culture modulates brain activity during empathy with anger.pdf

7/27/2019 Culture modulates brain activity during empathy with anger.pdf

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Culture modulates brain activity

during empathy with anger

Moritz de Greck1, Zhenhao Shi1, Gang Wang1,

Xiangyu Zuo1, Xuedong Yang2, Xiaoying Wang2,

Georg Northoff3, Shihui Han1

1 Department of Psychology, Peking University, Beijing, China2 Department of Radiology, Peking University First Hospital, Bei-

jing, China3 Institute of Mental Health Research, University of Ottawa, Otta-

wa, Canada

This is a free version of the paper NIMG-11-838R1

which has been peer-reviewed and accepted

by NeuroImage.

Corresponding authors:

Dr. med. Moritz de Greck

& Shihui Han, PhD

Department of Psychology

Peking University

5 Yiheyuan Road

100871 Beijing

China

Phone: 0086 1368 358 4552

Fax: 0086 106276 1081Email: [email protected], [email protected]

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Culture modulates empathy with anger

Abstract

Interdependent cultures (such asthe Chinese) and independent cul-tures (such as the German) differ

in their attitude towards harmonythat is more valued in interdepen-dent cultures. Interdependent andindependent cultures also differ intheir appreciation of anger - anemotion that implies the disrup-tion of harmony.

The present study investigated ifinterdependent and independent

cultures foster distinct brain acti-vity associated with empathic pro-cessing of familiar angry, familiarneutral, and unfamiliar neutral fa-ces.Using functional MRI, we scannedChinese and German healthy sub-jects during an intentional empathytask, a control task (the evaluati-on of skin color), and a baselinecondition. The subject groups werematched with regard to age, gen-der, and education.

Behaviorally, Chinese subjects de-scribed themselves as significantlymore interdependent compared toGerman subjects. The contrast in-tentional empathy for familiar an-gry > baseline revealed several

regions, including the left inferiorfrontal cortex, the left supplemen-tary motor area, and the left insula,

that showed comparable hemody-namic responses in both groups.However, the left dorsolateral pre-frontal cortex had stronger hemo-dynamic responses in Chinese sub-jects in the contrast intentionalempathy for familiar angry > ba-seline. Germans, in contrast, sho-wed stronger hemodynamic respon-ses in the right temporo-parietal

junction, right inferior and superi-or temporal gyrus, and left middleinsula for the same contrast. He-modynamic responses in the lat-ter three brain regions correlatedwith interdependences scores overall subjects.

Our results suggest that enhancedemotion regulation during empathywith anger in the interdependent li-festyle is mediated by the left dor-solateral prefrontal cortex. Increa-sed tolerance towards the expres-sion of anger in the independentlifestyle, in contrast, is associatedwith increased activity of the rightinferior and superior temporal gy-rus and the left middle insula.

Key words:

fmri, transcultural, emotion, empa-thy, anger

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Introduction

Interdependence describes a lifestyle, inwhich an individual is attuned to thesocial environment, adjusts his behavior

to others, and takes the perspective ofothers. Independence, in contrast, refersto a lifestyle, in which an individual pri-marily refers to his own thoughts andfeelings (Markus and Kitayama, 2010;Chiao et al., 2009). Typically, most Asi-an cultures engage an interdependentlifestyle, whereas in most Western cul-tures an independent lifestyle is preva-lent (Markus and Kitayama, 1991; Chiao

et al., 2009). Interestingly, both lifesty-les do not completely exclude each other.Rather, they can coexist to some degreein one and the same individual (Singelis,1994). Interdependent and independentlifestyles are considered to be responsiblefor a large amount of cultural differencesin emotional experience, cognition andbehavior (Markus and Kitayama, 1991).

A key concept, which is appreciated verydifferently in interdependent and inde-pendent cultures, is harmony. Harmony,which describes the balance, positivemood and social peace within a group,is important in interdependent culturesand often rooted in their cultural traditi-ons (Markus and Kitayama, 1991, Uno,1991 as described in Kim and Markus,1999). Independent cultures, in contrast,rather stress the importance of uniquen-

ess (Kim and Markus, 1999).For instance, as shown by Kwan et al.(1997), relationship harmony is moreimportant for life satisfaction in inter-dependent cultures (in this study HongKong students) compared to indepen-dent cultures (namely US students). Inindependent cultures (such as the Uni-ted states or Germany), in contrast, lifesatisfaction is closer related to the affec-

tive well-being of the individuals (Suhet al., 1998). Interestingly, in the study

conducted by Suh et al. Germans sho-wed the strongest correlation of affectivewell-being and life satisfaction.

In addition, two studies showed that, re-lative to individuals from independentcultures, individuals in interdependentcultures can tolerate disharmony lessand are more prone to react with depres-sive reactions to negative social events(Tafarodi and Smith, 2001; Chen et al.,2006). Individuals from interdependentcultures also seek less social support inthe case of stressing events in order to

maintain social harmony (Taylor et al.,2004).

Given the differential significance ofharmony for interdependent and inde-pendent cultures, one might also expectcultural differences in the appreciationof anger (Kvecses, 2000) because a cru-cial characteristic of anger is the disrup-tion of harmony (Markus and Kitaya-ma, 1991). Indeed, it is argued that theexpression of anger is less prevalent ininterdependent than in independent cul-tures (Markus and Kitayama, 1991). Ina study investigating the reaction of 11month old infants towards vocal expres-sions of emotions in the voice of theirmothers, infants from interdependentcultures reacted stronger to the vocalexpression of anger (but not joy or fe-ar) compared to independent cultures

(Miyake et al., 1986). The authors con-cluded, that the expression of anger hap-pens less often in interdependent cultu-res (and is related to extreme situations).Moreover, in interdependent cultures (inthis case China), the control of angeris related to high social functioning ofschool children (Zhou et al., 2004). In ad-dition, individuals from interdependentcultures tolerate less anger. When anger

was expressed in simulated negotiations(as part of recent study conducted by

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Adam and colleagues), Asians and Asi-an Americans made smaller concessions.In contrast, European Americans madelarger concessions (Adam et al., 2010).Moreover, there are differences between

interdependent and independent cultu-res concerning the suppression of anger.The suppression of anger can lead todepression in individuals from interde-pendent and independent cultures; ho-wever, the link between suppressed angerand depression is significantly strongerin interdependent cultures (Cheung andPark, 2010; Park et al., 2010).Interestingly, there is a special psychia-

tric disorder hwa-byung (English: firedisease or anger disease), which is ex-plicitly associated with the suppressionof anger and strictly bound to the Ko-rean (i.e. interdependent) culture (Min,2008; Min et al., 2009).

A suitable approach to investigate cultu-ral differences in emotional processing isto implement an empathy task. Regar-

ding this, empathy implies the capabilityto understand and share the emotionalstates of other creatures without losingthe ability to differentiate between onesown feelings and the feelings of others(Decety and Jackson, 2004; Preston andde Waal, 2002).To our knowledge, no study examinedcultural differences in emotional em-pathy so far. One study however, ex-plored differences in brain activity du-

ring Theory of Mind (TOM) - a pa-radigm, which is related to empathy -between interdependent and indepen-dent individuals. Investigating Americanand Japanese children using a cartoonTOM task, Kobayashi et al. (2007) foundstronger hemodynamic responses in theright temporo-parietal junction (TPJ) inAmerican children. The authors sugge-sted that diminished TPJ activity during

TOM might reflect a demoted sense of

self-other distinction in the Japanese cul-ture.

The current study investigated diffe-rences in brain activity during em-

pathy with anger between individualsstemming from interdependent and in-dependent cultures. For this, we usedfMRI and an empathy paradigm, whichwas recently introduced by our group(de Greck et al., 2011). The paradigmallowed us to investigate automatic aswell as intentional empathic responses,and to control for the effects of emotionand familiarity. (As recently shown by

Xu et al. (2009), in particular familiari-ty can significantly modulate empathicprocesses.) We recruited two groups ofhealthy subjects from an interdependentculture (namely China) and from an in-dependent culture (namely Germany).With regard to the avoiding attitude to-wards anger prevalent in interdependentcultures, we hypothesized less activity inChinese subjects (compared to German

subjects) during empathy with anger inregions typically involved in emotionalempathy and emotional processing suchas insula, anterior cingulate cortex, in-ferior frontal cortex and superior tem-poral sulcus (Blair et al., 1999; Carret al., 2003; de Greck et al., 2011; Hoo-ker et al., 2008, 2010; Jabbi et al., 2007;Jabbi and Keysers, 2008; Ochsner et al.,2004a; Phillips et al., 1997; Sprengel-meyer et al., 1998; Wicker et al., 2003).

In addition, we expected more activityin Chinese in brain regions connected toemotion regulation, such as the prefron-tal cortex (MacDonald et al., 2000; Ochs-ner et al., 2004b; Ochsner and Gross,2005; Vanderhasselt et al., 2006).Finally, considering the familiarity ofempathy and TOM, we expected stron-ger activity in the right TPJ in Germansubjects (Kobayashi et al., 2007).

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Methods

Participants

A group of Chinese students (n=16) anda group of German students (n=16) were

recruited in this study. Both groups we-re scanned in Beijing, China, using thesame fMRI scanner. Table 1 illustratessubjects information about the two cul-tural groups.

The study was approved by a local ethicscommittee. After a detailed explanationof the study design and any potential

risks, all subjects gave their written in-formed consent. All subjects were reim-bursed for their participation.

Table 1

Chinese Germans

Number 16 16

Age mean 22.9 years mean 23.3 years1

95% CI2: 22.3 - 23.5 years 95% CI: 22.2 - 24.3 years

Gender 10 f / 6 m3 10 f / 6 m

Culture 16 Han Chinese 16 Germansraised in China by raised in Germany by

Chinese parents German parents

Occupation 16 students 16 students

Table 1: Characteristics of the two subject groups1 There was no significant difference regarding the age of both groups(t(30)=0.681, p[two-tailed]=0.501). 2 The 95% confidence interval. 3 Inaddition, there was no significant difference with regard to the genderdistribution in both groups (2(1)=1, p=0.317).

Paradigm

Experimental designThe fMRI experiment was divided into

7 blocks of 312 s duration each. Prior toentering the scanner each subject read

detailed information of the paradigm intheir native language and completed a

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couple of trial runs in order to familia-rize fully with the task. While lying inthe scanner, the stimuli were displayedusing the software package Presentati-on (Neurobehavioral Systems, Albany,

CA, USA) and were projected onto amatte screen via an LCD projector, vi-sible through a mirror mounted on thehead coil. Each block started with 10spause to control for epi-saturation ef-fects. A total number of 24 trials (12intentional empathy trials and 12 trialsskin color evaluation trials) were pre-sented in a randomized order in eachblock. Figure 1 illustrates the intentio-

nal empathy task, the control task andthe baseline condition.

StimuliTwo sets of stimuli were used for Chine-se and German subjects. Each stimulusset consisted of 12 different face stimuli- four stimuli (two female, two male) ofeach condition (namely familiar angry,familiar neutral, and unfamiliar neu-

tral).Stimuli for Germans subjects for theconditions familiar angry and familiarneutral were taken from the Japane-se and Caucasian Facial Expressions ofEmotion (JACFEE) and Neutral Faces(JACNeuF)-battery provided by Mat-sumoto and Ekman (Matsumuto and

Ekman, 1988). Stimuli for German sub-jects for the condition unfamiliar neu-tral were photographed and preproces-sed for presentation by our own group(de Greck et al., 2011). These pictures

were taken in front of a comparable back-ground and under comparable conditionsto match them as close as possible to thefour pictures taken from the JACNeuFbattery.Stimuli for Chinese subjects for the con-dition familiar neutral were exactly tho-se stimuli, as presented to German sub-jects in the condition unfamiliar neu-tral. Analogously, stimuli for Chinese

subjects for the condition unfamiliarneutral were exactly the same stimuli aspresented to German subjects in the con-dition familiar neutral (i.e. these stimu-li were taken from the JACNeuF-picturebattery). Stimuli for Chinese subjects forthe condition familiar angry were alsophotographed and preprocessed for pre-sentation by our own group, as describedabove. Each stimulus was presented twi-

ce during each block: once during inten-tional empathy, once during skin colorevaluation.The term familiar as used in our studyrefers to the concept of race-based fa-miliarity and not personal familiarity(Liew et al., 2011).

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Figure 1. Paradigm

A cue indexed the task at the start of each trial. The cue had the shape of ablack circle with a small white circle in the North- or South-position. Thewhite circle in the North-position indexed an intentional empathy trial; the

white circle in the South-position cued a skin color evaluation trial. Inintentional empathy trials, subjects were instructed to empathize withperceived emotional or neutral faces. After a 4 s lasting viewing period,subjects were supposed to rate their subjective impression of empathycapability in the evaluation period, which lasted for 3.5 s. By virtuallymoving a red bar, they were instructed to make a statement on a visualanalogue scale. In control trials subjects were instructed to concentrate onthe skin color of the presented faces. Analogue to the intentional empathytask, a 4s lasting viewing period was followed by a 3.5s lasting evaluationperiod. After every trial a short inter trial interval of 1.2s to 1.8s duration

was presented. The face stimuli consisted of familiar angry, familiar neutral,and unfamiliar neutral faces. Both groups of subjects had different sets ofstimuli: For Chinese subjects familiar faces consisted of Chinese faces and

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unfamiliar faces consisted of Caucasian faces. For German subjects familiarfaces consisted of Caucasian faces and unfamiliar faces consisted of Chinesefaces. Because of time constraints, we did not include unfamiliar angrystimuli. After every 6 trials, a baseline trial was presented; during baselinetrials, the fixation cross was displayed for 6s or 7s.

Psychological scales

Interpersonal Reactivity Index (IRI)The Interpersonal Reactivity Index(IRI, Davis, 1983) is a commonly usedself evaluation questionnaire to measu-re the subjective impression of differentempathic skills. The IRI uses four sub-scales related to empathic fantasy, em-pathic concern, personal distress, andperspective taking.

Self-Construal Scale (SCS)The Self-Construal Scale (SCS, Singe-lis, 1994) bases on the concept of interde-pendent and independent self-construals,

which was introduced by Markus & Ki-tayama (Markus and Kitayama, 1991,2010). The SCS implements two scalesrelated to interdependence and inde-pendence.

Behavioral data analysis

Behavioral data where analy-zed using the software packagesPERL (http://www.perl.org) and R

(http://www.r-project.org/, R Develop-ment Core Team, 2009). Repeated mea-surements Analyses of Variance (ANO-VAs) and post-hoc independent samplest-tests were used to test for significantdifferences; Spearman correlations we-re implemented to analyze associationsbetween different behavioral scores.

fMRI data acquisition

The study was conducted using a Ge-neral Electrics 3 Tesla Magnetic Reso-nance Imaging Scanner. Functional data

(24 slices parallel to the AC-PC plane,slice thickness 5mm, TR 2000ms, TE30ms, flip angle =90 , 64 x 64 voxelsper slice with 3.75mm x 3.75mm x 5mm)were acquired in seven scanning sessionscontaining 156 volumes per session foreach subject. In addition, T1-weightedimages of each subject were recorded.

fMRI data analysis

The statistical analysis of thefMRI data was performed usingthe software packages Analysis ofFunctional NeuroImages (AFNI,http://afni.nimh.nih.gov/afni/, Cox,1996), Python (http://www.python.org),

PERL (http://www.perl.org) and R(http://www.r-project.org/, R Develop-ment Core Team, 2009).The first three volumes were discardedto compensate for saturation effects. Allfunctional images were slice-time cor-rected with reference to the acquisitiontime of the first slice and corrected formotion artifacts by realignment to thefirst volume. The images were spatially

normalized to a standard EPI-templateprovided by AFNI (TT_EPI) and re-sampled to 3mm x 3mm x 3mm. Final-ly, all functional images were smoothedwith an isotropic 6mm full-width halfmaximum Gaussian kernel. T1-weightedimages of each subject were normalizedto a standard T1-template provided byAFNI (TT_avg152T1).For each subject, regressors of interest

were created by the convolution of acanonical, fixed shape hemodynamic re-sponse function with the according sti-

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mulus time functions (Josephs et al.,1997). Regarding this, all relevant peri-ods (namely viewing periods with cor-rect later responses for both tasks andall three conditions, evaluation periods

with correct responses for both tasksand all three conditions, viewing andevaluation periods for tasks with incor-rect responses, and the baseline event)were included in the model. In additi-on, six movement parameters resultingfrom motion correction, as well as nineregressors for the 3rd degree polynomialmodel of the baseline of each block wereincluded as regressors to account for any

residual effects of head motion and ba-seline fluctuations respectively. Contrastimages were calculated by employing li-near contrasts to the parameter estima-tes for the regressors of each event. Theresulting contrast images were then sub-mitted to a second level random-effectsanalysis. Here, one-sample t-tests (inclu-ding the 16 Chinese and the 16 Germansubjects in one group) and independent

two sample t-tests (comparing the 16Chinese and the 16 German subjects)were applied (Friston et al., 1994). Tocontrol for the multiple testing problem,we performed a false discovery rate cor-rection (Nichols and Hayasaka, 2003)and calculated family-wise error proba-bilities. The anatomical localization andlabeling of significant activations wereassessed with reference to the standardstereo-tactic atlas of Talairach & Tour-

noux (Talairach and Tournoux, 1988)and by superimposition of the group con-trast images on a mean brain generatedby an average of each subjects normali-

zed T1-weighted image.In a second step, we performed a stati-stical analysis of the raw fMRI signals.Using the significant clusters from thedifferent contrasts as regions of interest,

we extracted fMRI signal timecoursesfrom activations found in the second le-vel analysis using sphere shaped regionsof interest with a radius of 5mm. Thetimecourses were linearly interpolatedand normalized with respect to a timewindow ranging from 0s to 30s after theonset of each event. fMRI signal chan-ges of every event were calculated withregard to the fMRI signal value of the

onset of the according event. Mean nor-malized fMRI signal values from twofollowing time steps (6s to 8s after on-set of the according event) were inclu-ded in the statistical analysis. We usedpaired t-tests, to analyze the effects ofthe factors task ([intentional empathyfor familiar angry+intentional empathyfor familiar neutral+intentional empa-thy unfamiliar neutral]-[control for fa-

miliar angry+control for familiar neu-tral+control for unfamiliar neutral]),emotion (intentional empathy for fa-miliar angry-intentional empathy forfamiliar neutral), and familiarity (in-tentional empathy for familiar neutral-intentional empathy unfamiliar neu-tral). In addition, Spearman correlati-ons were applied to analyze the associati-on of different behavioral scores (namelythe intra-scanner empathy ratings for

angry faces, the IRI personal distressscore and the SCS interdependence sco-re) with hemodynamic responses of ourregions of interest.

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Results

Behavioral results

Intra-scanner empathy ratings

We used a 2x3 factorial repeated measu-re analysis of variance (ANOVA) withGroup (Chinese vs. Germans) as abetween-subjects factor and Conditi-on (familiar angry, familiar neutral,and unfamiliar neutral) as a within-subjects factor to analyze mean intra-scanner empathy ratings. We detec-ted a significant main effect of Condi-tion (F(2,60)=50.793, p


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We tested for correlations betweenthe different behavioral scores (na-mely the intra-scanner empathy ra-tings for familiar angry, personaldistress, and interdependence) using

Spearman correlations. We found asignificant negative correlation bet-ween intra-scanner empathy ratingsduring familiar angry and interde-

pendence scores (r[Spearman]=-0.354,p[two-tailed]=0.047*; Figure 2.d). Wedid, however, neither find a signifi-cant correlation of personal distressscores with interdependence scores

(r[Spearman]=-0.070, p[two-tailed]=0.704) nora correlation of personal distress sco-res with intra-scanner empathy ratings(r[Spearman]=0.245, p[two-tailed]=0.176).

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Figure 2. Behavioral Results

2.a Intra-scanner empathy ratings.German subjects compared to Chinese subjects reported significantly moresubjective empathy during the condition unfamiliar neutral, whilst therewere no differences between both groups for the conditions familiar angry

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and familiar neutral.

2.b Interpersonal Reactivity Index (IRI).German subjects described significantly less personal distress and moreempathic concern compared to Chinese subjects. However, we did not find

significant differences with regard to the IRI scales empathic fantasy andperspective taking.

2.c Self-Construal Scale (SCS).Chinese subjects scored significantly higher with regard to theinterdependence scale of the SCS. There was, however, no difference withregard to the independence scale.

2.d Correlation between interdependence and intra-scanner empathy ratings.Subjects interdependence scores predicted their intra-scanner empathy

ratings for the condition familiar angry. Subjects, who described themselvesas interdependent, reported less subjective empathic understanding for angryfaces during the experiment.

fMRI results

Intentional empathy for familiar angry> baseline - transcultural constantsWe implemented a whole brain analy-sis of all 32 subjects to investigate thetranscultural constants of the contrastintentional empathy for familiar angry> baseline. Regarding this, we calcu-lated voxel-wise one-sample t-tests for

both groups and implemented an inclu-sive masking analysis that included onlythose clusters which showed significantactivity in both groups. Brain regionswith transcultural constant brain activi-ty included the bilateral inferior frontalgyrus, the bilateral supplementary motorarea, bilateral anterior insula, bilateralparahippocampal gyrus, and other areas(see Table 2).

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Table 2

no region BA x, y, z [mm] n p[FWE](C) p[FWE](G)

2.01 left inferior frontal gyrus 6 -42 -3 24 2342


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Table 2: Intentional empathy for familiar angry > baseline -

transcultural constants

The table lists the peak voxels of all clusters which showed significantactivation (p[FDR]0.05) in the contrast intentional empathy for familiarangry > baseline for both groups (inclusive masking). Clusters smaller

than 10 voxels were not considered.(x,y,z are coordinates referring to the Talairach & Tournoux stereo-tacticspace; n reflects the number of significant voxels inside the cluster;p[FWE](C) and p[FWE](G) show the probability that a cluster of the givensize might appear as a false positive in the group of Chinese (C) andGermans (G); the last three columns list the significances of the pairedt-tests (two-sided) investigating the effects of the factors task, emotion,and familiarity; e>c: intentional empathy > control; a>n: intentionalempathy for familiar angry > intentional empathy for familiar neutral;f>u: intentional empathy for familiar neutral > intentional empathy for

unfamiliar neutral;(

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: p


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Table 3

no region BA x, y, z [mm] t n p[FWE]

Chinese > Germans3.01 left dorsolateral prefrontal cortex 9 -44 -8 32 5.000 26 0.258

Germans > Chinese3.02 right temporo-parietal junction 40 55 45 31 6.796 113 < 0.001 3.03 right inferior temporal gyrus 20 57 16 -18 5.499 44 0.0333.04 right superior temporal gyrus 22 53 -12 -7 4.603 30 0.167 3.05 left middle insula 13 -41 -1 -9 4.991 13 0.819

Table 3: Intentional empathy for familiar angry > baseline - cultural differences

The table presents the centers of mass of all clusters which showed significant differences between

the contrast intentional empathy for familiar angry > baseline. Voxels with p[FDR]>0.05 were mwere masked, which were not included in a cluster of minimum 10 voxels. (x,y,z are coordinates Tournoux stereo-tactic space; n reflects the number of significant voxels inside the cluster; p[FWEa cluster of the given size might appear as a false positive; the last three columns list the significa(two-sided) investigating the effects of the factors task, emotion, and familiarity; e>c: intentia>n: intentional empathy for familiar angry > intentional empathy for familiar neutral; f>u: ifamiliar neutral > intentional empathy for unfamiliar neutral; (*): p


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Figure 3. Intentional empathy for familiar angry > baseline -

cultural differences

The figure presents all five regions which showed significant group differences

in the comparison of Chinese and Germans with regard to the the contrastintentional empathy for familiar angry > baseline (p[FDR]


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from the left DLPFC (r[Spearman]=0.304,p=0.091(*)) but not for the right TPJ(r[Spearman]=-0.031, p=0.867), the rightITG (r[Spearman]=0.148, p=0.418), theright STG (r[Spearman]=0.025, p=0.892),

or the left MI (r[Spearman]=0.276,p=0.126).

Modulation of hemodynamic responsesby taskWe used paired t-tests ([inten-tional empathy for familiar an-gry+intentional empathy for famili-ar neutral+intentional empathy forunfamiliar neutral]-[control for fami-

liar angry+control for familiar neu-tral+control for unfamiliar neutral])to investigate whether hemodynamic re-sponses of the regions listed in Table2 and 3 were modulated by the task.Several regions with transcultural con-stant activity showed stronger hemody-namic responses during intentional em-pathy compared to control: the bila-teral supplementary motor area (SMA,

2.04, 2.05), the bilateral anterior insula(AI, 2.06, 2.16), the bilateral putamen(2.07, 2.17), the bilateral posterior mid-brain (2.20, 2.21), the left middle tempo-ral gyrus (MTG, 2.23), and others (seeTable 2).The right STG (3.04) and left MI (3.05),which showed stronger activity in Ger-man subjects, also showed stronger acti-vity during intentional empathy (Table3).

In addition, several regions with trans-cultural constant activity showed theopposite effect (i.e. decreased hemody-namic responses during intentional em-pathy compared to control): the rightmiddle frontal gyrus (2.03), the left su-pramarginal gyrus (2.12), and the bila-teral precuneus (2.13, 2.19) (Table 2).The right TPJ (3.02), which was stron-ger activated in Germans, also showed

less activity during intentional empa-

thy (statistical trend - Table 3). In ad-dition, there were a number of regionswithout modulation by task (see Table 2and Table 3).

Modulation of hemodynamic responsesby emotionWe used paired t-tests (intentional em-pathy for familiar angry-intentionalempathy for familiar neutral) to inve-stigate whether hemodynamic responsesof regions listed in Tables 2 and 3 we-re modulated by emotion. A number ofregions, including the right SMA (2.05),the left MTG (2.23), the left putamen

(2.07), the left precuneus (2.13), the leftcuneus (2.14), the right AI (2.16), andothers, showed stronger hemodynamicresponses during intentional empathywith angry faces compared to neutralfaces (see Table).In addition, several regions of the con-trast intentional empathy for familiarangry > baseline did not show anymodulation emotion (Table 2). Many of

these regions are hence also listed for thecontrast intentional empathy for fami-liar neutral > baseline (Table 4) withsimilar or identical coordinates (for in-stance the left and right inferior frontalcortex (2.01/4.01, 2.15/4.03), the leftand right occipital cortex (2.10/4.12,2.08/4.10), the left and right cerebellum(2.11/4.13, 2.09/4.11), or the left andright parahippocampal gyrus (2.24/4.23,2.22/4.22)).

The same was the case for some of tho-se regions, which showed different acti-vity in both groups. The left DLPFC(3.01/5.01), the right inferior tempo-ral gyrus (3.03/5.03), and the left MI(3.05/5.02) showed activity in both con-trasts (intentional empathy for familiarangry > baseline (Table 3) and inten-tional empathy for familiar neutral >baseline (Table 5)).

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Table 4

no region BA x, y, z [mm] n p[FWE](C) p[FWE](G)

4.01 left inferior frontal gyrus 44 -42 -3 24 2591


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Table 4: Intentional empathy for familiar neutral > baseline -

transcultural constants

The table lists the peak voxels of all clusters which showed significantactivation (p[FDR]0.05) in the contrast intentional empathy for familiarneutral > baseline for both groups (inclusive masking). Voxels, which were

not included in a cluster of minimum 10 voxels, are not counted in. (x,y,zare coordinates referring to the Talairach & Tournoux stereo-tactic space; nreflects the number of significant voxels inside the cluster; p [FWE](C) andp[FWE](G) show the probability that a cluster of the given size might appearas a false positive in the group of Chinese (C) and Germans (G); the lastthree columns list the significances of the paired t-tests (two-sided)investigating the effects of the factors task, emotion, and familiarity;e>c: intentional empathy > control; a>n: intentional empathy forfamiliar angry > intentional empathy for familiar neutral; f>u: intentionalempathy for familiar neutral > intentional empathy for unfamiliar neutral;(

*)

: p


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Table 5

no region BA x, y, z [mm] t n p[FWE]

Chinese > Germans5.01 left dorsolateral prefrontal cortex 9 -45 -9 33 5.555 23 0.068

Germans > Chinese5.02 left middle insula 13 -39 -3 -6 6.122 19 0.145 5.03 right inferior temporal gyrus 20 54 18 -18 5.383 10 0.562

Table 5: Intentional empathy for familiar neutral > baseline - cultural differences

The table presents the centers of mass of all clusters which showed significant differences betweenthe contrast intentional empathy for familiar angry > baseline. Voxels with p[FDR]>0.05 were m

were masked, which were not included in a cluster of minimum 10 voxels. (x,y,z are coordinates Tournoux stereo-tactic space; n reflects the number of significant voxels inside the cluster; p[FWthat a cluster of the given size might appear as a false positive; the last three columns list the sigt-tests (two-sided) investigating the effects of the factors task, emotion, and familiarity; e>c: control; a>n: intentional empathy for familiar angry > intentional empathy for familiar neutraempathy for familiar neutral > intentional empathy for unfamiliar neutral; (*): p


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Modulation of hemodynamic responsesby familiarity

Paired t-tests (intentional empathy forfamiliar neutral > intentional empa-thy for unfamiliar neutral) were appliedto investigate whether hemodynamic re-sponses of regions listed in Tables 2 and3 were modulated by familiarity. Thiswas the case for a number of regions,which showed stronger hemodynamic re-sponses for the unfamiliar neutral com-pared to the familiar neutral condition:

the right SMA (2.05), the right occipital

cortex (2.08), the right AI (2.16), thebilateral midbrain (2.20, 2.21), and the

right parahippocampal gyrus (2.22).In addition, two regions with culture-related differences in hemodynamic re-sponses - the right STG (3.04) and theright MI (3.05) - showed stronger re-sponses during the unfamiliar conditionwhen compared to the familiar conditi-on.

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Discussion

Summary of findings

Questionnaire measurements indica-te differences in empathy and self-

construals between the subject groups.Chinese subjects reported more perso-nal distress and more interdependencerelative to German subjects.Comparing brain activity during empa-thy with anger of the two subject groupsshowed both transcultural constants andcultural differences. Cultural constantsincluded increased activity associatedwith intentional empathy for anger in

the bilateral inferior frontal gyrus (IFG),left supplementary motor area (SMA),left anterior insula (AI), and other brainregions. Cultural differences in empa-thy with anger were observed in the leftdorsolateral prefrontal cortex (DLPFC)where Chinese subjects showed stron-ger hemodynamic responses comparedto German subjects. Subjects hemody-namic responses in this region correla-ted with their personal distress scoresand their intra-scanner empathy ratingsfor the familiar angry faces (statisticaltrend).German subjects showed stronger he-modynamic responses associated withempathy for anger in the right temporo-parietal junction (TPJ), the right in-ferior temporal gyrus (ITG), the rightsuperior temporal gyrus (STG), and theleft middle insula (MI). There was a

significant correlation of hemodynamicresponses of the right ITG, right STG,and left MI with interdependence sco-res.The right STG and left MI revealedstronger hemodynamic responses duringintentional empathy compared to con-trol; whereas the right TPJ showed theopposite effect. The left DLPFC and theright ITG were not modulated by the

task at all. None of the five regions withculturally different activity showed a si-

gnificant modulation by emotion.

Brain regions with transcultural con-

stant activityBrain regions that were active in em-pathy for anger in both cultural groupsand revealed stronger activity for theintentional empathy task comparedto the control task included the bila-teral SMA, bilateral AI, and bilateralputamen - brain areas, which are wellknown for their involvement in empathy(Carr et al., 2003; Fan et al., 2011; Hoo-

ker et al., 2010, 2008; Jabbi and Keysers,2008; Jabbi et al., 2007; Lamm et al.,2007; Mathur et al., 2010; Singer et al.,2004). In addition, we found areas withtranscultural constant activity for thecontrast intentional empathy for fami-liar angry > baseline in both groups,but less activity during intentional em-pathy when compared to the controltask. The left inferior frontal gyrus, leftsupramarginal gyrus and bilateral pre-cuneus were among these regions.Interestingly, we did not find increasedactivity of the amygdala for this con-trast; in addition, the amygdala wasnot among those regions which revea-led culturally different activity. In sever-al previous studies the amygdala sho-wed reliable activity during the pro-cessing of emotional (including angry)faces (Derntl et al., 2009; Gur et al.,

2002; Hariri et al., 2002; Loughead et al.,2008; Whalen et al., 2001; Yang et al.,2002). However, a recent meta-analysissuggests, that the amygdala is not consi-stently involved in the processing of an-gry faces (Fusar-Poli et al., 2009). Thelack of amygdala activity in our studymight be explained by our task, whichfocused on empathic emotional sharingof the presented stimuli. It is likely that

the instruction to intentionally share theemotional state of the presented angry

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models led to reduced hemodynamic re-sponses in the amygdala, whilst we foundsignificant activity in the bilateral IFG,bilateral SMA and bilateral AI.

Brain regions with culture-based dif-ferences in brain activity

As initially hypothesized, the left DL-PFC showed stronger activity in Chi-nese subjects. In addition, its hemody-namic responses correlated with indi-vidual scores of personal distress andintra-scanner empathy ratings (statisti-cal trend). Since previous studies re-ported the involvement of the DLPFC

in emotion regulation and inhibition(MacDonald et al., 2000; Ochsner et al.,2004b; Ochsner and Gross, 2005; Shack-man et al., 2009; Vanderhasselt et al.,2006), one explanation of our findingis that the left DLPFC was activatedby subjects with high personal distressscores and high subjective impression ofempathy to protect themselves againstemotional over-arousal.

The right TPJ showed stronger hemody-namic responses in Germans, a findingwhich is also in accordance with our in-itial hypotheses; however, hemodynamicresponses did neither correlate with per-sonal distress nor interdependence sco-res. The TPJ is known to be involved inthe attribution of mental states towardsothers (theory of mind, TOM) in We-stern cultures (Castelli et al., 2000; Gal-

lagher et al., 2000; Mitchell, 2008; Saxeand Kanwisher, 2003; Saxe and Powell,2006; Saxe and Wexler, 2005).Moreover, the (right) TPJ is also knownfor its role in attention shifting (Asta-fiev et al., 2006; Corbetta et al., 2000;Corbetta and Shulman, 2002; Kincadeet al., 2005; Mitchell, 2008; Serenceset al., 2005; Shulman et al., 2003) (seethe paper of Mitchell (2008) for an over-

view about the overlap of brain activityrelated to TOM and attention shifting).

Interestingly, in a study comparing child-ren (at the age of 8 to 11 years) frominterdependent and independent cultu-res (Japanese and Americans) during anon-verbal TOM task, Kobayashi et al.

(2007) found the right TPJ with stron-ger hemodynamic responses in Americanchildren. The authors argued that dimi-nished self-other differentiation, whichis connected to interdependent cultu-res (Markus and Kitayama, 1991, 2010)might be the explanation for this fin-ding. Indeed, the TPJ is also known forits involvement in self-agency and self-awareness (Decety and Grzes, 2006;

Vogeley et al., 2001; Farrer and Frith,2002). Unfortunately, in this study wedid not test for self-other differentiation.The role of the right TPJ is more com-plex, however: In a recent study investi-gating culture-based differences in brainactivity during a Reading the mind inthe eyes-task, Adams et al. (2010) foundstronger activity in the right TPJ ininterdependent (i.e. Japanese) subjects

when compared to subjects stemmingfrom an independent culture (i.e. USA).In addition, the right TPJ was activa-ted more strongly in interdependent (i.e.Chinese) subjects when compared to in-dependent (i.e. Danish) subjects duringa task which included the self-reflectionof social attributes (Ma et al., in prepara-tion). At this time, a definite explanati-on of these complex cultural differencesin TPJ activity is certainly too early

and further research has to be done. Ho-wever, with regard to our finding thatcultural differences in TPJ activity areneither associated to interdependencenor to personal distress, one is temptedto assume that other factors could playan important role here - for instance ad-ditional differences related to language.

In addition, the right inferior tempo-

ral gyrus and the right superior tem-poral gyrus (temporal pole region) sho-

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wed stronger hemodynamic responses inGerman subjects; moreover, hemodyna-mic responses of both regions negativelycorrelated with interdependence sco-res. Both regions are known to play an

important role in social communicati-on, the attribution of mental states andthe understanding of intentions (Brittonet al., 2006; Castelli et al., 2000; En-rici et al., 2010; Freeman et al., 2010;Frith and Frith, 1999, 2003; Gallagherand Frith, 2003).

Finally, the left MI showed stronger he-modynamic responses in German sub-

jects; and again, hemodynamic respon-ses of this region negatively correlatedwith interdependence scores.Whilst the AI (which was amongst tho-se regions which displayed transculturalconstant activity) is known for its invol-vement in affective sharing (Fan et al.,2011; Jabbi et al., 2007; Keysers andGazzola, 2007; Singer et al., 2004) the MIis involved in perspective taking (Lamm

et al., 2007).Taken together, Chinese subjects sho-wed enhanced neuronal activity in re-gions associated to emotion regulation(right DLPFC), whereas German sub-jects showed stronger neuronal activityin regions connected to emotional under-standing and perspective taking (TPJ,ITG, STG, MI).

How culture affects brain activity du-

ring intentional empathy with angerAs behavioral studies show, individualsfrom interdependent and independentcultures differ in their attitude towardsanger, which is less often expressed andrelatively more controlled in interdepen-dent cultures (Markus and Kitayama,1991; Miyake et al., 1986; Zhou et al.,2004). The DLPFC is the key brainregion in the neuronal mechanisms of

this emotional control. Why do individu-als from interdependent cultures engage

their DLPFC in order to control theiranger responses? The answer to this istwofold: (i) because they are relativelymore afraid to be overwhelmed by nega-tive emotions (as shown by a significant

difference in personal distress and thecorrelation of personal distress scoreswith DLPFC activity) and (ii) becausethey value harmony more than individu-als from independent cultures (Markusand Kitayama, 1991) and have thereforea higher motivation to maintain harm-ony by the suppression of anger.Individuals from independent cultures incontrast do not only express anger more

often, they also can tolerate anger betterin social interactions (Adam et al., 2010).Our data suggest that the increased to-lerance of anger in less interdependentindividuals is related to increased neuro-nal activity in brain regions responsiblefor the understanding of social intenti-ons (TPJ, ITG, STG, and MI).In contrast to our initial hypotheses wedid not find culture based differences in

neuronal activity of key empathy regi-ons such as the AI, ACC, or IFG. Theseregions are reliably involved in basic em-pathic processes. The AI is responsiblefor interoceptive processing and crucial-ly involved in the conscious processingof emotions (Craig, 2009, 2004, 2002)and affective sharing (Fan et al., 2011;Jabbi et al., 2007; Keysers and Gazzo-la, 2007; Singer et al., 2004). The ACCwas in a recent review article by Shack-

man et al. (2011) described as beingresponsible for the integration of negati-ve affect, cognitive control, and pain aswell as the generation of aversely mo-tivated behavior. In addition, the ACChas been found to be active during emo-tional empathy (including empathy withpositive and neutral emotions) in sever-al studies (Blair et al., 1999; Carr et al.,2003; de Greck et al., 2011; Hooker et al.,

2008; Ochsner et al., 2004a). The IFG isa crucial part of the human mirror neu-

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ron system (MNS), a system which wasfirst detected in monkeys (Ferrari et al.,2003; Gallese et al., 1996; Rizzolatti andCraighero, 2004). The MNS consists ofbrain areas which are activated during

the generation of actions and also duringthe perception of (the same) actions per-formed by others (Carr et al., 2003; Gr-zes et al., 2003; Iacoboni, 2005; Iacoboniet al., 1999; Kaplan and Iacoboni, 2006)In addition, the human MNS includingthe IFG is reliably activated during em-pathy (Carr et al., 2003; de Greck et al.,2011; Kaplan and Iacoboni, 2006). Onepossible explanation for this negative fin-

ding, i.e. a lack differences in neuronalactivity of AI, ACC, and IFG betweenboth groups, might be that these regionsprovide empathic processes which aretoo basic to be influenced by culturaldifferences with regard to interdepen-dence.

Limitations

Concerning some limitations of our stu-

dy, we would like to mention that thedesign of our study did not include anunfamiliar angry condition. To inve-stigate the effect of familiarity, we hencerelied on the comparison of familiar neu-tral and unfamiliar neutral In futurestudies, it might be interesting to in-vestigate the effect of familiarity in thepresence of emotions.Another limitation concerns the possiblebias of genetic differences between the

groups of Chinese and Germans, sinceall Chinese were members of the EastAsian race, whereas the Germans weremembers of the Caucasian race. Hence,we can not exclude for certain, that gene-tic (and not cultural) differences between

both groups are responsible for the dif-ferences in brain activity. If one wantedto investigate cultural differences and atthe same time control for genetic dif-ferences, the ideal (but rare) subjects

would have been Chinese (raised in Chi-na) and Germans who are of Chineseorigin but born in Germany (and ide-ally raised by a German family) - andvice versa. This matter is even morecomplicated though: As has been shownby Chiao and Blizinsky (2010), geneticdifferences are inextricably intertwinedwith cultural differences. However, inthis study we concentrated on the effect

of culture on brain activity, whereas itwas not our aim to highlight the causesof cultural differences.

Conclusion

In summary, our brain imaging findingsindicate that the interdependent lifesty-le, which implies a relative high appre-ciation of harmony and lower anger ac-ceptance, leads to less neuronal activity

in regions responsible for the understan-ding of social intentions (inferior andsuperior temporal gyrus, middle insula)during intentional empathy with angryfaces.High ratings of personal distress ex-plained high activity in the dorsolate-ral prefrontal cortex during intentionalempathy with angry faces - probablyas a means to prevent emotional over-arousal.

Our findings are in concordance withprevious behavioral studies and providea neurobiological basis for the observedcultural differences between interdepen-dent and independent cultures in theirhandling with anger.

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Acknowledgements

The authors thank Yan Fan and Yina Mafor their help in the preparation of thestimuli. We further thank for the sup-

port by Claus Tempelmann and the staffof the Department of Neurology of theOtto-von-Guericke-University of Magde-burg in the acquisition of pilot data.We also thank Niall Duncan for helpfulpropositions to the script. Financially,this study was supported by the Scienceand Technology Fellowship Programmein China (STFP-25, to M.G.). We arealso indebted to the German Research

Foundation (DFG-SFB 779-A6), the Ho-pe of Depression Research Foundation(HDRF), the CRC and the EJLB Mi-

chael Smith Foundation for providing ge-nerous financial support (to G.N.), andto the National Natural Science Founda-tion of China (Project 30910103901), theNational Basic Research Program of Chi-na (973 Program 2010CB833903), andthe Fundamental Research Funds for theCentral Universities (providing generousfinancial support to S.H.).

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