191-192
voice, newborns, 117 stimulus and suckling, rat, 49
Spindle-delta-bursts, 136 Testing in infancy, 166
Stranger Temperament differences in rhesus
awareness, 185, 186 monkeys, 78-81, 86-89
reaction to, infants, 162-164 autonomic indices, 81-84
Strategies employed by infants, and behavioral, relation-
185, 189-190 ships, 84-86
Stress and noradrenalin, 64 heart rate, 82-84
Suckling Teratogeny and behavioral
and contraception, 202 development, 30-33
developmental analysis, rat, Timidity, individual differences,
39-55 rhesus monkeys, 78-81
anaesthesizing mother, autonomic indices, 81-84
effects, 40, 42, 46 and behavioral, relation-
by cannula, 46, 47 ships, 84-86
deterioration, 40-41 heart rate, 82-84
discrimination, 50 Toilet training, 207
gastric preloading, 42-44, 46 Toys, didactic, 230-235
and independent feeding,
relationship, 51-53 Uncles, role in child's
introduction of food pellets, upbringing, 210-211
43-45 Urban phenomenon, definition, 286
non-nutritional factors, Urbanesim, effect on child
44-45 behavior, 288-289
nutritional factors, 41-45 Urbanity, new concept, and child
odor conditioning, 49-50 behavior, 289-293
olfactory stimulus, 48-49 Urbanization influence on child
oral stimulation, 42-44, behavior, 283-294
50-51 change in local communities,
prolonging, 51 287-288
readin~ss, 40 concept of socialization,
decline, 44-45 283-285
measurement, 40 differentiation from
regulation of milk intake, education, 283-284
45-48 cultural and social change,
relationship to weaning, 285-288
51-53 and urbanesim, 288-289
rhythmic and arrhythmic, urbanity, new concept, 289-291
47-48
sensory control, 48-51
304 INDEX
Visual
contacts, 188, 1910192
(see also Face-to-face
communication)
system, at birth, 131
Voice
changes in contact with infant,
188, 193
mother's, recognition by new-
born, 11
Wariness
individual differences, rhesus
monkeys, 78-81, 86-89
autonomic, indices, 81-84
and behavioral, relation-
ships, 84-86
heart rate, 82-84
with strangers, relation to
game playing, 162-164
Weaning, 200-202
effects of methysergide or
saline, 52
independent feeding during,
relationship to suckling,
51-53
and suckling, relationship,
rat, 51-53

(Ettore Majorana International Science Series) Davide Csermely, Danilo Mainardi (Auth.), Alberto Oliverio, Michele Zappella (Eds.) - The Behavior of Human Infants-Springer US (1983)

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

(Ettore Majorana International Science Series) Davide Csermely, Danilo Mainardi (Auth.), Alberto Oliverio, Michele Zappella (Eds.) - The Behavior of Human Infants-Springer US (1983)

Uploaded by

Copyright:

Available Formats

The Behavior of

Volume 5 THE AGING BRAIN: Neurological and Mental Disturbances

Volume 6 THE LUNG IN ITS ENVIRONMENT

Volume 7 INVESTIGATION OF BRAIN FUNCTION

Volume 8 THE IMMUNOLOGY OF INFANT FEEDING

Volume 9 ADVANCES IN NEPHROUROLOGY

Volume 10 CELLULAR BIOLOGY OF THE LUNG

Volume 11 BIOELECTROCHEMISTRY I: Biological Redox Reactions

Volume 12 SELECTED TOPICS IN PREVENTIVE CARDIOLOGY

Volume 13 THE BEHAVIOR OF HUMAN INFANTS

Plenum Press • New York and London

Main entry under title

The Behavior of human infants.

(Ettore majorana international science series, Life sciences; v. 13)

Proceedings of the First workshop on the International School of Ethology on

© 1983 Plenum Press, New York

All rights reserved

No part of this book may be reproduced, stored in a retrieval system, or transmitted

The present workshop started with various requests on behalf of

If these three referral points are accepted as significant in the

informational input. The psychobiological approach allows a better

Following this approach we have been able, for example, to see

These data support the more recent interpretations of severe

At the end of the meeting it was apparent from the discussion

A Comparative Approach to Behavioral

A Developmental Analysis of Suckling

The Interpretation of Sensitive Periods 57

Social Development in Rhesus Monkeys:

And What of Fetal Audition? 93

Some Peculiarities of Electrical Brain

Interpersonal Abilities of Infants as

Patterns of Parent-Child Interaction in

The Psychobiology of the First Didactic

Development of Social Avoidance in

Parental Affiliation as a Key Reference

Urbanization as a Factor Influencing

Davide Csermely and Danilo Mainardi

If any of us can distinguish at first sight an infant mammal or

We assign the status of infant to an animal only if we recognize

Human "infant Gestalt" is quite similar to that of many other

The origin and evolution of infant form is evident when one

i.e. the moment of reproduction. An adult who has produced some

The place where the infant is encountered may be especially

INFANT SIGNALS IN ADOPTION OF YOUNG

In addition, different species have evolved similarities in the

in infant signals further increased the species' genetic benefit (in

Intraspecific and interspecific adoption in rodents has been an

Initially, we set out to study interspecific adoption between

A second parallel set of tests was done to see whether young of

Subsequent research (Mainardi et al., 1973) investigated several

Table 1. Adoption of Mice by Golden Hamster Females and Relationship

Females Days after Age of mouse Number of Adopted

those obtained on days 3 to 12 was carried out using Fisher's test

The second set of experiments was aimed at understanding whether

The third set of experiments was aimed at determining whether

Fig. 1. On the ordinate percentage of adoptions effected by

"Abnormal behavior" of this sort is also found in intraspecific

In the previous experiments it was possible to evoke retrieving,

Another experiment (Mainardi et al., 1976) analyzed an interest-

Another set of experiments (Favoriti et al., 1977) again inves-

Using nursing female mice we also studied intraspecific adoption

Table 2. Number of Hamsters and Mice Retrieved First in Every Group.

No. of Retrievals of Hamsters Mice Void