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A Key Role for Similarity in Vicarious Reward

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A Key Role for Similarity in Vicarious Reward
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  A Key Role for Similarity inVicarious Reward Dean Mobbs, 1 *  Rongjun Yu, 1 †  Marcel Meyer, 1,2 †  Luca Passamonti, 1,3 Ben Seymour, 4,5 Andrew J. Calder, 1 Susanne Schweizer, 1 Chris D. Frith, 4,6 Tim Dalgleish 1 G ameshowsareoneofthemostpopularandenduring genres in television culture. Yet why we possess an inherent tendency toenjoyseeingunrelatedstrangerswinin theabsenceof personal economic gain is unclear ( 1 ). One ex- planationisthatgameshoworganizersuse contestants who have similaritiestotheviewingpopulation,therebykin-dling their likeability, familiarity, andkin-motivatedresponses[e.g.,prosocial behavior ( 1 ,  2 )]. Social-cognitive ac-counts posit that, to simulate another  ’ sinternal states successfully, we must deem ourselves as similar to the target  person ( 3 ). We tested two predictions:Seeing a socially desirable contestant win will modulate neural systems as-sociatedwithreward,andthisreward-ingexperienceisfurtherinfluencedby perceived similarity to a contestant (i.e., similar attitudes and values).Volunteers first viewed films of two confederate contestants answer-ing questions about personal, social,and ethical issues. These contestantsexpressed themselves in either a so-cially desirable [SD (i.e., empathetic)]or socially undesirable [SU (i.e., in-appropriate values)] manner ( 4 ). Tocheck that this social judgment manip-ulationworked,volunteersperformeda likeableness trait rating task ( 5 ). Posi-tivetraitscoreswerehigherfortheSDcontestant, whereas negative traits weresignificantlyhigherfortheSUcontes-tant (  F   = 107.9,  P   < 0.0005) (Fig. 1A). Next, vol-unteers underwent functional magnetic resonanceimaging scanning while they viewed SD and SUcontestants playing a game where the contestantsmadedecisionsastowhetheranunseencardwould behigherorlowerthanasecondunseencard( 6  ).Acorrect decision resulted in the contestant winning£5 ( 4 ). The number of wins and probabilities of winning were identical across contestants. After volunteers watched thecontestantsplay,theyplayedthe game for themselves ( 4 ).Subjective ratings acquired after the experiment showed that volunteers perceived themselves to bemore similar to, and in agreement with, the SDcontestant (Fig. 1B), as well as found it morerewarding to see her win (Fig. 1C) (all  t   tests:  P   <0.05)( 4 ).Likewise,correlationswerefoundbetweensimilarity and agreeableness and between positivelikeablenessscores and howrewarding itwas to seetheSDcontestantwin.Bothempathyandperspective-takingscores( 4 )correlatedwithsimilaritytotheSDcontestant (all Pearson ’ s:  P   < 0.05) ( 4 ). No sex dif-ferences were found for similarity to SD and SUcontestants [see ( 4 ) for additional results].Forthebrain-imagingdata,wefirstexaminedthecorrelation between how rewarding the volunteersfounditwhenobservingtheSDversustheSUcon-testant winning ( 4 ). We found a significant increaseinventralstriatum(VS)activity,aregionalsoactivewhen the volunteers themselves won while playingthe game [Fig. 1D; see ( 4 ) for additional analysis]and known to be involved in the experience of rewardandelation( 7  ).WenextcorrelatedperceivedsimilarityscoresfortheSDversustheSUcontestant win, which resulted in elevated ventromedial pre-frontal cortex (vmPFC) and ventral anterior cin-gulate cortex (vACC) activity (Fig. 1E). Althoughsocialpsychologicalresearchshowsthatlikeabilityand similarity are closely correlated, subtraction of the likeability ratings from the similarity ratingsalso resulted in significantly more vACC activity(Fig. 1F), supporting this region ’ s putative role inself-other similarity ( 4 ,  8 ).We next tested whether the relationship betweenthe VS and vACC was influenced by perceived sim-ilarity. We used psychophysiological interaction toexamine connectivity between the VS and the vACC(using an independentVSseedfromthe self-play con-dition).Wesawasignificantpositiverelationshipbe-tween similarity and connectivity between these tworegionsfortheSD-versus-SUcontestantwincontrast (Fig. 1F). No such modulation was found for like-ability ratings ( 4 ). Given the vACC ’ s unidirectional projectionstotheVS,thevACCmaymodulatepos-itive feelings in situations relevant to the self ( 8 ).Untilnow,studiesoftheneuralrepresentationof others ’ mentalstateshavebeenconcernedwithnega-tiveemotions(e.g.,empathyforpain).Here,weshowthatsimilarmechanismstransfertoposi-tive experiences such that observing aSD contestant win increases both sub- jectiveandneuralresponsesinvicariousreward.Such vicarious reward increaseswith perceived similarity and vACC ac-tivity,aregionimplicatedinemotionandrelevancetoself( 3 , 9 ).Althoughotherso-cial preferences (e.g., fairness) ( 10 ) arelikelytoplayaroleinvicariousreward,our resultssupportaproximateneurobiologicalmechanism,possiblylinkedtokin-selectionmechanisms,whereprosocialbehaviorex-tends to unrelated strangers ( 2 ). References and Notes 1. E. Fehr, U. Fischbacher,  Nature  425 , 785(2003).2. J. H. Park, M. Schaller,  Evol. Hum. Behav. 26 , 158 (2005).3. J. P. Mitchell, C. N. Macrae, M. R. Banaji, Neuron  50 , 655 (2006).4. Materials and methods are available assupporting material on  Science  Online.5. N. H. Anderson,  J. Pers. Soc. Psychol.  9 ,272 (1968).6. K. Preuschoff, P. Bossaerts, S. R. Quartz, Neuron  51 , 381 (2006).7. D. Mobbs  et al .,  Neuron  40 , 1041 (2003).8. J. M. Moran  et al .,  J. Cogn. Neurosci.  18 ,1586 (2006).9. B. A. Völlm  et al .,  Neuroimage  29 , 90 (2006).10. T. Singer  et al .,  Nature  439 , 466 (2006).11. We thank M. Ewbank, R. Henson, and E. Hillfor their help. This work was conducted at the Cognition andBrain Sciences Unit and supported by the MRC. Supporting Online Material www.sciencemag.org/cgi/content/full/324/5929/900/DC1Materials and MethodsFigs. S1 to S5References6 January 2009; accepted 13 March 200910.1126/science.1170539 BREVIA 1 Cognition and Brain Sciences Unit, Medical Research Council(MRC), Cambridge CB2 7EF, UK.  2 Department of Psychology,University of Birmingham, Birmingham B15 2TT, UK.  3 ConsiglioNazionale delle Ricerche, ISN, Cosenza 87050, Italy.  4 WellcomeTrust Centre for Neuroimaging, University College London (UCL),London WC1N 3BG, UK.  5 The ESRC Centre for Economic Learn-ing and Social Evolution (UCL), Drayton House, Gordon Street,London WC1H OAN, UK.  6 Centre for Functional IntegrativeNeuroscience, Aarhus University, DK-800 Aarhus, Denmark.*To whom correspondence should be addressed. E-mail:dean.mobbs@mrc-cbu.cam.ac.uk † These authors contributed equally to this work. Fig. 1.  ( A ) Results from the trait likeability ratings showing SD and SU con-testantscoresforpositiveandnegativetraitattributions.Volunteers( B )perceivedthemselves as significantly more similar to the SD contestant and ( C ) found itmore rewarding to see the SD contestant win. Error bars indicate SEM. ( D )Significant activity associated with self-win (purple) and correlation betweenhow rewarding it was to see the SD versus the SU win (pink). ( E ) Correlationbetween similarity, vACC and vmPFC activity, and ( F ) psychophysiological inter-action showing connectivity values (i.e., connectivity during SD winning minusconnectivity during SU winning) and individual scores of similarity ( 4 ). 15 MAY 2009 VOL 324  SCIENCE  www.sciencemag.org 900    o  n   J  u   l  y   2   7 ,   2   0   0   9  w  w  w .  s  c   i  e  n  c  e  m  a  g .  o  r  g   D  o  w  n   l  o  a   d  e   d   f  r  o  m 
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