Professional Documents
Culture Documents
From the Medical University of South Carolina (JPL, ARH, JRD, RBL, MBH,
DEB, MSG) and Ralph H. Johnson VA Medical Center (JPL, MBH, MSG),
Charleston, South Carolina, and National Institute of Child Health and Human
Development (JDN), Bethesda, Maryland.
Address reprint requests to J.P. Lorberbaum, M.D., Department of Psychiatry,
Medical University of South Carolina, Charleston, SC 29425
Received June 15, 2001; revised February 7, 2001; revised August 20, 2001;
accepted September 5, 2001.
Introduction
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J.P. Lorberbaum et al
Initial Visit
We informed subjects that our goal was to identify brain regions
that activate when new mothers listen to different sounds and that
this information would help us have a better understanding of
mothering behavior. Subjects were not specifically informed of
the sounds they would be hearing, including the infant cries.
After giving informed consent, subjects underwent structured
clinical interviews for DSM-IV Axis I and II disorders (First et
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J.P. Lorberbaum et al
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5. Temporal filtering: The data were filtered using a Butterworth low frequency filter removing fMRI intensity patterns greater than twice the cycle lengths period (240 sec).
6. Statistical analysis: Using the SPM96 statistics function
and then MEDxs image calculator, the individual subject
fMRI data were statistically analyzed to generate unthresholded z maps for control noise minus rest, cry minus rest,
cry minus control noise, and control noise minus cry z
maps. These z maps contained a z score for each insidethe-brain voxel, whether the z score was positive, negative,
large, or small. In generating these z maps, we used the
SPM96 options for a delayed boxcar model, temporal
smoothing, and an uncorrected F threshold (UFp) of
0.999.
GENERATING GROUP STATISTICAL DATA USING A RANDOM EFFECTS ANALYSIS AND THEN A CLUSTER ANALY-
Data Analysis
We performed all data analysis on Sun SPARCstation workstations (Sun Microsystems, Mountain View, CA) using MEDx
3.2/SPM96 (Sensor Systems, Sterling, VA; Frackowiak et al
1997).
INDIVIDUAL SUBJECT FMRI DATA ANALYSIS. Our goal
here was to generate unthresholded z maps comparing control
noise versus rest, cry versus rest, and cry versus control noise for
each subject. To accomplish this, each subjects functional MRI
data were taken through the following steps:
1. Motion detection and correction: The data were motioncorrected to less than 2 2 2 mm in all planes using
Automatic Image Registration (Woods et al 1992). After
motion correction, all subjects had 1.4-mm movement
in all planes.
2. Spatial normalization: The data were then transformed into
Talairach space with output voxel dimensions 3 3 3
mm and a coronal bounding box of y 42 to 70 to
account for the fact that we did not obtain imaging data in
posterior brain regions.
3. Spatial smoothing: The data were then spatially smoothed
using a 6 6 6 mm gaussian kernel.
4. Intensity masking and normalization: Each image volume
was then intensity masked using a 35% of maximum
intensity inclusion threshold and intensity normalized so
that its mean signal intensity was 1000.
We only
discuss how we generated the uniquely activated by cries group
statistical map. An analogous method was used to generate the
uniquely activated by control sounds statistical map.
Our goal here was to find regions that were active with cries
but not with control noises and that were also statistically more
active with the cries than the control noises. To do this, we first
created a mask of voxels which had a z score 1.96 on the group
cry minus rest z map and 1.96 on the group control noise
minus rest z map. In this masked active with cry minus rest, not
active with control noise minus rest region, we then performed
a cluster analysis on the group cry minus control noise z map
using a z map threshold of z 1.96 and cluster statistical weight
of p .05. We also found local maxima on this uniquely
activated by cries group cluster map.
ACTIVATED BY CRIES AND CONTROL NOISES.
Results
Subtests and Ratings
Usable fMRI data existed on 10 of 11 mothers. One data
set was accidentally acquired with a different MRI field of
view from the others and was discarded. All the data
below refer to the 10 included subjects. Group demographics as well as Maternal and Infant Temperament Ratings
are displayed in Table 1. Mothers were 30.55 4.66 years
old, and their infants were 6.18 1.1 weeks old. Nine
mothers were married; the 10th mother was abandoned by
her husband during her pregnancy.
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Table 2. Mothers Retrospective Average Emotional Ratings during the Infant Cry Imaging Paradigm (Means Standard
Deviations Noted)
Emotional ratings
Control noises
(0 to 100)
Sadness
Anxiety
Anger
Frustration
Annoyance
Urge to help
4.8 5.0
31.5 28.4
5.8 5.4
17.9 28.5
35.5 25.8
7.9 11.6
5.2 4.9
35.1 29.3
13.0 10.3
24.7 27.2
43.2 29.9
14.8 26.2
a
b
c
Emotion
Scanner noises
during rest
(0 to 100)
Cries
(0 to 100)
Control noises
minus scanner
noises with rest
(100 to 100)
Cries minus
scanner noises
with rest
(100 to 100)
Cries minus
control noises
(100 to 100)
55.6 26.5
58.1 17.6
10.6 13.1
27.4 30.0
24.4 21.2
84.8 14.4
.4 6.9
3.5 20.3
7.2 8.7c
6.8 14.2
7.7 24.5
6.9 15.5
50.9 28.7c
26.6 40.0a
4.8 13.6
9.6 28.1
11.9 29.5
76.9 16.1c
50.5 24.1c
23.1 41.2b
2.4 8.5
2.7 28.1
19.6 24.2c
70.0 26.0c
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Figure 1. Brain regions more active when new mothers listen to infant cries than when they listen to white noise control sounds. This
figure displays active regions with cry minus control sounds (z 1.96; cluster extent threshold p .05) superimposed on high
resolution SPM96 structural magnetic resonance imaging template axial, coronal, and sagittal slices. Yellow is more active than red.
Regions of activation included: 1) midbrain regions in the vicinity of the hypothalamus/mammillary bodies, bilateral substantia
nigra/retrorubral fields, and central gray extending to the ventral tegmental area (axial slice); the pontine gray region is also active but
is not displayed); 2) ventral striatal/basal forebrain regions in the vicinity of the caudate/septal region/globus pallidus/nucleus
accumbens (NA)/bed of the stria terminalis (BNST); (coronal slice); the right putamen and more superior caudate is also active but is
not shown; the medial preoptic area (MPOA)/ventral bed nucleus of the stria terminalis (VBNST) region is not active but is labeled
in the coronal slice for comparison of approximate spatial relationship between the area of activation and this important maternal
behavior region in rodents; 3) anterior and posterior cingulate cortex, mesial prefrontal cortex, and medial thalamus (sagittal slice); 4)
paralimbic belt regions (right orbitofrontal-insula-temporal polar cortices); (axial slice); 5) a small portion of the right inferior part of
the dorsolateral prefrontal cortex (an extension of the right paralimbic belt cluster; not shown); 6) temporal lobe auditory and
association cortices (right left) (axial slice; right-sided activity shown only). As displayed on axial and sagittal slices, posterior brain
regions were not imaged. Furthermore, portions of the inferior orbitofrontal and anterior temporal regions were not fully visible due
to airtissue artifact (stippled region in sagittal slice).
REGIONS
WITH
CRY
MINUS
CONTROL
NOISE.
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Figure 2. Regions uniquely active when new mothers listen to infant cries. This figure displays regions uniquely active with cries
superimposed on the same high-resolution SPM96 structural magnetic resonance imaging template shown in the other figure. By
uniquely active with cries, we mean regions that are active with cry minus rest, not active with control noise minus rest, and additionally
more active with cries than with control noises. Regions of activation here are a subset of cry minus control noise active regions (Figure
1). Yellow is more active than red. Activations are quite similar to that of cry minus control noise with a few notable exceptions: 1) the
midbrains substantia nigra/retrorubral fields activated is no longer bilateral but is restricted to the left (axial slice); although there
appears to be no activity in the central gray/VTA region in the axial slice, there is still activity in this region just not at this axial level;
2) the cingulate cortex is no longer active and the cingulate/mesial prefrontal cortex cluster activation is now restricted to a small
pregenual mesial prefrontal cortex region (sagittal slice); notice that there is no longer mesial prefrontal/medial orbitofrontal subgenual
level activity (axial slice); 3) the right insula is no longer active, but there is still activity in the lateral orbitofrontal andtemporal polar
cortices (axial slice). Regions not imaged due to our chosen field of view and airtissue artifact are labeled similarly to Figure 1.
We define the posterior orbitofrontal cortex, temporal pole, and insula as the
paralimbic belt. These three structures are adjacent and histologically similar
(Mesulam 2000). They participate in linking cognition with emotion and
visceral states (Mesulam 2000) and are sometimes difficult to resolve separately in group fMRI studies. Mesulum (2000) referred to these three structures
as the olfactocentric paralimbic belt. The meaning of our paralimbic belt is the
same as Mesulams olfactocentric paralimbic belt.
7. Auditory and audiovisual association cortices bilaterally but with more activity on the right (namely,
BA 22 bilaterally and BA 20, 21, and 42 on the
right; Figure 1; Panel A).
ACTIVATIONS UNIQUE TO CRY. Activations unique
to cry were generally similar to those of cry minus control
noise (Figure 2 vs. Figure 1) with a few notable exceptions. There was no longer any cingulate activation and the
mesial prefrontal/anterior cingulate cluster active with cry
minus control noise was reduced to a small pregenual
mesial prefrontal cortex cluster (BA 9, 10) anterior to BA
32 from Talairach axial level z 2133 (see Table 1 and
Figure 1 vs. Figure 2: Panel C). In the right paralimbic
belt, activity was confined to the temporal polar (BA
38)/lateral orbitofrontal (BA 47) cortex region and there
was no longer any insula or medial orbitofrontal BA 11
activation (Figure 2: Panel A).
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Table 3. Brain Regions Active in Group Control Noise Minus Rest (CNMR), Cry Minus Rest (CMR), Cry Minus Control Noise
(CMCN), and Uniquely Active with Cry (C)
Local maxima from: cry minus rest, control noise minus rest, cry
minus control noise, and uniquely active with cry cluster maps
CNMR
Cluster Map
12
3 27
0 9
9
3
6 18
Striatum
18
9
24 12
6
6
0
12
12
6
18
6 3
18 9 6
15 18 6
27 12
3
12 15 3
Medial temporal cortex
18
0 15
Cingulate
18
3 42
3 18 39
6 15 36
18 18 33
0 6 30
0 24 30
21 9 30
6 21 27
21 36 15
21 36
3
3 24 9
9 18 9
21 18 12
Mesial Prefrontal Cortex
15 18 60
12 18 57
12 30 54
9 12 51
6 39 48
21 42 45
CMR
Cluster Map
CMCN
Cluster Map
C Cluster
Map
2.85
3.12
3.12
2.50
2.54
2.14
3.15
2.33
3.14
3.14
2.97
2.15
2.15
2.80
2.01
2.01
2.82
3.67
2.86
2.86
2.35
2.71
2.92
2.92
2.92
2.92
3.17
2.84
2.84
R. Caudate/Putamen
R. Putamen/Globus Pallidus
R.Caudate/Ventral Septal/Nuc.
accumbens/Globus Pallidus/Bed Nuc.
Stria Terminalis Region
R. Putamen/Caudate
R. Globus Pallidus/Amygdala
R. Putamen/Insula
L. Putamen/Insula
L. Caudate/Nuc. Accumbens Region
2.45
2.33
2.55
2.02
2.47
2.47
3.06
2.47
2.24
2.17
2.06
2.79
2.05
3.34
4.04
2.57
2.40
2.06
2.06
R. Amygdala
3.31
2.25
3.28
2.77
4.03
2.13
2.08
3.02
3.14
2.73
3.10
2.60
2.11
2.81
3.67
3.09
4.00
Superior
Superior
Superior
Superior
Superior
Superior
3.11
2.08
2.55
3.15
3.09
3.05
2.17
2.12
2.05
2.42
Frontal
Frontal
Frontal
Frontal
Frontal
Frontal
G.
G.
G.
G.
G.
G.
BA
BA
BA
BA
BA
BA
6
6
6/8
6
8
8
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439
Table 3. Continued
Local maxima from: cry minus rest, control noise minus rest, cry
minus control noise, and uniquely active with cry cluster maps
CNMR
Cluster Map
42
Superior Frontal G. BA 8
39
Superior Frontal G. BA 8
33
Medial Frontal G. BA 8/9
33
Superior Frontal G. BA 9
27
Superior Frontal G. BA 9/10
27
Superior Frontal G. BA 9/10
24
Medial Frontal G. BA 10
21
Medial Frontal G. BA 9/10
15
Superior Frontal G. BA 10
15
Superior Frontal G. BA 10
3
Medial Frontal G. BA 10
3
Medial Frontal G. BA 10
9
Superior Frontal G. BA 10
Cortex-Temporal Pole-Insula
18
R. Insula
0
R. Insula
3
R. Middle Frontal G. BA 10/47
3
R. Inferior Frontal G. BA 47/
Superior Temporal G. BA 22
39 57 3
R. Middle Frontal G. BA 10
30 24 9
R. Inferior Frontal G. BA 47/Insula
54 39 9
R. Inferior Frontal G. BA 47
36 54 12
R. Middle Frontal G. BA 11
15 51 12
R. Superior Frontal G. BA 11
63
9 12
R. Superior Temporal G. BA 38
45 39 15
R. Middle Frontal G. BA 11
51 27 18
R. Inferior Frontal G. BA 47/
Superior Temporal G. BA 38
36 21 24
R. Inferior Frontal G. BA 47/
Superior Temporal G. BA 38
48 12 24
R. Superior Temporal G. BA 38
27 12 15
L. Insula
36 39 12
L. Middle Frontal G. BA 10
36 54
6
L. Middle Frontal G. BA 10
27 27 3
L. Inferior Frontal G. BA 47
39 24 3
L. Insula
39 39 6
L. Middle Frontal G. BA 47
36 51 6
L. Middle Frontal G. BA 10
51
3 9
L. Superior Temporal G. BA 38
27 48 15
L. Superior Frontal G. BA 11
21 36 18
L. Middle Frontal G. BA 11
45
9 21
L. Superior Temporal G. BA 38
Dorsolateral Prefrontal Cortex
45 12 51
R. Middle Frontal G. BA 6
54
9 42
R. Middle Frontal G. BA 6/8
45 21 39
R. Middle Frontal G. BA 8
39
9 33
R. Middle Frontal G. BA 9
51 30 27
R. Middle Frontal G. BA 9
45
3 27
R. Inferior Frontal G. BA 9
51 15 24
R. Inferior Frontal G. BA 44
39 33 21
R. Middle Frontal G. BA 46
33 21 21
R. Inferior Frontal G. BA 45
33 42 15
R. Middle Frontal G. BA 46
54 21 12
R. Inferior Frontal G. BA 44/45
51 36 12
R. Inferior Frontal G. BA 46
42 30
6
R. Inferior Frontal G. BA 45
CMR
Cluster Map
CMCN
Cluster Map
C Cluster
Map
2.37
3.24
2.59
3.40
1.98
2.24
3.50
2.26
2.44
2.38
2.26
2.01
2.77
2.89
3.01
3.86
2.37
3.07
3.35
2.29
2.89
3.01
3.86
2.28
2.31
3.15
3.25
2.37
3.88
3.70
2.90
3.05
2.85
2.77
2.63
2.65
2.44
2.33
2.17
2.72
2.84
2.46
4.02
3.56
2.15
2.08
2.19
2.04
2.14
2.28
2.12
2.04
2.20
3.31
3.45
2.15
2.57
3.40
3.39
3.47
3.26
3.39
3.21
2.91
2.59
3.31
3.04
2.95
3.03
2.62
2.54
2.02
2.75
2.57
2.66
2.79
2.12
4.09
4.98
3.69
3.12
2.16
2.94
2.56
2.11
2.62
2.92
4.35
3.80
3.54
2.22
3.12
3.09
2.04
4.18
3.24
2.45
2.90
2.90
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Table 3. Continued
Local maxima from: cry minus rest, control noise minus rest, cry
minus control noise, and uniquely active with cry cluster maps
CNMR
Cluster Map
6
R. Inferior Frontal G. BA 45
3
R. Inferior Frontal G. BA 44
48
L. Middle Frontal G. BA 8
27
L. Middle Frontal G. BA 9
3
L. Inferior Frontal G. BA 45
Association Cortices
9
R. Superior Temporal G. BA 22/42
(Posterior Superior Temporal Sulcus)
66 27
6
R. Superior Temporal G. BA 22/42
(Posterior Superior Temporal Sulcus)
63 21
0
R. Superior Temporal G. BA 22/21
(Central Superior Temporal Sulcus)
57 21 9
R. Middle Temporal G. BA 21
(Central Superior Temporal Sulcus)
66 12 3
R. Middle Temporal G. BA 21
(Central Superior Temporal Sulcus)
66
0
0
R. Superior Temporal G. BA 22
(Anterior Superior Temporal Sulcus)
57 3 6
R. Middle Temporal G. BA 21
(Anterior Superior Temporal Sulcus)
51 6 12
R. Middle Temporal G. BA 21
(Anterior Superior Temporal Sulcus)
54
9 18
R. Middle Temporal G. BA 21/38
(Anterior Superior Temporal Sulcus)
63 9 12
R. Superior Temporal G. BA 42/22
66 24 9
R. Middle Temporal G. BA 21
51 27 12
R. Middle Temporal G. BA 20/21
60 3 15
R. Inferior Temporal G. BA 21
48 21 15
R. Middle Temporal G. BA 20
39 18 21
R. Inferior Temporal G. BA 20
51 6 33
R. Inferior Temporal G. BA 20
57 21
3
L. Superior Temporal G. BA 22
(Central Superior Temporal Sulcus)
45 18
3
L. Superior Temporal G. BA 22
39 9 15
L. Middle Temporal G. BA 20/21
42
3 21
L. Middle Temporal G. BA 21
Somatosensory Cortex
36 18 27
R. Postcentral G. BA 3/1/2
CMCN
Cluster Map
C Cluster
Map
CMR
Cluster Map
2.89
2.07
3.01
3.06
3.04
2.13
3.81
3.92
2.17
3.13
4.60
3.95
3.09
1.97
2.39
1.98
2.39
2.39
2.20
3.82
3.54
3.54
2.02
2.45
2.23
2.23
2.11
2.69
2.97
2.97
2.95
2.06
1.99
1.99
2.97
3.29
2.28
3.27
2.06
2.03
2.03
2.16
2.87
2.89
3.83
2.12
2.45
2.50
2.56
3.11
2.36
1.98
2.82
2.99
2.63
2.57
1.97
2.82
2.45
2.05
2.51
3.31
2.45
4.44
2.67
2.57
3.09
2.20
CNMR, control minus noise rest; Ant, anterior; Post, posterior; G, gyrus; L, left; R, right; Nuc., nucleus; BA, Broadmans area; VTA, ventral tegmental area; CMR, cry
minus rest; CMCN, cry minus control noise.
There
was only a small cluster more active with control noises
than cries. This cluster included the right somatosensory
cortex and right posterior insula. No brain regions were
uniquely active with control noises.
Discussion
Hypothesized Findings
Consistent with our first hypothesis concerning emotional
ratings, mothers had higher ratings of sadness and urges to
help with cries than with control sounds and rest. Consistent with our second hypothesis regarding brain activity
with cry minus control noise, the anterior and posterior
cingulate cortices, medial thalamic nuclei, bilateral mesial
prefrontal cortex, and right orbitofrontal cortex were all
active. The anterior cingulate activation in this study was
pre- and supragenual in contrast to the subgenual activation of our pilot study. The mesial and right orbitofrontal
activity, however, did extend to the subgenual level
activity of our pilot study. Finally, we hypothesized that
these same regions would be uniquely active with cries.
Partially consistent with this hypothesis, all these regions
except the cingulate uniquely activated with the cries in
this experiment. Although thresholding effects may be
important in why the medial thalamus (i.e., part of the
thalamocingulate division) uniquely activated with cries
and the cingulate cortex did not, the medial thalamus can
be active independent of the cingulate. In fact, the medial
thalamus has strong connections with several regions that
are uniquely active with cry, including the paralimbic belt,
inferior dorsolateral and mesial prefrontal cortex, septal
region, and banks of the superior temporal sulcus (Mesulam 2000). That the cingulate cortex did not uniquely
activate with the cries means it is possible that its
activation with cry minus control noise may be due to
mere auditory perceptual, cognitive, or emotional enhancement; however, one should use caution in deciding
that regions more active with cries than control noises but
not uniquely active with the cries (such as the cingulate)
are unimportant in maternal behavior. These nonunique
regions could simply just be potentially more sensitive to
cries than other stimuli. Additionally, some neurocircuitry
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J.P. Lorberbaum et al
Limitations
Several issues should be considered in interpreting our
findings. First, we used the same standard infant cry
recordings for all subjects. A mothers brain response to
hearing her own infant cry may be different (Wiesenfeld
and Klorman 1978). Second, we only studied mothers 1 to
2 months postpartum and did not have a control group of
fathers or nonmothers. Thus, we are unable to say that the
pattern of activity observed in this study was unique to
mothers. Third, one might argue that as the anterior
cingulate is known to be involved in attentional processing
(Bush et al 1998), a mothers increased cingulate response
with cries compared with control sounds may be simply a
function of attending more to meaningful baby cries than
to meaningless white noise control sounds. Although
selective attention is likely an important aspect of a
mothers response to infant cries, future studies with
attentional controls are needed. Fourth, it is possible that
BIOL PSYCHIATRY
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Conclusions
This study and our earlier pilot study are the first to use
modern techniques of functional imaging to study the
brain basis of human maternal behavior. Consistent with
our hypotheses, the cingulate, thalamus, mesial prefrontal
cortex, and right orbitofrontal cortex activate more when
mothers listen to infant cries than when they listen to white
noise control sounds. Partially consistent with our hypotheses, all these regions except the cingulate uniquely
activated with the cries in this experiment. Furthermore,
we also found that other regions believed to be potentially
important in rat maternal behavior studies activated with
cry minus control noise and were uniquely activated by
cries. Namely, we found activation in the vicinity of the
hypothalamus, central gray/VTA, substantia nigra/retrorubral fields, caudate/nucleus accumbens/globus pallidus/lateral septal region/BNST, and putamen. We also
found a right hemisphere asymmetry to cortical activity
consistent with the left-sided infant carrying hypothesis. In
sum, these results are generally consistent with those
found on the neural basis of maternal behavior in nonhuman mammals. Improved understanding of the regional
brain basis of parenting and social bonding more generally
would likely aid in research into normal emotions such as
love, separation anxiety, and grief. More knowledge
would also likely be important in understanding abnormal
behavior such as depression, anxiety disorders, schizophrenia, autism, and child maltreatment in which social
bonding problems may exist (Insel 1997).
444
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We are indebted to Paul D. MacLean for planting the seed for the idea of
scanning mothers while they listen to infant cries. The authors thank Ken
Brown for his help with phone screening all subjects. The authors thank
both James C. Ballenger and George W. Arana for administrative
support. We would like to thank the Functional Neuroimaging Division
of the Medical University of South Carolina, Solvay Pharmaceuticals,
and National Institute of Health Grant No. R01 NS 40259 for supporting
the current project.
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