Neural Mechanisms of the Rejection-Aggression Link

University of Kentucky University of Kentucky

UKnowledge UKnowledge

Psychology Faculty Publications Psychology

5-1-2018

Neural Mechanisms of the Rejection-Aggression Link Neural Mechanisms of the Rejection-Aggression Link

David S Chester Virginia Commonwealth University

Donald R Lynam Purdue University

Richard Milich University of Kentucky richardmilichukyedu

C Nathan DeWall University of Kentucky nathandewallukyedu

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Repository Citation Repository Citation Chester David S Lynam Donald R Milich Richard and DeWall C Nathan Neural Mechanisms of the Rejection-Aggression Link (2018) Psychology Faculty Publications 151 httpsuknowledgeukyedupsychology_facpub151

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Digital Object Identifier (DOI) httpsdoiorg101093scannsy025

NotesCitation Information NotesCitation Information Published in Social Cognitive and Affective Neuroscience v 13 no 5 p 501-512

copy The Author(s) (2018) Published by Oxford University Press

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (httpcreativecommonsorglicensesby-nc40) which permits non-commercial re-use distribution and reproduction in any medium provided the original work is properly cited For commercial re-use please contact journalspermissionsoupcom

This article is available at UKnowledge httpsuknowledgeukyedupsychology_facpub151

Neural mechanisms of the rejectionndashaggression linkDavid S Chester1 Donald R Lynam2 Richard Milich3 and C Nathan DeWall3

1Department of Psychology Virginia Commonwealth University Richmond VA 23284 USA 2Department ofPsychological Sciences Purdue University West Lafayette IN 47907 USA and 3Department of PsychologyUniversity of Kentucky Lexington KY 40506 USA

Correspondence should be addressed to David S Chester Department of Psychology Virginia Commonwealth University 808 West Franklin StRichmond VA 23284 USA E-mail dschestervcuedu

Abstract

Social rejection is a painful event that often increases aggression However the neural mechanisms of this rejectionndashaggression link remain unclear A potential clue may be that rejected people often recruit the ventrolateral prefrontalcortexrsquos (VLPFC) self-regulatory processes to manage the pain of rejection Using functional MRI we replicated previous linksbetween rejection and activity in the brainrsquos mentalizing network social pain network and VLPFC VLPFC recruitment duringrejection was associated with greater activity in the brainrsquos reward network (ie the ventral striatum) when individuals weregiven an opportunity to retaliate This retaliation-related striatal response was associated with greater levels of retaliatoryaggression Dispositionally aggressive individuals exhibited less functional connectivity between the ventral striatum andthe right VLPFC during aggression This connectivity exerted a suppressing effect on dispositionally aggressive individualsrsquogreater aggressive responses to rejection These results help explain how the pain of rejection and reward of revengemotivate rejected people to behave aggressively

Key words aggression social rejection reward frontostriatal fMRI

Introduction

It is not hard to imagine how an individual pushed against theirwill to the fringes of a community might react violentlytowards the perceived sources of such pain Yet our under-standing of the precise neural mechanisms that link experien-ces of rejection to aggressive retaliation is imperfect In whatfollows we summarize a brain imaging project that sought tounderstand the biological and psychological forces that drivethe rejectionndashaggression link Specifically we tested whetherthe neural regulation of the pain of rejection magnified the sub-sequent lsquosweetnessrsquo or reward of taking revenge upon thesource of rejection We then tested whether this interplaybetween regulatory and reward reactivity was linked to greaterseverity of the aggressive retaliatory response Building on thiswe tested whether this mechanism helped explain why somepeople tend to be more dispositionally aggressive than others

The rejectionndashaggression link

Social rejection occurs when active attempts at social inclusionand belonging are rebuffed by the targets of affiliative acts(Williams 2009) Such experiences are pervasive and have long-term adverse effects on human health Indeed social rejectionis reliably linked to greater anxiety depression and learnedhelplessness (Leary 1990 Williams 2009) These internalizedconsequences of rejection are juxtaposed against this phenom-enonrsquos more externalizing consequences such as aggressionSocial rejection is one of the most well-established causes ofaggression (Leary et al 2006 Ren et al 2018) In laboratory set-tings rejected individuals exhibit heightened aggressive behav-ior towards both their rejecters and innocent bystanders(Twenge et al 2001 Buckley et al 2004) As evidence that thisphenomenon extends out into the broader world experiencesof rejection are thematic among the lives of the majority of

Received 3 October 2017 Revised 25 February 2018 Accepted 19 March 2018

VC The Author(s) (2018) Published by Oxford University PressThis is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (httpcreativecommonsorglicensesby-nc40) which permits non-commercial re-use distribution and reproduction in any medium provided the original work is properly citedFor commercial re-use please contact journalspermissionsoupcom

501

Social Cognitive and Affective Neuroscience 2018 501ndash512

doi 101093scannsy025Advance Access Publication Date 28 March 2018Original article

Dow

nloaded from httpsacadem

icoupcomscanarticle-abstract1355014956231 by U

niversity of Kentucky Libraries user on 16 January 2019

school shooters (Leary et al 2003) Investigations into the psy-chological processes that motivate the rejectionndashaggression linkhave revealed anger (Chow et al 2008) hostile cognitive biases(DeWall et al 2009) disinhibition (Rajchert and Winiewski2016) non-adherence to societal norms (Poon and Teng 2017)and desires to re-establish feelings of control (Warburton et al2006 Wesselmann et al 2010) as likely motivations Althoughthe psychological mechanisms of this effect are becoming wellexplicated the neural mechanisms of the rejectionndashaggressionlink remain largely unexamined

Neural correlates of rejection

Rejection threatens the fundamental human need for socialconnections (MacDonald and Leary 2005) Social Pain OverlapTheory posits that the brain evolved to respond to this socialinjury with a broad and powerful recruitment of multiple neuralsystems that include brain regions critical to the experience ofpain (Eisenberger and Lieberman 2004)

Social pain DACC and anterior insula As outlined in Social PainOverlap Theory social pain is the aversive affective andsomatic response to perceptions of social rejection (Eisenbergerand Lieberman 2004 Eisenberger 2012) As evidence of thisfunctional neuroimaging has associated experimental induc-tions of exclusion with activity in brain regions associated withthe affective component of pain anterior insula dorsal anteriorcingulate cortex (DACC Eisenberger et al 2003 Eisenberger2012 Rotge et al 2014) Reactivity of the DACC to rejection isassociated with greater retaliatory aggression though onlyamong individuals with relatively poor executive functioning(Chester et al 2014) This finding offers initial evidence that thebrainrsquos social pain response to rejection may exert a motivatinginfluence on subsequent aggressive retaliation

Regulation of social pain VLPFC Social pain like physical pain isnot an unchecked response to stimuli Instead robust regula-tory mechanisms exist to modulate neural pain reactivity (Price2000) Numerous studies point to the ventrolateral prefrontalcortexrsquos (VLPFC) role in responding to socially painful events(Eisenberger et al 2003 Chester and DeWall 2014) In this con-text the VLPFC exerts a regulatory role that inhibits the subjec-tive experience of pain by inhibiting brain regions that generatethe distressing experience of pain (Eisenberger et al 2003Yanagisawa et al 2011 Kawamoto et al 2012) These findingsfit with a much larger literature demonstrating the critical roleof the VLPFC in regulating distress and negative affect (Wageret al 2008)

Affect regulation is one of an array of functions in theVLPFC which largely involve inhibition (Aron et al 2014)Indeed the VLPFC is a relatively large and heterogeneous regionof the prefrontal cortex that is anatomically and functionallyheterogeneous (Levy and Wagner 2011) Most posterior regionsthat are close to the motor regions of the frontal lobe tend tofacilitate the inhibition of concrete motor and behavioralresponses (pars opercularistriangularis Levy and Wagner2011 Aron et al 2014) whereas more anterior VLPFC regionstend to subserve the inhibition and regulation of more abstractemotional and cognitive processes (pars triangularisorbitalisWager et al 2008 Buhle et al 2014) Yet how might VLPFCrecruitment during rejection impact the neural underpinningsof retaliatory aggression

Neural correlates of retaliatory aggression

Retaliatory aggressive behavior is associated with greater activ-ity in a host of cortical regions during the act (dorsomedial PFCposterior cingulate cortex anterior and posterior insula Krameret al 2007 Lotze et al 2007 Dambacher et al 2014 Chester andDeWall 2016 Emmerling et al 2016) Germane to this projectretaliatory aggression has also been linked to activity in theventral striatum during the aggressive act a neural region reli-ably linked to the experience of pleasure and reward (Chesterand DeWall 2016) The VLPFC exerts a robust regulatory influ-ence on the ventral striatum the connectivity of which predictsgreater self-regulatory success (eg Wagner et al 2013)Retaliatory aggression is associated with reduced connectivitybetween the ventral striatum and the VLPFC potentially indi-cating a dysregulated reward response (Buades-Rotger et al2016 Chester and DeWall 2016 Chester 2017) These findingssuggest that a likely neural mechanism underlying retaliatoryaggression is a magnified and dysregulated striatal responsethat may serve to reinforce such aggressive acts Our results fur-ther fit with psychological research that implicates reward andpleasure as central components of revenge-seeking tendencies(Chester and DeWall 2018b) The pleasure of retaliation likelymotivates aggression in both prospective and concurrent man-ners with individuals seeking out acts of retaliatory aggressionfor the anticipated and currently felt rewards it bringsHowever it remains unknown how such striatal mechanismsinteract with neural responses to rejection

The excessive recruitment model

Conventionally VLPFC recruitment during aversive experiencesis theorized to be an adaptive regulatory response (Wager et al2008) Indeed self-regulation failures (eg aggression) that occurbecause of aversive experiences (eg rejection) are thought toarise from an under-recruitment of the VLPFC (Heatherton andWagner 2011) Recent work has called for modification to thisprevailing paradigm suggesting that while this conceptualiza-tion of VLPFC recruitment may be correct in the short-term(ie effective inhibition of distress during the aversive experi-ence) such VLPFC recruitment undermines longer-term self-regulatory success (Chester and DeWall 2014 Chester and Riva2016 Chester et al 2016) As evidence for this new approachperforming aversive taxing and prefrontally mediatedtasks has been linked to subsequent self-regulatory failure(eg Inzlicht and Gutsell 2007) Participants who were attempt-ing to restrict their calorie intake exhibited greater reward reac-tivity to food stimuli and less functional connectivity betweenreward regions and the lateral PFC after they had to repeatedlyregulate their attention away from a distracting stimulus(Wagner et al 2013) When racially biased Whites interactedface-to-face with a Black individual their lateral PFC recruit-ment to Black faces predicted subsequent self-control impair-ment (Richeson et al 2003) These findings suggest that greaterlateral PFC recruitment during aversive experiences may notprove adaptive in the long-term

In the context of rejection greater VLPFC recruitment duringrejection predicted a magnified and prefrontally dysregulatedventral striatum response to appetitive cues on a subsequentlab task (Chester and DeWall 2014) Extending outside of thelab greater rejection-related VLPFC activity was associated withself-regulatory failures and increased cravings (Chester andDeWall 2014) These results formed the basis of the excessiverecruitment model which posits that VLPFC recruitment inresponse to aversive experiences undermines subsequent

502 | Social Cognitive and Affective Neuroscience 2018 Vol 13 No 5

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self-regulation by impairing the VLPFCrsquos regulatory effects onthe ventral striatum (Chester and DeWall 2014 Chester andRiva 2016 Chester et al 2016)

Further evidence for this model was found by observing thatindividuals who chronically experienced self-regulatory failurein response to aversive experiences also exhibited an exacer-bated VLPFC response to aversive situations (Chester et al2016) This greater VLPFC response was associated with poorerinhibitory success and predicted greater alcohol consumption 1month and 1 year later It is important to note that self-regulation is not localized to the VLPFC but is subserved by ahost of other regions including the dorsolateral and dorsome-dial PFC (Kober et al 2010) The excessive recruitment modelmay indeed apply to these other regions yet the evidence formaking such claims about these other brain regions is currentlylacking As such our hypotheses focus on the role of the VLPFCin self-regulatory failure Because aggression can be construedas a self-regulatory failure (Denson et al 2012) this excessiverecruitment model might help explain why rejected peoplebehave aggressively Further this model may help explainlarger patterns of aggressive behavior that extend beyond theindividual rejection incident

Trait aggression a potential reinforcing role of striatalresponses to revenge

Physical aggression is typically thought of in the context of asingle act but aggression is also a dispositional trait-like con-struct (Buss and Perry 1992) Trait aggression shows substantialgeneralizability across cultures between-individual variabilitypredictive validity of actual aggressive behavior and within-individual test-retest reliability (Huesmann et al 1984 Buss andPerry 1992 Cote et al 2006 Gerevich et al 2007 Webster et al2014) Together these findings provide substantial support forthe existence of physical aggressiveness as a personality trait

The underlying neurobiology of trait physical aggressionremains largely unknown with few published studies on thistopic (eg Carre et al 2013) An unexamined neural mechanismmight underlie trait aggression striatally mediated reinforce-ment The ventral striatumrsquos role in promoting the reinforce-ment of behaviors that become habitual (eg cocaine andalcohol abuse) is well-established (Everitt and Robbins 2005) Asa behavior that recruits the ventral striatum (Chester andDeWall 2016) retaliatory aggression is a candidate for an actthat can become striatally reinforced leading to durable pat-terns of aggressive behavior across time and situations

The present study

The main goal of this project was to better understand the neu-ral mechanisms of the rejectionndashaggression link and how theymight contribute to larger patterns of aggressive traits Basedoff the excessive recruitment model (Chester et al 2016) wepredicted that greater VLPFC activity during social rejectionwould be associated with more ventral striatum activity duringopportunities for retaliatory aggression Seeking to replicateprevious work (Chester and DeWall 2016) we further predictedthat ventral striatum activity during retaliatory opportunitieswould positively correlate with greater actual retaliation Thesefindings would support a temporal sequence whereby VLPFCactivity during rejection promotes subsequent retaliationthrough a magnified ventral striatum response We further pre-dicted that dispositionally physically aggressive individualswould exhibit greater dysregulation in the ability of the VLPFC

to functionally inhibit the ventral striatum during retaliatoryaggression

To test these predictions a sample of undergraduates expe-rienced social acceptance and then rejection from twosame-sex strangers and then were given an opportunity toaggressively retaliate against one of their rejecters allwhile undergoing functional magnetic resonance imaging(fMRI) Participants then reported the extent of their aggressivetraits and another measure of whether participants typicallyexperienced pleasure during retaliatory aggression whichserved to assist our reverse inference that the ventral striatumactivity that we expected to observe during retaliatory aggres-sion reflected reward and not some other process

Materials and methodsEthics statement

All participants provided informed consent before performingany research procedures and all research procedures were con-ducted in accordance with human participants protection regu-lations as set forth by governmental and institutional policiesWe as authors declare no conflicts of interest relevant to theresearch described in our manuscript Data from a subset ofthese participants have been published in a separate manu-script (Chester and DeWall 2018a)

Participants

Participants were 60 healthy right-handed English-fluentyoung adults (38 females 22 males age M frac14 2028 SDfrac14 277range 18ndash30) Participants were either undergraduates recruitedthrough the introductory psychology subject pool in exchangefor credit towards their coursersquos research requirement and animage of their brain or general community members recruitedin exchange for $50 and an image of their brain Exclusionarycriteria were assessed by an online questionnaire whichincluded body mass index above 30 claustrophobia colorblindness mental or neural pathology metallic objects in thebody prior head trauma and psychoactive medication use

Materials

Angry mood improvement inventory The 32-item Angry MoodImprovement Inventory (AMII) assesses the degree to whichindividuals tend to control and express their aggressive behav-ior to improve their mood when they are upset (Bushman et al2001) The eight-item Expression-Outwards subscale of the AMIIassesses the tendency to express aggression outwardly in orderto experience mood repair (sample items lsquoTo improve my moodwhen I am upset I express my angerrsquo lsquoTo improve my moodwhen I am upset I strike out at whatever angers mersquo)Participants indicate the frequency of these mood-motivatedactions along a 1 (Never) to 5 (Often) scale

Brief aggression questionnaire To measure trait physical aggres-sion we employed the Brief Aggression Questionnaire (BAQWebster et al 2014) The BAQ contains 12 items that comprisefour factors anger (sample item lsquoI have trouble controlling mytemperrsquo) hostility (sample item lsquoI sometimes feel that peopleare laughing at me behind my backrsquo) physical aggression (sam-ple item lsquoGiven enough provocation I may hit another personrsquo)and verbal aggression (sample item lsquoMy friends say that Irsquom

D S Chester et al | 503

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somewhat argumentativersquo) Participants responded to eachitem along a 1 (disagree) to 7 (agree) scale

Procedure

Participants arrived at the neuroimaging laboratory where theyhad the study explained to them which entailed a cover storythat the study was actually examining the role of brain func-tioning during various cognitive tasks in promoting alcohol mis-use Further participants were instructed that they would becompleting the study with two partners who were in nearbytesting rooms To ensure the believability of this deception par-ticipants were told that they were the first participant to arriveand then asked to select a piece of paper that would determinewhich of the three MRI scanners they would be placed in (inreality there was only one MRI scanner) After being lsquoassignedrsquoto their MRI scanner participants were then screened to ensurethey would be safe and comfortable in the MRI environmentand then practiced the aggression task they would complete inthe MRI scanner Participants were then placed in an MRI scan-ner and had a high-resolution structural scan taken of theirbrain (see MRI Data Acquisition amp Preprocessing section formore details)

Cyberball task To induce an experience of social rejection in thefunctional neuroimaging environment we employed theCyberball social rejection task (Williams et al 2000 Eisenbergeret al 2003 Chester et al 2014) In this task participants wereinstructed to play a virtual ball-tossing game with two fictitiouspartners The ostensible purpose of the task was for participantsto mentally visualize the task as if it were occurring in real lifeso that we might understand the neural underpinnings of thehuman imagination The task proceeded across three blocks Inthe first two blocks participants received an equal number ofball-tosses from their two partners for 60 s per block(Acceptance condition) However in the third block after 30 sparticipants stopped receiving the ball from their partners whocontinuously threw it back-and-forth to one another for 50 s(Rejection condition) Baseline activation was captured by 10 slsquoRestrsquo trials that preceded each of the three blocks Total tasktime was 3 m 50 s

Aggression task After the rejection task participants completedan aggression task used in previous fMRI studies of aggression(Kramer et al 2007 Chester and DeWall 2016) In this task par-ticipants competed against one of their fictitious Cyberball part-ners who was supposedly in an MRI scanner nearby to see whocould press a button faster As an ostensible motivational com-ponent of the task participants were punished if they lost thecompetition via an aversive noise blast Conversely if partici-pants won the competition their opponent heard the noise blastand they did not Crucially the volume of the noise blast deliv-ered to their opponent was set by the participant and served asthe measure of aggressive behavior

The task consisted of 14 blocks with each block containingsix trials Each block began with a 10 s fixation cross that mod-eled baseline neural activity Then participants completed a75 s aggression trial in which they pressed a button that set thevolume of their partnerrsquos noise blast A blank screen thenappeared for a jittered duration (051015 s) which gave wayto a competition trial in which participants pressed a button asfast as they could when a red square appeared on the screen(454035 s duration) Participants then saw what volume leveltheir opponent set for them (5 s duration) Finally participants

saw whether they won or lost the competition (5 s duration) Ifparticipants lost the competition they heard an aversive noiseblast that varied from 1 (silence) to 4 (extremely loud thoughnot dangerous) Whether a given aggression trial was precededby their opponent setting a loud (3 4) or soft (1 2) volume leveldetermined whether the given trial was retaliatory (after a loudblast) or non-retaliatory (after a soft blast) Such retaliatory andnon-retaliatory trials were split fairly evenly (six retaliatory andeight non-retaliatory) and randomly presented with the excep-tion of the first trial which was always non-retaliatory Winsand losses were randomized and split evenly (seven wins andseven losses) Each of the 14 blocks lasted for 325 s for a totaltask time of 7 m 35 s

Participants completed a series of other functional scansthat were part of a separate project on impulsivity and thenexited the scanner Participants were placed in a nearby testingroom and completed a computerized battery of questionnairesincluding a demographics survey the Brief AggressionQuestionnaire and the Angry Mood Improvement InventoryParticipants were then fully debriefed about the deceptioninherent in the study and escorted from the laboratory withthanks At the onset of this debriefing was a structured suspi-cion probe that an experimenter verbally administered to eachparticipant (eg what do you think this study was about) Noparticipants expressed significant suspicion about the deceptiveelements of the study

MRI data acquisition and preprocessing

All MRI data were obtained using a 30 tesla Siemens MagnetomTrio scanner Echo planar BOLD images were acquired with aT2-weighted gradient across the entire brain with a 3D shim(matrix sizefrac14 64 64 field of viewfrac14 224 mm echo timefrac14 28 msrepetition timefrac14 25 s 35 mm3 isotropic voxel size 40 inter-leaved axial slices flip anglefrac14 90) To allow for registration tonative space a coplanar T1-weighted MP-RAGE scan was alsoacquired from each participant (1 mm3 isotropic voxel sizeecho timefrac14 256 ms repetition timefrac14 169 s flip anglefrac14 12)

The Oxford Center for Functional MRI of the Brain (FMRIB)rsquosSoftware Library (FSL version 50) was used to conduct all pre-processing and fMRI analyses (Smith et al 2004 Woolrich et al2009) Reconstructed functional volumes underwent headmotion correction to the median functional volume using FSLrsquosMCFLIRT tool FSLrsquos Brain Extraction Tool was used to removenon-brain tissue from all functional and structural volumesusing a fractional intensity threshold of 05 After a series ofdata quality checks functional volumes underwent interleavedslice-timing correction pre-whitening spatial smoothing (usinga 5 mm full-width-half-maximum Gaussian kernel) and tempo-ral high-pass filtering (120 s cutoff) These processed brain vol-umes were then fed into subsequent data analyses

Statistical analyses Functional MRI

Preprocessed fMRI datasets from both the rejection and aggres-sion tasks were analyzed using two levels of general linearmodels

First level (within-participants) Each participantrsquos whole-brainfunctional volumes were entered into a fixed-effects analysisthat modeled trials as events using a canonical double-gammahemodynamic response function with a temporal derivativeRegressors for the rejection task included Acceptance andRejection blocks while leaving lsquoRestrsquo trials un-modeled lsquoGet


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Readyrsquo trials were modeled as a nuisance regressor Regressors-of-interest for the aggression task included RetaliatoryAggression and Non-Retaliatory Aggression while leaving fixa-tion trials un-modeled Competition Pre-Competition HighProvocation Low Provocation Win and Lose trials wereincluded as nuisance regressors All six head motion parame-ters from each participant were modeled as nuisance regressorsfor each task

For the rejection task linear contrasts compared rejection toacceptance (RejectiongtAcceptance contrast) For the aggres-sion task linear contrasts compared retaliatory and non-retaliatory aggression to each other and to baseline fixationtrials (Retaliatory AggressiongtNon-Retaliatory Aggressioncontrast Retaliatory AggressiongtBaseline contrast Non-Retaliatory AggressiongtBaseline contrast) Resulting contrastimages from these analyses were first linearly registered tonative space structural volumes and then spatially normalizedto a Montreal Neurological Institute (MNI) stereotaxic spacetemplate image (resampled into 2 2 2 mm3 voxels)

Second level (across-participants) Each participantrsquos contrast vol-umes from the first level were then fed into FLAME 1rsquos grouplevel mixed effects GLM that created group average maps for allfour contrasts across the entire brain Cluster-based threshold-ing was applied to each of the group activation maps (Worsley2001 Heller et al 2006) Clusters were determined by applying aZgt 23 threshold to the voxels of each of the group-averagewhole-brain activation maps Family-wise error correction wasthen applied to each cluster based on Gaussian random fieldtheory (Plt 005)

Psychophysiological interaction analysis To assess functional con-nectivity during retaliatory aggression a psychophysiologicalinteraction (PPI) analysis was performed with the bilateral ven-tral striatum as a seed region-of-interest (ROI) using an anatom-ically and functionally defined region-of-interest (ROI) maskfrom the Wake Forest University Pickatlas (Maldjian et al 2003)This took the form of a first level within-participants analysiswith the addition of two new regressors to the previouslydescribed GLM the mean-centered timecourse of ventral stria-tum activity across the aggression task and an interaction termmultiplying the ventral striatum timecourse by retaliatoryaggression trials Linear contrasts compared the interactionbetween participantsrsquo ventral striatum timecourses and retalia-tory aggression and their interaction to participantsrsquo implicitbaseline Activation maps from this analysis were then fed intoa whole-brain regression analysis in which brain activity esti-mates from the PPI analysis were correlated with participantsrsquotrait physical aggression levels Clusters were determined byapplying a Zgt 23 threshold to each of the group-averagewhole-brain activation maps Family-wise error correction wasthen applied to each cluster based on Gaussian random fieldtheory (Plt 005) All tests were two-tailed

Statistical analyses mediation modeling ROI creationand parameter estimate extraction

In order to test whether participantsrsquo VLPFC recruitment duringrejection predicted greater subsequent aggression throughgreater striatal activity during retaliatory aggression we con-ducted a mediation analysis (using the PROCESS version 20macro for SPSS model 4 5000 bias-corrected and accelerated re-samples Hayes 2012) VLPFC activity was obtained from 8 mmspherical ROIs centered on peak activation voxels from the

rejection main effect contrast Voxels were determined to bewithin the VLPFC using the Automated Anatomical Labeling(AAL) atlasrsquo opercular orbital and triangular portions of theinferior frontal gyrus (Tzourio-Mazoyer et al 2002) Functionaldata from the voxels that comprised each ROI were converted tounits of percent signal change averaged across each participantand extracted as outlined by Mumford J httpmumfordboluclaeduperchange_guidepdf

Another such mediation model was run except that connec-tivity estimates from the Retaliatory Aggression PPI analysiswere entered as a mediator instead of VLPFC recruitment dur-ing rejection This additional exploratory mediation analysisserved the purpose of examining whether striatum-based func-tional connectivity helped to explain the link between VLPFCrecruitment during rejection and subsequent retaliatory aggres-sion All tests were two-tailed

Open practices

De-identified data necessary to reproduce all analyses from thisproject have been made publicly available at httpsosfion5bwhfiles

ResultsDescriptive statistics

BAQ One participant failed to complete the Brief AggressionQuestionnaire Analyses were constrained to the PhysicalAggression subscale of this questionnaire as the aggressivebehavior measured by our MRI task was physical as opposed toverbal in nature Physical Aggression subscale scores exhibitedsubstantial variability across the scalersquos possible 1ndash7 rangeMfrac14 292 SDfrac14 170 observed rangefrac14 100ndash700 Cronbachrsquosafrac14 084

AMII One participant failed to complete the Angry MoodImprovement Inventory We calculated Express-Outwardsafrac14 074 Express-Inwards afrac14 081 Control-Outwards afrac14 084and Control-Inwards afrac14 077 subscale scores by averagingacross each participantrsquos corresponding responses Express-Outwards subscale scores exhibited substantial variabilityacross the scalersquos possible 1ndash5 range Mfrac14 219 SDfrac14 049observed rangefrac14 138ndash338 and were positive correlated withtrait physical aggression from the BAQ r(57)frac14 038 Pfrac14 0003

Aggression task Volume settings were internally consistentafrac14 91 and thus averaged across all 14 trials of the aggressiontask as well as the six retaliatory trials afrac14 81 and eight non-retaliatory trials afrac14 85 to create three aggression scores (ietotal retaliatory and non-retaliatory) for each participant possi-ble range of 1ndash4 Validating our within-subjects provocationmanipulation participants selected louder noise blasts afterhigh provocation (ie retaliatory aggression Mfrac14 258 SDfrac14 087observed rangefrac14 100ndash400) than after low provocation (ienon-retaliatory aggression Mfrac14 241 SDfrac14 079 observedrangefrac14 100ndash400) t(59)frac14 296 Pfrac14 0004 Cohenrsquos ddependent-

meansfrac14 041


Social rejection (compared to social acceptance) was both posi-tively and negatively associated with large swaths of neuralactivity (see Tables 1 and 2) The positively associated regions


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included anticipated brain areas previously associated withsocial pain (bilateral anterior insula thalamus) and social painregulation (VLPFC Eisenberger 2012 Figure 1) Additional activ-ity was observed in what is popularly known as the mentalizingnetwork [dorsomedial prefrontal cortex (DMPFC) posterior cin-gulate cortexprecuneus (PCC) bilateral temporoparietal junc-tion (TPJ) and bilateral temporal pole (TP) Figure 1 Frith andFrith (2006)]

Within the VLPFC ROI three local maxima were observedThree VLPFC ROI masks were constructed by creating 8 mmbinary spheres around each local maximum (Figure 2)Parameter estimates from this rejection contrast wereextracted in the form of percent BOLD signal change from eachof these three VLPFC ROIs for use in later correlational andmediation analyses


Across the entire brain retaliatory aggression (as compared tonon-retaliatory aggression) was positively associated withactivity in the right [952 voxels peak voxel Zfrac14 368 MNI coordi-nates (x y z) 34 14 24] and left (688 voxels peak voxelZfrac14 462 coordinates 50 20 8) posterior insula and nega-tively associated with activity in the occipital lobe (2101 voxelspeak voxel Zfrac14492 coordinates 38 88 6) Parameter esti-mates from this retaliatory aggression contrast in the form ofpercent signal change were extracted from the bilateral ventralstriatum for use in later correlational and mediation analysesReplicating previous research (Chester and DeWall 2016) retali-atory aggression related activity in the ventral striatum wasassociated with higher scores on the Expression-Outwards sub-scale of the Angry Mood Improvement Inventory (AMII)r(57)frac14 033 Pfrac14 0010 even after using multiple linear regressionto control for the other three AMII subscales bfrac14 030t(54)frac14 218 Pfrac14 0034

Crucially the neuroimaging results from the RetaliatoryAggressiongtNon-Retaliatory Aggression contrast only reflectthe opportunity to engage in retaliatory aggression and do notreflect the actual neural correlates of retaliatory aggressivebehavior itself We regressed participantsrsquo retaliatory aggressionscores onto whole-brain neural activity from the RetaliatoryAggressiongtNon-Retaliatory Aggression contrast to identifythe true neural correlates of retaliatory aggression Whole-brainregression analyses revealed no significant correlates of retalia-tory aggressive behavior However when analyses were con-

strained to the bilateral ventral striatum using an ROI approachwe observed significant positive associations with the left(9 voxels peak voxel Zfrac14 288 coordinatesfrac1412 4 10) andright (10 voxels peak voxel Zfrac14 263 coordinatesfrac14 14 6 12)ventral striatum (Figure 3)

Frontostriatal associations with retaliatory aggression

Of the three spherical VLPFC ROIs rejection-related activity inthe most rostral of the ROIs was positively associated with bilat-eral ventral striatum activity during retaliatory aggression(Retaliatory AggressiongtNon-Retaliatory Aggression contrast)r(58)frac14 0346 Pfrac14 0007 Bilateral ventral striatum activity duringretaliatory aggression was associated with greater retaliatoryaggression r(58)frac14 0342 Pfrac14 0007 This pattern of correlationssuggested the presence of an indirect effect

To test this potential indirect effect bilateral ventral stria-tum activity during retaliatory aggression was modeled as amediator of the effect of VLPFC activity during rejection on sub-sequent retaliatory aggressive behavior Based off the previ-ously significant association with aggression-related activity inthe ventral striatum parameter estimates from the most rostralVLPFC ROI was modeled as the independent variable A signifi-cant indirect effect was observed from this model Bfrac14 141SEfrac14 070 95 CIfrac14 030 322 This overall model explained1190 of the variance in retaliatory aggression F(2 57)frac14 385Pfrac14 0027 (Figure 4)

Table 2 Brain regions negatively associated with RejectgtAcceptduring Cyberball

Cluster Voxels Brain region Peak Z Peak x y z

1 7616 Posterior insula 654 38 6 16Precentral gyrus 569 30 14 64

533 36 16 66Supplemental motor area 526 4 6 54Postcentral gyrus 514 48 34 56

498 52 28 502 834 Dorsolateral PFC 429 40 44 8

367 46 28 28360 34 32 28358 34 24 24346 40 34 34329 38 52 16

3 478 Superior parietal lobule 377 30 48 68Supramarginal gyrus 356 48 36 54Postcentral gyrus 351 42 28 40Superior parietal lobule 346 36 46 64Postcentral gyrus 309 46 32 50Superior parietal lobule 302 32 54 64

Notes and Sources Each cluster is displayed with rows for all local maxima

Table 1 Brain regions positively associated with RejectgtAccept dur-ing Cyberball


1 25 205 VLPFCanterior insula 607 48 22 12598 52 22 12588 46 36 6581 56 26 12

Temporoparietal junction 577 50 44 20Middle temporal gyrus

temporal pole568 56 10 16

2 10 661 VLPFC 646 42 20 26Temporoparietal junction 600 46 66 22Middle temporal gyrus


Temporoparietal junction 572 50 66 18565 44 70 24

Anterior insula 561 36 24 63 9239 Dorsomedial PFC 752 10 52 36

709 8 46 30701 6 46 26

4 1492 Posterior cingulate cortex 549 4 54 345 1382 Thalamuscaudate 534 6 10 106 1218 Occipital cortex 503 12 94 47 599 Brainstem 353 4 30 30



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Does VLPFC activity simply reflect stronger affectiveresponses to rejection

An alternative account for our findings could be that the VLPFCactivity we observed during social rejection might simply reflecta greater affective response to this event and not the regulatory

account we have proposed If this alternative explanation is cor-rect then we should be able to replicate the positive associa-tions that were observed between VLPFC activity (duringrejection) and ventral striatum activity (during aggression) withother neural regions that subserve social pain (ie the DACCand anterior insula Eisenberger 2012)To test whether this was

Fig 1 Greater neural activity from the RejectgtAccept contrast of the Cyberball task in bilateral anterior insula VLPFC and mentalizing network Coordinates are in

MNI space

Fig 2 (AndashC) Spherical VLPFC ROIs constructed by centering each sphere on one of three local maxima from the RejectgtAccept contrast (D) All three ROIs displayed

simultaneously red voxels display overlap between ROIs B and C Coordinates are in MNI space


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the case we extracted rejection-related activation from theDACC and bilateral anterior insula (for DACC mask see Chesteret al 2015 anterior insula mask see Chester et al 2014) and cor-related them with retaliatory-aggression-related activity in thebilateral ventral striatum Failing to support this alternativeaccount VLPFC activity was unassociated with DACCr(58)frac14012 Pfrac14 0378 or anterior insula r(58)frac14001 Pfrac14 0929activity during rejection

Dispositional aggression and frontostriatal connectivityduring retaliatory aggression

Dispositional physical aggression was positively associatedwith retaliatory aggression r(57)frac14 029 Pfrac14 0029 though notwith greater ventral striatum activity during retaliatory aggres-sion r(57)frac14 010 Pfrac14 0435 Subsequent analyses tested whethertrait physical aggression was associated with altered functionalconnectivity between cortical brain regions and the bilateralventral striatum during retaliatory aggressive behaviorThe combined psychophysiological interaction (PPI) andwhole-brain regression analyses revealed a single negativelycorrelated cluster in the right VLPFC (peak voxel Zfrac14421Pfrac14 0004 MNI coordinates [x y z]frac14 34 52 6 529 contiguousvoxels Figure 5 Brodmannrsquos Areas 46 and 47) though somevoxels extended into the rostral (Brodmannrsquos Area 10) and ven-tral (Brodmannrsquos Area 11) medial PFC

In a post hoc exploratory fashion functional connectivityestimates from the VLPFC cluster observed in the RetaliatoryAggression PPI analysis were entered as a mediator into a medi-ation analysis (the size of these connectivity units were so smallthat we artificially inflated them by multiplying them times 100for this analysis so that effect size estimates would be inter-pretable) Retaliatory aggression was modeled as the dependent

variable and trait physical aggression was modeled as the inde-pendent variable A significant indirect effect was observedfrom this model Bfrac14008 SEfrac14 004 95 CIfrac14018 001whereby trait physical aggression predicted more retaliatoryaggression through reduced functional connectivity betweenthe ventral striatum and VLPFC during retaliatory aggressionThis overall model explained 1717 of the variance in retalia-tory aggression F(2 56)frac14 580 Pfrac14 0005 (Figure 6) As an indica-tor of statistical suppression the direct effect of trait physicalaggression on retaliatory aggression became stronger after con-trolling for the indirect effect of frontostriatal connectivity(Figure 6 Mackinnon et al 2000)

Discussion

Why do rejected people behave aggressively Although rejec-tion reliably increases aggression it remains unclear whatneurological mechanisms help explain this relationship Ourinvestigation fills this gap in the literature by offering a compre-hensive account of the neural correlates of rejection-relatedaggression Building off of the excessive recruitment model(Chester and DeWall 2014 Chester et al 2016) we examinedwhether taxing the brainrsquos regulatory functions during rejectionwould promote subsequent retaliatory aggression by unleash-ing neural reward circuitry which would motivate retaliationby rendering such revenge more enticing

Fig 3 Bilateral ventral striatum activity associated with greater retaliatory

aggressive behavior on the aggression task

Fig 4 An indirect effect whereby ventrolateral prefrontal cortex (VLPFC) activity

during rejection was associated with greater retaliatory aggression through

greater bilateral ventral striatum (VS) activity during such retaliatory aggression

Values represent unstandardized regression coefficients and the value in paren-

theses represent the direct effect (ie the total effect minus the indirect effect)

Plt 001

Fig 5 Reduced functional connectivity between the seed region in the ventral

striatum (red) and the ventrolateral prefrontal cortex (blue) among individuals

higher in trait physical aggression Coordinates are in MNI space

Fig 6 An indirect effect whereby dispositional physical aggressiveness was

associated with greater aggression through less functional connectivity between

the ventral striatum (VS) and ventrolateral prefrontal cortex (VLPFC) during

such retaliatory aggression Values represent unstandardized regression

coefficients and the value in parentheses represent the direct effect Plt 005

Plt 001 Plt 0001


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Implications for the neuroscience of social rejection

We replicated previous research demonstrating that socialrejection compared to acceptance is associated with greateractivity in brain networks that subserve social pain (anteriorinsula Eisenberger et al 2003) social pain regulation (VLPFCChester and DeWall 2014) and mentalizing about othersrsquo mindstate (Falk et al 2014) These replications support Social PainOverlap Theoryrsquos central tenet that rejection is a markedly pain-ful experience that recruits the affective and less often somaticaspects of the brainrsquos pain circuitry (Eisenberger and Lieberman2004 Eisenberger 2012) Notably absent from our observed neu-ral correlates of rejection was the DACC which is typicallyobserved in experiences of social rejection (Kawamoto et al2012) It remains uncertain why this region was not reactive torejection in our experiment

Implications for the neuroscience ofretaliatory aggression

Opportunities to retaliate against one of the participantsrsquorejecters were associated with greater activity in the posteriorinsula which replicates previous work on retaliatory aggression(Chester and DeWall 2016 Emmerling et al 2016) The posteriorinsularsquos role in somatic and visceral interoception (Craig 2011)may indicate that retaliatory aggression is experienced as aphysically grounded state or signify an alertness to somaticcues When actual retaliatory aggressive behavior was corre-lated with these retaliatory brain activity estimates weobserved significant positive associations in the bilateral ven-tral striatum (Chester and DeWall 2016) The added sensitivitygained from using the whole-brain regression approach sug-gests that this approach may be useful to researchers who regu-larly model the types of trials employed in their tasks asexplanatory variables but less commonly model participantsrsquoactual responses to those task features

Adopting an ROI approach we also replicated the associa-tion between activity in the ventral striatum during retaliatoryaggression and the extent of actual retaliation that participantsinflicted on their opponents (Chester and DeWall 2016)Further we replicated the correlation between such striatalactivity and participantsrsquo self-reported tendencies to reactaggressively in order to improve their mood (as in Chester andDeWall 2016) This replication lends confidence to ourstriatum-reward reverse inference which is further supportedby the extensive evidence for the ventral striatumrsquos involve-ment in reward (Burgdorf and Panksepp 2006 Ikemoto 2007Sabatinelli et al 2007 Kringelbach and Berridge 2009 Berridgeand Kringelbach 2013) A reliably observed striatal response toretaliatory aggression supports the growing literature implicat-ing positive affect pleasure and reward and central psychologi-cal components of retaliatory aggression (Chester 2017 Chesterand DeWall 2018b)

Neurochemical nuances of reward

However lsquorewardrsquo is a heterogeneous construct and these vari-ous sub-processes are subserved by distinct neurobiologicalpathways that fMRI cannot currently estimate (Berridge andRobinson 2003) Indeed lsquolikingrsquo or pleasure is likely to be medi-ated by opioid transmitter pathways and spiny neurons in theshell of the ventral striatum whereas motivational componentsof lsquowantingrsquo is likely to be mediated by dopaminergic transmit-ter pathways in this same region (Kringelbach and Berridge2009) Imaging and pharmacological techniques that measure

and manipulate neural dopamine and opioid levels and bindingsites are needed to better investigate whether lsquowantingrsquo or lsquolik-ingrsquo is at play in retaliatory aggression Disentangling theseexperiences is crucial for a comprehensive understanding ofaggressionrsquos phenomenological qualities

Support for the excessive recruitment modelsometimes less is more

In support of the excessive recruitment model of self-regulatoryfailure (Chester and DeWall 2014 Chester et al 2016) anteriorVLPFC recruitment during rejection was associated with greaterventral striatum activation during retaliatory aggression TheVLPFC-striatum circuitrsquos role in successful self-regulation issupported by these findings and further suggests that retalia-tory aggression is a rewarding activity as similar findings areobserved in other rewarding behaviors such as unhealthy eating(Wagner et al 2013) Crucially only the most anterior ROI in ourrejection-related VLPFC cluster was associated with striatalactivity during aggression The specificity of our findings to theanterior VLPFC can be interpreted in the light of research dem-onstrating that behavioral inhibition is localized to posteriorVLPFC subregions and emotional and cognitive inhibition islocalized to the anterior VLPFC (Aron et al 2014 Buhle et al2014) As such we can potentially infer that the VLPFCrsquos regula-tion of social pain and not the aggressive motor act itself iswhat predicted subsequent increases in retaliation-relatedstriatal activity Further the null association between VLPFCactivity during rejection and activity in the DACC and anteriorinsula undermine the potential alternative account that ourVLPFC activation did not reflect self-regulation but rather moreintense affective responses to rejection

These findings cast doubt on lsquothe more lateral PFC thebetterrsquo approaches to the neuroscience of self-regulation andsupport the excessive recruitment model (Chester and DeWall2014 Chester et al 2016) However it may be that the excessiverecruitment model only holds for situations characterized bynegative affect (eg rejection) as other research has found thatgreater VLPFC recruitment to self-regulatory challenges outsideof this affect context are predictive of self-regulatory successnot failure (Lopez et al 2014) Further chronic recruitment ofbrain regions can increases their plasticity and baseline activity(eg Teneback et al 1999) If this was the case then individualswho show exacerbated recruitment of the VLPFC during eachaversive event would eventually trait this brain region tobecome more flexible and robust promoting better emotion-regulation Future work is needed to understand how someforms of cortical recruitment can lead to adaptive or maladap-tive changes in behavior

A reinforcement model of trait aggression

Dispositionally and physically aggressive individuals exhibitedless functional connectivity between the VLPFC and ventralstriatum during retaliatory aggression Further this connectiv-ity exerted a suppressing effect on their aggression suggestingthat without such neural control over reward circuitry thosehigh in aggressive traits would act much more aggressivelythan they typically do

Such dysregulated reward activity during retaliatory belliger-ence might explain how aggressive traits are developed andmaintained Classic models of aggression emphasize distinctsocial-cognitive and affective-learning mechanisms as the proc-ess through which some individuals develop to be more


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aggressive than others (eg the General Aggression ModelAnderson and Bushman 2002) This project argues for a moreintegrated conceptualization of affective and cognitive proc-esses in these models in which cognitive control mechanismsand affective impulses dynamically interact to reinforce aggres-sive behavior These results also suggest avenues for futureresearch to investigate how striatally mediated reinforcementprocesses can be altered to reduce the occurrence of physicallyaggressive dispositions However it remains unclear if theVLPFC connectivity with the striatum represents inhibition ofthe affective reward experience or a more general and behavio-ral inhibition of aggressive impulses The anterior nature of thisVLPFC cluster does suggest that the inhibition targeted affectiveand not the behavioral processes yet more work is needed to becertain

A role for appraisal processes

Emotional responses to situations are determined by theappraisals of those situations (Siemer et al 2007 Brosch et al2010) Further such emotional appraisals can fundamentallyalter the neural responses to emotional stimuli (Brosch andSander 2013 Buhle et al 2014) Emotional responses to socialrejection and aggression are no exception For instance exter-nalizing responses to rejection are contingent upon theappraisal of the event (Sandstrom et al 2003) The presentresearch failed to include measures or manipulations ofappraisal processes However establishing the role of subjectiveappraisals beyond the objective experimental manipulationswe employed is critical to understanding the neural mecha-nisms of the rejectionndashaggression link

Limitations and future directions

Our findings must be considered in light of the sample whichconsisted of 60 undergraduates and pose some concerns for thegeneralizability of our findings and the extent to which ouranalyses were sufficiently powered The fact that most of ourfindings were close replications of previous studies which welinked together in the same sample provide some confidencethat our results were not merely due to sampling error An addi-tional concern is that all findings were correlational in natureFuture work that experimentally modulates these neural sys-tems such as brain stimulation and pharmacological techni-ques can circumvent this issue The reverse inferences that wemade are also limitations as the neural activity we observedmay not actually be reflective of the psychological processes weinterpreted them to signify (Poldrack 2006) Our striatum-reward associations were supported by self-report evidence butmore work is needed to ensure the fidelity of our reverse infer-ences Further the association between retaliatory aggressionand ventral striatum activity (displayed in Figure 3) wasobserved in a relatively small number of voxels (ie 19) whichpotentially undermines the reliability of these findingsHowever voxels from the entire anatomical region were used inall other analyses which provides more inferential confidencethan just using the significant voxels form the regressionanalysis

Each of our aggression-related neural activity estimates mayhave been biased by the interleaved baseline fixation screensthat we used which may have been influenced by residual reac-tivity to previous elements of the task Future work may benefitfrom using baseline estimates that are acquired before theaggression task Finally the ways in which striatal activity

motivates aggression are unable to be articulated given ourdata It may be that the anticipation of the striatal reward asso-ciated with aggression prospectively motivates such behaviorConversely it may be that the reward experienced during theaggressive act motivates more severe acts of aggression inorder to magnify the ongoing hedonic experience Research thatis able to disentangle the anticipated vs in-the-moment motiva-tional capabilities of aggressionrsquos rewarding qualities is a neces-sary future endeavor Our rejection block was also confoundedwith the duration of the Cyberball task which may have pro-duced spurious patterns of brain activity such as those weobserved in the visual and auditory cortices Finally readersshould use caution when interpreting our findings because wedid not correct for the multiple comparisons that were madeacross the various VLPFC regions-of-interest

Conclusions

Does the pain of rejection promote the sweetness of revengeOur findings suggest that the answer to this question is yesalbeit indirectly People are motivated to maintain their socialconnections but also to avoid having those connections inflictexcessive costs upon them (McCullough et al 2013) Pain andpleasure are two proximate mechanisms that evolution mayhave co-opted to motivate individuals to avoid rejection (iesocial pain) and to seek retribution against those who harmthem (ie aggressive pleasure) By understanding how copingwith the pain of rejection impacts our self-regulatory abilitiesand how these regulatory changes render retaliation an appeti-tive option we may better understand how to prevent theaggressive dividends that rejection often yields

Funding

This work was supported by the National Institute on DrugAbuse (award DA05312 Lynam Milich and DeWall) theFoundation for Personality and Social Psychologyrsquos HeritageInitiative (Chester) and the Robert S Lipman Research Fundfor the Prevention of Drug and Alcohol Abuse (Chester)

Conflict of interest None declared

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Berridge KC Kringelbach ML (2013) Neuroscience of affectbrain mechanisms of pleasure and displeasure Current Opinionin Neurobiology 23(3) 294ndash303

Berridge KC Robinson TE (2003) Parsing reward Trends inNeurosciences 26(9) 507ndash13

Brosch T Pourtois G Sander D (2010) The perception and cat-egorisation of emotional stimuli a review Cognition andEmotion 24(3) 377ndash400

Brosch T Sander D (2013) Comment the appraising braintowards a neuro-cognitive model of appraisal processes inemotion Emotion Review 5(2) 163ndash8

Buades-Rotger M Brunnlieb C Munte TF Heldmann MKramer UM (2016) Winning is not enough ventral striatumconnectivity during physical aggression Brain Imaging andBehavior 10(1) 105ndash14


Dow




Buckley KE Winkel RE Leary MR (2004) Reactions toacceptance and rejection effects of level and sequence of rela-tional evaluation Journal of Experimental Social Psychology 40(1)14ndash28

Buhle JT Silvers JA Wager TD et al (2014) Cognitive reap-praisal of emotion a meta-analysis of human neuroimagingstudies Cerebral Cortex 24(11) 2981ndash90

Burgdorf J Panksepp J (2006) The neurobiology of positiveemotions Neuroscience and Biobehavioral Reviews 30(2) 173ndash87

Bushman BJ Baumeister RF Phillips CM (2001) Do peopleaggress to improve their mood Catharsis beliefs affect regu-lation opportunity and aggressive responding Journal ofPersonality and Social Psychology 81(1) 17ndash32

Buss AH Perry M (1992) The aggression questionnaire Journalof Personality and Social Psychology 63(3) 452ndash9

Carre JM Murphy KR Hariri AR (2013) What lies beneaththe face of aggression Social Cognitive and AffectiveNeuroscience 8(2) 224ndash9

Chester DS (2017) The role of positive affect in aggressionCurrent Directions in Psychological Science 26(4) 366ndash70

Chester DS DeWall CN (2014) Prefrontal recruitment duringsocial rejection predicts greater subsequent self-regulatoryimbalance and impairment neural and longitudinal evidenceNeuroImage 101(1) 485ndash93

Chester DS DeWall CN (2016) The pleasure of revenge retali-atory aggression arises from a neural imbalance towardreward Social Cognitive and Affective Neuroscience 11(7)1173ndash82

Chester DS DeWall CN (2018a) Aggression is associated withgreater subsequent alcohol consumption Shared neural basisin the ventral striatum Aggressive Behavior 44(3) 285ndash93

Chester DS DeWall CN (2018b) Personality correlates ofrevenge-seeking Multidimensional links to physical aggres-sion impulsivity and aggressive pleasure Aggressive Behavior44(3) 235ndash45

Chester DS Eisenberger NI Pond RS Richman SBBushman BJ DeWall CN (2014) The interactive effect ofsocial pain and executive functioning on aggression an fMRIexperiment Social Cognitive and Affective Neuroscience 9(5)699ndash704

Chester DS Lynam DR Milich R Powell DK AndersenAH DeWall CN (2016) How do negative emotions impairself-control A neural model of negative urgency NeuroImage132(1) 43ndash50

Chester DS Pond RS DeWall CN (2015) Alexithymia isassociated with blunted anterior cingulate response to socialrejection implications for daily rejection Social Cognitive andAffective Neuroscience 10(4) 517ndash22

Chester DS Riva P (2016) Brain mechanisms to regulate nega-tive reactions to social exclusion In Riva P Eck J editorsSocial Exclusion Psychological Approaches to Understanding andReducing Its Impact Cham Switzerland Springer InternationalPublishing

Chow RM Tiedens LZ Govan CL (2008) Excluded emotionsthe role of anger in antisocial responses to ostracism Journal ofExperimental Social Psychology 44(3) 896ndash903

Cote S Vaillancourt T LeBlanc JC Nagin DS Tremblay RE(2006) The development of physical aggression from toddler-hood to pre-adolescence a nation wide longitudinal study ofCanadian children Journal of Abnormal Child Psychology 34(1)68ndash82

Craig AD (2011) Significance of the insula for the evolution ofhuman awareness of feelings from the body Annals of the NewYork Academy of Sciences 1225(1) 72ndash82

Dambacher F Sack AT Lobbestael J Arntz A Brugman SSchuhmann T (2014) Out of control evidence for anteriorinsula involvement in motor impulsivity and reactive aggres-sion Social Cognitive and Affective Neuroscience 10(4) 508ndash16

Denson TF DeWall CN Finkel EJ (2012) Self-control andaggression Current Directions in Psychological Science 21(1) 20ndash5

DeWall CN Twenge JM Gitter SA Baumeister RF (2009)Itrsquos the thought that counts the role of hostile cognition inshaping aggressive responses to social exclusion Journal ofPersonality and Social Psychology 96(1) 45ndash59

Eisenberger NI (2012) The pain of social disconnection exam-ining the shared neural underpinnings of physical and socialpain Nature Reviews Neuroscience 13(6) 421ndash34

Eisenberger NI Lieberman MD (2004) Why rejection hurts acommon neural alarm system for physical and social painTrends in Cognitive Sciences 8(7) 294ndash300

Eisenberger NI Lieberman MD Williams KD (2003) Doesrejection hurt An fMRI study of social exclusion Science302(5643) 290ndash2

Emmerling F Schuhmann T Lobbestael J Arntz ABrugman S Sack AT (2016) The role of the insular cortex inretaliation PLoS One 11(4) e0152000

Everitt BJ Robbins TW (2005) Neural systems of reinforce-ment for drug addiction from actions to habits to compulsionNature Neuroscience 8(11) 1481ndash9

Falk EB Cascio CN OrsquoDonnell MB et al (2014) Neuralresponses to exclusion predict susceptibility to social influ-ence Journal of Adolescent Health 54(5) S22ndash31

Frith CD Frith U (2006) The neural basis of mentalizingNeuron 50(4) 531ndash4

Gerevich J Bacskai E Czobor P (2007) The generalizability ofthe BussndashPerry Aggression Questionnaire International Journalof Methods in Psychiatric Research 16(3) 124ndash36

Hayes AF (2012) PROCESS a versatile computational tool forobserved variable mediation moderation and conditionalprocess modeling (Version 20) [Software] Available httpwwwafhayescompublicprocess2012pdf [August 18 2017]

Heatherton TF Wagner DD (2011) Cognitive neuroscience ofself-regulation failure Trends in Cognitive Sciences 15(3) 132ndash9

Heller R Stanley D Yekutieli D Rubin N Benjamini Y(2006) Cluster-based analysis of fMRI data NeuroImage 33(2)599ndash608

Huesmann LR Eron LD Lefkowitz MM Walder LO (1984)Stability of aggression over time and generationsDevelopmental Psychology 20(6) 1120ndash34

Ikemoto S (2007) Dopamine reward circuitry two projectionsystems from the ventral midbrain to the nucleusaccumbensndasholfactory tubercle complex Brain Research Reviews56(1) 27ndash78

Inzlicht M Gutsell JN (2007) Running on empty neural sig-nals for self-control failure Psychological Science 18(11) 933ndash7

Kawamoto T Onoda K Nakashima KI Nittono HYamaguchi S Ura M (2012) Is dorsal anterior cingulate cor-tex activation in response to social exclusion due to expect-ancy violation An fMRI study Frontiers in EvolutionaryNeuroscience 4 11

Kober H Mende-Siedlecki P Kross EF et al (2010)Prefrontalndashstriatal pathway underlies cognitive regulation ofcraving Proceedings of the National Academy of Sciences 107(33)14811ndash6

Kramer UM Jansma H Tempelmann C Munte TF (2007)Tit-for-tat the neural basis of reactive aggression NeuroImage38(1) 203ndash11


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Kringelbach ML Berridge KC (2009) Towards a functionalneuroanatomy of pleasure and happiness Trends in CognitiveSciences 13(11) 479ndash87

Leary MR (1990) Responses to social exclusion social anxietyjealousy loneliness depression and low self-esteem Journalof Social and Clinical Psychology 9(2) 221ndash9

Leary MR Kowalski RM Smith L Phillips S (2003) Teasingrejection and violence case studies of the school shootingsAggressive Behavior 29(3) 202ndash14

Leary MR Twenge JM Quinlivan E (2006) Interpersonalrejection as a determinant of anger and aggression Personalityand Social Psychology Review 10(2) 111ndash32

Levy BJ Wagner AD (2011) Cognitive control and right ven-trolateral prefrontal cortex reflexive reorienting motor inhibi-tion and action updating Annals of the New York Academy ofSciences 1224(1) 40ndash62

Lopez RB Hofmann W Wagner DD Kelley WMHeatherton TF (2014) Neural predictors of giving in to temp-tation in daily life Psychological Science 25(7) 1337ndash44

Lotze M Veit R Anders S Birbaumer N (2007) Evidence for adifferent role of the ventral and dorsal medial prefrontal cor-tex for social reactive aggression an interactive fMRI studyNeuroImage 34(1) 470ndash8

MacDonald G Leary MR (2005) Why does social exclusionhurt The relationship between social and physical painPsychological Bulletin 131(2) 202ndash23

MacKinnon DP Krull JL Lockwood CM (2000) Equivalenceof the mediation confounding and suppression effectPrevention Science 1(4) 173ndash81

Maldjian JA Laurienti PJ Kraft RA Burdette JH (2003) Anautomated method for neuroanatomic and cytoarchitectonicatlas-based interrogation of fMRI data sets NeuroImage 19(3)1233ndash9

McCullough ME Kurzban R Tabak BA (2013) Puttingrevenge and forgiveness in an evolutionary context Behavioraland Brain Sciences 36(1) 41ndash58

Poldrack RA (2006) Can cognitive processes be inferred fromneuroimaging data Trends in Cognitive Sciences 10(2) 59ndash63

Poon KT Teng F (2017) Feeling unrestricted by rules ostra-cism promotes aggressive responses Aggressive Behavior 43(6)558ndash67

Price DD (2000) Psychological and neural mechanisms of theaffective dimension of pain Science 288(5472) 1769ndash72

Rajchert J Winiewski M (2016) The behavioral approach andinhibition systemsrsquo role in shaping the displaced and directaggressive reaction to ostracism and rejection Personality andIndividual Differences 88(1) 272ndash9

Ren D Wesselmann ED Williams KD (2018) Hurt peoplehurt people ostracism and aggression Current Opinion inPsychology 19(1) 34ndash8

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Rotge JY Lemogne C Hinfray S et al (2014) A meta-analysisof the anterior cingulate contribution to social pain SocialCognitive and Affective Neuroscience 10(1) 19ndash27

Sabatinelli D Bradley MM Lang PJ Costa VD Versace F(2007) Pleasure rather than salience activates human nucleus

accumbens and medial prefrontal cortex Journal ofNeurophysiology 98(3) 1374ndash9

Sandstrom MJ Cillessen AH Eisenhower A (2003)Childrenrsquos appraisal of peer rejection experiences impact onsocial and emotional adjustment Social Development 12(4)530ndash50

Siemer M Mauss I Gross JJ (2007) Same situationndashdifferentemotions how appraisals shape our emotions Emotion 7(3)592

Smith SM Jenkinson M Woolrich MW et al (2004)Advances in functional and structural MR image analysis andimplementation as FSL NeuroImage 23(1) S208ndash19

Teneback CC Nahas Z Speer AM et al (1999) Changes inprefrontal cortex and paralimbic activity in depression follow-ing two weeks of daily left prefrontal TMS Journal ofNeuropsychiatry and Clinical Neurosciences 11(4) 426ndash35

Twenge JM Baumeister RF Tice DM Stucke TS (2001) Ifyou canrsquot join them beat them effects of social exclusion onaggressive behavior Journal of Personality and Social Psychology81(6) 1058ndash69

Tzourio-Mazoyer N Landeau B Papathanassiou D et al(2002) Automated anatomical labeling of activations in SPMusing a macroscopic anatomical parcellation of the MNI MRIsingle-subject brain NeuroImage 15(1) 273ndash89

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

Wagner DD Altman M Boswell RG Kelley WMHeatherton TF (2013) Self-regulatory depletion enhancesneural responses to rewards and impairs top-down controlPsychological Science 24(11) 2262ndash71

Warburton WA Williams KD Cairns DR (2006) When ostra-cism leads to aggression the moderating effects of controldeprivation Journal of Experimental Social Psychology 42(2)213ndash20

Webster GD DeWall CN Pond RS et al (2014) The briefaggression questionnaire psychometric and behavioral evi-dence for an efficient measure of trait aggression AggressiveBehavior 40(2) 120ndash39

Wesselmann ED Butler FA Williams KD Pickett CL(2010) Adding injury to insult unexpected rejection leads tomore aggressive responses Aggressive Behavior 36(4) 232ndash7

Williams KD (2009) Ostracism A temporal need-threat modelIn Zanna MP editor Advances in Experimental SocialPsychology New York NY Academic Press

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Worsley KJ (2001) Statistical analysis of activation imagesFunctional MRI An Introduction to Methods 14(1) 251ndash70

Yanagisawa K Masui K Onoda K et al (2011) The effects ofthe behavioral inhibition and activation systems on socialinclusion and exclusion Journal of Experimental SocialPsychology 47(2) 502ndash5


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Neural Mechanisms of the Rejection-Aggression Link

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NotesCitation Information

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nsy025-TF1


Digital Object Identifier (DOI) httpsdoiorg101093scannsy025

NotesCitation Information NotesCitation Information Published in Social Cognitive and Affective Neuroscience v 13 no 5 p 501-512

copy The Author(s) (2018) Published by Oxford University Press

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (httpcreativecommonsorglicensesby-nc40) which permits non-commercial re-use distribution and reproduction in any medium provided the original work is properly cited For commercial re-use please contact journalspermissionsoupcom

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Abstract



Introduction






501



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The present study






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Dow












Open practices






meansfrac14 041




Dow


















367 46 28 28360 34 32 28358 34 24 24346 40 34 34329 38 52 16












709 8 46 30701 6 46 26




Dow








MNI space




Dow









Discussion









Plt 001









Plt 001 Plt 0001


Dow



















Dow











Conclusions


Funding












Dow











































Dow









































Dow





Repository Citation




nsy025-TF2

nsy025-TF1









Open practices






meansfrac14 041




Dow


















367 46 28 28360 34 32 28358 34 24 24346 40 34 34329 38 52 16












709 8 46 30701 6 46 26




Dow








MNI space




Dow









Discussion









Plt 001









Plt 001 Plt 0001


Dow



















Dow











Conclusions


Funding












Dow











































Dow









































Dow





Repository Citation




nsy025-TF2

nsy025-TF1















367 46 28 28360 34 32 28358 34 24 24346 40 34 34329 38 52 16












709 8 46 30701 6 46 26




Dow








MNI space




Dow









Discussion









Plt 001









Plt 001 Plt 0001


Dow



















Dow











Conclusions


Funding












Dow











































Dow









































Dow





Repository Citation




nsy025-TF2

nsy025-TF1





MNI space




Dow









Discussion









Plt 001









Plt 001 Plt 0001


Dow



















Dow











Conclusions


Funding












Dow











































Dow









































Dow





Repository Citation




nsy025-TF2

nsy025-TF1






Discussion









Plt 001









Plt 001 Plt 0001


Dow



















Dow











Conclusions


Funding












Dow











































Dow









































Dow





Repository Citation




nsy025-TF2

nsy025-TF1
















Dow











Conclusions


Funding












Dow











































Dow









































Dow





Repository Citation




nsy025-TF2

nsy025-TF1








Conclusions


Funding












Dow











































Dow









































Dow





Repository Citation




nsy025-TF2

nsy025-TF1








































Dow









































Dow





Repository Citation




nsy025-TF2

nsy025-TF1






































Dow





Repository Citation




nsy025-TF2

nsy025-TF1

Neural Mechanisms of the Rejection-Aggression Link

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