Love flows downstream mothersrsquo and childrenrsquos

neural representation similarity in perceiving

distress of self and familyTae-Ho Lee1 Yang Qu2 and Eva H Telzer1

1Department of Psychology and Neuroscience The University of North Carolina at Chapel Hill Chapel HillNC 27599-3270 USA and 2Department of Psychology Stanford University Stanford CA 94305 USA

Correspondence should be addressed to Eva H Telzer Department of Psychology and Neuroscience The University of North Carolina at Chapel Hill 235 ECameron Avenue Chapel Hill NC 27599-3270 USA E-mail ehtelzeruncedu

Abstract

The current study aimed to capture empathy processing in an interpersonal context Motherndashadolescent dyads (Nfrac1422)each completed an empathy task during fMRI in which they imagined the target person in distressing scenes as eitherthemselves or their family (ie child for the mother mother for the child) Using multi-voxel pattern approach we com-pared neural pattern similarity for the self and family conditions and found that mothers showed greater perceptual simi-larity between self and child in the fusiform face area (FFA) representing high selfndashchild overlap whereas adolescentsshowed significantly less selfndashmother overlap Adolescentsrsquo pattern similarity was dependent upon family relationshipquality such that they showed greater selfndashmother overlap with higher relationship quality whereas mothersrsquo pattern sim-ilarity was independent of relationship quality Furthermore adolescentsrsquo perceptual similarity in the FFA was associatedwith increased social brain activation (eg temporal parietal junction) Mediation analyses indicated that high relationshipquality was associated with greater social brain activation which was mediated by greater selfndashmother overlap in the FFAOur findings suggest that adolescents show more distinct neural patterns in perceiving their own vs their motherrsquos distressand such distinction is sensitive to motherndashchild relationship quality In contrast mothersrsquo perception for their own andchildrsquos distress is highly similar and unconditional

Key words representational similarity analysis (RSA) motherndashchild dyads empathy maternal empathy adolescentselfndashother overlap

Introduction

Emotional experiences often occur in an interpersonal contextFor example parents may experience more negative feelingsthemselves when their child is upset Experiencing empathywith regard to othersrsquo pain or distress is found across speciesincluding rodents non-human primates and humans ininfants as young as a few months of age as well as across manyforms of social relationships (eg for strangers loved ones etcPreston and De Waal 2002 Decety 2011 b Batson 2009) At its

most basic core empathy facilitates parental care of their off-spring and paves the way for successful social and emotionaldevelopment in youth (Mikulincer et al 2001 De Waal 2008Decety 2011 b) A parentsrsquo ability to perceive and respond toemotional cues of their offspring such as hunger pain or dis-tress is essential for survival and has been hardwired at theneural level to promote parental care in mammalian species asan innate protective system for their offspring (Decety 2011 b)Indeed studies have shown that parental empathic experiences

Received 1 June 2017 Revised 28 August 2017 Accepted 16 October 2017

VC The Author (2017) Published by Oxford University PressThis is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (httpcreativecommonsorglicensesby-nc40) which permits non-commercial re-use distribution and reproduction in any medium provided the original work is properly citedFor commercial re-use please contact journalspermissionsoupcom

1916

Social Cognitive and Affective Neuroscience 2017 1916ndash1927

doi 101093scannsx125Advance Access Publication Date 23 October 2017Original article

and neural engagement of the empathy network are moreintensified when parents see their own childrsquos pain comparedwith an unknown childrsquos pain (Leibenluft et al 2004 Goubertet al 2008) Similarly when mothers make caregiving decisionsfor their child neural activation in the empathy networkincluding the prefrontal cortex (PFC) limbic and sensoryregions increases to meet the needs of their child (Ho et al2014) Although emerging evidence supports maternal empathyfor their own childrsquos emotions it is unclear whether childrenrsquosempathy is equivalent to their parentsrsquo emotional perception oftheir offspring Thus the current study aimed to capture empa-thy processes in an interpersonal context within parentndashchilddyads

One important aspect of empathy is the phenomenon bywhich one blurs the line between self and other (Davis et al1996 Hodges and Klein 2001 Decety and Sommerville 2003Galinsky et al 2005 Decety and Lamm 2006 Batson 2009)Theories suggest that understanding othersrsquo emotions andactions begin by perceptually representing or mirroring othersrsquofeelings and actions onto onersquos own states (Rizzolatti et al 2001Preston and De Waal 2002 Gallese 2007 Keysers and Gazzola2009) According to Preston and de Waalrsquos (2002) perceptionndashaction model the initial perception of othersrsquo states can leadperceivers to have high selfndashother mental representation in feel-ings and actions thereby eliciting emotional contagion andempathic responses as behavioral outcomes Perceiving othersrsquoemotion (ie perceptual encoding) enables individuals to simu-late othersrsquo states as onersquos own states and thereby forms selfndashother overlap (Rizzolatti et al 2001 Gallese 2007 Keysers andGazzola 2009) That is how we perceive othersrsquo emotions couldbe an important gateway to how we share mental representa-tions with others for empathic actions An important considera-tion for the emergence of empathy is thus whether individualsshow a similar representation of the self and other during per-ceptual encoding and whether such perceptual similarity facili-tates further empathic responding

Perceptual representation for selfndashother overlap can be char-acterized as a bottom-up process because it requires one todetect and encode othersrsquo states first (Singer 2006 Decety2011a) Indeed studies have shown that empathic responsesduring the observation of othersrsquo pain are associated withincreased activation in early perception-sensory regions suchas extrastriate body area fusiform gyrus and sensory-motorarea (eg Jackson et al 2005 Lamm et al 2007 Lamm andDecety 2008) This bottom-up process may influence social cog-nitive top-down modulation in which the perceptual represen-tation for others is evaluated to make subsequent inferences forothersrsquo situation (Decety and Sommerville 2003 Jackson andDecety 2004 Singer 2006 Decety 2011a) For example socialcognitive regions such as the temporal parietal junction (TPJ)medial PFC (MPFC) and posterior cingulate cortex (PCC) showincreased activity for in-group memberrsquos pain (Amodio andFrith 2006 Adams et al 2010 Cheon et al 2010 Mathur et al2010 Morrison et al 2012) along with increased neural activa-tion of sensory-perception regions (Azevedo et al 2013 Zuo andHan 2013) In this vein researchers highlight the importance ofboth affective and cognitive components of empathy that influ-ence the extent of empathic concern and potential prosocialbehavior (Decety 2005 Eisenberg and Eggum 2009 Goubertet al 2009) In this model the bottom-up affective componenthelps perceivers to increase personal distress and attention forunderstanding otherrsquos affective states and the top-down cogni-tive component regulates perceiverrsquos emotional arousal andleads to prosocial behavior by recruiting cognitive control

resources However too much personal distress induced byemotional arousal and contagion can impede the perceiverrsquosempathic behaviors as it depletes cognitive resources to regu-late their own affective arousal thereby failing to attend toothersrsquo needs (Eisenberg and Eggum 2009)

Previous work has focused on the neural involvement ofeither early sensory-perception processes (eg Singer et al2004 Jackson et al 2005) or higher-order social cognitive proc-esses (eg Saxe et al 2004) independently instead of conceptu-alizing empathy as a continuum from the initial representationat the perception level to later social cognitive processes Thusempirical research which integrates how the self and others arerepresented during the initial perception and how this percep-tual representation is associated with mentalizing processeswill shed light on our understanding of how empathy arises inthe brain In the current study we scanned both mothers andtheir adolescent child as they engaged in a task that measuresempathic responses when perceiving their own and eachotherrsquos distress We sought to examine how empathic experien-ces are modulated by perceptual representation based on theperception-action perspective (Preston and De Waal 2002Preston 2007) In particular we examined perceptual encodingof selfndashother overlap in the fusiform face area (FFA) andwhether higher perceptual similarity is associated withempathic responses in socialndashcognitive brain regions Our per-ceptual similarity analysis of selfndashother overlap focused on neu-ral patterns in the FFA because evidence indicates that the FFAis involved in the initial encoding of faces as an early visual per-ception process (Ghuman et al 2014) Importantly the mentalimagination of faces and encoding emotionality and socialinformation from faces significantly increases neural activationin the FFA (OrsquoCraven and Kanwisher 2000 Adolphs 2009Sabatinelli et al 2011) To quantify the representation similar-ity we adopted the representational similarity analysis (RSAKriegeskorte et al 2008) as a form of multi-voxel patternapproach This pattern-focused approach allows us to test howneural representations when perceiving self and other are simi-lar by focusing on signal variations of neural response acrossvoxels (ie multi-voxel pattern) rather than simply changes inthe overall fMRI magnitude between parent and adolescentgroups (ie univariate neural activation)

We tested three key hypotheses First mothersrsquo perceptualrepresentation of distress for self and child would be highlysimilar as evidenced by greater neural pattern similarity in theFFA regardless of the quality of their relationship In contrastadolescents would show less similar perceptual representationof distress for self and mother and such representational simi-larity would depend upon their relationship quality Previousstudies have indicated that parental concerns for their offspringare stable and unconditional regardless of social environmentalfactors (Acock and Bengtson 1980 Leibenluft et al 2004Goubert et al 2008 Proulx and Helms 2008 Driscoll and Pianta2011) For instance parentsrsquo perception of closeness to theirchild is stable as parents focus on deemphasizing conflicts andincreasing support in their roles as parents for their childrsquoswell-being (Acock and Bengtson 1980 Proulx and Helms 2008Driscoll and Pianta 2011) Indeed following pregnancy moth-ersrsquo socioemotional neural system shifts to support empathyand care of their child (Hoekzema et al 2016) In contrast theadolescent period is marked by a social reorientation away fromparents and towards peers (Nelson et al 2005) Adolescentsreport decreased closeness in parentndashchild relationship quality(Tsai et al 2013) combined with exaggeration of conflicts todiminish closeness with parents as a means of establishing

T-H Lee et al | 1917

autonomy (Fuligni and Eccles 1993 Larson et al 1996 Collinsand Steinberg 2006) Thus adolescentsrsquo perceptual representa-tion of distress for self and mother would be more conditionalsuch that adolescents will only show high neural pattern simi-larity in the FFA when they report stronger relationship quality

Second we tested whether perceptual encoding (ie repre-sentational pattern similarity in the FFA) is associated withhigher social cognitive processing Perceptual representationsimilarity in the FFA an index of selfndashfamily overlap was usedas a regressor in a univariate general linear model (GLM) analy-sis to link initial perception to subsequent empathic processesin social brain regions which include the TPJ MPFC and PCC(Saxe et al 2004) In other words the level of neural engagementin the social brain when processing family and self will dependon the perceptual similarity in the FFA As suggested by theoriesof empathy (eg Preston and de Waalrsquos 2002) the initial percep-tual representation process for othersrsquo states subsequently elic-its emotional contagion and empathic response Although thesluggish nature of the fMRI signal does not allow us to testdirect temporal influences between processes we hypothesizedthat higher perceptual similarity in the FFA a neural index ofselfndashfamily perceptual overlap would be associated with greaterneural recruitment of mentalizing processes in social brainregions

Finally we performed mediation analyses to test an inte-grated model linking motherndashchild relationship quality the per-ceptual similarity in selfndashndashfamily overlap and neuralengagement of social brain regions We hypothesized thatgreater relationship quality in adolescents would be associatedwith the recruitment of social brain regions during empathicresponses and this path would be mediated by greater encod-ing of perceptual similarity in the FFA Whereas relationshipquality would be a key predictor of perceptional similarity andsocial brain responding in adolescents we predicted that rela-tionship quality would not influence empathic responses inmothers because mothersrsquo socioemotional system is more sta-ble and invariable for their offspring (Acock and Bengtson 1980Proulx and Helms 2008 Driscoll and Pianta 2011 Hoekzemaet al 2016)

Materials and methodsParticipants

Twenty-two healthy motherndashadolescent dyads were recruitedto participate in this study (adolescents Magefrac14 1390 yearssdfrac14 011 21 female mothers Magefrac14 4426 years sdfrac14 157100 female) Mothers and their adolescent child each under-went an fMRI scan on the same day Participants were compen-sated $50 each for their participation All participants providedwritten informed consent and assent approved by theInstitutional Review Board

Task design and procedure

The task was modified from prior work on neural processing ofempathy a task which has reliably recruited neural regionsinvolved in mentalizing (Rameson et al 2012 Morelli et al2014) During the task adolescents and mothers each saw indi-viduals expressing emotional distress in negative contexts (egat a funeral or being bullied) with instructions to perceive thetarget face as either their family member (family-conditionmother for the childrsquos scan or child for the motherrsquos scan) orthemselves (self-condition) Participants were instructed to

imagine the person in the picture as themselves and to take theperspective of the person in the picture during the self-condition For the family-condition participants wereinstructed to imagine the person in the picture as their parentchild and to take the perspective of the person in the picture asif it were their family member When the target individualsappeared in the social scenes with many other people a whitearrow was inserted to guide participants to the target face (seeFigure 1A) The stimulus conditions were balanced by gender oftarget face The gender of faces was not matched to the subjectand participants were instructed to imagine the person in eachimage as themselves (self-condition) or their family member(family-condition) regardless of the gender of the person Theage of the target face for each group (eg family and self) wasmatched Each trial lasted between 8 and 92 s and was followedby 2 s rating phase consisting of a 10-point Likert scale to indi-cate how they felt from 5 (very negative) to 5 (very positive)1

Two independent blocks for self- and family conditions con-sisted of 12 event-related trials each (ie mixed-design) Eachblock was separated by a 5-s blank screen and inter-trial inter-vals were inserted between trials to separate the BOLD signaljittered between 20 and 32 s (meanfrac14 24 s)

fMRI data acquisition and analysis

Image acquisition preprocessing and registration Imaging datawere collected using a 3T-Siemens Trio MRI scanner with a 32-channel matrix coil High-resolution structural images (T1-MPRAGE) were acquired first (repetition time or TRfrac14 19 s echotime or TEfrac14 23 ms matrix sizefrac14 256 256 field of view orFOVfrac14 230 mm flip angle or FAfrac14 90 1 mm isotropic voxel) T2-weighted echoplanar images were acquired during the emotionperception task (38 slices with 03 mm inter-slice gap TRfrac14 2 sTEfrac14 25 ms matrixfrac14 92 92 FOVfrac14 230 mm FAfrac14 90 voxel size25 25 mm slice thicknessfrac14 3 mm)

Preprocessing was carried out using FEAT (FMRI ExpertAnalysis Tool) Version 600 part of FSL (FMRIBrsquos SoftwareLibrary Smith et al 2004) The following pre-statistics process-ing was applied motion correction using MCFLIRT (Jenkinsonet al 2002) non-brain removal using BET (Smith 2002) grand-mean intensity normalization of the entire 4D data set by a sin-gle multiplicative factor spatial smoothing applied only for uni-variate whole-brain analysis with Gaussian kernel of full widthat half maximum 6 mm For univariate analysis registrationmatrix was estimated additionally between functional imageshigh-resolution structural images and standard MontrealNeurological Institute (MNI) 2-mm brain using FLIRT (Jenkinsonand Smith 2001 Jenkinson et al 2002)

RSA (multi-voxel pattern analysis) For the RSA we first estimatedsingle-trial activation patterns for each trial using least squaressingle methods (Mumford et al 2012) where each single-levelGLM included regressors for a current trial and all other remain-ing trials with temporal derivate regressor We included the

1 A repeated measure of ANOVA (condition self and family X groupmother and adolescent) found that there was no main effect of condi-tion or interaction (all ps gt 029) but a significant main effect of group(p frac14 0001) indicating mothers rated painful scenes as more negativethan adolescents regardless of stimulus types (children -084 vs moth-ers -219) Subsequent t-tests indicated that all ratings for both selfand family conditions of mothers and adolescents were significantlydifferent from 0 (0 frac14 rating as non-arousing all ps lt 0001) indicatingthat both mothers and children perceived painful scenes as negativeacross all stimulus types

1918 | Social Cognitive and Affective Neuroscience 2017 Vol 12 No 12

rating phase in the model as a regressor of non-interest (ie nui-sance regressor) as well as motion regressors (six motionparameters and motion-outlier points) For each participantthe standardized voxel-wise pattern activity (ie z-transformedparameter estimates) was extracted and vectorized within theFFA region of interest (ROI) (see ROI selection for more details)The extracted patterns were then analyzed by calculating pair-wise Pearson coefficient (ie similarity value) between each trialwith every possible pair of other trials (Figure 1B) and thenapplied Fisherrsquos r-to-z transformation producing a symmetric24 24 similarity matrix for each dyad and the ROI (Figure 1C)Finally the average of selfndashfamily similarity values was used forsubsequent analyses (eg Visser et al 2011)

Univariate group-level analysis with RSA as a covariate To assesshow perceptual encoding (ie representational pattern similar-ity in FFA) is associated with higher-level social cognitive proc-essing an additional standard two-stage mixed-effects analysiswas performed The GLM of the BOLD signal for each perceptiontype (family and self) was estimated with temporal derivateregressors at the first level using a double-gamma hemody-namic response function We added the rating phase in the

model as a regressor of non-interest (ie nuisance regressor) tothe design matrix as well as motion regressors (six motionparameters and motion-outlier points) The individualsrsquo datawere then inputted into a random-effects model using clusterdetection statistics with outlier-deweighting at a threshold ofZgt 23 and a cluster probability of Plt 005 (one-tailed) correctedfor whole-brain multiple comparisons using Gaussian RandomField Theory In particular we entered each individualrsquos FFAsimilarity values (demeaned for each group) as covariates in thegroup-level analysis to examine how perceptual similarity inthe FFA to self and other is associated with neural encoding ofself and other in socialndashcognitive regions

ROI selection In this study we indexed neural representation atthe encoding stage by examining neural pattern similaritywithin the FFA a key region in visual face encoding (Kanwisheret al 1997) We constructed the ROI mask of a priori voxels asso-ciated with lsquoFFArsquo lsquoemotional facersquo lsquofacesrsquo and lsquoface perceptionrsquofrom the reversed inference map (qlt 01 FDR-corrected) in theNeuroSynth database (httpwwwneurosynthorg downloadedon 24 November 2015) The final FFA voxels were then selectedalong with the ventral temporal cortex at Zfrac14 371 (Figure 1B atotal 321 voxels)

Family relationship quality

To capture a comprehensive measure of relationship qualitybetween mothers and adolescent children three measureswere assessed from both mothers and adolescent children fam-ily cohesion (Family Adaptation and Cohesion Evaluation ScalesII inventory FACE II Olson et al 1979) family conflict (Ruizet al 1998 Telzer et al 2014) and family identity (Tyler andDegoey 1995) We created a composite score of positive familyrelationship quality by taking the score of family cohesionreverse-scored family conflict and family identity with higherscores indicating more positive parentndashchild relationships Thiscomposite score provides us with a comprehensive measure ofrelationship quality using these three dimensions (Qu et al2015) Details for each scale are as follows

Family cohesion Participants completed the Cohesion subscaleof the FACE II (Olson et al 1979) They responded to 10 itemsthat assessed how close they feel and how much time theyspend with their mother [child] on a 5-point Likert scale from 1(almost never) to 5 (almost always) Sample items included lsquoMymother [child] and I do things togetherrsquo lsquoMy mother [child] andI are supportive of each other during difficult timesrsquo and lsquoMymother [child] and I feel close to one anotherrsquo (internal consis-tency afrac14 081 for mother afrac14 088 for child) The 10 items wereaveraged and higher scores indicate greater relationshipcloseness

Family conflict Parentndashchild conflict was assessed by 10 items(Ruiz et al 1998 Telzer et al 2014) (eg lsquoYou and your parents[child] had a serious argument or fightrsquo and lsquoYou and yourparents [child] yelled or raised your voices at each otherrsquo)Participants reported how true each item was for them in thepast month on a 5-point scale ranging from lsquoalmost neverrsquo tolsquoalmost alwaysrsquo (afrac14 088 and 092 for mother and child respec-tively) The 10 items were averaged such that higher scoresindicate greater conflicts with family members

Family identity Participants completed an eight-item scale thatassessed the extent to which their family is an important aspectof their identity (Tyler and Degoey 1995) Using a 5-point scalefrom 1 (strongly disagree) to 5 (strongly agree) participants indi-cated how much their sense of self was internalized to theirfamily value (eg lsquoI feel like a valued member of my familyrsquo andlsquoMy family is important to the way I think of myself as a personrsquoafrac14 083 and 087 for mother and child respectively) The eightitems were averaged and higher scores indicate greater inter-nalized family values

Fig 1 (A) Experimental condition for mothers and adolescent children (B) schematic procedure of computing similarity values within the region of interest between

trials and (C) example of the representational similarity matrix

T-H Lee et al | 1919

ResultsRSA perceptual similarity for self and family

To examine how mothers and adolescent children perceive theemotional distress of their family and self at the perceptuallevel we compared the similarity value in FFA of mothers whenperceiving their own and their childrsquos emotional distress and ofadolescents when perceiving their own and their motherrsquos emo-tional distress As shown in Figure 2A mothers showed greaterneural similarity in perceptual representation in the FFA whenperceiving emotional distress in self vs child (Mfrac14 024sdfrac14 006) whereas their adolescent children showed signifi-cantly less neural pattern similarity between the conditions(Mfrac14 017 sdfrac14 007) paired-t(20)frac14411 Plt 005 95 confi-dence interval (CI) 50 000 bootstrap resamplingfrac14009 to 003 Thatis mothersrsquo perception of their childrsquos emotional distress withineach dyad is more similar to their own emotional distress com-pared with their own adolescent childrsquos perception of self andmother

As hypothesized childrenrsquos perceptual similarity wasdependent upon their family relationship quality such that theyshowed greater perceptual similarity when they reported higherrelationship quality r(22)frac14 045 Plt 005 95 CI 50 000 bootstrap

resamplingfrac14 009ndash072 whereas mothersrsquo neural pattern similaritywas high and independent of relationship quality r(21)frac14 007Pgt 005 95 CI 50 000 bootstrap resamplingfrac14042 to 052 (Figure 2B)To rule out the possibility of ceiling effects relating to the findingthat there was no association between motherrsquos perceptual simi-larity and relationship quality compared to adolescents we com-pared the relationship quality in dyads and found no significantdifference between mother and child paired-t(21)frac14014Pgt 005 95 CI 50 000 bootstrap resamplingfrac14038 to 032 This resultindicates that the null finding for mothers was not due to ceilingeffects for relationship quality In sum mothers show high selfndashchild overlap in perceptual similarity in the FFA regardless oftheir relationship quality with their child In contrast adolescentchildren only showed high perceptual similarity in the FFA whenthey also reported high relationship quality with their familysuggesting that adolescent childrenrsquos selfndashfamily overlap isdependent upon their relationship quality

Group-level univariate analysis with FFA similaritypredicting social brain activation for self and family

To test the prediction that higher neural similarity for self andfamily at the perceptual level is associated with neural process-ing in higher-level socialndashcognitive regions we examinedwhich brain regions covaried with perceptual similarity in theFFA To this end we used FFA similarity from the self and fam-ily conditions and regressed this similarity value onto neuralactivation when perceiving self vs familyrsquos emotional distress(selfgt family) Note that greater activation for this contrast rep-resents greater differences in neural responses to self and fam-ily We found that greater perceptual similarity between selfand family in adolescents was negatively associated with neu-ral activation in several social brain regions including bilateralTPJ PCC and mPFC (Figure 3A and Table 1) suggesting thatgreater similarly in the FFA at the encoding stage was associ-ated with lower differentiation of self and family in the socialbrain processing for empathy

Next we regressed family relationship quality onto neuralactivation when perceiving self vs familyrsquos emotional distressand found negative correlations in several social brain regionsas a function of adolescentsrsquo family relationship quality (Figure3B and Table 2) That is adolescents who reported greater rela-tionship quality showed lower differentiation of self and familyin the social brain during empathic responding Social brainregions of mothers were not modulated by the perceptual simi-larity for self and child (see Table 1 for local maxima regions inthe clusters)

Mediation analysis

To integrate the results of perceptual similarity in the FFA neu-ral engagement in the social brain and family relationship qual-ity we performed a mediation analysis We tested whetherrelationship quality (ie independent variable) is associatedwith less differentiation of self and family in socialndashcognitiveregions (ie outcome) through increased perceptual similarity inthe FFA (ie mediator) To this end we extracted and averagedactivation from the social brain regions which were identified inthe analyses above and performed mediation analyses usingthe mediation toolbox in Matlab (Wager et al 2008) As shown

Fig 2 (A) Whisker plot for the neural pattern similarity between self and family condition calculated within FFA ROI Black and white bar within indicate mean and

median respectively Red-colored dots indicate individualrsquos similarity point one mother had extremely low similarity value (0002 gray-colored square) that was far

less than 25 sd under the mean We excluded this mother for the final analyses (B) Scatter plots of the similarity values and relationship quality for adolescents and

mothers Dotted lines indicate 95 CI of the regression line Note that all statistical results remained same when the outlier mother was included 95 CIfrac14009

to003 for panel A and 95 CIfrac14029 to 068 for panel B

1920 | Social Cognitive and Affective Neuroscience 2017 Vol 12 No 12

in Figure 4 the path between family relationship quality andperceptual similarity in the FFA for self and mother (path aafrac14 005 Plt 005 95 CI 50 000 bootstrap resamplingfrac14 001ndash009) andthe path between perceptual similarity and social brain regionsidentified in the univariate analysis (path b bfrac14250 Plt 00595 CI 50 000 bootstrap resamplingfrac14407 to 120) were statisticallysignificant Importantly the mediation effect was significant(abfrac14011 Plt 005 95 CI 50 000 bootstrap resamplingfrac14025 to001) indicating that greater perceptual similarity for self andfamily explains the link between strong family relationshipquality and less differentiation in the social brain for self vsfamily Only adolescents showed this significant mediatingeffect whereas mothers did not (abfrac14 001 Pgt 005 95 CI 50 000

bootstrap resamplingfrac14007 to 009) In sum these results suggestthat not only is the quality of the relationship important forhigh perceptual similarity for both the self and their family butalso that high selfndashother overlap at the perceptual level explainsthe link between family relationship quality and empathicresponding in higher-level socialndashcognitive regions

Discussion

In this study we examined mothers and their childrsquos empathicneural representations for the self and family Using represen-tation similarity analysis we found that mothersrsquo perceptualsimilarity in the FFA for self and their childrsquos emotional distresswas significantly higher compared to their childrsquos selfndashmotherperceptual similarity indicating that mothers show high selfndashchild overlap compared to their adolescent child In contrastadolescentsrsquo perceptual similarity was dependent upon theirrelationship quality such that they showed high selfndashotheroverlap for their motherrsquos emotional distress and their ownonly when they reported high relationship quality with theirfamily It is worth noting that these similarity results werebased on within-family comparisons indicating that eachmother shows higher perceptual similarity than her own childMoreover this initial perceptual representation in the fusiformin adolescents was associated with neural activation in social

brain regions required to put oneself in anotherrsquos shoes (Saxeet al 2006) whereas no such modulatory effects of perceptualsimilarity on the social brain were found in mothers Consistentwith previous evidence showing that parentsrsquo perspective totheir child is more stable and robust whereas adolescent chil-dren begin to reduce closeness with their parents as a means ofestablishing autonomy (Acock and Bengtson 1980 Proulx andHelms 2008 Driscoll and Pianta 2011) these results suggestthat mothersrsquo empathy to their child is more unconditionalcompared to that of their adolescent child Finally the media-tion model confirmed that family relationship quality is associ-ated with adolescentrsquos mental representation for both the selfand their family at the perceptual (ie fusiform perceptual rep-resentation similarity) and higher-level social cognitive process-ing level

Mothersrsquo attention is unconditionally directed toward theiroffspring to understand make sense of and respond to theirchildrsquos feelings and behaviors across the lifespan This mater-nal empathic bias has deep evolutionary underpinnings at theneural level to be selective and protective of her own offspring(De Waal 2008 Decety 2011 b) such that mothersrsquo empathypromotes positive developmental outcomes such as moodstability and regulated stress reactivity in developing youth(Abraham et al 2017) Our findings support this perspectivefor maternal empathy by showing that maternal empathicprocesses for their child are more robust compared to chil-dren In our mediation model we found that mothersrsquo mental-izing process for their childrsquos emotional distress wasmodulated by neither the relationship quality nor the degreeof selfndashchild overlap in the FFA It is possible that motherswere at ceiling with less variability in perceptual similarity inthe FFA as well as social brain activation Importantly a recentneuroimaging study revealed that brain regions associatedwith empathy are dramatically reconfigured after pregnancyin a motherrsquos brain (Hoekzema et al 2016) which enablesmothers to be more selective and sensitive to their own off-spring In other words the neural connections in mothersrsquobrains become fine-tuned and strengthened to utilize neuralresources optimally for their own offspring This neural recon-figuration is enduring for mothers after pregnancy and intoadolescence highlighting mothersrsquo strong selfndashchild overlapIn contrast adolescents are establishing a sense of identity byexpanding their social network spending more time and shar-ing their affection with others outside of the family (Larsonet al 1996) Unlike mothers adolescentsrsquo brains are morelikely to be sensitive to their social environment (Blakemoreand Mills 2014) particularly their peers (Nelson et al 2005)Therefore adolescentsrsquo mental representations are more flexi-ble depending on social contexts (Crone and Dahl 2012) Thusthis study suggests that adolescentsrsquo empathy is more condi-tional whereas mothers show empathy for their child that isstable and unconditional

The current findings elaborate upon previous theories(Rizzolatti et al 2001 Preston and De Waal 2002 Gallese2007 Keysers and Gazzola 2009) by showing how empathicexperiences arise based on the interaction of two differentprocesses the bottom-up perceptual encoding process and thetop-down social cognition process Theories of empathy pro-pose that empathy to others includes various mental andbehavioral phenomena such as shared and vicarious emo-tional experiences associated with prosocial (helping) reac-tions as a result of perceiving othersrsquo emotional states(Preston and De Waal 2002 Singer 2006 Preston 2007Decety 2011a) Therefore an approach to integrate these two

Fig 3 Negatively covaried social brain regions (circled area) with (A) the

increased familyndashself perceptual similarity of FFA (B) the degree of family rela-

tionship quality in familyndashself contrast of adolescent children See also Table 1

and 2 for other clusters

T-H Lee et al | 1921

empathy components (lsquoperception and actionrsquo or lsquobottom-upand top-down processingrsquo) with a continuum perspective iscritical for understanding empathic experiences The currentstudy demonstrates that perceptual representation similarityin the fusiform representing an initial mental representationof selfndashother emotional distress is an important gateway toneural activation involved in higher social cognitive process-ing Interestingly this two-component model was only validfor adolescents

In our study the quality of perceptual representation at theencoding level in the FFA was quantified using RSA as a form ofmulti-voxel pattern approach Employing neural patternapproach allows us to examine neural representational patternsin the perceptual region (ie FFA for facial expression) ratherthan simply examining whether this region shows differentialneural activation to self vs othersrsquo emotional distress (ie

univariate analysis) To our knowledge this is the first study toexamine how perceptual representation at the encoding level isrelated to the degree of empathy processing at the socialndashcogni-tive level However it should be noted that our model implyingthe temporal aspects of empathic experience from the initialencoding to later social cognition could not be tested directlyAlthough we built this model based on previous theories andempirical evidence in empathy (Rizzolatti et al 2001 Prestonand De Waal 2002 Jackson et al 2005 Singer 2006 Gallese2007 Lamm et al 2007 Lamm and Decety 2008 Keysers andGazzola 2009 Decety 2011a) the sluggish nature of the BOLDsignal precludes our ability to test the model in a temporal man-ner and thus the current results cannot confirm causalityexplicitly between these two distinct processes Experimentaldesigns that can disentangle these two processes in a causalmanner would help us to probe the temporal influences

Table 1 Brain regions which correlated with perceptual similarity on family-self condition in adolescents

Adolescent

MNI

SelfgtFamily H BA Z-score k x y z

Perceptual similarity negative covariationTemporal parietal junction (TPJ) L 39 421 279 34 68 44

R 39 417 468 42 64 48Medial PFC (mPFC) L 11 364 28 4 36 12Posterior cingulate gyrus (PCC) ndash ndash 412 209 2 28 28Angular gyrusinferior parietal lobe (IPL) R 40 355 63 46 52 54Anterior cingulate gyrus (ACC) ndash 32 378 194 6 42 4Brain stem ndash ndash 298 43 10 30 10Insula L 4 402 186 42 8 16

L 13 341 85 40 8 0R 1 275 28 44 18 16

Dorsal lateral PFC (DLPFC) L 46 317 53 40 44 6R 9 286 22 42 40 34

Inferior temporal gyrus (ITG) R 37 359 47 56 52 16DLPFC R 8 407 137 42 16 52Auditory cortex R 41 293 20 62 24 12Primary somatosensory cortex R 1 313 60 62 16 36Secondary somatosensory cortex R 40 311 20 42 26 18Primary motor cortex R 6 337 151 42 10 64Superior parietal lobule (SPL) R 7 311 22 30 54 62Superior temporal gyrus (STG) R 41 327 49 68 26 10TPJ R 40 395 181 64 24 42

R 40 338 45 56 36 52Fusiform gyrus R 37 365 67 40 56 16Thalamus L 50 333 151 14 30 8

Perceptual similarity positive covariation No significant activationsMothers

Perceptual similarity negative covariationAuditory Cortex L 41 332 58 40 22 10

L 41 308 29 42 34 10Insula L 6 335 88 52 2 2

L 13 29 20 42 10 0R 6 274 20 54 4 8

Primary somatosensory cortex L 4 42 88 64 12 18Secondary somatosensory cortex L 40 301 29 54 26 16Primary motor cortex R 6 341 39 64 4 16STG R 22 444 30 68 12 0

L 6 374 31 54 2 0Perceptual similarity positive covariation No significant activations

Notes Reported regions and their lsquolocal maximarsquo were at 50 probability locations on the HarvardndashOxford atlas with more than 20 voxels H hemisphere

BA Brodmann area k the number of voxels

1922 | Social Cognitive and Affective Neuroscience 2017 Vol 12 No 12

Table 2 Brain regions which correlated with mother-child relationship quality on family-self condition in adolescents

Adolescent

MNI

Selfgt Family H BA Z-score k x y z

Relationship quality negative covariationMedial PFC (mPFC) L 10 397 125 2 50 12

R 10 355 79 2 50 10L 10 345 74 6 54 4R 10 314 23 4 48 8

Posterior cingulate cortex (PCC) 31 322 212 4 30 46Temporal parietal junction (TPJ) L 19 382 394 44 66 20Anterior cingulate gyrus (ACC) 32 35 371 6 6 36Amygdala L 34 395 230 26 2 20

R 49 352 123 26 2 10Angular gyrusinferior parietal lobe (IPL) L 39 35 21 56 54 24

R 39 276 48 60 50 36Insula L 13 44 255 40 14 2

R 44 426 266 42 6 6R 13 421 250 38 8 6L 4 417 216 42 8 16

Orbitofrontal cortex (OFC) L 47 43 197 28 34 14R 337 176 22 12 16

mPFC L 10 384 240 2 62 2R 286 22 2 62 2

Auditory cortex R 41 385 59 46 28 12R 41 337 31 44 22 12L 41 314 30 40 22 10

Hippocampus L 54 376 219 28 16 18R 54 309 121 28 32 6

Inferior frontal gyrus (IFG) L 45 362 29 52 16 0L 45 335 54 40 22 6R 9 265 20 56 28 16

Inferior temporal gyrus (ITG) L 37 349 108 36 38 28R 20 306 24 58 30 26

Lateral occipital cortexmdashinferior division R 37 345 67 54 64 12L 19 309 32 50 70 12

Lingual gyrus L 19 318 70 8 60 2Middle temporal gyrus (extended to posterior superior temporal sulcus pSTS) R 21 398 38 62 2 18

R 37 363 106 60 54 10L 39 324 32 56 58 6R 21 306 115 66 24 20L 21 299 54 56 26 8

Basal ganglia pallidum R 51 365 87 22 6 2L 341 34 26 16 0

Putamen R 49 388 258 24 8 10L 49 375 273 30 14 0

Parahippocampal gyrus L 37 346 31 28 30 22Primary somatosensory cortex L 1 372 138 56 18 30

R 40 369 112 66 16 20Secondary somatosensory cortex R 40 459 85 58 24 18

L 40 324 119 48 34 20Superior temporal gyrus (STG) R 22 392 27 56 2 2

R 22 372 58 68 14 2L 22 353 23 42 16 4R 22 302 26 56 2 14

Primary motor cortex R 6 417 101 42 10 56Supplementary motor area R 6 286 21 6 4 52Precuneous L 18 296 31 14 58 16Supramarginal gyrus L 21 405 99 62 26 38

R 40 39 164 62 22 36R 40 315 80 56 36 52

Fusiform gyrus R 37 406 66 38 32 20

(continued)

T-H Lee et al | 1923

between the bottom-up and top-down processes in empathicexperiences

Nonetheless some evidence highlights the importance ofearly sensory-perception processing for later socialndashcognitiveprocessing For example emotion perception studies have dem-onstrated that emotional information is pre-evaluated duringthe early encoding in perception-sensory regions such assomatosensory and early visual cortex (eg Stolarova et al 2005Greening et al 2016) Importantly early sensory-perceptionbottom-up processing shifts the quality of later cognitivetop-down processing such that impairment of somatosensoryprocessing can impair recognition of face emotions at the latertop-down stage (Adolphs et al 2000) Similarly event-relatedpotential (ERP) research has shown that late top-down process-ing in face emotion recognition reflected by late the cognitivecomponent (400ndash800 ms) is significantly modulated dependingon how face stimuli are encoded at the early bottom-up stagerepresented at the early sensory-perception component (200ndash300 ms Lee et al 2010) Thus it is plausible that social brainregion changes observed in the current study are influenced byperceptual representation at the encoding level first Our regres-sion model using mediation also supports this pathway suchthat perceptual similarity in the FFA significantly mediated theassociation between relationship quality and social brain acti-vation to self and family

In the current study we recruited mothers and adolescentsusing dyadic recruitment (ie mothers and adolescents from

the same family) which is a strength of the sample Howeverthe sample size is relatively small precluding our ability toexamine sex differences among adolescents or between moth-ers and fathers Furthermore our adolescent-only sample doesnot allow us to probe why adolescents show less selfndashotheroverlap compared to adults (ie mothers) For example it is pos-sible that there may be linear increases in selfndashfamily overlapacross development as social cognitive abilities increase acrossthis age range Thus recruitment of pre-adolescent childrenwould further enable us to probe whether the effects we foundchange linearly with age Moreover examining other targets inthe task (eg peers) would help us tease apart whether thesource of low selfndashmother overlap is due to adolescents begin-ning to show greater selfndashother overlap with their peers as theytransition into adolescence (Nelson et al 2005) Longitudinalresearch and studies recruiting larger and different samplesincluding children adolescents peers and other family mem-bers (eg sibling and father) will help to unpack developmentaltrajectories in empathic responding for self and other

This study shows that relationship quality may set the stagefor socialndashcognitive processing and may positively affect braindevelopment in socialndashcognitive regions Such developmentmay have broader implications for empathy development andadolescentsrsquo ability to mentalize and take the perspective ofothersrsquo emotions Our results can inform future interventionsfor increasing empathy and related prosocial behavior by eluci-dating the role of relationship quality in promoting socialndash

Table 2 (continued)

Adolescent

MNI

Selfgt Family H BA Z-score k x y z

R 37 349 101 50 44 22R 37 299 25 32 68 14

Temporal pole R 38 394 281 56 8 16L 38 383 105 54 14 8

Thalamus L 50 324 128 10 16 4R 309 71 22 24 12

Relationship quality positive covariation No significant activationsMothers

Relationship quality negative covariation No significant activationsRelationship quality positive covariation No significant activations

ACC 24 353 50 0 28 16

Notes Reported regions and their lsquolocal maximarsquo were at 50 probability locations on the HarvardndashOxford atlas with more than 20 voxels H hemisphere BA

Brodmann area k the number of voxels

Fig 4 Perceptual similarity in the FFA mediates the link between perceived family connectedness and social brain activation in adolescents Note that asterisk indi-

cates statistical significance at Pfrac14005 (95 CI) based on 50 000 bootstrapping resampling

1924 | Social Cognitive and Affective Neuroscience 2017 Vol 12 No 12

between the bottom-up and top-down processes in empathicexperiences

Nonetheless some evidence highlights the importance ofearly sensory-perception processing for later socialndashcognitiveprocessing For example emotion perception studies have dem-onstrated that emotional information is pre-evaluated duringthe early encoding in perception-sensory regions such assomatosensory and early visual cortex (eg Stolarova et al 2005Greening et al 2016) Importantly early sensory-perceptionbottom-up processing shifts the quality of later cognitivetop-down processing such that impairment of somatosensoryprocessing can impair recognition of face emotions at the latertop-down stage (Adolphs et al 2000) Similarly event-relatedpotential (ERP) research has shown that late top-down process-ing in face emotion recognition reflected by late the cognitivecomponent (400ndash800 ms) is significantly modulated dependingon how face stimuli are encoded at the early bottom-up stagerepresented at the early sensory-perception component (200ndash300 ms Lee et al 2010) Thus it is plausible that social brainregion changes observed in the current study are influenced byperceptual representation at the encoding level first Our regres-sion model using mediation also supports this pathway suchthat perceptual similarity in the FFA significantly mediated theassociation between relationship quality and social brain acti-vation to self and family

In the current study we recruited mothers and adolescentsusing dyadic recruitment (ie mothers and adolescents from

the same family) which is a strength of the sample Howeverthe sample size is relatively small precluding our ability toexamine sex differences among adolescents or between moth-ers and fathers Furthermore our adolescent-only sample doesnot allow us to probe why adolescents show less selfndashotheroverlap compared to adults (ie mothers) For example it is pos-sible that there may be linear increases in selfndashfamily overlapacross development as social cognitive abilities increase acrossthis age range Thus recruitment of pre-adolescent childrenwould further enable us to probe whether the effects we foundchange linearly with age Moreover examining other targets inthe task (eg peers) would help us tease apart whether thesource of low selfndashmother overlap is due to adolescents begin-ning to show greater selfndashother overlap with their peers as theytransition into adolescence (Nelson et al 2005) Longitudinalresearch and studies recruiting larger and different samplesincluding children adolescents peers and other family mem-bers (eg sibling and father) will help to unpack developmentaltrajectories in empathic responding for self and other

This study shows that relationship quality may set the stagefor socialndashcognitive processing and may positively affect braindevelopment in socialndashcognitive regions Such developmentmay have broader implications for empathy development andadolescentsrsquo ability to mentalize and take the perspective ofothersrsquo emotions Our results can inform future interventionsfor increasing empathy and related prosocial behavior by eluci-dating the role of relationship quality in promoting socialndash

Table 2 (continued)

Adolescent

MNI

Selfgt Family H BA Z-score k x y z

R 37 349 101 50 44 22R 37 299 25 32 68 14

Temporal pole R 38 394 281 56 8 16L 38 383 105 54 14 8

Thalamus L 50 324 128 10 16 4R 309 71 22 24 12

Relationship quality positive covariation No significant activationsMothers

Relationship quality negative covariation No significant activationsRelationship quality positive covariation No significant activations

ACC 24 353 50 0 28 16

Notes Reported regions and their lsquolocal maximarsquo were at 50 probability locations on the HarvardndashOxford atlas with more than 20 voxels H hemisphere BA

Brodmann area k the number of voxels

Fig 4 Perceptual similarity in the FFA mediates the link between perceived family connectedness and social brain activation in adolescents Note that asterisk indi-

cates statistical significance at Pfrac14005 (95 CI) based on 50 000 bootstrapping resampling

1924 | Social Cognitive and Affective Neuroscience 2017 Vol 12 No 12

cognitive processing Thus interventions designed to enhancerelationship quality with others may promote greater selfndashotheroverlap thereby enhancing empathy and prosocial relation-ships in youth

To our knowledge this is the first study to directly examineempathy processes with a continuum perspective from the ini-tial perceptual representation to the later mentalizing stage atthe neural level by employing both multivariate (ie representa-tional neural pattern analysis) and univariate approaches (iegeneral linear model) Moreover by scanning both mothers andtheir children we compared how adolescentsrsquo and their moth-ersrsquo empathy for their family and the self are similar Our resultssuggest that mothers have unconditional empathic responsesto their childrsquos emotional distress based on higher selfndashchildoverlap in their mental representation whereas adolescentsrsquoempathy is more conditional This study contributes to ourknowledge about empathy processes with the critical impor-tance of perceptual representation in mentalizing othersrsquo emo-tional distress

Funding

This work was supported by the National Institute of Health(1R01DA039923) and generous funds from the Departmentof Psychology at the University of Illinois UrbanaChampaign

Conflict of interest None declared

ReferencesAbraham E Raz G Zagoory-Sharon O Feldman R (2017)

Empathy networks in the parental brain and their long-termeffects on childrenrsquos stress reactivity and behavior adaptationNeuropsychologia

Acock AC Bengtson VL (1980) Socialization and attributionprocesses actual versus perceived similarity among parentsand youth Journal of Marriage and the Family 42(3) 501ndash15

Adams RB Rule NO Franklin RGet al (2010) Cross-culturalreading the mind in the eyes an fMRI investigation Journal ofCognitive Neuroscience 22(1) 97ndash108

Adolphs R (2009) The social brain neural basis of social knowl-edge Annual Review of Psychology 60 693ndash716

Adolphs R Damasio H Tranel D Cooper G Damasio AR(2000) A role for somatosensory cortices in the visual recogni-tion of emotion as revealed by three-dimensional lesion map-ping Journal of Neuroscience 20(7) 2683ndash90

Amodio DM Frith CD (2006) Meeting of minds the medialfrontal cortex and social cognition Nature Reviews Neuroscience7(4) 268ndash77

Azevedo RT Macaluso E Avenanti A Santangelo VCazzato V Aglioti SM (2013) Their pain is not our pain brainand autonomic correlates of empathic resonance with thepain of same and different race individuals Human BrainMapping 34(12) 3168ndash81

Batson CD (2009) These Things Called Empathy eight Related butDistinct Phenomena Cambridge MA MIT press

Blakemore S-J Mills KL (2014) Is adolescence a sensitiveperiod for sociocultural processing Annu Rev Psychol 65187ndash207

Cheon BK Mathur VA Chiao JY (2010) Empathy as culturalprocess insights from the cultural neuroscience of empathyWorld Cultural Psychiatry Research Review 5(1) 32ndash42

Collins WA Steinberg L (2006) Adolescent Development inInterpersonal Context Hoboken NJ Wiley

Crone EA Dahl RE (2012) Understanding adolescence as aperiod of socialndashaffective engagement and goal flexibilityNature Reviews Neuroscience 13(9) 636ndash50

Davis MH Conklin L Smith A Luce C (1996) Effect of per-spective taking on the cognitive representation of persons amerging of self and other Journal of Personality and SocialPsychology 70(4) 713ndash26

De Waal FB (2008) Putting the altruism back into altruism theevolution of empathy Annual Review of Psychology 59(1)279ndash300

Decety J (2005) Perspective taking as the royal avenue to empa-thy In Malle B and Hodges S D (Eds) Other Minds HowHumans Bridge the Divide Between Self and Others (pp 135-149)New York NY Guilford Press

Decety J (2011a) Dissecting the neural mechanisms mediatingempathy Emotion Review 3(1) 92ndash108

Decety J (2011) The neuroevolution of empathy Annals of theNew York Academy of Sciences 1231(1) 35ndash45

Decety J Lamm C (2006) Human empathy through the lens ofsocial neuroscience The Scientific World Journal 6 1146ndash63

Decety J Sommerville JA (2003) Shared representationsbetween self and other a social cognitive neuroscience viewTrends in Cognitive Sciences 7(12) 527ndash33

Driscoll K Pianta RC (2011) Mothersrsquo and fathersrsquo perceptionsof conflict and closeness in parent-child relationships duringearly childhood Journal of Early Childhood amp Infant Psychology (7)1ndash24

Eisenberg N Eggum ND (2009) Empathic responding sympa-thy and personal distress In Decety J amp Ickes W (Eds) TheSocial Neuroscience of Empathy (pp 71-83) Cambridge MA MITPress

Fuligni AJ Eccles JS (1993) Perceived parent-child relation-ships and early adolescentsrsquo orientation toward peersDevelopmental Psychology 29(4) 622ndash32

Galinsky AD Ku G Wang CS (2005) Perspective-taking andself-other overlap fostering social bonds and facilitating socialcoordination Group Processes amp Intergroup Relations 8(2) 109ndash24

Gallese V (2007) Before and below lsquotheory of mindrsquo embodiedsimulation and the neural correlates of social cognitionPhilosophical Transactions of the Royal Society B Biological Sciences362(1480) 659ndash69

Ghuman AS Brunet NM Li Y et al (2014) Dynamic encodingof face information in the human fusiform gyrus NatureCommunications 5(5672) 1ndash10

Goubert L Craig K Buysse A (2009) Perceiving others in painexperimental and clinical evidence on the role of empathy InDecety J and Ickes W (Eds) The Social Neuroscience of Empathy(pp 153ndash65) Cambridge MA MIT Press

Goubert L Vervoort T Sullivan MJ Verhoeven K CrombezG (2008) Parental emotional responses to their childrsquos painthe role of dispositional empathy and catastrophizing abouttheir childrsquos pain The Journal of Pain 9(3) 272ndash9

Greening SG Lee TH Mather M (2016) Individual differencesin anticipatory somatosensory cortex activity for shock is posi-tively related with trait anxiety and multisensory integrationBrain sciences 6(1) 2

Ho SS Konrath S Brown S Swain JE (2014) Empathy andstress related neural responses in maternal decision makingFrontiers in neuroscience 8 152ndash78

Hodges SD Klein KJ (2001) Regulating the costs of empathythe price of being human The Journal of Socio-Economics 30(5)437ndash52

T-H Lee et al | 1925

Hoekzema E Barba-Muller E Pozzobon C et al(2016)Pregnancy leads to long-lasting changes in human brain struc-ture Nature Neuroscience 20(2) 287ndash96

Jackson PL Decety J (2004) Motor cognition a new paradigmto study selfndashother interactions Current Opinion in Neurobiology14(2) 259ndash63

Jackson PL Meltzoff AN Decety J (2005) How do we perceivethe pain of others A window into the neural processesinvolved in empathy NeuroImage 24(3) 771ndash9

Jenkinson M Bannister P Brady M Smith S (2002) Improvedoptimization for the robust and accurate linear registrationand motion correction of brain images NeuroImage 17(2)825ndash41

Jenkinson M Smith S (2001) A global optimisation method forrobust affine registration of brain images Medical Image

Analysis 5(2) 143ndash56Kanwisher N McDermott J Chun MM (1997) The fusiform

face area a module in human extrastriate cortex specializedfor face perception Journal of Neuroscience 17(11) 4302ndash11

Keysers C Gazzola V (2009) Expanding the mirror vicariousactivity for actions emotions and sensations Current Opinion

in Neurobiology 19(6) 666ndash71Kriegeskorte N Mur M Bandettini P (2008) Representational

similarity analysismdashconnecting the branches of systems neu-roscience Frontiers in Systems Neuroscience 2 1ndash28

Lamm C Batson CD Decety J (2007) The neural substrate ofhuman empathy effects of perspective-taking and cognitiveappraisal Journal of Cognitive Neuroscience 19(1) 42ndash58

Lamm C Decety J (2008) Is the extrastriate body area (EBA)sensitive to the perception of pain in others Cerebral Cortex18(10) 2369ndash73

Larson RW Richards MH Moneta G Holmbeck G DuckettE (1996) Changes in adolescentsrsquo daily interactions with theirfamilies from ages 10 to 18 disengagement and transforma-tion Developmental Psychology 32(4) 744

Lee K-Y Lee T-H Yoon S-J et al (2010) Neural correlates oftopndashdown processing in emotion perception an ERP study ofemotional faces in white noise versus noise-alone stimuliBrain Research 1337 56ndash63

Leibenluft E Gobbini MI Harrison T Haxby JV (2004)Mothersrsquo neural activation in response to pictures of their chil-dren and other children Biological Psychiatry 56(4) 225ndash32

Mathur VA Harada T Lipke T Chiao JY (2010) Neural basisof extraordinary empathy and altruistic motivationNeuroImage 51(4) 1468ndash75

Mikulincer M Gillath O Halevy V Avihou N Avidan SEshkoli N (2001) Attachment theory and reactions to othersrsquoneeds evidence that activation of the sense of attachmentsecurity promotes empathic responses Journal of Personality

and Social Psychology 81(6) 1205Morelli SA Rameson LT Lieberman MD (2014) The neural

components of empathy predicting daily prosocial behaviorSocial Cognitive and Affective Neuroscience 9(1) 39ndash47

Morrison S Decety J Molenberghs P (2012) The neuroscienceof group membership Neuropsychologia 50(8) 2114ndash20

Mumford JA Turner BO Ashby FG Poldrack RA (2012)Deconvolving BOLD activation in event-related designs formultivoxel pattern classification analyses NeuroImage 59(3)2636ndash43

Nelson E Leibenluft E McClure E Pine D (2005) The socialre-orientation of adolescence a neuroscience perspective on

the process and its relation to psychopathology PsychologicalMedicine 35(2) 163ndash74

OrsquoCraven KM Kanwisher N (2000) Mental imagery of facesand places activates corresponding stimulus-specific brainregions Journal of Cognitive Neuroscience 12(6) 1013ndash23

Olson DH Sprenkle DH Russell CS (1979) Circumplexmodel of marital and family systems I Cohesion and adapt-ability dimensions family types and clinical applicationsFamily Process 18(1) 3ndash28

Preston SD (2007) A Perception-Action Model for EmpathyCambridge UK Cambridge University Press

Preston SD De Waal FB (2002) Empathy its ultimate andproximate bases Behavioral and Brain Sciences 25(01) 1ndash20

Proulx CM Helms HM (2008) Mothersrsquo and fathersrsquo perceptionsof change and continuity in their relationships with young adultsons and daughters Journal of Family Issues 29(2) 234ndash61

Qu Y Fuligni AJ Galvan A Telzer EH (2015) Buffering effectof positive parentndashchild relationships on adolescent risk tak-ing a longitudinal neuroimaging investigation DevelopmentalCognitive Neuroscience 15 26ndash34

Rameson LT Morelli SA Lieberman MD (2012) The neuralcorrelates of empathy experience automaticity and prosocialbehavior Journal of Cognitive Neuroscience 24(1) 235ndash45

Rizzolatti G Fogassi L Gallese V (2001) Neurophysiologicalmechanisms underlying the understanding and imitation ofaction Nature Reviews Neuroscience 2(9) 661ndash70

Ruiz S Gonzales N Formoso D (1998) Paper Presentedat the Multicultural Multidimensional Assessment ofParent-Adolescent Conflict The Biennial Meeting 1998 of theSociety for Research on Adolescence San Diego CA

Sabatinelli D Fortune EE Li Q et al (2011) Emotional percep-tion meta-analyses of face and natural scene processingNeuroImage 54(3) 2524ndash33

Saxe R Carey S Kanwisher N (2004) Understanding otherminds linking developmental psychology and functional neu-roimaging Annual Review of Psychology 55(1) 87ndash124

Saxe R Moran JM Scholz J Gabrieli J (2006) Overlappingand non-overlapping brain regions for theory of mind and selfreflection in individual subjects Social Cognitive and AffectiveNeuroscience 1(3) 229ndash34

Singer T (2006) The neuronal basis and ontogeny of empathy andmind reading review of literature and implications for futureresearch Neuroscience amp Biobehavioral Reviews 30(6) 855ndash63

Singer T Seymour B OrsquoDoherty J Kaube H Dolan RJ FrithCD (2004) Empathy for pain involves the affective but notsensory components of pain Science 303(5661) 1157ndash62

Smith S (2002) Fast robust automated brain extraction HumanBrain Mapping 17(3) 143ndash55

Smith SM Jenkinson M Woolrich MW et al (2004)Advances in functional and structural MR image analysis andimplementation as FSL NeuroImage 23 208ndash19

Stolarova M Keil A Moratti S (2005) Modulation of the C1 vis-ual event-related component by conditioned stimuli evidencefor sensory plasticity in early affective perception Cerebral cor-tex 16(6) 876ndash87

Telzer EH Gonzales N Fuligni AJ (2014) Family obligationvalues and family assistance behaviors protective and riskfactors for MexicanndashAmerican adolescentsrsquo substance useJournal of Youth and Adolescence 43(2) 270ndash83

Tsai KM Telzer EH Fuligni AJ (2013) Continuity and discon-tinuity in perceptions of family relationships from adoles-cence to young adulthood Child Development 84(2) 471ndash84

1926 | Social Cognitive and Affective Neuroscience 2017 Vol 12 No 12

Tyler TR Degoey P (1995) Community family and the socialgood the psychological dynamics of procedural justice andsocial identification Nebraska Symposium on Motivation 42 53ndash91

Visser RM Scholte HS Kindt M (2011) Associative learningincreases trial-by-trial similarity of BOLD-MRI patterns TheJournal of Neuroscience 31(33) 12021ndash8

Wager TD Davidson ML Hughes BL Lindquist MAOchsner KN (2008) Prefrontal-subcortical pathways media-ting successful emotion regulation Neuron 59(6) 1037ndash50

Zuo X Han S (2013) Cultural experiences reduce racial bias inneural responses to othersrsquo suffering Culture and Brain 1(1)34ndash46

T-H Lee et al | 1927

• nsx125-FN1
• nsx125-TF1
• nsx125-TF2

Tyler TR Degoey P (1995) Community family and the socialgood the psychological dynamics of procedural justice andsocial identification Nebraska Symposium on Motivation 42 53ndash91

Visser RM Scholte HS Kindt M (2011) Associative learningincreases trial-by-trial similarity of BOLD-MRI patterns TheJournal of Neuroscience 31(33) 12021ndash8

Wager TD Davidson ML Hughes BL Lindquist MAOchsner KN (2008) Prefrontal-subcortical pathways media-ting successful emotion regulation Neuron 59(6) 1037ndash50

Zuo X Han S (2013) Cultural experiences reduce racial bias inneural responses to othersrsquo suffering Culture and Brain 1(1)34ndash46

T-H Lee et al | 1927

• nsx125-FN1
• nsx125-TF1
• nsx125-TF2