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This study tested whether mothers with interpersonal violence-related posttraumatic stress disorder (IPV-PTSD) vs healthy controls (HC) would show greater limbic and less frontocortical activity when viewing young children during separation compared to quiet play. Mothers of 20 children (12–42 months) participated: 11 IPV-PTSD mothers and 9 HC with no PTSD. During fMRI, mothers watched epochs of play and separation from their own and unfamiliar children. The study focused on comparison of PTSD mothers vs HC viewing children in separation vs play, and viewing own vs unfamiliar children in separation. Both groups showed distinct patterns of brain activation in response to viewing children in separation vs play. PTSD mothers showed greater limbic and less frontocortical activity (BA10) than HC. PTSD mothers also reported feeling more stressed than HC when watching own and unfamiliar children during separation. Their self-reported stress was associated with greater limbic and less frontocortical activity. Both groups also showed distinct patterns of brain activation in response to viewing their own vs unfamiliar children during separation. PTSD mothers’ may not have access to frontocortical regulation of limbic response upon seeing own and unfamiliar children in separation. This converges with previously reported associations of maternal IPV-PTSD and atypical caregiving behavior following separation.
Group comparisons of activation when mothers view their own and unfamiliar children during separation vs play. Two panels each containing three columns of contrast images are presented that test the a priori hypothesis that PIV-PTSD mothers exhibit reduced mPFC activation and greater limbic activation vs control mothers when viewing child mental states during separation vs during play, in both their own and in unfamiliar children. Each of the two panels is divided into three columns that represent the following: (A and D) group differences in fMRI signal with greater activation in PTSD mothers compared to controls in red and greater activation in controls in blue (i.e. the contrast of the activations in column B with the activations in column C. (B and E) group average fMRI signal in PTSD mothers when viewing separation compared with play and (C and F) HC mothers when viewing separation compared with play. For columns, B and E, and C and F, increases in signal while viewing separation relative to play are shown in red and decreases are in blue. The left-most three columns of this figure (A–C) show neural activity in PTSD and HC mothers while viewing their own children during separation relative to play. The right-most three columns (D–F) show neural activity in PTSD and HC mothers while viewing unfamiliar children during separation relative to play. These are transaxial views with Talairach z-coordinates shown to the far right of the row of corresponding slices, representing the slices positioned from superiorly to inferiorly (top to bottom). The left side of the brain (L) is displayed on the left side of the image. We report voxels using a P-value threshold 25 adjacent pixels, a conjoint requirement which, based on an approximation formula, yields a conservative effective P
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An fMRI study of the brain responses of
traumatized mothers to viewing their
toddlers during separation and play
Daniel S. Schechter,
1,2
Dominik A. Moser,
1
Zhishun Wang,
2
Rachel Marsh,
2
XueJun Hao,
2
Yunsuo Duan,
2
Shan Yu,
2
Benjamin Gunter,
2
David Murphy,
2
Jaime McCaw,
2
Alayar Kangarlu,
2
Erica Willheim,
2
Michael M. Myers,
2
Myron A. Hofer,
2
and Bradley S. Peterson
2
1
Division of Child and Adolescent Psychiatry, Department of Child and Adolescent Medicine, University of Geneva Hospitals and Faculty of
Medicine, 51 Boulevard de la Cluse, 2e Etage, 1205 Geneva, Switzerland and
2
Department of Psychiatry, Columbia University College of
Physicians & Surgeons, 1051 Riverside Drive, Unit 40, New York, NY 10032 U.S.A
This study tested whether mothers with interpersonal violence-related posttraumatic stress disorder (IPV-PTSD) vs healthy con-
trols (HC) would show greater limbic and less frontocortical activity when viewing young children during separation compared to
quiet play. Mothers of 20 children (1242 months) participated: 11 IPV-PTSD mothers and 9 HC with no PTSD. During fMRI,
mothers watched epochs of play and separation from their own and unfamiliar children. The study focused on comparison of PTSD
mothers vs HC viewing children in separation vs play, and viewing own vs unfamiliar children in separation. Both groups showed
distinct patterns of brain activation in response to viewing children in separation vs play. PTSD mothers showed greater limbic
and less frontocortical activity (BA10) than HC. PTSD mothers also reported feeling more stressed than HC when watching own
and unfamiliar children during separation. Their self-reported stress was associated with greater limbic and less frontocortical
activity. Both groups also showed distinct patterns of brain activation in response to viewing their own vs unfamiliar children
during separation. PTSD mothers may not have access to frontocortical regulation of limbic response upon seeing own and
unfamiliar children in separation. This converges with previously reported associations of maternal IPV-PTSD and atypical care-
giving behavior following separation.
Keywords: maternal PTSD; early childhood; functional neuroimaging; emotion regulation; corticolimbic pathways; interpersonal
violence
INTRODUCTION
Adults with posttraumatic stress disorder (PTSD) have dif-
ficulty regulating their emotions when new experiences
remind them of one or more aspects of their trauma (New
et al., 2009). Neuromaging studies of PTSD patients have
reported significant activation in brain regions implicated
in the processing and regulation of emotions and arousal
(Etkin and Wager, 2007; Bluhm et al., 2009). These studies
have shown that limbic responses to either positively or
negatively valenced emotional stimuli, such as facial expres-
sions or evocative verbal descriptions of interpersonal con-
flict, are exaggerated in adults who have interpersonal
violence-related PTSD (IPV-PTSD), even when the stimuli
have no apparent direct connection to the traumatic events
previously experienced (Shin et al., 2005). Medial prefrontal
cortical (mPFC) activation that is known to regulate limbic
activity within the brain is, in contrast, diminished in PTSD
patients compared with controls during the processing of
similar stimuli (Gilboa et al., 2004).
While there are no previously published neuroimaging stu-
dies of women with IPV-PTSD who are mothers in response
to their children, behavioral studies indicate that the use of
neuroimaging could help us to understand caregiving behav-
ior that differentiates these women from healthy controls
(HC) (i.e. ‘atypical caregiving behavior’), and thus help ad-
dress such behavior clinically. For example, mothers who have
IPV-PTSD in comparison to healthy mothers show impaired
reading of child affect, less empathic responsiveness and less
availability for joint attention, particularly after a social stres-
sor such as motherchild separation (Lyons-Ruth and Block,
1996; Schechter et al., 2010). Specifically, following child sep-
aration, mothers’ emotional availability to respond to child
bids for engagement in joint attention to play was negatively
correlated with their IPV-PTSD symptom severity (Schechter
et al., 2010). The present MRI study was, in fact, nested in that
Received 22 February 2011; Accepted 19 September 2011
Advance Access publication 22 October 2011
The authors acknowledge the following funding sources that have made the work reported in this article
possible: Grants awarded to Daniel S. Schechter, M.D. from: the National Institute of Mental Health (K23
MH068405); International Psychoanalytical Association Research Advisory Board; Sackler Institute of
Developmental Psychobiology at Columbia University; Bender-Fishbein Fund at Columbia University; Swiss
National Science Foundation, National Centre for Competence in Research on the Synaptic Bases of Psychiatric
Disorders (SYNAPSY- CC4); Gertrude von Meissner Foundation, University of Geneva Faculty of Medicine; Grant
awarded to Rachel Marsh, M.D. from the National Institute of Mental Health (K02 MH746771). Grant awarded
to Bradley S. Peterson, M.D. from the National Institute of Drug Abuse (DA017820).
Correspondence should be addressed to Daniel S. Schechter, M.D., Chief of Pediatric Consult-Liaison and
Parent-Child Research Units, Division of Child and Adolescent Psychiatry, Department of Child and Adolescent
Medicine, University of Geneva Hospitals and Faculty of Medicine, 51 Boulevard de la Cluse, 2e Etage, 1205
Geneva, Switzerland. E-mail: daniel.schechter@hcuge.ch, jm2042@columbia.edu
doi:10.1093/scan/nsr069 SCAN (2012) 7, 969^979
ßThe A uthor (2 011). Published by Oxford Univer sity Pres s.F or Permission s, plea se email: journ als.permissio ns@ou p.com
at Columbia University Libraries on January 3, 2014http://scan.oxfordjournals.org/Downloaded from
behavioral study. While, no previous MRI studies to our
knowledge have directly examined the neural circuits that
could underlie these in PTSD-mothers’ atypical caregiving
behavior, several imaging studies investigated neural activity
among healthy parents in response to infant cries and faces
(Swain et al., 2007; Strathearn et al., 2008). One study that
used video excerpts of toddlers during play and separation
reported activation of the mPFC in healthy mothers when
viewing responses of their child during separation vs play
(Noriuchi et al., 2008). This study found specific coordinated
neural activity in cortical (i.e. mPFC, anterior cingulate and
insula) and subcortical (i.e. amygdala, anterior entorhinal and
perirhinal cortex) regions that participate in the emotion pro-
cessing in response to viewing the video excerpts.
We also assessed brain activity in these corticolimbic cir-
cuits, but in a sample of mothers with marked IPV-PTSD
compared to those without IPV-PTSD within an inner-city
community that is rarely recruited for neuroimaging studies.
Our overall goal has been to understand the circuitry in a
mother’s brain that might hinder vs support her capacity to
respond sensitively to her child’s affective communication
under stress. Our curiosity has been fueled by our study of
maternal emotional availability for joint focus of attention as
mentioned above (Schechter et al., 2010), as well as by an
additional observation of IPV-PTSD mothers’ tendency to
‘misread’ child affective communication (Fraiberg et al.,
1975). With respect to this latterpoint,wepreviouslystudied
clinically referred mothers with IPV-PTSD, who prior to video
feedback, frequently misread their child’s anxious facial expres-
sions as angry and controlling, and only after therapeutic inter-
vention were able to see and describe their child’s separation
anxiety and helplessness (Schechter et al., 2006). In the present
study, we therefore describe the functioning of neural systems
that subserve emotional reactions by mothers with IPV-PTSD
and non-traumatized comparison mothers while watching
videos of their own and unfamiliar toddlers displaying distress
responses during separation or when playing quietly.
Hypotheses
Mothers with IPV-PTSD as compared to HC will show in
response to viewing their own and unfamiliar children in
separation (stressful condition) as contrasted with play
(non-stressful condition) the following:
(1) greater activation of fearresponse circuitry (i.e. amyg-
dala, entorhinal and perirhinal cortices, and hippocam-
pus). We expect that this response will be stronger for
own than for unfamiliar children, but will be generalized
also to unfamiliar children.
(2) less activation of higher cortical areas [i.e. superior
frontal gyrus (SFG)/Mpfc] that are involved in down-
regulation of the fear response (Shin et al., 2006) and
(3) greater self-reported stress on a post-MRI scan interview.
Additionally, we expect that mothers’ self-reported stress in
response to seeing their own and unfamiliar children in sep-
aration (vs play) and clinician-assessed PTSD symptom se-
verity will both be associated with greater activation of
fearresponse circuitry and less activation of corticofrontal
areas (i.e. mPFC) that are known to regulate limbic response
when continuous analyses are applied across the entire
sample. Given previous behavioral findings of less maternal
emotional availability following separation, we might also
expect less activation of brain regions associated with em-
pathy (i.e. the insula) in PTSD vs HC mothers in response
to viewing children during separation vs play (Decety, 2010).
In testing these hypotheses, this is the first study ever to
examine how IPV-PTSD, considered as a disorder of emo-
tion regulation, affects mothers’ neural response to viewing
their own and unfamiliar preschool-age children in a situ-
ation that renders the child helpless and vulnerable.
It newly examines how this neural response might corres-
pond to subjective reports of parenting stress and obser-
vations of parental interactive behavior before and after
separation such as we have described in previous articles
(Schechter et al., 2010). Specifically, this study will help char-
acterize how IPV-PTSD mothers process young children’s
emotional communication in the context of maternal IPV-
PTSD (as compared to HC) in response to seeing them in a
stressful (separation) vs non-stressful (play) condition.
METHODS
Participants
Recruitment
We obtained informed consent from participants both for
the non-MRI and nested MRI study reported here according
to procedures approved by the Columbia University Medical
Center’s Institutional Review Board. Recruitment from pedi-
atric community clinics is described in further detail in the
Supplementary Materials (see also Schechter et al., 2010).
Twenty mothers who either had a diagnosis of IPV-PTSD
(PTSD mothers) or who did not (HC) and who had both
joined the larger motherchild study and were eligible for
imaging (i.e. not pregnant) were scanned.
Sample characteristics
Mothers (19 right-handed, 1 left-handed) of 20 children
(10 boys, 10 girls), 1242 (mean 24 8) months of age,
participated. The single left-handed subject, when subtracted
and then re-added to the sample, did not significantly alter
results within or between groups.
Procedures
Procedures for visits prior to MRI scan
The protocol consisted of two 2-h videotaped visits follow-
ing informed consent and screening (Schechter et al., 2010).
During an initial videotaped interview, PTSD and HC
mothers underwent a variety of psychometric examinations
to assess their life-events history and psychopathology. Most
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importantly, lifetime and current diagnoses of PTSD was
determined using the Clinician Administered PTSD Scale
(CAPS) (Blake et al., 1995see Supplementary Data and
Schechter et al., 2010), which has extremely high interrater
reliability (Cicchetti et al., 2009). The diagnosis of current
PTSD at the time of participation was confirmed by
self-report using the PTSD symptom checklist-short version
(PCL-S) (Weathers et al., 1996see Supplementary Data and
Schechter et al., 2010).
One to 2 weeks after the initial videotaped maternal inter-
view, the mothers and their children returned for a video-
taped interaction. The protocol used to structure this visit
was the Crowell procedure (Crowell et al., 1988) as modified
by Zeanah et al. (2000) It consisted of two repetitions of
the following motherchild interactions: (i) playing together
as they did at home using a range of toys provided (8 min),
(ii) separating (3 min) and (iii) reuniting (3 min). fMRI sti-
muli were drawn from interaction sequences (i) and (ii).
Stimuli
Mother viewed six different, silent, 40-s video excerpts of
three different children, each during the two conditions: sep-
aration and play: (i) own child, (ii) unfamiliar boy and
(iii) unfamiliar girl. The unfamiliar children were of similar
mean age, drawn from a similar Hispanic and African
American inner-city community, and were filmed in a simi-
lar parentchild interaction protocol to ours, but at another
institution.
Selection of stimuli
A research assistant who was blind to casecontrol status
among mothers’ own children selected the silent excerpts for
the fMRI stimulus in play and separation: mothers viewed the
play excerpt observed to show the most joy and reciprocally the
separation excerpt with the strongest child emotional response.
Selection of separation video excerpts
The two separation segments during the videotaped inter-
action protocol were rated without sound on a 5-point
Separation Distress Scale (SDS; Schechter and McCaw,
2005) by two graduate-student raters independently, who
were both naı
¨ve to group membership (rating 0 ¼no observ-
able distress, 4 ¼agitation). The consistency of the child’s
response to separation across the both episodes of video-
taped separation, as a measure of testretest reliability was
robust (Cronbach’s ¼0.82). The episode in which the child
was more distressed was shown in the scanner. Interrater
reliability was excellent (ICC ¼0.95, P< 0.001). For own
child, raters found the mean stress on separation to be
2.31 (s.d. ¼1.35; range 1.54.0); unfamiliar boy was rated
‘2’ and girl ‘4’. Concordance between raters’ and mothers’
estimation of child distress was high (Cronbach’s ¼0.83).
Both genders of unfamiliar children were included in an
effort to control for gender mix among own-child stimuli.
Study design
The study design (Supplementary Figure S1) consisted of
four runs, each lasting 11 min12 s, and each containing
two blocks during which mothers viewed six 40-s video ex-
cerpts per block, displayed in a pseudorandom order, coun-
terbalanced within and across runs. Thus, mothers viewed
each of the six 40-s film clips eight times. Eye tracking and
vocal reminders by the technician to pay attention to the
screen between runs were used to ensure that mothers
were attending to stimuli.
Postscan interviews of mothers about their response
to stimuli
A postscan interview developed by the authors assessed sub-
jective (self-reported) ‘stress’ (displeasure) and ‘fun’ (pleas-
ure) experienced in response to viewing each of the six
excerpts on a 5-point rating scale from ‘0’ as ‘least’ to ‘4’
as ‘most’.
Image acquisition and pre-processing
Briefly, imaging was performed under GE 3T scanner.
Standard fMRI preprocessing procedures including slice
timing and motion corrections, and spatial normalization
and smoothing were performed under SPM and MATLAB.
See Supplementary Data for details.
Hypothesis-driven analyses
The Blood Oxygen-Level Dependent (BOLD) response from
each run was first assessed using a General Linear Model
containing seven time-dependent functions representing
each stimulus type (resting gaze fixation and six videos)
and one constant (baseline BOLD signal). Contrast images
representing the differential effect of the video presentations
on voxel-wise BOLD signals were created for each subject. A
contrast specifying ‘separation vs play’ was the difference in
estimated neural activity during the viewing of the child in
the separation condition compared with estimated activity
during the viewing of the child during free play (condition).
Results for this are not discussed but can be found in the
Supplementary Table S3. To examine hypotheses 1 and 2
(see page 4), we performed paired-samples t-tests that com-
pare BOLD activation in subjects with PTSD to the BOLD
activation in HC when watching scenes of separation vs play,
once for own children and once for unfamiliar children. To
examine within-group differences in activation associated
with the familiarity of the children (i.e. own vs unfamiliar),
we performed paired-sample t-tests comparing activity when
viewing their own child vs unfamiliar children for the sep-
aration relative to play contrast. We report significant
changes in voxels using a P0.025 threshold (i.e. a
two-tailed P0.05) together with the requirement that the
activation occurred in an empirically derived spatial cluster
greater than 25 adjacent voxels. This conjoint cluster-size
requirement which is based on an approximation formula
(Friston et al., 1994), yields a conservative effective
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P< 0.000005. The combined application of a statistical
threshold and cluster filter reduces substantially the
false-positive identification of activated voxels at any given
threshold (Forman et al., 1995).
Group differences with respect to maternal self-reported
stress experienced when looking at their own and unfamiliar
children during separation were tested using independent
t-tests.
To investigate the neural correlates of this same variable of
maternal self-reported stress, we entered into a regression
model BOLD signal change, detected by the contrast of separ-
ation relative to free play as the dependent variable and as a
predictor, the maternal self-rated stress score from the
post-MRI interview. Similarly, to investigate the neural correl-
ates of maternal PTSD symptom severity, we entered into a
similar regression model as a predictor, a composite of z-scores
based on the CAPS score from the initial interview with
motherand the maternal self-reported PCL-S that was ad-
ministered during the scanning visit. These analyses also use
aP0.025 threshold with a minimum cluster size of 25 voxels.
RESULTS
Characteristics of PTSD vs HC groups
The IPV-PTSD case group (n¼11) was rigorously defined
by clinician rating on the CAPS and PCL-S scores
(Supplementary materials; Schechter et al., 2010): 11 PTSD
mothers (30 6 years old) and 9 HC mothers (31 7 years
old), 5 of whom had limited violence exposure that they did
not rate as traumatic and to which they did not attribute
PTSD symptoms (one with prior domestic violence and four
with histories of excessive corporal punishment for a defined
period). These nine HC mothers had neither the diagnosis of
PTSD nor subthreshold PTSD, and were not suffering from
major depression.
As expected (Shea et al., 2004), PTSD was significantly
more often comorbid with major depressive disorder
(MDD) and greater severity of depressive symptoms.
Overall dissociative symptom scores (DESs) were similarly
elevated for PTSD (27 20) and minimal for HC (5 1.5;
t
1
¼3.6, P< 0.01). The degree of naively rated child distress
on silent video excerpts depicting children during separation
also did not differ between groups (Table 1).
PTSD and HC groups did not differ significantly in terms
of child age or gender (Table 1). Cases differed only from
controls on background variables with respect to lower house-
hold income and number of years of education (P< 0.05),
despite no group difference in attainment of a high-school
diploma or General Educational Diploma (GED) (P> 0.3).
Consequently, we included household income and number
of years of education as covariates in the model for neural
activation during the viewing of separation vs play and
noted no significant effects.
Imaging results
Mothers viewing their own children during separation
vs free play
Neural activity when viewing their own children during sep-
aration vs free play (‘separation-play’) was compared across
Table 1 Demographic and clinical characteristics of subjects
a
PTSD cases
(n¼11)
HC (n¼9) t-test and
2
statistics (df ¼18)
t-value or
2
Significance (P)
Mean age of mother 29.5 (7.1) 30.4 (7.2) 0.31 0.76
Mean age of child (months) 25.4 (7.9) 21.9 (7.8) 0.98 0.34
Number of boys 6 4 1.34 0.20
Number of mothers with high school diploma or equivalent (GED) 6 7 1.17 0.37
Mean years of the mothers education 11.9 (1.4) 14.3 (3.4) 2.15 0.05
Mean income in $1000 increments 25.5 (18.6) 54.4 (32.1) 2.53 0.02
Mean number of violent events 25 (17.4) 8.7 (8.9) 2.71 0.02
Recent domestic violence (%) 64 0 4.18 0.002
Mothers who attempted suicide (%) 45 0 2.89 0.02
History of child protection involvement (%) 45 0 2.90 0.02
PSI-SF mean score 47.6 (15.4) 20 (12.4) 3.38 0.006
CAPS mean score (lifetime PTSD) 88.5 (15.6) 18.3 (16) 9.40 <0.001
Baseline mean PCLS (current PTSD) 43.3 (17.2) 19.9 (9.7) 3.80 <0.001
Scan mean PCLS (current PTSD) 43.7 (13.5) 13.2 (10.2) 5.58 <0.001
MDD diagnosis on MINI 7.0 (63.6) 0.0 (0.0) 5.87 0.02
Baseline mean BDI 18.7 (13.2) 5.2 (4.8) 3.91 0.004
Scan mean BDI 16.2 (12.6) 3.3 (4.6) 3.77 0.002
DES mean score 25.8 (21.4) 5 (5.2) 3.12 0.009
Borderline personality screen (PDQ-IV) 3 (27.2%) 2 (22.2%) 0.27 0.54
Mean child distress (independently rated) 2.5 (1.4) 2.1 (1.3) 0.56 0.58
a
Means are reported with standard deviations; 19/20 subjects were right-handed.
PSI-SF, parenting stress index-short form; PCLS, post-traumatic stress symptoms checklist-short version; MINI, Mini International Neuropsychiatric Interview; BDI,
Beck Depression Inventory; DES, Dissociative Experiences Scale; PDQIV, Personality Disorders Questionnaire.
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two groups: for 11 PTSD mothers vs 9 HC (group-by-
condition inter action, see Figure 1A).
PTSD mothers vs HC (Figure 1A and B) exhibited signifi-
cantly greater activation in the bilateral anterior entorhinal
cortex (AEC, BA34) and the left caudate.
HC compared to PTSD mothers (Figure 1A and C)
exhibited significantly greater activation in higher cortical
regions (SFG; BA8,10) and bilateral superior parietal lobes
(SPL; BA7).
Maps for separation vs rest (‘separation-rest’) and play vs
rest (‘play-rest’) suggested that the group difference in these
activations originated in response to separation rather than
to play (Supplementary Figure S2).
In response to seeing their own children in separation vs
play (Figure 1A), we noted apparent activation of the
left insula (BA13) in the PTSD mothers compared to HC,
which actually represents ‘deactivation’ among HC (i.e. acti-
vation while seeing their own child in play, which is also
a control condition, as confirmed by separation vs
rest and play vs rest maps (Supplementary Table S1 and
Figure S2).
Mothers viewing unfamiliar children during separation
vs with free play
PTSD vs HC mothers (Figure 1D and E) exhibited signifi-
cantly greater activation in limbic regions: the right amyg-
dala, bilateral AEC (BA34), left perirhinal cortex (BA35); as
well as the left caudate and the L > R fusiform gyrus (BA37).
HC vs PTSD mothers (Figure 1D and F) when viewing
unfamiliar children in separation vs play did not exhibit
significantly greater activation in the SFG (BA8,10).
However, PTSD mothers activated the L middle frontal
gyrus (MFG; BA10) significantly more than HC.
Maps for separation vs rest and play vs rest suggested that
this group difference originated in response to separation
rather than to play (Supplementary Figure S2).
In response to seeing unfamiliar children in separation-
play (Figure 1D), we noted activation of the left insula
(BA13) in the PTSD vs HC mothers that was similar to
that which we noted in response to mothers viewing their
own child. The origin of this apparent activation is again
a ‘deactivation’ among HC (i.e. activation in response to
viewing play), as was true in response to mothers viewing
their own child. Separation- and play-rest maps showed
that HC mothers activated the insular cortex more than
PTSD mothers when seeing their own and unfamiliar chil-
dren play (Supplementary Table S2 and Supplementary
Figure S2).
Within-group differences in viewing children in
separation by own vs unfamiliar child
We assessed group differences in activation associated with
the familiarity of the children (i.e. own vs unfamiliar) during
separation only as per our a priori hypothesis (familiarity-
by-condition interaction) separately in PTSD and HC
mothers (Figure 2).
Among PTSD mothers, activation differed significantly
when viewing their own vs unfamiliar children (Figure 2C),
with greater activation in response to viewing unfamiliar
children as compared to own children in AEC and peri-
rhinal cortices, as well as caudate and cerebellum, fusiform
gyrus; as well as higher cortical areas (SFG [BA8,10]).
Among HC mothers, we noted greater activation in re-
sponse to viewing unfamiliar children than own children in
the higher cortical regions [bilateral SPL (BA7) and MFG
(L > R (BA10)] (Figure 2C). This pattern of activity in HC
mothers derived from more prominent deactivation when
viewing their own children in separation compared to un-
familiar children (Figure 2F vs C).
In general, PTSD mothers activated more strongly to
viewing unfamiliar children as compared to their own and
HC mothers reacted more strongly to viewing their own
children as compared to unfamiliar as supported by group
comparisons (i.e. omnibus test) (Supplementary Table S2).
Postscan maternal interview data
The analysis of post-MRI interviews revealed a main effect of
condition on the mothers’ level of self-reported stress
[F(1,20) ¼138.02, P< 0.001), indicating that both groups
experienced less stress when watching children (either their
own or unfamiliar) during play than during separation. We
also noted an interaction of group-by-condition
[F(1,20) ¼11.37, P¼0.002), which derived from significant-
ly less stress in HC than in PTSD mothers when watching
their own and unfamiliar children during separation but
disproportionately greater stress in PTSD mothers when
viewing their own child during separation as examined by
independent t-tests [t-own child (1,18) ¼2.59, P< 0.05;
t-unfamiliar(1,18) ¼2.15, P< 0.05], see Supplementary
Table S4. These group differences cannot be accounted for
by differences in independently rated child behavior during
separation [t(1,18) ¼0.56; P¼0.58].
To evaluate relations between self-report measures of
stress and neuroimaging, we assessed correlations of
within-group BOLD signal changes with post-MRI interview
responses. In both HC and PTSD mothers, when seeing their
own and unfamiliar children during separation (Figure 3),
self-reported levels of stress correlated inversely with activa-
tion of dorsal SFG (BA10), and positively with activation of
the caudate. The more stress HC mothers reported in re-
sponse to seeing their own and unfamiliar children during
separation the more they deactivated the bilateral AEC.
PTSD motherswho reported more stress than HC in the
same conditionsdiffered significantly from this pattern of
activation.
We also entered into a regression model BOLD signal
change, detected by the contrast of separation relative to
free play as the dependent variable, and as a predictor,
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a composite of z-scores based on the CAPS and PCL-S
scores of the mother (Table 2). Across the entire sample,
limbic regions were activated in response to viewing separ-
ation of mothers own and unfamiliar children (i.e. bilateral
amygdala, perirhinal, AEC and hippocampus), as well as
motor planning areas (i.e. bilateral caudate and cerebellum).
Scatter plots were checked to ensure that no outliers had
skewed these results.
Fig. 1 Group comparisons of activation when mothers view their own and unfamiliar children during separation vs play.Two panels each containing three columns of contrast
images are presented that test the a priori hypothesis that PIV-PTSD mothers exhibit reduced mPFC activation and greater limbic activation vs control mothers when viewing child
mental states during separation vs during play, in both their own and in unfamiliar children. Each of the two panels is divided into three columns that represent the following:
(Aand D) group differences in fMRI signal with greater activation in PTSD mothers compared to controls in red and greater activation in controls in blue (i.e. the contrast of the
activations in column B with the activations in column C. (Band E) group average fMRI signal in PTSD mothers when viewing separation compared with play and (Cand F)HC
mothers when viewing separation compared with play. For columns, B and E, and C and F, increases in signal while viewing separation relative to play are shown in red and
decreases are in blue. The left-most three columns of this figure (AC) show neural activity in PTSD and HC mothers while viewing their own children during separation relative
to play. The right-most three columns (DF) show neural activity in PTSD and HC mothers while viewing unfamiliar children during separation relative to play. These are
transaxial views with Talairach z-coordinates shown to the far right of the row of corresponding slices, representing the slices positioned from superiorly to inferiorly (top to
bottom). The left side of the brain (L) is displayed on the left side of the image. We report voxels using a P-value threshold <0.05 together with the requirement that the
activation occurred in a spatial cluster >25 adjacent pixels, a conjoint requirement which, based on an approximation formula, yields a conservative effective P< 0.000005. The
color bars depict P-values for the threshold of the respective statistical contrast without adjustment for the conjoint requirement of the special cluster. aec, anterior entorhinal
cortex; amy, amygdala; cd, caudate; dacc, dorsal anterior cingulate cortex; dorsolateral prefrontal cortex; fusi, fusiform gyrus; ins, insula; peri, perirhinal cortex; mfg, middle frontal
gyrus; mtg, medial temporal gyrus; sfg, superior frontal gyrus; spl, superior parietal lobe; stg, superior temporal gyrus; thal, thalamus; vacc, ventral anterior cingulate cortex.
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DISCUSSION
Most mothers would say that viewing their child placed in a
vulnerable situation such as separation from mother in the
laboratory would not be a pleasurable experience. Yet what
we have found in this study is that mothers with IPV-PTSD
find it particularly stressful to view young children during
separation; while they differed less than HC when viewing
young children during play. IPV-PTSD mothers compared
to HC respond to seeing both their own and unfamiliar
toddlers during separation with significantly greater (i) acti-
vation of specific fear circuit-related regions [for own child
(Figure 1A): AEC; for unfamiliar children (Figure 1D):
amygdala, AEC and perirhinal cortex] and (ii) self-report
feeling stressed (Supplementary Table S4). Support for our
Fig. 2 Within-group comparison of activation when mothers view their own and unfamiliar children. This figure shows group differences in activation associated with the
familiarity of the children (i.e. own vs unfamiliar) during separation compared with play (i.e. testing a familiarity-by-condition interaction) separately in PTSD and HC mothers.
Two panels each containing three columns of contrast images are presented that test the a priori hypothesis that PTSD mothers compared to HC would display greater neural
activation in response to unfamiliar children in separation vs play. The two panels representing these separate comparisons are: (A) PTSD and (B) HC. Each panel is subdivided
into three columns: (A and D) own child in separation vs play, (B and E) unfamiliar children in separation vs play and (C and F) own child in contrast to unfamiliar children in
separation vs play. Increases in signal while viewing own child relative to unfamiliar children are shown in red and decreases are in blue. Orientation and statistical thresholding
are the same as in Figure 1. aec, anterior entorhinal cortex; amy, amygdala; cd, caudate; dacc, dorsal anterior cingulate cortex; dlpfc, dorsolateral prefrontal cortex; fusi, fusiform
gyrus; ins, insula; mfg, middle frontal gyrus; mtg, medial temporal gyrus; pcu, precuneus; peri, perirhinal cortex; sfg, superior frontal gyrus; spl, superior parietal lobe; stg,
superior temporal gyrus; thal, thalamus; vacc, ventral anterior cingulate cortex.
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a priori hypotheses as per these group findings is strength-
ened by the results of the continuous analyses in which ma-
ternal self-reported stress during separation was also
associated with failure to deactivate the AEC in PTSD
mothers compared to HC (Figure 3). Continuous standar-
dized maternal PTSD symptom severity scores were also
correlated with activation of the fear circuit-related regions:
amygdala, AEC, perirhinal cortex and hippocampus in re-
sponse to viewing both own and unfamiliar children during
separation (Table 2.).
Only HC mothers showed activation of the SFG (i.e.
mPFC) in response to seeing their own children during sep-
aration (Figure 1A). Thus, PTSD mothers displayed greater
activation of fear circuit-related regions with less top-down
regulation by the SFG. This finding also converges with
higher levels of maternal self-reported stress among PTSD
mothers in response to separation and may provide the
neural underpinnings for our prior behavioral observations;
namely, mothers’ emotional availability for coordinated
joint attention during play upon reunion after separation
negatively correlated to the severity of their IPV-PTSD
symptoms (Schechter et al., 2010).
We speculate that the present neuroimaging study’s find-
ings as well as those of our previous behavioral study may be,
in part, explained by ‘the polyvagal theory’ (Porges, 2007),
which postulates that the subject goes into a ‘survival’ mode
rather than ‘affiliative’ mode when confronted with a trau-
matic reminder (i.e. for an IPV-PTSD motheras we have
speculated, viewing her own and other toddlers left alone
and helpless). In the ‘survival mode’, the brain and sympa-
thetic nervous system focus on the preparation for fight or
flightincluding related motor planning (i.e. caudate and
cerebellum activation) at the expense of socialemotional
availability and parasympathetic nervous system activity
(Schechter et al., 2005; Austin et al., 2007).
As an alternative hypothesis, this activation pattern may
also represent a difference of the degree of normative hyper-
vigilance that is observed among mothers of infants and very
Fig. 3 Neural correlates of mothers’ self-reported stress in response to separation. The figure displays the maps of correlations of the mothers’ self-reported level of stress with
neural activation when viewing their own and unfamiliar children during separation-play in control and PTSD groups. Red indicates a positive correlation and blue indicates an
inverse correlation. The correlations are compared across the two diagnostic groups in the right-most columns. Orientation and statistical thresholding is the same as in Figure 1.
aec, anterior entorhinal cortex; amy, amygdala; cd, caudate; dlpfc, dorsolateral prefrontal cortex; fusi, fusiform gyrus; dacc, dorsal anterior cingulate cortex; ins, insula; mfg,
middle frontal gyrus; mtg, medial temporal gyrus; peri, perirhinal cortex; sfg, superior frontal gyrus; spl, superior parietal lobe; thal, thalamus; vacc, ventral anterior cingulate
cortex.
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young childrenwhich in exaggerated form has been
hypothesized to be associated with parental anxiety disorders
(Leckman et al., 2004). We think that such potentially exag-
gerated hypervigilance might be related to increased mater-
nal emotion dysregulation among the PTSD mothers that is
triggered by seeing the child in a helpless position during
separation. This state of mind may be reminiscent of trau-
matized mother’s state of mind during interpersonal vio-
lence exposure. It has been shown in multiple studies that
individuals with IPV-PTSD have difficulty downregulating
their own fear and helplessness in the face of negative and
arousing emotional stimuli (Gilboa et al., 2004; New et al.,
2009; Jovanovic and Ressler, 2010; Schechter et al., 2010).
The findings of increased activation in fear circuitry-related
areas (i.e. limbic), motor planning areas (i.e. caudate) and
facial emotion processing areas (i.e. fusiform gyrus) among
PTSD mothers compared to HC, when viewing own and
unfamiliar children during separation, support this inter-
pretation. Decreased activation in the SFG among PTSD
mothers in the same conditions further supports this view.
The SFG has been implicated previously in the regulation
of fear and anxiety states in response to viewing negatively
valenced, arousing emotional stimuli (Numan and Insel,
2003; Leckman et al., 2004; Shin et al., 2005; Marsh et al.,
2009). The absence of SFG activation in response to negative
arousing emotional stimuli has also been associated with the
presence of increased anticipatory anxiety, alexithymia and
dissociative phenomena, and reduced self-awareness (Gilboa
et al., 2004; New et al., 2009). These explanations do not
account for the group difference between responses to own
vs unfamiliar child during viewing of separation among
mothers with PTSD as compared to HC. The amount and
intensity of activation to viewing unfamiliar vs own children
during separation were greater particularly among IPV-
PTSD mothers. We wondered whether this might be due
to greater child distress in at least one of the unfamiliar
children than in most of the mothers’ own children.
In an effort to address this potential confounder, we con-
trolled for the different levels of child distress among the
unfamiliar children during separation (boy with score dis-
tress score of ‘2’ and girl with ‘4’) by repeating the contrasts
post hoc with each child separately. Results concerning the
brain regions involved in our hypotheses were remarkably
similar. Thus, we think that the novelty of seeing the un-
familiar children contributed to this greater overall activa-
tion, with certain specific brain areas affected in relation to
the recognition of the unfamiliar children as novel stimuli
particularly among the PTSD mothers as follows: upon view-
ing unfamiliar children, PTSD mothers access the MFG
(BA10) likely in the service of autobiographical memory re-
trieval perhaps to differentiate novel from familiar stimuli
(Burianova and Grady, 2007).
HC as compared to PTSD mothers deactivated the insular
cortex upon viewing their own and unfamiliar children in
play vs separation. While beyond the scope of this article,
this observation raises a question that merits further study;
namely, how the two groups differed in recruitment of emo-
tional processing circuitry in response to play, as a likely
nonstressful child stimulus that evokes positive affect
(Strathearn et al., 2009).
Limitations
This study has several limitations. These include a relatively
small sample size and the inherent limitations in statistical
power that follow. Of note, this inner-city sample of
violence-exposed mothers with PTSD is rarely represented
in the affective neuroscience literature and is difficult to re-
cruit into a multivisit study including neuroimaging.
An additional limitation included unexpected group dif-
ferences with respect to household income and number of
years of maternal educationdespite no significant group
differences with respect to mothers’ having completed a
high school education or its equivalent. We covaried these
sociodemographic factors with no significant change in re-
sults. However, it is clearly beyond the scope of this study to
test whether these sociodemographic factors are predictive of
PTSD caseness and/or whether having PTSD increases im-
pairment that in turn limits the affected individual’s likeli-
hood of social, economic and academic success. Larger
epidemiologic studies have shown that poverty and poor
education can be both risk factors for and effects of chronic
violence exposure and related PTSD (Koenen et al., 2007).
Table 2 Interactions of familiarity (own vs unfamiliar children) by condition (separation vs free play) by group (PTSD vs controls)
Region of interest Side Brodmann’s
area
MNI coordinates t-value z-score POrigins
xyz
Cortical regions
STG, temporal pole Left > Right 38,22,21 44 0 24 3.46 2.99 0.001 Separation
Limbic areas
Amygdala, entorhinal cortex Left/Right 34,28 28 2 16 2.81 2.52 0.006 Separation
Hippocampus, perirhinal cortex Left > Right 28,35 16 812 2.68 2.43 0.008 Separation
Other regions
Cerebellum Left > Right 0 44 44 2.86 2.57 0.005 Separation
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Another important limitation pertains to the stimuli used.
The naturalistic video clips of subjects own children, while
having the advantage of providing more ecologically valid
stimuli that were individualized for each mother, contained
differing levels of distress across children. Even though naı
¨ve
raters found no significant group differences in levels of
child distress during separation, greater rigor could be
applied to creating the unfamiliar child stimuli and in fur-
ther constraining the breadth of ages among own and un-
familiar children. And as mentioned above, the levels of
distress among the two unfamiliar children differed signifi-
cantly from one another. Despite our post hoc analyses to
control for this potential confounder, we cannot fully dis-
miss the possibility that these differing distress levels altered
the results with regards to response to child separation
stimuli.
The present study demands replication and expansion
both with a larger sample and with two control groups:
one with IPV exposure but no PTSD and one with
neither PTSD nor IPV exposure (Adenauer et al., 2010).
Additionally, given the characteristic failure among IPV-
PTSD patients to extinguish hyperarousal in response to
evocative stimuli, further studies might also test whether
IPV-PTSD mothers habituate less to video-stimuli depicting
their own and unfamiliar children in separation as compared
to play (Wessa and Flor, 2007).
CONCLUSIONS
This article reports findings from the first study ever to char-
acterize neural activation of violence-exposed parents with
PTSD compared to HC in response to viewing very young
children during separation as compared to free play. The
study suggests that IPV-PTSD mother’s viewing their own
and unfamiliar children during this interpersonally stressful
condition of separation triggers patterns of neural activation
that are similar to those triggered in response to traumatic
reminders among adult PTSD patients (Francati et al., 2007;
New et al., 2009). Namely, activation of the amygdala and
surrounding input and output regions (i.e. AEC and peri-
rhinal cortex) in response to seeing very young children in
separation is associated with greater PTSD symptom sever-
ity. While the SFG was not recruited by IPV-PTSD mothers
in response to viewing their own child in separation, it was,
in response to viewing unfamiliar children. The opposite was
true for HC (i.e. the SFG was activated when seeing own
children but not when seeing unfamiliar ones). The latter
group activated this region in response to viewing their
own children but not unfamiliar children. Given these find-
ings, this study may help to clarify the neural underpinnings
of atypical maternal behavior of IPV-PTSD mothers during
interactions with their young children following interperson-
al stressors such as separation (Fraiberg et al., 1975; Lyons-
Ruth et al., 1999; Schechter et al., 2010). Understanding the
neural basis for parental stress and its impact on caregiving
behavior is particularly important given that longitudinal
follow-up studies have suggested that the children of IPV-
PTSD mothers are at risk for long-term disturbances in their
capacity to self-regulate their emotions, arousal and behavior
(Lieberman et al., 2005; Schechter et al., 2007; Dutra et al.,
2009).
SUPPLEMENTARY DATA
Supplementary Data are available at SCAN online.
Conflict of Interest
None declared.
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It is currently unknown whether differences in neural responsiveness to infant cues observed in postpartum affective disturbance are specific to depression/anxiety or are better attributed to a common component of internalizing distress. It is also unknown whether differences in mothers' brain response can be accounted for by effects of past episodes, or if current neural processing of her child may serve as a risk factor for development of future symptoms. Twenty-four mothers from a community-based sample participated in an fMRI session viewing their 3-month- old infant during tasks evoking positive or negative emotion. They were tracked across the ensuing 15 months to monitor changes in affective symptoms. Past and current episodes of depression and anxiety, as well as future symptoms, were used to predict differences in mothers' hemodynamic response to their infant in positive compared to negative emotion contexts. Lower relative activation in largely overlapping brain regions involving frontal lobe structures to own infant positive vs. negative emotion was associated with concurrent (3-month) depression diagnosis and prospective (3-18 month) depression and anxiety symptoms. There was little evidence for impacts of past psychopathology (more limited effect of past anxiety and nonsignificant effect of past depression). Results suggest biased maternal processing of infant emotions during postpartum depression and anxiety is largely accounted for by a shared source of variance (internalizing distress). Furthermore, differential maternal responsiveness to her infant's emotional cues is specifically associated with the perpetuation of postpartum symptoms, as opposed to more general phenotypic or scarring effects of past psychopathology.
... Research undertaken specifically with mothers who have family violence-related PTSD have been assessed as demonstrating limited capacity to read the emotional cues of their infant (Huth-Bocks et al. 2004;Schechter et al. 2012). Should the Refuge itself not possess the capacity to reflect on the mind of the mother, and therefore her capacity to reflect on the mind of the infant, it may be that neither infant not mother are having their emotional or developmental needs met adequately in the context of recovery from violence and the transition to motherhood. ...
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Almost nothing is known about how the infant may experience being in a women’s Refuge (Shelter) setting with their mother after fleeing family violence, despite the high numbers of infants and young children in Refuges or Shelters. This research was concerned with exploring how the infant experienced refuge within a Refuge setting post family violence. Using a non-intrusive, ethically informed, ‘infant led’ approach, this research involved ten infants (aged 3 weeks to 16 months), ten mothers, and 13 staff in eight Refuges from three countries: Australia, Scotland and England. Data was collected through infant observation, interviews with mothers and then staff. Presented is a synthesis of a research methodology which was led by the infant, drew on concepts of ‘inter-subjectivity’ and used a constructivist grounded theory method. Infants were often lost from view within the Refuge setting. The mother, herself traumatised, was expected to be the refuge for her infant. Only the obviously distressed infant was assisted, and where available, from outside specialist workers. It was often too painful for the adults, both mothers and staff, to see or reflect on the infant’s possible trauma. Significantly, in all cases the motivation for each mother to enter Refuge was ensuring their infant’s safety. Concern for their infant or young child can be a powerful catalyst for women leaving a violent relationship. Refuges (Shelters) are in a unique position to respond to the infant in their own right whilst helping to heal and grow the infant/mother relationship.
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The field of neuroscience has largely overlooked the impact of motherhood on brain function outside the context of responses to infant stimuli. Here, we apply spectral dynamic causal modelling (spDCM) to resting-state fMRI data to investigate differences in brain function between a group of 40 first-time mothers at one-year postpartum and 39 age- and education-matched women who have never been pregnant. Using spDCM, we investigate the directionality (top-down vs bottom-up) and valence (inhibition vs excitation) of functional connections between six key brain regions implicated in motherhood: the dorsomedial prefrontal cortex, ventromedial prefrontal cortex, posterior cingulate cortex, parahippocampal gyrus, amygdala, and nucleus accumbens. We show a selective modulation of inhibitory pathways related to differences between (1) mothers and non-mothers, (2) the interactions between group and cognitive performance and (3) group and social cognition, and (4) differences related to maternal caregiving behaviour. Across analyses, we show consistent disinhibition between cognitive and affective regions suggesting more efficient, flexible, and responsive behaviour, subserving cognitive performance, social cognition, and maternal caregiving. Together our results support the interpretation of these key regions as constituting a parental caregiving network. The nucleus accumbens and the parahippocampal gyrus emerging as hub regions of this network, highlighting the global importance of the affective limbic network for maternal caregiving, social cognition, and cognitive performance in the postpartum period.
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The presence of perinatal mood and anxiety disorders has typically been associated with decreases in the quality of mother–infant interactions. However, maternal anxiety symptoms during the postpartum period have been less studied than other mental health disorders like depression. In the current study, we examined associations among symptoms of maternal anxiety, maternal perceived stress, and mother–infant behavioral synchrony in the early postnatal period. Eighty‐one mother–infant dyads participated in this study when the infants were 3 months old. Surveys were given to obtain demographic information and current maternal mental health symptoms, and dyads completed a 5‐min free‐play task to measure behavioral synchrony. Results indicated that maternal anxiety symptoms were positively associated with behavioral synchrony, but only for mothers reporting moderate levels of perceived stress. These findings highlight the differential impact of maternal postpartum mental health on behavioral synchrony and suggest that higher maternal anxiety symptoms during the postnatal period may play an adaptive role in fostering more dynamic mother–infant interactions.
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In this chapter, the authors present their approach to assessing infant–parent relationships. They begin by reviewing several areas of research that support a focus on relationships. They then describe the overall model of infant–parent relationship assessment and elaborate the basic premises that guide their approach. Next, they describe the dimensions of the relationship that seem important to measure and the process and methods they employ to assess them. Finally, they describe an approach to conceptualize the overall level of relationship adaptation/disturbance. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
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The Neurobiology of Parental Behavior takes an integrative approach that analyzes the neural underpinnings of parental behavior in mammals, including humans.
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