Orofacial mechanoreceptors in humans: Encoding characteristics and

responses during natural orofacial behaviors

Mats Trulsson and Roland S Johansson1

Karolinska Institute, Dept. of Odontology, SE-141 04 Huddinge, Sweden.
1
Ume University, Dept. of Integrative Medical Biology, Sections for Physiology, SE-901 87 Ume, Sweden.
Summary. We used microneurography to characterize stimulus-encoding properties of low-threshold mechanoreceptive afferents in human orofacial tissues. Signals were recorded from single afferents in the infraorbital, lingual and
inferior alveolar nerves while localized, controlled, mechanical stimuli were delivered to the facial skin, lips, oral
mucosa and teeth. We likewise analyzed activity in these afferents during orofacial behaviors such as speech,
chewing and biting. The afferents in the soft tissues functionally resemble four types described in the human hand:
hair follicle afferents, slowly adapting (SA) type I and type II afferents and fast adapting (FA) type I afferents.
Afferents in the facial skin, lips and buccal mucosa respond not only to contact with environmental objects, but also
to contact between the lips, changes in air pressure generated for speech sounds, and to facial skin and mucosa
deformations that accompany lip and jaw movements associated with chewing and swallowing. Hence, in addition
to exteroceptive information, these afferents provide proprioceptive information. In contrast, afferents terminating
superficially in the tongue do not signal proprioceptive information about tongue movements in this manner. They
only respond when the receptive field is brought into contact with other intraoral structures or objects, e.g., the teeth
or food. All human periodontal afferents adapt slowly to maintained tooth loads. Populations of periodontal
afferents encode information about both which teeth are loaded and the direction of forces applied to individual
teeth. Most afferents exhibit a markedly curved relationship between discharge rate and force amplitude, featuring
the highest sensitivity to changes in tooth load at low forces (below 1 N). Accordingly, periodontal afferents
efficiently encode tooth load when subjects first contact, hold, and gently manipulate food by the teeth. In contrast,
only a minority of the afferents encodes the rapid and strong force increase generated when biting through food. We
conclude, that humans use periodontal afferent signals to control jaw actions associated with intraoral manipulation
of food rather than exertion of jaw power actions.

Introduction
The central nervous system requires signals from orofacial mechanoreceptors for the
sensorimotor regulation of oral behaviors (see Lund 1991; Trulsson and Johansson 1996b). This
chapter briefly reviews recent physiological findings regarding the encoding of mechanical
events by human orofacial mechanoreceptive afferents, including their responses during natural
orofacial behaviors. For a more detailed account, the reader is referred to the original articles

cited. The neural data were gathered in studies on young adult volunteers, using the
microneurographic technique introduced by Vallbo and Hagbarth (1968). The infraorbital nerve,
that innervates the lower eyelid, skin, and mucous membranes of the cheek and upper lip, was
impaled by the microelectrode close to its exit through the infraorbital foramen (Johansson et al.
1988a). The lingual and inferior alveolar nerves were approached through the oral cavity and
impaled near the mandibular foramen (Johansson and Olsson 1976; Trulsson and Essick 1997).
The lingual nerve innervates the anterior part of the tongue, and the inferior alveolar nerve the
teeth and gingiva of the lower jaw, the lower lip and the chin. After insertion in the target nerve,
multi-unit activity was first recorded, then the electrode was carefully adjusted to obtain impulse
responses from a single afferent.

Mechanoreceptors in orofacial soft tissues

Multi-unit activity indicates that the innervation territories of individual nerve fascicles vary
considerably. For the infraorbital nerve, most fascicle fields encompass a part of the upper lip
and the corner of the mouth (Fig. 1 A, top) (Johansson et al. 1988a; see also Nordin and
Thomander 1989). For the lingual nerve, all fascicle fields include the tip of the tongue (Trulsson
and Essick 1997). This suggests that the perioral region and the tip of the tongue are areas with a
particularly high density of mechanoreceptive innervation.
Single unit recordings reveal that the mechanoreceptive innervation of orofacial soft tissues
comprises afferents with both rapidly and slowly adapting response properties. A majority of the
afferents in the facial skin and the transitional zone of the lip is slowly adapting with small and
well-defined receptive fields (Fig. 1 A, middle and bottom) (Johansson et al. 1988a; Edin et al.
1995; see also Nordin and Hagbarth 1989). Likewise, only slowly adapting afferents are present
in our limited sample from the buccal mucosa (Johansson et al. 1988a). On the contrary, the
majority of the afferents terminating superficially in the tongue, which show extremely small and
well defined receptive fields, adapt fast to maintained tissue deformation (Fig. 2 A) (Trulsson
and Essick 1997). It is noteworthy that the extraordinarily high acuity of the tip of the tongue for
form and texture is associated with a preponderance of rapidly adapting afferent. Mainly based
on recordings from afferents of the distal fingerpads of the monkey, it has been inferred that
slowly adapting afferents, rather than rapidly adapting afferents, are largely responsible for the
perception of spatial form and texture (Johnson and Hsiao 1992; Blake et al., 1997).
In general, the mechanoreceptive afferents that supply the human facial skin, lips and oral
mucosa show properties similar to those of tactile afferents of the human hand, i.e. hair follicle
afferents and three types of afferents described in the glabrous skin (FA I, SA I and SA II
afferents; see Johansson and Vallbo 1983). Slowly adapting (SA) afferents with a high dynamic

sensitivity and an irregular discharge during maintained tissue deformation resemble the slowly
adapting type I units (SA I) in the hairy and glabrous skin of the human hand. Another group of
slowly adapting afferents, characterized by a regular discharge rate and spontaneous activity, are
similar to the slowly adapting type II (SA II) units. An important feature of SA II units is an
exquisite sensitivity to lateral skin stretch applied far from the zone of maximal sensitivity.
Rapidly adapting afferents in the orofacial region resemble those of the fast adapting type I (FA
I) units in the glabrous skin of the hand. Importantly, no afferents encountered showed response
properties akin to those of Pacinian-corpuscle afferents (FA II), which is in agreement with
psychophysical findings in man (Barlow 1987).

'a:

0.2 s
'a:

1s

Open

FA
SA

100
imp/s
0.2 s

50
imp/s
1s

Figure 1. A, Receptive fields of nerve fascicles (top) and single tactile afferents (middle and bottom) identified in
records from the infraorbital (top and middle) and the inferior alveolar (bottom) nerves. B E, Afferent activity
during speech gestures and chewing movements recorded from the infraorbital nerve. B and C illustrate multi-unit
and single-unit activity evoked when the subject said ['a:pA], respectively. B, Audio signal, rectified and filtered
nerve signal and microelectrode record represented in top, middle and bottom traces, respectively. C, Slowly
adapting afferent with receptive field located in the buccal mucosa about 1 cm lateral to the corner of the mouth.
Audio signal, microelectrode record, and instantaneous discharge frequency represented in top, middle and bottom
traces, respectively. Arrowheads in B and C indicate a moment of rapid labial movements resulting in 'pop-puff'
sounds in the audio record. D and E, Multi-unit and single-unit activity during chewing movements, respectively
(mouth opening during chewing cycle; jaw displacement ca. 1 cm). D, Top trace, solid curve indicate the phases of
jaw movements as recorded with a transducer-equipped von Frey hair held under the chin, and dashed curves (drawn
by eye) indicate estimated vertical jaw displacements; middle trace and bottom trace as in B. E, Same slowly
adapting afferent as in C. Top trace as in D; middle trace and bottom trace as in C. (A, adapted from Johansson et al.
1988a and Edin et al. 1995; B E, adapted from Johansson et al. 1988b)

Afferent signals during natural orofacial behaviors. We recorded signals from the infraorbital nerve during natural orofacial behaviors including speech gestures, chewing, licking, and
swallowing. Figures 1 B and C give examples of afferent responses when the subject was asked
to say ['a:pA] ('apa' is the Swedish word for monkey). A tri-phasic response characterizes the

multi-unit activity from fascicles that encircle the corner of the mouth (see middle trace of Fig. 1
B). These three phases correspond to (1) mouth opening, (2) lip closure (arrow) and (3) the
build-up of intraoral air pressure and lip-opening movement for the [p]-release. Figure 1 C
exemplifies a single mucosa afferent that responded to the second phase, i.e., lip closure. Thus,
recordings from single afferents indicate that the multi-unit activity originates from signals in
individual skin and mucosa afferents that respond to diverse phases of multi-phasic speech
gestures.
Figures 1 D and E show recordings obtained when the subject performed chewing
movements. The multi-unit signal in Fig. 1 D exhibits two peaks of afferent activity during each
cycle of vertical jaw displacement one peak during jaw opening and another during closing.
Thus, the mechanoreceptive afferents respond primarily to jaw movements rather than to the
position of the jaw. Figure 1 E exemplifies responses from a slowly adapting mucosa afferent
during chewing. This afferent responded most vigorously during jaw opening; other afferents
preferred jaw-closing movements.

50
imp/s

0.5 s
out
40
imp/s

1s

in

out

Figure 2. Responses of single mechanoreceptive afferents recorded from the lingual nerve during active tongue
movements. A, Data from a rapidly adapting, superficial unit that exhibited a small receptive field on the tip of the
tongue. A burst of impulses (marked by the gray bars) was elicited each time the subject moved the tongue so that
the receptive field was brought into contact with a lower incisor tooth. Top trace, instantaneous discharge frequency;
bottom trace, sampled neurogram. The receptive fields of 22 superficial mechanoreceptive afferents on the tongue
(FA-black fields, SA-white fields) are shown to the right. B, Data from a slowly adapting, deep unit that responded
each time the subject protruded the tongue. Upper tracing, the solid curve indicates the phase of the rhythmic tongue
movement as recorded with a transducer-equipped von Frey hair held close to the tip of the tongue; dashed curve
(drawn by eye) estimates horizontal tongue displacement (maximum excursion ca 10 mm in amplitude). Care was
taken to assure that the receptive field (shown to the right) defined by local perpendicular pressure of the dorsal
lingual mucosa did not contact oral structures during the active tongue movements. Middle and lower tracings as in
A. (Adapted from Trulsson and Essick, 1997.)

The superficial mechanoreceptive afferents in the human tongue do not respond to tongue
movements as such, unless the receptive field of the afferent is brought in contact with other
intraoral structures and objects (Trulsson and Essick, 1997). The fast adapting afferent in Figure
2 A responded each time the subject moved the tongue so that the receptive field on the tip of the

tongue contacted a lower incisor. However, afferents deep in the tongue (probably muscle
spindle endings) encode information about voluntary tongue movements in the absence of direct
contact with the receptive field (Fig. 2 B).
In sum, mechanoreceptors in the facial skin, lips and buccal mucosa encode contact with
environmental objects as expected. However, cutaneous and mucosal afferents also discharge
vigorously during contact between the lips, air pressures generated for speech sounds, and to the
deformations/strains of the facial skin and mucosa associated with various phases of voluntary
lip and jaw movements. Subsequent human studies have largely substantiated these findings
(Nordin and Thomander 1989; Nordin and Hagbarth 1989; Furusawa 1992). Hence,
mechanoreceptors of orofacial soft tissues (except for superficial receptors of the tongue)
provide proprioceptive information about orofacial movements. Changes in the strain pattern of
relevant skin/mucosa areas probably mediate the proprioceptive sensitivity of these afferents
(also see Edin and Abbs 1991; Edin 1992). Since the perioral area of the human face lacks
muscle spindles, tendon organs, and joint receptors, it is a model system for the study of the
contributions of cutaneous afferents to proprioception (e.g., Connor and Abbs 1998).

Periodontal mechanoreceptors
Periodontal mechanoreceptors terminate among the collagen fibers in the periodontal ligament
which attaches the root of the tooth to the alveolar bone, and encode temporal, spatial, and
intensive aspects of forces acting on the dentition (Trulsson and Johansson 1996b). We recorded
signals from single periodontal afferents in the inferior alveolar nerve in response to forces
applied to the surfaces of a nylon cube cemented above the edge of the receptor bearing tooth,
most often an incisor. Human periodontal afferents continuously discharge during sustained
tooth loads, i.e., they are slowly adapting.
Spatial aspects of tooth loads. Periodontal afferents exhibit receptive fields broadly tuned for
the direction of tooth loading (Figs. 3 A and B) (Trulsson et al. 1992). Typically, the afferents
respond to forces applied to the receptor bearing tooth in two to four of six directions tested
(lingual, labial, mesial, distal, upward, downward). These receptive field properties agree with
those observed in the cat (Sakada and Kamio 1971; Karita and Tabata 1985) in contrast to those
in the dog which appear to have narrower receptive fields (Hannam 1970). Due to the broad
directional tuning, an individual periodontal afferent provides ambiguous information about the
direction of a force applied to the tooth. However, population vector analysis, similar to that
introduced by Georgopoulos et al. (1983) for cortical neurons, reveals that information about the
precise direction of force is represented reliably in the activity of the population of periodontal
afferents (Fig. 3 C). Population analyses based on artificial neural networks yield the same

conclusion (Edin and Trulsson 1992).

Li

A
Li

La

Me

Di

25
imp/s

75
imp/s

Me

Di

250
mN
Up

Do

Up

1s

Li

La
La

Li
Me

10
imp/s

Di

Up

Me

Di

Up

Do
La

Do

Do

Figure 3. A-B, Responses of a single periodontal afferent to forces of standardized amplitudes (250 mN) applied
in six orthogonal directions to the receptor-bearing tooth, an incisor. A, Neurograms with the corresponding force
records above. Dashed horizontal lines indicate the period of the static responses. B, Vectorial presentation of the
static responses to stimulations in the horizontal plane (left) and in the axial directions (right). The length of the
vectors is proportional to the mean impulse frequency during five stimulations in each direction and the direction of
the vector represents the stimulus direction. The circle represents the spontaneous discharge rate with the radius
indicating its intensity. The thick arrow represents an estimate of the most efficient excitatory stimulus direction in
the horizontal plane, i.e., the 'preferred direction'. C, Estimated capacity of a population of human periodontal
afferents to encode force direction shown as a neuronal population vector (heavy dashed lines with arrow-head)
calculated for six force stimulation directions and viewed in the sagittal (left), horizontal (middle) and frontal (right)
planes. For each cluster, the vectors indicated by the thin lines with a common origin represent responses in
individual afferents. The direction of these vectors represents the preferred directions of the afferents (heavy arrow
B), whereas the length of the vectors represents the size of their static responses to the current stimulation direction;
the actual stimulation direction is represented by the position of the clusters relative to the tooth. Thus, the separate
clusters all represent the same neuronal population. The population vector is the vectorial sum of the vectors of the
individual afferents. Note the separate calibrations for the individual afferent vectors and the resultant vector (left
and right circle, respectively). That the neuronal population vector (calculated for the six stimulation directions)
corresponded well to the applied stimulation direction indicate that directional information about the forces striking
the tooth is expressed in the population of periodontal afferents. A C, Force directions: Li= lingual, La= labial,
Me= mesial, Di= distal, Do= downward and Up= upward. (Adapted from Trulsson et al., 1992.)

About half of the human periodontal afferents respond to loading of a group of adjacent
teeth, typically two to four teeth (Trulsson 1993). Each afferent exhibit the highest response rates
to stimulation of one particular tooth, with a gradual and rather sharp decline in responsivity to
loads applied to the adjacent teeth. Mechanical coupling between neighboring teeth (interdental
contacts and transseptal collagen fibers) generates the multiple-tooth receptive fields rather than
branching of single afferents to more than one tooth. However, the multiple-tooth characteristic
of the receptive fields does not necessarily degrade the ability of the central nervous system to
locate uniquely a force stimulus striking a particular tooth. Overlapping peripheral receptive
fields are indeed characteristic of all sensory systems and may actually improve the acuity of

spatial representations. Furthermore, the responses elicited through stimulation of the teeth
adjacent to the receptor-bearing tooth may provide information regarding magnitudes of tooth
loads and their directions (Edin and Trulsson 1992).
Intensive aspects of tooth loads. To study the encoding of intensity of tooth loads by human
periodontal afferents we delivered various ramp-and-hold shaped force profiles to the receptor
bearing tooth in its most responsive direction (Fig. 4 A) (Trulsson and Johansson 1994). We first
analyzed the relationship between the amplitude of the steady state (hold) force and the steady
state discharge rate. For each periodontal afferent investigated, the steady state discharge rate
was approximately proportional to F/(F+c), where F represents the force, and c the force at
which half the estimated maximum discharge rate is attained. This transform implies that the
discharge rate increases more or less linearly until F approaches c and then levels off (Fig. 4 B).
Interestingly, we subsequently discovered that this non-linear transform is compatible with a
biomechanical model of the periodontal ligament, implying a squeezing of the nerve endings
when the surrounding collagen fibers are stretched (Fig. 4 C) (cf. Swett and Schoultz, 1975).

'Hyperbolic' afferents

'Nearly-linear' afferents

100
Steady state response (imp/s)

1N

Coll
age
n fib
res

50
s
fibre
gen
Colla

0
0

1s

Coll
age
n fib
res

3
2
Steady state force (N)

Tooth

Alveolar
bone

Figure 4. Responses of periodontal afferents to steady state forces of various amplitudes applied to the receptorbearing tooth in the most responsive direction. A, Examples of force stimulation and nerve recordings of a single
afferent during stimuli of four different amplitudes. The time bar marks the period during which the steady state
response and steady state force was measured. B, Stimulus-response functions for 19 periodontal afferents. The
curves fitted to the data are defined by the F/(F+c) transform described in text. Solid and dashed curves refer to
afferents showing a hyperbolic stimulus-response relationship (n = 15) and a nearly-linear relationship (n = 4),
respectively. The curve labeled a refer to the same afferent as illustrated in A. C, A simple mechanical model of the
periodontal ligament accounting for the F/(F+c) transform. Elastic tissues (represented by springs) are interspersed
between strands of collagen fibers attaching the tooth to the alveolar bone with three hypothetical relationships
between bundles of collagen fibers and the interleaved tissues. In the two upper cases, these tissues would be
subjected to compressional stress and in the lower case tensile stress when the collagen fibers are under tension
during tooth loading (F). The small spring in series with a force transducer (Td; nerve endings sensitive to stress)
represents sub-portions of the interspersed tissue. (Adapted from Trulsson and Johansson, 1994.)

A majority of the afferents (15/19) show a marked curved (hyperbolic) relationship

between the steady state discharge rate and the amplitude of the hold force (Fig. 4 B).

Accordingly, these afferents show low c-values (< 1.2 N) and feature the highest sensitivity to
changes in static force at force levels below some 1 N. At higher forces, the sensitivity gradually
decreases. Moreover, for these hyperbolic afferents the sensitivity to changes in force (dynamic
sensitivity) decreases in parallel with the static sensitivity as the force increases. These afferents
exhibit similarly curved stimulus-response relationships also in the less responsive stimulation
directions, but the discharge rates are lower. Hyperbolic stimulus-response relationships similar
to those of most human periodontal afferents are also characteristic of periodontal afferents in
animal studies (Pfaffmann 1939; Ness 1954; Hannam 1969; Hannam and Farnsworth 1977). A
minority of the human afferents (4/19), however, exhibits nearly linear stimulus-response
relationships (nearly-linear afferents in Fig. 4 B). Thus, these afferents efficiently encode force
also at high forces (c-value between 5 and 22 N).

Normal periodontal sensibility

Anesthesia of the periodontium

Hold-and-split
peanut

Hold-and-split
peanut
10 N

10 N
0.5 s

normal, hold-and-split trials

anesthesia, hold-and-split trials

20

30

20

10

10

0
0

3
2
Hold force, N

D4
Hold force, N

Frequency of trials, %

Static sensitivity, imp/s/N

0.5 s

3
2
1
0
Nat Den Imp

Nor Ane

Figure 5. A and B, Examples of force profiles (five superimposed trials) obtained during the hold-and-split task
with peanuts during normal periodontal sensibility and during anesthesia of the periodontium, respectively. Note the
considerably higher and more variable hold forces produced by the subjects during the periodontal anesthesia. C,
Frequency distribution of hold forces spontaneously adopted by the subjects; solid and dashed line histograms refer
to trials with normal sensibility and trials with anesthesia of the periodontium, respectively. Superimposed curves
represent the sensitivity to changes in tooth load of human periodontal afferents. The three dotted curves refer to the
mean +/- one standard deviation of the first force differential averaged across the 19 periodontal afferents in Fig. 4
B. (Adapted from Trulsson and Johansson, 1996a). D, Left histogram show mean hold forces employed by subjects
in the natural (Nat), denture (Den) and implant (Imp) groups. Average values for individual subjects are indicated by
filled circles (n=20). Right bar histograms represent the mean hold force by subjects during normal conditions (Nor)
and during periodontal anesthesia (Ane). Vertical lines the range of average values for individual subjects.

To capture the responses of human periodontal afferents to arbitrary load profiles we

developed a quantitative model that successfully incorporates both the static and dynamic
sensitivity of the afferents. In this model, the discharge rate of an afferent is the weighted sum of

a static response component derived from the F/(F+c) transform (described above) and a
dynamic response component derived from a high pass filtering of the same transform. The
model parameters (weight factors, time constants of the filter etc.) are characteristic for each
individual afferent. The modeled discharge rates turned out to be practically identical to those
actually measured for novel force stimulations, i.e., stimuli that were not included during the
development of the model (for further details see Trulsson and Johansson 1994).
Role of periodontal afferents in the control of jaw actions. Because of their overall high
sensitivity to low forces, we hypothesized that the periodontal afferents of the front teeth are
particularly suited to convey information about the contact state between food and the dentition
during initial contact and holding maneuvers. To test the hypothesis we selected a common oral
behavior for study: Holding and biting through a piece of food using the front teeth (Trulsson
and Johansson 1996a). During this hold and split task, illustrated in Fig. 5 A, we recorded the
time varying forces while subjects bit on either half a peanut or a piece of biscuit. The forces at
which the food split (peanuts 18.4 +/- 4.7 N, biscuit 9.1 +/- 3.0 N; mean +/- SD) was larger, by
an order of magnitude, than the forces exerted while the subjects just held the food between the
incisors (0.62 +/- 0.32 N). From the obtained force records, we simulated the discharge in
individual periodontal afferents using the developed model. This simulation indeed demonstrate
that the majority of the afferents responds intensely at the time of initial contact and maintain an
ongoing discharge while subjects hold the food between the teeth. Noteworthy, the discharge rate
does not substantially increase during execution of the force ramp used to split the food particles.
These observations together with the following evidence indicate that subjects use
periodontal afferent information to specify the level of force during the hold phase of our holdand-split task. First, the distribution of hold forces are skewed to coincide with the range over
which periodontal afferents are most sensitive to changes in force (Fig. 5 C). That is, subjects
chose to use hold forces great enough to achieve a stable clasp, but they automatically avoid
higher forces that compromise the sensitivity of most afferents to force changes. Second, during
anesthesia of the periodontal tissues, the hold forces are considerably greater and show greater
variability both during the individual trials and between trials (Fig. 5 C; also compare the force
profiles in Figs. 5 A and B) (Trulsson and Johansson, 1996a). Finally, high hold force levels are
observed for patients lacking periodontal receptors, i.e., patients treated with dental prosthesis
supported only by the oral mucosa or osseointegrated implants (Trulsson and Gunne 1998).
Thus, we conclude that periodontal afferent signals play a decisive role in the specification of the
force level when humans manipulate and hold substances between the teeth.
Acknowledgments
This work was supported by the Swedish Medical Research Council (project no. 8667) and Ume University.

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