This article was downloaded by: [Moskow State Univ Bibliote]On: 13 February 2014, At: 14:48Publisher: RoutledgeInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House,37-41 Mortimer Street, London W1T 3JH, UK

Social NeurosciencePublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/psns20

Empathy, ToM, and self–other differentiation: An fMRIstudy of internal statesRenate L. E. P. Reniersa, Birgit A. Völlmb, Rebecca Elliotta & Rhiannon Corcoranc

a Neuroscience and Psychiatry Unit, University of Manchester, Manchester, UKb Section of Forensic Mental Health, University of Nottingham, Nottingham, UKc Division of Psychiatry, University of Nottingham, Nottingham, UKPublished online: 03 Dec 2013.

To cite this article: Renate L. E. P. Reniers, Birgit A. Völlm, Rebecca Elliott & Rhiannon Corcoran (2014) Empathy,ToM, and self–other differentiation: An fMRI study of internal states, Social Neuroscience, 9:1, 50-62, DOI:10.1080/17470919.2013.861360

To link to this article: http://dx.doi.org/10.1080/17470919.2013.861360

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) containedin the publications on our platform. However, Taylor & Francis, our agents, and our licensors make norepresentations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of theContent. Any opinions and views expressed in this publication are the opinions and views of the authors, andare not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon andshould be independently verified with primary sources of information. Taylor and Francis shall not be liable forany losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoeveror howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use ofthe Content.

This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in anyform to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions

Empathy, ToM, and self–other differentiation: An fMRIstudy of internal states

Renate L. E. P. Reniers1, Birgit A. Völlm2, Rebecca Elliott1, and Rhiannon Corcoran3

1Neuroscience and Psychiatry Unit, University of Manchester, Manchester, UK2Section of Forensic Mental Health, University of Nottingham, Nottingham, UK3Division of Psychiatry, University of Nottingham, Nottingham, UK

This study used functional magnetic resonance imaging to examine the neural substrates of empathy, Theory ofMind (ToM), and self–other differentiation involved in the adaptive understanding of people’s internal states.Three conditions were distinguished in both sad and neutral (no obvious emotion) contexts. The empathycondition involved imagining what another person is feeling while the more cognitively loaded ToM conditioninvolved imagining what would make another person feel better. The self-reference condition required participantsto imagine how they would feel in someone else’s situation. Areas previously implicated in empathy, ToM, andself–other differentiation were identified within the different conditions, regardless of emotional context.Specifically, the frontal and temporal poles responded more strongly for ToM than for empathy. The self-referencecondition was associated with stronger dorsolateral prefrontal response than the empathy condition, while thereverse comparison revealed a stronger role for right frontal pole. Activations in frontal pole and orbitofrontalcortex were shared between the three conditions. Contrasts of parameter estimates demonstrated modulation byemotional context. The findings of common and differential patterns of responding observed in prefrontal andtemporal regions suggest that within the social cognition network empathy, ToM and self–other differentiationhave distinct roles that are responsive to context.

Keywords: Empathy; Theory of Mind; Self–other differentiation; fMRI.

Human social behavior is largely based on the interpreta-tion of the actions of others, enabling a high degree ofadaptability in the social world. This adaptability hasbeen built upon abilities such as empathy and Theory ofMind (ToM) (Frith &Blakemore, 2003; Rankin, Kramer,& Miller, 2005; Völlm et al., 2006). Empathy encom-passes our ability to be sensitive to and vicariouslyexperience other people’s feelings and to create work-ing models of emotional states (Reniers, Corcoran,Drake, Shryane, & Völlm, 2011). ToM refers to our

ability to represent other people’s mental states such asbeliefs, knowledge, and intentions (Shamay-Tsoory,Tomer, Berger, & Aharon-Peretz, 2003). Thesemechanisms help us to understand and predict thesocial world, and facilitate pro-social behavior(Baron-Cohen, Richler, Bisarya, Gurunathan, &Wheelwright, 2003; Vreeke & van der Mark, 2003).Our ability to integrate our representations of otherpeople’s beliefs and intentions with our beliefs abouttheir feelings within specific contexts, while

Correspondence should be addressed to: Renate L. E. P. Reniers, Neuroscience and Psychiatry Unit, University of Manchester,Manchester, UK. E-mail: r.l.e.p.reniers@bham.ac.uk

The authors would like to thank the Magnetic Resonance Imaging Facility of the University of Manchester for funding the scans and theirassistance in fMRI acquisition, Dr. Shane McKie for his assistance with data analyses and the Neuroscience & Psychiatry Unit for funding theparticipant reimbursement.

The authors report no conflict of interest.Present address for Renate L. E. P. Reniers: School of Psychology, University of Birmingham, Birmingham, UK; Rhiannon Corcoran:

Institute of Psychology Health and Society, University of Liverpool, Liverpool, UK.

SOCIAL NEUROSCIENCE, 2014Vol. 9, No. 1, 50–62, http://dx.doi.org/10.1080/17470919.2013.861360

© 2013 Taylor & Francis

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

14:

48 1

3 Fe

brua

ry 2

014

simultaneously inhibiting our own perspective, leads toan understanding of these people’s internal states(Leiberg & Anders, 2006). Our ability to monitorand manipulate cognitive and emotional processes pre-vents confusion between ourselves and others (Decety& Jackson, 2006; Decety & Sommerville, 2003) andhelps us to regulate feelings of personal distress andanxiety (Decety & Jackson, 2006).

The concepts of empathy and ToM are closelyrelated. Some authors (e.g., Blair, 2005) equate cogni-tive empathy to ToM, defining it as the representationof the internal mental state of another individual.However, we suggest that although cognitive empathyis likely to rely on many of the same underlying abil-ities that facilitate ToM, cognitive empathy involvesthe attribution of emotions as opposed to cognitionsand this may dissociate the two constructs at psycho-logical and neural levels (Reniers et al., 2011).

Consistent with this view, evidence shows thatempathy and ToM engage common as well as distinctneuronal networks. Research on empathy (Damasio,Tranel, & Damasio, 1990; Eslinger, 1998; Hynes,Baird, & Grafton, 2006; Shamay-Tsoory et al., 2003;Shamay-Tsoory, Tomer, & Aharon-Peretz, 2005;Shamay-Tsoory, Tomer, Goldsher, Berger, & Aharon-Peretz, 2004; Völlm et al., 2006), suggests involve-ment of orbitofrontal, dorsolateral, and (ventro)medialprefrontal regions. The more cognitive components ofempathy have been linked to medial prefrontal cortex,temporal poles, temporoparietal junction, occipitotem-poral cortices, thalamus, and cerebellum, while affec-tive components are linked to orbitofrontal cortex,paracingulate, anterior and posterior cingulate cortex,amygdala, premotor cortex, and insula (Rankin et al.,2005; Shamay-Tsoory et al., 2005; Völlm et al., 2006).Studies on ToM have consistently implicated frontalpole, anterior medial prefrontal cortex, temporal poles,and temporoparietal junction (Brunet, Sarfati, Hardy-Bayle, & Decety, 2000; Frith & Frith, 1999; Frith &Frith, 2003; Gallagher & Frith, 2003; Saxe &Kanwisher, 2003; Saxe & Powell, 2006; Sommeret al., 2007; Van der Meer, Groenewold, Nolen,Pijnenborg, & Aleman, 2011; Völlm et al., 2006).These findings highlight overlap in the neural corre-lates of empathy and ToM but at the same time empha-size the distinct socio-cognitive features andunderlying neurobiological mechanisms.

Empathy and ToM consider other people’s feelingsand mental states but rely on processes such as self-reflection and personal experiences to correctly identifythese feelings and mental states in their social contexts.These processes of self-reflection help to identify theappropriate response to the person’s situation as well asidentification of one’s own corresponding emotional

state (Reniers et al., 2011). While evaluating externallyand internally generated emotional and cognitive infor-mation, it is important that we maintain the distinctionbetween our own internal states and those of others toprevent confusion or misattribution of emotions thatmay result in feelings of distress and anxiety. Thisprocess of self–other differentiation is thought todepend on frontal pole, superior frontal gyrus, somato-sensory cortex, precuneus, and inferior parietal cortex(Decety & Sommerville, 2003; Ruby & Decety, 2001,2004). The frontal pole, superior frontal gyrus, posteriorcingulate, superior temporal sulcus, temporal pole, pre-cuneus, and inferior parietal cortex seem to be specifi-cally involved in third-person perspective taking, whilesomatosensory cortex, postcentral gyrus, and inferiorparietal cortex are reportedly more involved with thefirst-person perspective (Ruby & Decety, 2001, 2003,2004).

Völlm et al. (2006) conducted the first functionalmagnetic resonance imaging (fMRI) study examiningthe neural correlates of empathy and ToM in a singlestudy, thereby allowing direct comparison of associatedareas of signal change. The authors concluded thatempathy and ToM both rely on networks associatedwith making inferences about internal states of othersbut that empathic responding requires the additionalrecruitment of networks involved in emotional proces-sing. The current study aimed to further advance ourunderstanding of the neural substrates of empathy, ToM,and self–other differentiation involved in the under-standing of people’s internal states. The paradigm cho-sen relies on the adoption of distinct perspectives thatallow the separation of information that, when inte-grated, models the full appreciation of internal statescharacteristic of human social interaction. The first ofthe three conditions used was designed to explore pre-dominant empathic responses toward another personand was called the “Empathy” condition. When askedto imagine what another person is feeling it is believedthat we put ourselves in the other person’s shoes toconsider emotional and situational cues from their per-spective and reach a level of understanding of this per-son’s feelings. This enables us to build up a workingmodel of the person’s emotional state (Reniers et al.,2011). The second condition, labeled the “ToM” condi-tion, was designed to increase demands on higher orderreasoning skills by asking the participant to decide whatcould be done to make another person feel better. Thiscondition uses the working model of the person’s emo-tional state (established in the empathy condition) toformulate a context appropriate action. This approachwas chosen because of the extra layer of cognitiveprocessing that is required in comparison to consideringwhat another person is feeling. This condition thus

EMPATHY, TOM, SELF–OTHER DIFFERENTIATION 51

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

14:

48 1

3 Fe

brua

ry 2

014

involves a degree of empathic processing, but addition-ally it involves careful consideration of a person’s inten-tions and beliefs, key elements of ToM. The thirdcondition, the “Self-reference” condition, focuses onthe distinction between self and other. This involvescomparing the established working model of the other’sfeelings (established in the empathy condition) to howone considers one would feel in this situation. Therecognition of another person’s emotion elicits an emo-tional response to this person’s feelings and, using self-reflection and insight, leads to identification of one’sown feelings (Reniers et al., 2011). Visual and situa-tional cues are used to represent the other person’scognitive and emotional state. Crucial in this is therealization that these states are part of the other person’ssubjective experience (Decety, 2011). By shifting therepresentational stance, one’s own likely cognitive andemotional state can be shaped (Reniers et al., 2011). It islikely that such simulations draw on self-referential pro-cesses and invoke past experiences of similar situations.

Strong empathic experiences have typically beenassociated with events in negative contexts such as theloss of a loved one or the sight of a person in distress. Ithas also been suggested that events with negativevalence have a greater and more lasting impact upon usthan events with positive valence (Baumeister,Bratslavsky, & Finkenauer, 2001; Rozin & Royzman,2001; Vaish, Grossmann, & Woodward, 2008). Thishighlights the importance of emotional valence in thecontext of socio-cognitive processes. All conditionswere therefore performed in sad and neutral (no obviousemotion) emotional contexts to investigate whethernegative emotional valence modulates blood oxygena-tion level dependent (BOLD) response within and acrossconditions. To our notion, this study is the first to con-trast specifically sad feelings with neutral (no overt)emotions in a comparison of empathy and ToM-relatedprocesses involved in the inference of other people’sinternal states. We hypothesized that social cognitiveactivations would be enhanced in the sad condition,due to the greater emotional salience of the stimuli.

Our analyses focused on activations within areasmost consistently associated with social cognition: fron-tal pole, medial and dorsolateral prefrontal cortex, orbi-tofrontal cortex, anterior cingulate, temporal poles, andtemporoparietal junction. These areas were hypothe-sized to show differential activations for the three con-ditions. Based on prior work (see, e.g., Abu-Akel &Shamay-Tsoory, 2011; Shamay-Tsoory, 2011; Völlmet al., 2006), increased activations in orbitofrontal cortexand anterior cingulate were predicted for the empathycondition compared to the ToM and self-referenceconditions. We anticipated that the higher order con-text-dependent reasoning required in the ToM condition

would, in comparison to the empathy condition, beassociated with increased activations in medial prefron-tal cortex, temporal poles, and temporoparietal junction(see, e.g., Frith & Frith, 2003; Gallagher & Frith, 2003;Saxe & Powell, 2006). We anticipated increased BOLDresponse in anterior cingulate (Phan, Wager, Taylor, &Liberzon, 2002) and frontal pole (Gilbert et al., 2006) inthe self-reference condition, compared to the empathycondition, because of its likely relationship with perso-nal experiences. Differential activations in the frontalpole, and medial and dorsolateral prefrontal cortex(see, e.g., Decety & Sommerville, 2003; Ruby &Decety, 2004; Schmitz, Kawahara-Baccus, & Johnson,2004) were predicted for comparisons between the con-ditions mediating others’ versus own emotions (empa-thy versus self-reference).

Activations specifically associated with sad contextwere predicted in the anterior cingulate, lateral orbito-frontal cortex, and medial prefrontal cortex (Phan et al.,2002; Seitz et al., 2008). We also explored the interac-tion between emotion and condition, and predictedstrongest enhancement of response by sad context forthe self-reference condition in association with therecollection of emotional personal experiences.Autobiographical recall is required for inferring inter-nal states (Corcoran, 2000; Concoran & Frith, 2003;Gallagher & Frith, 2003) and while emotions enhancememory consolidation (Canli, Zhao, Brewer, Gabrieli,& Cahill, 2000; Hamann, Ely, Grafton, & Kilts, 1999),they may be particularly intense in the case of personalevents (Salas, Radovic, & Turnbull, 2012).

Although prior literature suggests plausible ROIs, asdetailed above, these ROIs are not always consistentacross studies, with considerable variation in both whichregions respond, and where the peak of activation inlarger regions is located. We therefore adopted a wholebrain analysis strategy, as recommended by Liebermanand Cunningham (2009), and detailed below.

METHODS & MATERIALS

Participants

Participants were 15 right-handed healthy volunteers,aged between 18 and 40 years. As gender differencesfor social cognition have been reported (Baron-Cohen& Wheelwright, 2004; Reniers et al., 2011; Russell,Tchanturia, Rahman, & Schmidt, 2007), we restrictedour sample to males. Further exclusion criteria were:non-fluent English, an estimated IQ below 85, self-reported treatment for any psychiatric illness withinthe last year, consumption of more than 20 units ofalcohol per week, history of serious head injury (more

52 RENIERS ET AL.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

14:

48 1

3 Fe

brua

ry 2

014

than 5 minutes loss of consciousness or overnighthospital stay), serious medical or neurological condi-tions, claustrophobia, and other contraindications forfMRI. Participants were screened for Axis I psychia-tric disorders using the M.I.N.I. (Sheehan et al., 1998)and the IQ was estimated using the Quick QT(Ammons & Ammons, 1962). The average IQ ofparticipants was 105 (SD = 8, range 93–120). Allparticipants had been in education for a minimum of13 years. The mean age of the group was 27 (SD = 5,range 21–40) and all indicated a country of origin inEurope, with 12 specifying the United Kingdom. Allparticipants scored in the average range for males onthe Questionnaire of Cognitive and AffectiveEmpathy (Reniers et al., 2011). Participants gaveinformed consent and were reimbursed for their timeand effort. Ethical approval was granted by the NorthManchester Research Ethics Committee.

Scanning task

The scanning tasks required participants to view sadand neutral (no obvious emotion) pictures. Pictureswere taken from the International Affective PictureSystem (IAPS) (Lang, Bradley, & Cuthbert, 1997)and sourced from the internet. The findings of apilot study (n = 24) asking people to rate the feelingsof the main character for levels of sadness, happiness,and fearfulness (“How happy/sad/frightened?”) on a5-point Likert scale ranging from “Not happy/sad/frightened at all” (score = 1) to “Extremely happy/sad/frightened” (score = 5) determined which imageswere selected for the imaging study. The picturesselected for the sad category received highest ratingson sadness (Mdn = 3.90) and lowest ratings on happi-ness and fearfulness (Mdn = 1.42 and Mdn = 2.33,respectively). Neutral pictures were rated low on allthree selection criteria (sadness Mdn = 1.81; happinessMdn = 2.48; fearfulness Mdn = 1.50). Compared to theneutral pictures, the sad images were scored signifi-cantly lower on happiness (z = –2.13, p < .05, with aneffect size (Field, 2005; Rosenthal, 1991) of r = .37)and significantly higher on sadness (z = –2.20, p < .05,r = .36) and fearfulness (z = –2.37, p < .05, r = .40).

Three tasks were performed during scanning withthe same pictures being evaluated in each condition.In the empathy condition participants imagined whatthe main character in the picture was feeling. In theToM condition participants imagined what wouldmake the main character in the picture feel better. Inthe self-reference condition participants imagined howthey would feel if they were the main character in thepicture. After scanning, participants described what

they had imagined during the scanning task for aselection of pictures. This suggested compliancewith the requirements of the task conditions.

The task comprised a block design, with eighteenblocks in total and each type of block repeatedthree times (i.e., three each of empathy-sad, empathy--neutral, ToM-sad, ToM-neutral, self-reference-sad,self-reference-neutral). Each block consisted of sixtrials of either sad or neutral pictures. Equal numbersof male and female characters were seen across condi-tions. Each picture appeared once in each condition.Conditions and trials were pseudo-randomized. Eachblock was preceded by the instructions for that blockwhich stayed on the screen for 10 seconds. The pictureswere presented for 5 seconds and separated by a fixa-tion cross that appeared for 500 milliseconds.Participants did not respond overtly during the scan-ning conditions but, to maintain focus, they were askedto press a button when the fixation cross appeared onthe screen. Figure 1 shows a schematic representationof a trial. The total task duration was 11.5 minutes.

Data acquisition

Functional magnetic resonance (fMRI) images wereacquired using a 3 Tesla Philips Achieva (PhilipsMedical Systems, Eindhoven, the Netherlands) scanner.T2*-weighted volumes were acquired using a single-shot echo-planar (EPI) pulse sequence. Each volumecomprised 34 axial slices of 3-mm thickness with aslice gap of 0.5 mm (TR = 2 seconds, TE = 35 milli-seconds, in-plane resolution of 2.5 × 2.5 mm). A T1-weighted structural scan was also acquired for eachsubject for co-registration and to exclude any structuralabnormality. No abnormalities were reported.

Data analysis

The imaging data were processed using StatisticalParametric Mapping (SPM5, Friston, The WelcomeDepartment of Cognitive Neurology, London, UK)with a random effects model (http://www.fil.ion.ucl.ac.uk/spm). Individual scans were realigned using themiddle scan as a reference, movement corrected usingArtRepair if movement > 2 degrees, normalized into“standard space” (Talairach & Tournoux, 1988) usingMNI templates (Montreal Neurological Institute) andsmoothed with a 7 × 7 × 10 mm Gaussian kernel.

Statistical analysis of the imaging data was carriedout using the general linear model with a delayedboxcar waveform to model BOLD signal changes tothe sad relative to the neutral condition. At the first

EMPATHY, TOM, SELF–OTHER DIFFERENTIATION 53

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

14:

48 1

3 Fe

brua

ry 2

014

level, goodness-of-fit (beta) values for each contrastresulted in a contrast map for each individual. At thesecond level, the statistical parametric maps from eachindividual were combined in random effects analyses.The main effect of condition and the interaction withsad emotional context were examined using ANOVAwithin which we considered comparisons betweenempathy versus ToM and empathy versus self-refer-ence. Note, we did not consider a direct comparisonbetween ToM and self-reference to be theoreticallymeaningful, as it would involve a twofold comparisonof self versus other as well as “feeling” versus “feelingbetter”. Therefore, we did not directly compare theseconditions. To produce an acceptable balance betweenType I and II error rates, statistical significance for pre-hypothesized areas was based on a combined intensityand cluster-size threshold (Lieberman & Cunningham,2009). Spatial extent threshold was determined by1,000,000 Monte Carlo simulations conductedusing AphaSim (AFNI; Cox, 1996), which yielded acluster extent of 23 voxels at a voxel-wise threshold ofp < .001. This joint voxel-wise and cluster-size thresh-old corresponds to a false-positive discovery rate of 5%across the whole brain. For non-hypothesized areas,peak activations in clusters of a minimum of 23 con-tiguous voxels are reported if they met the criterion ofp < .05 whole brain FDR corrected.

RESULTS

Main effect of emotional context

Neural responses to neutral pictures were subtractedfrom those to sad pictures across all conditions to revealareas of increased signal associated with a sad emo-tional context (Table 1). Significant activations were

found in the posterior cingulate, temporal pole, fusiformgyrus, lingual gyrus, and middle occipital gyrus.

Effect of sad emotional context on eachcondition

To investigate the effect of emotional context on eachcondition, pairwise contrasts of sad versus neutral foreach condition were explored (Table 1). For the empa-thy condition, sad context was associated withincreased signal change in the anterior medial frontalcortex, ventrolateral prefrontal cortex, posterior cingu-late and cingulate gyrus, temporal pole, temporopar-ietal junction, bilateral cuneus, lingual gyrus, middleoccipital gyrus, and the cerebellum.

For the ToM condition, sad context was associatedwith significant responses in the temporal pole, tempor-oparietal junction, (pre)cuneus, and the lingual gyrus.

For the self-reference condition, sad context was asso-ciated with significant response in the fusiform gyrus.

Main effects of condition

To investigate the main effect of condition, brainactivations across sad and neutral conditions werecontrasted for (1) empathy and ToM and (2) empathyand self-reference (Table 2).

Empathy > ToM revealed no areas of significantsignal change in hypothesized areas.

ToM > empathy was associated with significantactivations in bilateral frontal pole and left temporalpole (Figure 2).

For empathy > self-reference, significant signalchanges were found in the right frontal pole(Figure 3a).

Figure 1. Schematic representation of an empathy trial.The trial presents an example of a sad stimulus in the empathy condition.

54 RENIERS ET AL.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

14:

48 1

3 Fe

brua

ry 2

014

TABLE1

Maineffe

ctofemotio

nalc

ontext

oneach

conditio

n

Maineffect

(ES+TS+SR

S)–

(EN+TN+SR

N)

Empa

thy

ES–EN

ToM

TS–TN

Self-reference

SRS–SR

N

Talairach

coordina

tes

Talairach

coordina

tes

Talairach

coordina

tes

Talairach

coordina

tes

Region

BA

Left/right

Cluster

size

xy

zZ-score

Cluster

size

xy

zZ-score

Cluster

size

xy

zZ-score

Cluster

size

xy

zZ-score

Anteriormedial

frontalcortex

9L

32−3

4827

3.10

Ventrolateral

prefrontal

cortex

45R

108

5723

153.79

Cingu

late

gyrus

24R

117

10−13

393.51

Posterior

cingulate

30L

49−3

−48

193.37

31R

5210

−47

383.39

Temporalpo

le38

L44

−45

14−18

3.44

65−4

513

−28

3.76

38R

3245

16−24

3.26

Temporoparietal

junctio

n39

R81

48−75

103.66

5952

−41

193.11

Precuneus

7R

4210

−50

383.72

Cun

eus

17L

^−1

0−90

55.59

^−13

−92

54.93

18R

^18

−92

115.12

17R

^20

−89

45.59

Fusiform

gyrus

37R

^42

−59

−9

4.86

355

43−62

−12

4.80

Lingu

algy

rus

18R

2040^

13−83

−2

5.65

^20

−78

−84.31

^20

−78

−5

4.07

17R

1570^

15−86

−25.80

1159

^15

−86

−2

5.89

Middleoccipital

gyrus

18L

^−35

−83

−8

5.23

^−4

5−73

−24.07

19L

^−37

−80

45.04

Decliv

eL

^−2

2−76

−11

4.74

R^

22−76

−11

4.40

Notes:^Cluster

breakdow

n.E=Empathycondition,T=To

Mcondition,SR=Self-referencecond

ition,S=sad,

N=neutral,BA

=Brodm

annarea.

EMPATHY, TOM, SELF–OTHER DIFFERENTIATION 55

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

14:

48 1

3 Fe

brua

ry 2

014

Self-reference > empathy revealed significantlystronger activations in the bilateral dorsolateral pre-frontal cortex (Figure 3b + c).

Shared activations across conditions

Conjunction analyses were conducted to reveal areasof activation shared across conditions. The empathy,ToM, and self-reference conditions in both sad andneutral contexts commonly activated the left frontalpole ([0 57 13], z = 4.16), and a cluster in the middleoccipital gyrus ([47 –68 3], z = Inf) extending intoparahippocampal gyrus, cuneus, fusiform gyrus, cul-men, and declive. When the conjunction for just thesad context was examined, activations were againreported in the frontal pole ([0 57 17], z = 4.87), andbilateral middle occipital gyrus ([–45 –77 7], z = 6.89;[50 –68 3], z > 7) extending into thalamus, parahip-pocampal gyrus, superior temporal gyrus, (pre)cuneus, fusiform gyrus, culmen, and uncus.Additional activations were found in the left orbito-frontal cortex ([–30 35 –18], z = 4.48) and fusiformgyrus ([–40 –52 –15], z = 5.89).

Modulation of condition by sad emo-tional context

This was explored by looking at the interaction termsof the ANOVA. Empathy > ToM (sad > neutral)revealed no areas of significant signal change inhypothesized areas.

ToM > empathy (sad > neutral) revealed strongeractivation clusters for the ToM condition in the rightdorsolateral prefrontal cortex ([38 31 31], z = 3.37).Response in this region was higher in the empathycondition (neutral) than in the other three conditions.

Empathy > self-reference (sad > neutral) resulted insignificant signal changes in the anterior medial pre-frontal cortex ([8 47 1], z = 3.76). In this region,contrasts of parameter estimates suggest that sad con-text had opposite effects to the empathy and self-reference conditions (increasing and decreasingresponse, respectively).

Self-reference > empathy (sad > neutral) revealedno areas of significant signal change in the hypothe-sized areas.

DISCUSSION

This study investigated the neural substrates of empa-thy, ToM, and self–other differentiation involved inthe adaptive understanding of people’s internal states.It uniquely allowed for direct comparison of empathy,

TABLE2

Maineffe

ctofco

ndition

Empa

thy>ToM

(ES+EN)–(TS+TN)

ToM

>Empa

thy

(TS+TN)–(ES+EN)

Empa

thy>Self-reference

(ES+EN)–(SRS+SR

N)

Self-reference>Empa

thy

(SRS+SR

N)–(ES+EN)

Talairach

coordina

tes

Talairach

coordina

tes

Talairach

coordina

tes

Talairach

coordina

tes

Region

BA

Left/right

Cluster

size

xy

zZ-score

Cluster

size

xy

zZ-score

Cluster

size

xy

zZ-score

Cluster

size

xy

zZ-score

Frontal

pole

10L

82−3

6220

3.21

10R

3913

528

3.38

4323

6213

3.20

Dorsolateralprefrontal

cortex

9L

35−25

3431

3.43

9R

4423

3634

3.53

Temporalpo

le21

L88

−43

11−33

3.76

Notes:E=Empathycondition,T=To

Mcondition,SR=Self-referencecond

ition,S=sad,

N=neutral,BA

=Brodm

annarea.

56 RENIERS ET AL.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

14:

48 1

3 Fe

brua

ry 2

014

ToM, and self–other differentiation processes undersubtly different contexts to advance our understandingof the neural substrates associated with these pro-cesses. As predicted, areas previously implicated inempathy, ToM, and self–other differentiation wereidentified for the different conditions, regardless ofemotional context. Specifically, the context-dependentreasoning requirements of the ToM condition gaverise to activation in frontal and temporal poles overand above that seen in these areas in relation to theempathy condition. The self-reference condition wasassociated with stronger dorsolateral prefrontalresponse than the empathy condition, while thereverse comparison revealed a stronger role for rightfrontal pole. Activations in frontal pole and orbito-frontal cortex were shared between conditions.

Contrasts of parameter estimates demonstrated thatthe conditions were modulated by emotional contextsuch that the right dorsolateral prefrontal cortex wasmost responsive for empathy under neutral context inToM compared to empathy. In the empathy versusself-reference comparison, sad context enhanced ante-rior medial prefrontal responses to empathy.

Sad emotional context

Activations specifically associated with sad contextwere found in medial prefrontal cortex, but not inlateral orbitofrontal cortex and anterior cingulate aswas predicted. These activations were only observedfor the empathy condition but not the ToM and self-

Figure 2. ToM compared to empathy regardless of emotional context.Bilateral frontal pole (a + b) and left temporal pole (c) activity associated with the ToM compared to empathy condition. Crosshairs at (–3 6220), (13 52 8), and (–43 11–33). Plotted bars from left to right: ToM neutral context, empathy neutral context, ToM sad context, and empathysad context.

Figure 3. Comparison of self-reference and empathy regardless of emotional context.Right frontal pole (a) activity associated with the empathy compared to self-reference condition regardless of emotional context. Bilateraldorsolateral prefrontal cortex (b + c) activity associated with the self-reference compared to empathy condition regardless of emotional context.Crosshairs at (23 62 13), (–25 34 31), and (23 36 34). Plotted bars from left to right: empathy neutral context, self-reference neutral context,empathy sad context, and self-reference sad context.

EMPATHY, TOM, SELF–OTHER DIFFERENTIATION 57

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

14:

48 1

3 Fe

brua

ry 2

014

reference conditions. Increased activity in the medialprefrontal cortex was observed in the empathy condi-tion when sad context was compared to neutral contextand in the interaction between empathy and self-refer-ence in a sad versus neutral context. Increased activityin the medial prefrontal cortex has previously beenassociated with emotion processing (Krämer,Mohammadi, Donamayor, Samii, & Munte, 2010;Phan et al., 2002), including inferring other people’semotions (Hynes et al., 2006) and judging their emo-tional state (Farrow et al., 2001), and with reflectingupon one’s own emotions (Gusnard, Akbudak,Shulman, & Raichle, 2001; Lane et al., 1997).Functions of this region have thus been associatedwith attending to others’ as well as our own mentalstates (Frith & Frith, 2003), consistent with our find-ings of involvement in empathy and self-referentialperspective taking.

Traditionally, the right temporoparietal junction hasbeen implicated in the attribution of beliefs to otherpeople (Mitchell, 2008; Saxe & Kanwisher, 2003; Saxe& Powell, 2006; Saxe & Wexler, 2005). In addition,studies on empathy (e.g., Hynes et al., 2006) reportincreased activity in the right temporoparietal regionsfor inferring others’ emotions. We found that sad con-text enhanced response in right temporoparietal junc-tion for both empathy and ToM. This suggests theimportance of this region in both empathy and ToMwhen the context is emotionally salient.

Recent research has pointed out that, in addition toinvolvement in the attribution of beliefs and emotionsto other people, the right temporoparietal junctionmay subserve a process of attention reorienting thatis not specific to social contexts (Mitchell, 2008;Young, Dodell-Feder, & Saxe, 2010). Attention reor-ientation to clues elsewhere in the scene is likely toaid the generation of an internal working modelrequired in the empathy condition. We reported invol-vement of a more anterior region of right temporopar-ietal junction in the empathy condition (sad > neutral)compared to the ToM condition (sad > neutral). Adirect comparison (ToM > empathy) resulted in justbelow threshold activation in the more posteriorregion of right temporoparietal junction. We mayhave highlighted an important functional segregationwithin the temporoparietal junction here and suggestthat the relatively posterior region may be selectivefor considering the beliefs of other people (Mitchell,2008; Young et al., 2010) while the more anterior partmay subserve a different process, like attention reor-ientation (Mitchell, 2008). It is possible to speculatethat attention reorientation is one of the mechanismsthat people with autism use to infer the inner experi-ences of others as for people with autism all emotional

displays are ambiguous and so they may need togather information from elsewhere to disambiguateemotional situations. Thus, in our paradigm the empa-thy condition may be challenging our informationprocessing systems in the same way as emotionalstimuli in general challenge the information proces-sing systems of those with autism.

Empathy > ToM

No areas of significant signal increase were found forEmpathy > ToM, regardless of emotion, nor in theinteraction with sad emotional context. At first glance,this finding appears inconsistent with Völlm et al.(2006) who suggested that, like ToM, empathy relieson networks associated with making inferences aboutmental states of others but with additional recruitmentof networks involved in emotional processing.However, the ToM condition in the current studybuilt upon the empathic working model that wasdeveloped to support the empathy condition by askingparticipants what would make the main character inthe picture feel better. This explicit consideration ofthe representation of the other’s feelings will haverecruited emotional regions equivalent to thoseinvolved in the empathy condition. Our “ToM” con-dition therefore involved both empathic processingand more cognitive appraisal, and can thus be con-ceptualized as involving both ToM and empathy.

ToM > Empathy

The frontal pole is reliably recruited when internallygenerated information requires evaluation (Christoff& Gabrieli, 2000; Christoff, Ream, Geddes, &Gabrieli, 2003) and several studies have reported acti-vation of this region when participants overtly putthemselves in the shoes of others (Decety &Sommerville, 2003). We observed response in tworegions of frontal pole (a dorsomedial region and amore ventral region on the right) when ToM wascontrasted with empathy, irrespective of emotionalcontext. Activation of a more lateral part of rightfrontal pole was observed when empathy was com-pared to self-reference, irrespective of emotional con-text. The finding of a response in right frontal pole forboth ToM > empathy and empathy > self-referencehighlights an important role for this region in socialcognition and, more particularly, the internal consid-eration and evaluation of others’ and our own feelingsat different layers of complexity/sophistication(Christoff et al., 2003). In addition, our findings

58 RENIERS ET AL.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

14:

48 1

3 Fe

brua

ry 2

014

support suggestions of functional segregation withinthe frontal pole. The medial region of the frontal polehas been linked to mentalizing (Gilbert et al., 2006)and this is consistent with the extra context-dependentreasoning required in our ToM condition. Decidingwhat would make a person feel better also includes afuture component, consistent with suggestions ofinvolvement of this region in future thinking(Burgess, Simons, Dumontheil, & Gilbert, 2005).Evidence points to specific involvement of the morelateral part of the frontal pole in episodic memoryretrieval (Gilbert et al., 2006) and inhibiting the self-perspective when taking another’s perspective (Ruby& Decety, 2001). The latter evidence is consistentwith our finding of increased BOLD response in thisregion for empathy > self-reference, irrespective ofemotion. It seems that the process of evaluating self-generated information is not restricted solely to con-texts of high emotional valence.

It has been argued that the anterior cingulate maysignal the dorsolateral prefrontal cortex when high-levelcontrol is required (Gilbert & Burgess, 2008). This isreflected in involvement of right dorsolateral prefrontalcortex in the cognitive aspects of understanding mentalstates (Kalbe et al., 2010) andmay explain our finding ofincreased signal changes in right dorsolateral prefrontalcortex associated with the neutral empathy conditionwhen the interaction between ToM and empathy in sadversus neutral context was explored.

Left temporal pole activity was observed in theoverall sad versus neutral comparison and in the sadversus neutral contrast in the empathy condition.Left temporal pole activity was also observed whenToM was compared to empathy, irrespective of emo-tional context. This pattern of response in left tem-poral pole reflected activity associated with ToM,irrespective of emotional context, but also activityassociated with empathy in sad context. It has beensuggested that we draw on our past experiences toinfer the internal states of others (Corcoran, 2000;Corcoran & Frith, 2003; Gallagher & Frith, 2003).The current findings are consistent with conjecturesproposing that the left temporal pole is recruitedwhen wider semantic and emotional informationneeds to be gathered from past experience (Frith &Frith, 2003) and with its association with autobio-graphical recall (Fink et al., 1996; Gallagher & Frith,2003; Leiberg & Anders, 2006; Olson, Plotzker, &Ezzyat, 2007; Ruby & Decety, 2004).

Other’s versus own emotions

Differential activations in frontal pole, and medial anddorsolateral prefrontal cortex were predicted and

observed for the contrasts mediating others’ versusown emotions. Although not traditionally labeled aself–other distinction region (Decety & Sommerville,2003; Ruby & Decety, 2001, 2003, 2004), the dorso-lateral prefrontal cortex was bilaterally recruited whenself-reference was compared to empathy, irrespectiveof emotional context. While the rostral area of frontalpole is recruited when internally generated informa-tion needs evaluating, the dorsolateral prefrontal cor-tex becomes activated when externally generatedinformation is being evaluated (Christoff et al.,2003; Christoff & Gabrieli, 2000). This evaluationprocess facilitates new ways of behaving andapproaching unfamiliar situations (Gilbert &Burgess, 2008). Our data suggests that this processmay be most important under first-person perspectiveconditions where we imagine ourselves in someoneelse’s situation.

Shared activations across conditions

Activations in frontal pole and orbitofrontal cortexwere shared between conditions. Activation in frontalpole was reported regardless of emotional contextwhile orbitofrontal activation was specifically relatedto conditions with sad emotional context. While theseactivations provide evidence for a shared social cog-nitive underpinning, together with the differential acti-vations reported between the conditions, they alsoprovide support for the suggestion that within a com-mon social cognition network, distinct social pro-cesses may be uniquely presented.

Limitations

One limitation of this study is the absence of a low-level task that did not concern internal states. Addinga condition in which participants are instructed tothink about aspects of the stimuli irrelevant to theemotional task (e.g., gender), may provide valuableinformation on the areas involved in empathy, ToM,and self–other differentiation more generally.Furthermore, empathy is not something we experiencejust in negative contexts and therefore, future researchshould include the effect of a positive context.

The pictures used in this study varied in terms oftheir emotional ambiguity meaning that it was notalways easy to simulate around the uncertain natureof the scenarios. This was particularly the case in theToM-neutral context condition that required partici-pants to infer what would make another person feelbetter when, in fact, it was unclear how the person was

EMPATHY, TOM, SELF–OTHER DIFFERENTIATION 59

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

14:

48 1

3 Fe

brua

ry 2

014

feeling in the first instance (providing no clear workingmodel upon which to build context-dependent reason-ing). It furthermore needs mentioning that there weremore pictures depicting people in groups in sad contextthan in neutral context and the enhanced interpersonalnature of the stimuli can therefore not be fully ruled outas an alternative explanation for the increased activa-tions found in sad compared to neutral contexts.

The ToM condition did not directly query theintentions or beliefs of the main character but insteadasked what would make the main character feel better.While processing this question does rely strongly onToM skills, it may also have necessitated the devel-opment of a more sophisticated working model ofcognitive empathy. This may have contributed to thelack of differential activation reported for theEmpathy >ToM comparison. Future studies couldfurther examine the dissociable mechanisms underly-ing ToM versus high-level cognitive empathy.Employment of techniques that are more sensitive inteasing out fine distinctions between activations incommonly recruited regions, such as multi-voxel pat-tern analysis, will be important tools to furtheradvance our knowledge in this field.

Clinical implications

While the findings of this study go some way toexplaining empathy, ToM, and self–other differentia-tion processes in relation to their functional anatomy,they may also have important implications for socio-cognitive remediation in different clinical groups. Ourfindings have demonstrated that asking a participant toperform essentially the same task in different ways bygiving him/her slightly different instructions results indistinct activations in a variety of brain regions.Focusing on a specific method of emotional informa-tion processing to arrive at an empathic or ToM judg-ment could prove useful in the treatment ofpersonality disorders for example. More explicitly, ifpsychological treatments can provide a method ofinducing empathic judgments that distinguishesbetween self and other’s emotions, this would proveparticularly useful when a dysfunctional internalmodel of the self is implicated in the clinical disorder(Morrison, 2004).

Conclusion

General agreement is emerging that empathy, ToM,and self–other differentiation are mediated by a

complex neural network in which prefrontal and tem-poral structures play an important role but wheredifferent kinds of processing are related to differentareas and strengths of activation. Importantly, thisstudy differed from previous studies because directcomparison between empathy, ToM, and self–otherdifferentiation processes under subtly different con-texts was possible. The results of the current study,combined with those of previous neuroimaging stu-dies, suggest that integrated cognitive activity invol-ving shared representations, emotional processing andregulation, self–other differentiation and integration ofpast experiences leads to adequate ToM and an appro-priate empathic experience. Future research consistingof more detailed neuropsychological and behavioraltesting in large groups of healthy volunteers andpatients, together with imaging studies focusing onthe mechanisms of empathy, ToM and self–other dif-ferentiation will provide a more comprehensive pic-ture of the functional anatomy of these socio-cognitive processes in their various guises.

Original manuscript received 5 February 2013Revised manuscript accepted 28 October 2013

First published online 2 December 2013

REFERENCES

Abu-Akel, A., & Shamay-Tsoory, S. (2011).Neuroanatomical and neurochemical bases of theory ofmind. Neuropsychologia, 49(11), 2971–2984.

Ammons, R. B., & Ammons, C. H. (1962). The Quick Test.Missoula, MT: Psychological Test Specialists.

Baron-Cohen, S., Richler, J., Bisarya, D., Gurunathan, N., &Wheelwright, S. (2003). The systemizing quotient: Aninvestigation of adults with Asperger syndrome or high-functioning autism, and normal sex differences.Philosophical Transactions of the Royal Society ofLondon. Series B, Biological Sciences, 358(1430), 361–374.

Baron-Cohen, S., & Wheelwright, S. (2004). The empathyquotient: An investigation of adults with Asperger syn-drome or high functioning autism, and normal sex differ-ences. Journal of Autism and Developmental Disorders,34(2), 163–175.

Baumeister, R. F., Bratslavsky, E., & Finkenauer, C. (2001).Bad is stronger than good. Review of GeneralPsychology, 5(4), 323–370.

Blair, R. J. R. (2005). Responding to the emotions of others:Dissociating forms of empathy through the study oftypical and psychiatric populations. Consciousness andCognition: An International Journal, 14(4), 698–718.

Brunet, E., Sarfati, Y., Hardy-Bayle, M. C., & Decety, J.(2000). A PET investigation of the attribution of inten-tions with a nonverbal task. NeuroImage, 11(2), 157–166.

Burgess, P. W., Simons, J. S., Dumontheil, I., & Gilbert, S. J.(2005). The gateway hypothesis of rostral prefrontalcortex (area 10) function. In J. Duncan, I. Phillips &

60 RENIERS ET AL.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

14:

48 1

3 Fe

brua

ry 2

014

P. McLeod (Eds.), Measuring the mind: Speed,control, and age (pp. 217–248). Oxford: OxfordUniversity Press.

Canli, T., Zhao, Z., Brewer, J., Gabrieli, J. D., & Cahill, L.(2000). Event-related activation in the human amygdalaassociates with later memory for individual emotionalexperience. Journal of neuroscience, 20(19), RC99.

Christoff, K., & Gabrieli, J. D. E. (2000). The frontopolarcortex and human cognition: Evidence for a rostrocaudalhierarchical organization within the human prefrontalcortex. Psychobiology, 28(2), 168–186.

Christoff, K., Ream, J. M., Geddes, L. P., & Gabrieli, J. D.(2003). Evaluating self-generated information: Anteriorprefrontal contributions to human cognition. BehavioralNeuroscience, 117(6), 1161–1168.

Corcoran, R. (2000). Theory of Mind in Other ClinicalPopulations. In S. Baron-Cohen, H. Tager-Flusberg &D. Cohen (Eds.), Understanding other minds:Perspectives from autism and developmental cognitiveneuroscience (2nd ed.). Oxford: University Press.

Corcoran, R., & Frith, C. D. (2003). Autobiographical mem-ory and theory of mind: Evidence of a relationship inschizophrenia. Psychological medicine, 33(5), 897–905.

Cox, R. W. (1996). AFNI: Software for analysis and visua-lization of functional magnetic resonance neuroimages.Computers and Biomedical Research, 29, 162–173.

Damasio, A. R., Tranel, D., & Damasio, H. (1990).Individuals with sociopathic behavior caused by frontaldamage fail to respond autonomically to social stimuli.Behavioural Brain Research, 41, 81–94.

Decety, J. (2011). The neuroevolution of empathy. Annals ofthe New York Academy of Sciences, 1231, 35–45.

Decety, J., & Jackson, P. L. (2006). A Social-NeurosciencePerspective on Empathy. Current Directions inPsychological Science, 15(2), 54–58.

Decety, J., & Sommerville, J. A. (2003). Shared representa-tions between self and other: A social cognitive neu-roscience view. Trends in Cognitive Sciences, 7(12),527–533.

Eslinger, P. J. (1998). Neurological and neuropsychologicalbases of empathy. European Neurology, 39(4), 193–199.

Farrow, T. F., Zheng, Y., Wilkinson, I. D., Spence, S. A.,Deakin, J. F., Tarrier, N., . . . Woodruff, P. W. (2001).Investigating the functional anatomy of empathy andforgiveness. NeuroReport, 12(11), 2433–2438.

Field, A. (2005). Discovering statistics using SPSS (2nded.). London: SAGE Publications.

Fink, G. R., Markowitsch, H. J., Reinkemeier, M.,Bruckbauer, T., Kessler, J., & Heiss, W. D. (1996).Cerebral representation of one’s own past: Neural net-works involved in autobiographical memory. TheJournal of Neuroscience: The official journal of theSociety for Neuroscience, 16(13), 4275–4282.

Frith, C., & Frith, U. (1999). Understanding other mindsperspectives from developmental cognitive neuroscience.Oxford: Oxford University Press.

Frith, U., & Blakemore, S. J. (2003). Social cognition.Paper presented at the Foresight Cognitive SystemsProject, London.

Frith, U., & Frith, C. D. (2003). Development and neuro-physiology of mentalizing. Philosophical Transactionsof the Royal Society of London. Series B, BiologicalSciences, 358(1431), 459–473.

Gallagher, H. L., & Frith, C. D. (2003). Functional imagingof “theory of mind.” Trends in Cognitive Sciences, 7(2),77–83.

Gilbert, S. J., & Burgess, P. W. (2008). Executive function.Current Biology, 18(3), R110–114.

Gilbert, S. J., Spengler, S., Simons, J. S., Steele, J. D.,Lawrie, S. M., Frith, C. D, & Burgess, P. W. (2006).Functional specialization within rostral prefrontal cortex(area 10): A meta-analysis. Journal of CognitiveNeuroscience, 18(6), 932–948.

Gusnard, D. A., Akbudak, E., Shulman, G. L., & Raichle,M. E. (2001). Medial prefrontal cortex and self-referen-tial mental activity: Relation to a default mode of brainfunction. Proceedings of the National Academy ofSciences of the United States of America, 98(7), 4259–4264.

Hamann, S. B., Ely, T. D., Grafton, S. T., & Kilts, C. D.(1999). Amygdala activity related to enhanced memoryfor pleasant and aversive stimuli. Nature Neuroscience,2(3), 289–293.

Hynes, C. A., Baird, A. A., & Grafton, S. T. (2006).Differential role of the orbital frontal lobe in emotionalversus cognitive perspective-taking. Neuropsychologia,44(3), 374–383.

Kalbe, E., Schlegel, M., Sack, A. T., Nowak, D. A.,Dafotakis, M., Bangard, C., & Brand, M. (2010).Dissociating cognitive from affective theory of mind: ATMS study. Cortex, 46(6), 769–780.

Krämer, U. M., Mohammadi, B., Donamayor, N., Samii, A.,& Munte, T. F. (2010). Emotional and cognitive aspectsof empathy and their relation to social cognition—anfMRI—study. Brain research, 1311, 110–120.

Lane, R. D., Reiman, E. M., Bradley, M. M., Lang, P. J.,Ahern, G. L., Davidson, R. J., … Schwartz, G. E.(1997). Neuroanatomical correlates of pleasant andunpleasant emotion. Neuropsychologia, 35(11), 1437–1444.

Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (1997).International affective picture system (IAPS): Technicalmanual and affective ratings. Gainesville, FL: NIMHCenter for the Study of Emotion and Attention,University of Florida.

Leiberg, S., & Anders, S. (2006). The multiple facets ofempathy: A survey of theory and evidence. Progress inbrain research, 156, 419–440.

Lieberman, M. D., & Cunningham, W. A. (2009). Type Iand Type II error concerns in fMRI research: Re-balancing the scale. Social Cognitive and AffectiveNeuroscience, 4(4), 423–428.

Mitchell, J. P. (2008). Activity in right temporo-parietaljunction is not selective for theory-of-mind. CerebralCortex, 18(2), 262–271.

Morrison, J. (2004). Understanding others by understandingthe self: Neurobiological models of empathy and theirrelevance to personality disorders. The Canadian Childand Adolescent Psychiatry Review, 13(3), 68–73.

Olson, I. R., Plotzker, A., & Ezzyat, Y. (2007). TheEnigmatic temporal pole: A review of findings on socialand emotional processing. Brain, 130(Pt 7), 1718–1731.

Phan, K. L., Wager, T., Taylor, S. F., & Liberzon, I. (2002).Functional neuroanatomy of emotion: A meta-analysis ofemotion activation studies in PET and fMRI.NeuroImage, 16(2), 331–348.

EMPATHY, TOM, SELF–OTHER DIFFERENTIATION 61

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

14:

48 1

3 Fe

brua

ry 2

014

Rankin, K. P., Kramer, J. H., & Miller, B. L. (2005).Patterns of cognitive and emotional empathy in fronto-temporal lobar degeneration. Cognitive and BehavioralNeurology: Official Journal of the Society for Behavioraland Cognitive Neurology, 18(1), 28–36.

Reniers, R. L. E. P., Corcoran, R., Drake, R., Shryane,N. M., & Völlm, B. A. (2011). The QCAE: A question-naire of cognitive and affective empathy. Journal ofPersonality Assessment, 93(1), 84–95.

Rosenthal, R. (1991). Meta-analytic procedures for socialresearch (Revised ed.). Newbury park, CA: Sage.

Rozin, P., & Royzman, E. B. (2001). Negativity bias, nega-tivity dominance, and contagion. Personality and SocialPsychology Review, 5(4), 296–320.

Ruby, P., & Decety, J. (2001). Effect of subjective per-spective taking during simulation of action: A PETinvestigation of agency. Nature Neuroscience, 4(5),546–550.

Ruby, P., & Decety, J. (2003). What you believe versus whatyou think they believe: A neuroimaging study of con-ceptual perspective-taking. The European Journal ofNeuroscience, 17(11), 2475–2480.

Ruby, P., & Decety, J. (2004). How would you feel versushow do you think she would feel? A neuroimaging studyof perspective-taking with social emotions. Journal ofCognitive Neuroscience, 16(6), 988–999.

Russell, T. A., Tchanturia, K., Rahman, Q., & Schmidt, U.(2007). Sex differences in theory of mind: A male advan-tage on Happé’s “cartoon” task. Cognition & Emotion,21(7), 1554–1564.

Salas, C. E., Radovic, D., & Turnbull, O. H. (2012). Inside-out: Comparing internally generated and externally gen-erated basic emotions. Emotion, 12(3), 568–578.

Saxe, R., & Kanwisher, N. (2003). People thinking aboutthinking people. The role of the temporo-parietal junc-tion in “theory of mind.” NeuroImage, 19(4), 1835–1842.

Saxe, R., & Powell, L. J. (2006). It’s the thought that counts:Specific brain regions for one component of theory ofmind. Psychological Science: A Journal of the AmericanPsychological Society, 17(8), 692–699.

Saxe, R., & Wexler, A. (2005). Making sense of anothermind: The role of the right temporo-parietal junction.Neuropsychologia, 43(10), 1391–1399.

Schmitz, T. W., Kawahara-Baccus, T. N., & Johnson, S. C.(2004). Metacognitive evaluation, self-relevance, and theright prefrontal cortex. NeuroImage, 22(2), 941–947.

Seitz, R. J., Schafer, R., Scherfeld, D., Friederichs, S.,Popp, K., Wittsack, H. J., . . . Franz, M. (2008).Valuating other people’s emotional face expression: Acombined functional magnetic resonance imaging and

electroencephalography study. Neuroscience, 152(3),713–722.

Shamay-Tsoory, S. G. (2011). The neural bases for empathy.Neuroscientist, 17(1), 18–24.

Shamay-Tsoory, S. G., Tomer, R., & Aharon-Peretz, J.(2005). The neuroanatomical basis of understanding sar-casm and its relationship to social cognition.Neuropsychology, 19(3), 288–300.

Shamay-Tsoory, S. G., Tomer, R., Berger, B. D., & Aharon-Peretz, J. (2003). Characterization of empathy deficitsfollowing prefrontal brain damage: The role of the rightventromedial prefrontal cortex. Journal of CognitiveNeuroscience, 15(3), 324–337.

Shamay-Tsoory, S. G., Tomer, R., Goldsher, D., Berger, B. D.,& Aharon-Peretz, J. (2004). Impairment in cognitive andaffective empathy in patients with brain lesions:Anatomical and cognitive correlates. Journal of Clinicaland Experimental Neuropsychology, 26(8), 1113–1127.

Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Amorim, P.,Janavs, J., Weiller, E., . . . Dunbar. G. C. (1998). TheMini-International Neuropsychiatric Interview (M.I.N.I.): The development and validation of a structured diag-nostic psychiatric interview for DSM-IV and ICD-10.The Journal of clinical psychiatry, 59(Suppl 20), 22–33.

Sommer, M., Dohnel, K., Sodian, B., Meinhardt, J.,Thoermer, C., & Hajak, G. (2007). Neural correlates oftrue and false belief reasoning. NeuroImage, 35(3),1378–1384.

Talairach, J., & Tournoux, P. (1988). Co-Planar StereotaxicAtlas of the Human Brain (1st ed.). New York, NY:Thieme Medical Publishers.

Vaish, A., Grossmann, T., & Woodward, A. (2008). Not allemotions are created equal: The negativity bias in social-emotional development. Psychological Bulletin, 134(3),383–403.

Van der Meer, L., Groenewold, N. A., Nolen, W. A.,Pijnenborg, M., & Aleman, A. (2011). Inhibit yourselfand understand the other: Neural basis of distinct pro-cesses underlying theory of mind. NeuroImage, 56(4),2364–2374.

Vreeke, G. J., & van der Mark, I. L. (2003). Empathy, anintegrative model. New Ideas in Psychology, 21, 177–207.

Völlm, B. A., Taylor, A. N., Richardson, P., Corcoran, R.,Stirling, J., McKie, S., . . . Elliott, R. (2006). Neuronalcorrelates of theory of mind and empathy: A functionalmagnetic resonance imaging study in a nonverbal task.NeuroImage, 29(1), 90–98.

Young, L., Dodell-Feder, D., & Saxe, R. (2010). What getsthe attention of the temporo-parietal junction? An fMRIinvestigation of attention and theory of mind.Neuropsychologia, 48(9), 2658–2664.

62 RENIERS ET AL.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

14:

48 1

3 Fe

brua

ry 2

014