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Social Neuroscience

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Social priming modulates the neural response toostracism: a new exploratory approach

Caitlin M. Hudac

To cite this article: Caitlin M. Hudac (2018): Social priming modulates the neuralresponse to ostracism: a new exploratory approach, Social Neuroscience, DOI:10.1080/17470919.2018.1463926

To link to this article: https://doi.org/10.1080/17470919.2018.1463926

Accepted author version posted online: 10Apr 2018.Published online: 16 Apr 2018.

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ARTICLE

Social priming modulates the neural response to ostracism: a new exploratoryapproachCaitlin M. Hudac a,b

aDepartment of Psychiatry and Behavioral Sciences, University of Washington, Seattle, WA, USA; bCenter on Human Development andDisability, University of Washington, Seattle, WA, USA

ABSTRACTThe present study sought to evaluate whether social priming modulates neural responses toostracism, such that making arbitrary interpersonal decisions increases the experience of socialexclusion more than making arbitrary physical decisions. This exploratory event-related potential(ERP) study utilized the Lunchroom task, in which adults (N = 28) first selected one of two optionsthat included either interpersonal or physical descriptors. Participants then received ostracismoutcome feedback within a lunchroom scenario in which they were either excluded (e.g. sittingalone) or included (e.g. surrounded by others). While the N2 component was sensitive to primingdecision condition, only the P3 component discriminated between ostracism decisions. Furtherinspection of the neural sources indicated that the amygdala, anterior cingulate cortex, andsuperior temporal gyrus were more engaged for exclusion than inclusion conditions during bothN2 and P3 temporal windows. Evaluation of temporal source dynamics suggest that the effects ofostracism are predominant between 250–500 ms and were larger following interpersonal thanphysical decisions. These results suggest that being ostracized evokes a larger neural responsethat is modulated following priming of the social brain.

ARTICLE HISTORYReceived 8 October 2017Revised 7 February 2018Published online 18 April2018

KEYWORDSOstracism; social exclusion;social priming; event-relatedpotentials; source estimation

Introduction

Ostracism (i.e. being ignored and/or excluded) is anintensely negative social experience with destructiveconsequences for aspects of fundamental social needsand general affective well-being (Baumeister & Leary,1995; Williams, 2006, 2007). This is not an uncommonphenomenon and recent studies suggest that peopleare ostracized on a daily basis (Nezlek, Wesselmann,Wheeler, & Williams, 2015). Even brief exposure toostracism elevates negative affect (Buckley, Winkel, &Leary, 2004; Chow, Tiedens, & Govan, 2008) and mod-erates self-reported levels of belonging, self-esteem,and meaningful existence (Zadro, Williams, &Richardson, 2004). At a biological level, social exclusionis associated with symptoms of stress, including heigh-tened pupillary reactivity (Silk et al., 2012), modulationof heart rate (Gunther Moor, Crone, & van der Molen,2010; Wager et al., 2009), and increased salivary cortisol(Blackhart, Eckel, & Tice, 2007).

Much of the work targeting neural mechanismsunderlying ostracism and social exclusion haveemployed the Cyberball paradigm, a popular task com-paring peer engagement versus peer exclusion

(Williams, Cheung, & Choi, 2000; Williams & Jarvis,2006). In this virtual game, participants ostensibly taketurns tossing a ball between two or more players, andthe proportion of throws is manipulated so that theparticipant experiences a period in time without receiv-ing the ball from the other players (i.e. social exclusion)in contrast with other periods of fair play (i.e. socialinclusion). Over the past decade, the Cyberball taskhas been shown to engage a broad range of socialbrain regions during periods of exclusion, includingthe anterior cingulate cortex (ACC), anterior insula,and ventral prefrontal cortex (Bolling et al., 2011;Masten, Eisenberger, Pfeifer, & Dapretto, 2010; Mooret al., 2012; see Eisenberger, 2012b for review). In theseminal functional imaging study, Nieuwenhuis, Yeung,van den Wildenberg, and Ridderinkhof (2003) foundthat greater activation within the ACC, a region impli-cated in the affective distress of physical pain(Eisenberger, 2012a; Sawamoto et al., 2000; van derMeulen, van IJ Zendoorn, & Crone, 2016), positivelycorrelated with greater self-reported distress duringexclusion periods. In contrast, greater activation withinthe ventrolateral prefrontal cortex, a region implicated

CONTACT Caitlin M. Hudac chudac@uw.edu Department of Psychiatry and Behavioral Sciences, University of Washington, CHDD Box 357920,Seattle, WA 98195.

Supplemental data for this article can be accessed here.

SOCIAL NEUROSCIENCE, 2018https://doi.org/10.1080/17470919.2018.1463926

© 2018 Informa UK Limited, trading as Taylor & Francis Group

in the inhibition and regulation of distress (Kalisch,Wiech, Herrmann, & Dolan, 2006; Riva, Romero Lauro,DeWall, & Bushman, 2012), negatively correlated withreduced distress. Subsequent work has confirmed cor-respondence between social distress and social brainactivation, particularly within the ACC and insula(Eisenberger, 2012b). Taken together, these results sug-gest that this network of brain regions is sensitive tothe experience of ostracism.

Evidence from event-related potentials (ERP)

Despite the reliability of this paradigm, there is conten-tion on whether these activation patterns indeed reflectthe active experience and processing of social pain(Eisenberger, 2003, 2012b), considering the poor tem-poral specificity of functional imaging. An event-relatedpotentials (ERP) approach provides an opportunity tobetter understand the immediate response to socialexclusion at the millisecond level, and ERP studiesimplicate several key components in the Cyberballtask: First, an early N2 component occurring over fron-tal electrodes between 100–250 ms post-stimulus onsetis sensitive to exclusion (Sreekrishnan et al., 2014;Themanson, Khatcherian, Ball, & Rosen, 2013; Weschke& Niedeggen, 2013). Other work noted the N2 is notaffected by the probability of receiving the ball toss(Gutz, Küpper, Renneberg, & Niedeggen, 2011;Niedeggen, Sarauli, Cacciola, & Weschke, 2014), butmay instead be related to conflict monitoring(Themanson et al., 2013).

Second, a mid-latency P3 component elicitedbetween 250–600 ms post-stimulus onset is increasedduring exclusion periods across posterior (Crowley, Wu,Molfese, & Mayes, 2010; Themanson et al., 2015) andcentral (Gutz et al., 2011) electrodes. P3 positivity isknown to be responsive to target stimuli (Comerchero& Polich, 1999) and is thought to reflect higher-levelcognitive processes, including attention reorienting(Donchin & Coles, 2010; Katayama & Polich, 1998;Linden, 2005) and reward significance (Keil et al., 2002;Yeung & Sanfey, 2004). Ostracism responses as reflectedby the P3 component decrease in amplitude over thecourse of the experiment (Kawamoto, Nittono, & Ura,2013) and are also reduced as a function of involve-ment (Niedeggen et al., 2014), suggestive of the sensi-tivity of the P3 to context and motivation.

However, others have proposed that these ERPresponses are independent of the social context of theCyberball paradigm (Somerville, Heatherton, & Kelley,2006; Weschke & Niedeggen, 2015a) and instead maybe indicative of reorienting attention following an affec-tive response (Cacioppo et al., 2013). For instance, one

event-related potential (ERP) study by Weschke andNiedeggen (2016) revealed that the P3 component issimilarly responsive to reduced target probability forvisual oddball (i.e. seeing oddball target) andCyberball (i.e. receiving the ball in the exclusion block)tasks. Similarly, Cyberball tasks within a nonsocial con-text (e.g. ball tosses with a computer instead of playerswho were physically present) show no P3 differentia-tion between exclusion and inclusion. Other work sug-gests that the N2 amplitude was increased duringexclusion periods with physical players present(Weschke & Niedeggen, 2013). As has been previouslynoted (Themanson et al., 2015), the active nature of theexclusion period restricts the ability to draw conclusionsin comparison to the inclusion period, which is inher-ently passive (i.e. watching others throw the ball). Onepossible explanation is that both exclusion and inclu-sion periods activate an attention monitoring systemthat elicit N2 and P3 components to a greater orequivalent degree as an ostracism response system.Recent behavioral findings also indicate that while theCyberball inclusion condition may be effective as acontrol condition, it may be less specific to the uniqueeffects of being social included (Simard & Dandeneau,2017). To better delineate between ostracism responseand attention monitoring systems, the current study (a)implemented a new paradigm to address the inequityof participant involvement across conditions, and (b)utilized source estimation to better understand theneural substrates associated with the N2 and P3 thatare involved in ostracism.

Current study objectives

This study sought to evaluate whether neural corre-lates are differentially engaged in response to socialexclusion and social inclusion when the amount ofactive involvement preceding the ostracism event iscontrolled across conditions. To this end, theLunchroom paradigm was developed, previouslyused to explore stereotyped cues (Kiat, Straley, &Cheadle, 2017). This paradigm is set in a social con-text (a lunchroom table) in which ostracism feedbackwas presented as a discrete event following a deci-sion, rather than as part of an ongoing interaction asin the Cyberball paradigm. In this way, the paradigmwas designed to include equivalent levels of subjectengagement for each condition, such that subjectsmade an active decision and passively awaited theostracism outcome (inclusion or exclusion). Wehypothesized that social exclusion outcomes wouldgenerate larger neural ostracism responses, as cap-tured by the N2 and P3 components.

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The structure of our paradigm provided an opportu-nity to address an additional question: Considering thecomplex and often dynamic nature of ostracism out-comes (Chester & Riva, 2016), is it possible to be moreor less affected by being ostracized? Thus, our secondobjective was to evaluate how the experience of ostra-cism is influenced by everyday situations, such as mak-ing decisions that may have dynamic consequenceswith friends and others. Specifically, this study testedwhether engagement of the social brain prior to beingostracized would modulate the response to socialexclusion. In our paradigm, participants made an arbi-trary decision between options differing in either pos-sessive descriptors (e.g. “parent’s tie”) or physicaldescriptors (e.g. “purple tie”) before receiving ostracismfeedback. This manipulation was designed to primeparticipants by making them decide between peoplewho own the object (interpersonal condition with pos-sessive descriptor) or between kinds of objects (physicalcondition with physical descriptor). Recent neuroima-ging work employing similar social priming techniques(Higgins & Eitam, 2014) suggests a network of brainregions are responsible for different kinds of implicitpriming (Wang & Hamilton, 2015), including the ACCduring priming of social engagement. Thus, it washypothesized that priming engagement of the socialbrain would increase the salience of ostracism, andsubsequently, the response to social exclusion wouldbe larger in the interpersonal relative to the physicalcondition.

Lastly, this study sought to bridge the gap betweenERP and functional imaging studies by utilizing sourceestimation to better understand the temporal dynamicsof the neural sources underlying the N2 and P3 com-ponents. Specifically, neural sources engaged duringeach respective time window were evaluated to betterunderstand the generators of each component.Secondarily, source estimates were extracted acrossthe full ERP time window to understand the dynamicprocess by which these sources are engaged over time.Aligned with prior imaging results, a set of brainregions engaged during ostracism were targeted,including the ACC, cingulate gyrus, medial frontalgyrus, and insula (Eisenberger, 2012b). In addition,other key social brain regions were predicted to beheightened during the interpersonal priming decisionpreceding the ostracism outcome, including the amyg-dala, superior temporal gyrus (STG), and fusiform gyrus(Adolphs, 2008; Allison, Puce, & McCarthy, 2000; VanOverwalle, 2009). In addition, we evaluated the superiorparietal lobule (SPL) due to its association with socialattention (Nummenmaa & Calder, 2009), particularly inreference to biological motion (Stevens, Fonlupt,

Shiffrar, & Decety, 2000) and thinking about the inten-tions of others(Molenberghs, Cunnington, & Mattingley,2012; Pelphrey, Morris, & McCarthy, 2004). It was pre-dicted that ostracism brain regions implicated in pro-cessing social pain would be more active duringexclusion relative to inclusion events and that this con-trast would be heightened following interpersonaldecisions.

Materials and methods

Participants

Adults (N = 29, 16 female) between 18 and 32 years oldenrolled and completed this study. Sixteen of theseparticipants were undergraduate students and receivedcourse credit for their participation. Subsequent to ERPdata preprocessing, one female participant wasexcluded due to excessive blinks. Thus, this studyreflects data collected from 28 adults (15 female,M = 22.71, SD = 5.01 years). All participants had normalor corrected-to-normal vision and were screened forneurological and psychiatric disorders. The local ethicalreview board approved this project and all participantsgave written informed consent.

Design and procedure

In this paradigm (see Figure 1 for paradigm design),participants selected avatars to represent themselvesand were then introduced to two other charactersrepresenting their best friends. Participants were toldthat they would be given a choice between two optionsand that this decision was the basis for whether or nottheir best friends would sit with them at the lunchroomtable. For each trial, participants were presented withtwo options that had the same noun. Decision themesfor the noun included objects, activities, food, andclothing. The interpersonal condition varied in posses-sive descriptor between the two options (e.g. grand-mother’s casserole versus parent’s casserole). There were10 possible possessive descriptors: “boss”, “classmate”,“coworker”, “friend”, “grandparent”, “parent”, “partner”,“roommate”, “sibling”, and “teacher”. The physical con-dition varied in physical descriptor between the twooptions (e.g. tofu casserole versus chicken casserole).The same noun was included for both decision types,such that each noun was included once as the basis forboth physical and interpersonal decision trials. A full listof arbitrary decisions is available in SI Table 1. All parti-cipants saw the same trials, such that decision pairswere fixed and led to a predetermined outcome feed-back. For instance, regardless of whether a participant

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chose “curly hair” or “straight hair”, this decision led toan exclusion outcome. However, the order of trial pre-sentation was random. Participants were given up to3000 ms to make their decision.

After indicating their decision, participants receivedostracism outcome feedback via a lunchroom scenario

where they were either excluded (avatar sitting alone)or included (avatar surrounded by best friends). Theostracism outcome feedback was visually presentedfor 1000 ms. To increase the salience of the outcome,after the initial 1000 ms, an auditory token was pre-sented for 500 ms while the image remained on the

Table 1. Ostracism results for ERP components. Positive differences indicate a larger effect (i.e. greater amplitude or faster latency)for exclusion relative to inclusion outcomes. Significant differences (p < .05) are noted in bold.

Interpersonal ostracism effect Physical ostracism effect

Component Measure Region Difference t(193) p Difference t(193) p

N2 Amplitude Left frontal 0.62 0.47 0.637 −0.30 −0.23 0.820(µV) Medial frontal 0.85 1.3 0.199 −0.14 −0.21 0.833

Right frontal 0.51 0.42 0.676 0.11 0.09 0.926Medial central −0.64 −0.91 0.366 −1.10 −1.57 0.119

Latency Left frontal −4.37 −0.53 0.597 −3.13 −0.38 0.705(ms) Medial frontal 17.39 1.67 0.099 1.43 0.14 0.891

Right frontal 21.84 1.84 0.069 −1.97 −0.17 0.869Medial central 19.58 2.34 0.022 0.58 0.07 0.945

P3 Amplitude Left frontal 1.78 0.84 0.404 0.25 0.12 0.907(µV) Medial frontal 4.38 2.07 0.041 1.91 0.91 0.368

Right frontal 3.15 1.87 0.064 2.85 1.7 0.093Medial central −0.55 −0.45 0.656 −2.34 −1.91 0.060

Latency Left frontal −9.68 −0.46 0.649 31.38 1.48 0.142(ms) Medial frontal 6.07 0.35 0.727 −0.40 −0.02 0.981

Right frontal 16.24 0.99 0.327 35.16 2.14 0.036Medial central 8.47 0.62 0.537 9.18 0.67 0.503

Figure 1. Schematic of paradigm design. Following an initial fixation, trials began with a decision phase in which participantsselected one of two options that required the participant to make an arbitrary physical or interpersonal decision. The participant-selected avatar (i.e. to represent themself; shown here with a green shirt) was either included or excluded at the lunch table. ERPswere time-locked to the onset of the outcome phase. An auditory token (300 ms) was presented subsequently to increase thesalience of the outcome.

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screen for another 1000 ms. A social and biologicalsound of a male voice exclaiming “Yeah!” was pre-sented during inclusion trials, and a nonsocial and non-biological sound of three descending tones (e.g. “sadtrombone”) was presented during exclusion trials.Although a formal measurement of subjective experi-ence was not collected, research assistants recordedqualitative data in response to two follow up questionsfor 24 of the 28 participants (transcripts available in SITable 2). Notably, 50% reported negative feelings (e.g.being upset or sad) when their friends did not sit withthem and an additional 33.3% reported being confusedor uncertain about why they were excluded, whichsuggests that the manipulation was successful.

Of the 160 total trials, participants saw 40 trials foreach of the four conditions based upon decision andostracism outcome: Interpersonal Exclusion,Interpersonal Inclusion, Physical Exclusion, andPhysical Inclusion. Stimuli were presented usingE-Prime 2.0 software (Psychological Software Tools,Inc., Pittsburgh, PA) on a separate computer that inte-grated with ongoing electroencephalography (EEG)data collection to mark events. Subjects were seated60–80 cm away from a Tobii TX300 (Tobii Technology,Falls Church, VA), which served as the monitor forstimuli presentation and an eye tracker. Eye trackingdata was not analyzed for this study. The monitor waspositioned at eye level and adjusted to capture eyeposition and display the stimuli at a visual angle of18.1° horizontal and 20.8° vertical.

EEG recording and processing

EEG was acquired using a 256-channel AgAgCl high-density electrode array to record visual ERPs using NetStation® 4.4.2 software (Electric Geodesic, Inc., EGI,

Eugene, OR). Electrode impedances recorded beforeand after the task were below 60 kΩ to maximizesignal-to-noise ratio, producing high-quality signals forsubsequent analyses. The ongoing EEG signals weredigitized at 4 milliseconds intervals for each of the256 electrode sites. High-pass filters were set to 0.1 Hzand low-pass filters to 30 Hz with a gain of 10 kΩ.Epochs were time-locked to the onset of the ostracismoutcome, thus were segmented from continuous EEGwith a 100 ms baseline period prior to ERP onset to700 ms following onset (i.e. prior to auditory tokens).Segmentation accounted for event offset, recordedmonthly to verify the timing of event markers, andanti-alias filtering offset. Voltage shifts greater than150 µV during the epoch (e.g. eye blinks) were classi-fied as artifacts and ocular artifact correction was imple-mented. For epochs and electrode channels on whichartifacts were detected, the ERP signal was deleted andreplaced with an average signal interpolated fromimmediately adjacent electrode locations followingstandard procedures. Manual data quality checks forall epochs and channels were conducted to ensurethat other artifacts (e.g. electrical noise) were not sub-sequently included. Remaining epochs were then refer-enced again to the average of all electrodes, baselinecorrected, and averaged across conditions.

ERP extraction and analysis

ERP extraction focused on two electrode regions (fron-tal and central) across left, medial, and right hemi-spheres (Figure 2; see Supplemental Material for list ofsensors). Visual inspection of the grand-averaged wave-form indicated a negative deflection between80–280 ms that was most prominent across left frontal,medial frontal, and medial central clusters that

Table 2. Ostracism results for brain source engagement. Positive differences (Diff.) indicate a more source engagement innanoamperes (nAmp) for exclusion relative to inclusion outcomes. Significant differences (p < .05) are noted in bold.

Interpersonal ostracism effect Physical ostracism effect

Component Region Diff (nAmp) t(193) p Diff (nAmp) t(193) p

N2 Amygdala 0.086 2.01 0.046 0.084 1.96 0.052Anterior cingulate cortex 0.037 2.50 0.013 0.027 1.82 0.070Cingulate gyrus −0.001 −0.03 0.977 −0.029 −1.62 0.106Fusiform gyrus −0.023 −0.86 0.391 0.039 1.46 0.145Insula 0.017 1.69 0.092 0.009 0.91 0.367Medial frontal gyrus 0.013 0.89 0.374 0.002 0.11 0.910Superior parietal lobule −0.071 −0.79 0.433 −0.068 −0.76 0.451Superior temporal gyrus 0.033 2.4 0.017 0.001 0.08 0.934

P3 Amygdala 0.173 2.52 0.012 0.073 1.06 0.289Anterior cingulate cortex 0.139 4.16 <.0001 0.073 2.16 0.032Cingulate gyrus 0.026 0.98 0.326 −0.026 −0.99 0.323Fusiform gyrus −0.031 −0.79 0.433 0.074 1.86 0.064Insula 0.042 2.02 0.045 0.012 0.57 0.570Medial frontal gyrus 0.092 3.43 0.001 0.035 1.31 0.193Superior parietal lobule −0.056 −0.41 0.681 −0.100 −0.74 0.459Superior temporal gyrus 0.102 3.32 0.001 0.021 0.7 0.487

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resembled the N2, which is relatively early compared tothe representation of the N2 by prior studies startingapproximately 120–130 ms (Niedeggen et al., 2014;Weschke & Niedeggen, 2013). However, although sev-eral social exclusion studies define the N2 as a laterlatency negative deflection, a negative deflectionbeginning between 80–100 ms is evident in the ERPwaveforms (Sreekrishnan et al., 2014; Themanson et al.,2013; Weschke & Niedeggen, 2013). The P3 wasdetected as the most positive value in the200–550 ms time window that was consistent withthe beginning of the positive deflection (see Figure 2)and prior work using the lunchroom framework (Kiatet al., 2017), though this time window is early in refer-ence to prior work (Comerchero & Polich, 1999).Although Kiat et al. (2017) focused on lateral centralelectrodes, the scalp topographies from the currentstudy were not as robust across lateral central andposterior clusters (see Figure 3) and were subsequentlyremoved from analyses. Although we noted a shift fromposterior to anterior medial electrodes across the timewindow, we opted to focus on the frontal P3 due to itsprominence in the latter part of the time window.

Peak amplitude and latency were extracted for eachparticipant and condition for the N2 (negative peaks)and the P300 (positive peaks) across the declared timewindows within the three frontal clusters and medialcentral electrode clusters (electrodes available inSupplemental Material). Multilevel models were gener-ated in SAS 9.3 using PROC MIXED separately for each

component (N2, P3) and cluster (left frontal, medialfrontal, right frontal, medial central) with a randomintercept to capture individual difference variancebetween subjects. The model parameters included afull factorial design between arbitrary priming decision(2: interpersonal, physical) and ostracism outcome (2:exclusion, inclusion). Least square difference correctionfor multiple corrections was applied for post-hoc pair-wise comparisons.

Source estimation and analysis

Source waveforms were generated for candidate brainregions using a finite difference model through theGeoSource® software program (v2.0; ElectricalGeodesics, Inc., Eugene, OR). The program implementsa forward modeling approach to accurately compute theelectrode locations in relation to brain tissue. Finite dif-ference model estimates were constrained by theMontreal Neurological Institute (MNI) average adult mag-netic resonance imaging database. Tissue volumes wereparceled using 7-mm voxels, each serving as a dipolesource location with three orthogonal orientations (in x,y, and z orientations). The finite difference model appliedestimations across a total of 2447 source dipole triplets.Conductivity values used in the finite difference modelincluded 0.25 S/m for brain, 1.8 S/m for cerebral spinalfluid, 0.018 S/m for skull, and 0.44 S/m for scalp (Ferree,Eriksen, & Tucker, 2000). Weighting was placed equally

Figure 2. Grand-average waveforms. Grand-average waveforms are plotted across frontal and central electrode clusters from 0 to700 ms post-outcome onset. Line color indicates exclusion (red) and inclusion (blue) outcomes. Line type indicates priming decision(interpersonal, solid; physical, dashed). Voltage is plotted positive up.

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across locations with regularization carried out viaTikhonov (1 × 10−2) using standardized low-resolutionbrain electromagnetic tomography as a constraint. Eighta priori candidate brain source regions were extracted forboth the N2 and P3: Amygdala, anterior cingulate cortex(ACC), cingulate gyrus, fusiform gyrus, insular cortex,medial frontal gyrus, superior parietal lobule (SPL), andsuperior temporal gyrus (STG).

First, identical to ERP multilevel design, multilevelmodels were generated in SAS 9.4 using PROC MIXEDseparately for each source region and time window totest effects of priming decision, ostracism outcome, andthe subsequent interaction with a random subject inter-cept. Mean source estimates were created viaGeoSource for each individual during both ERP tem-poral windows (N2, 80–280 ms; P3, 200–550 ms).

Second, to characterizing the temporal dynamicsassociated with source engagement of ostracismresponses, source engagement was estimated viaGeoSource using a moving window approach with100 ms bins offset by 50 ms (i.e. 0–100 ms,50–150 ms, and so on). Multilevel models were identicalto N2 and P3 time window analyses with the additionof a main effect and interactions of time bin to test forongoing dynamic changes.

Results

Behavioral results

There were no reaction time differences during the deci-sion phase, t(54) = .71, p = .71, between interpersonal(M = 1288.0 ms, SD = 622.3) and physical decisions(M = 1227.1 ms, SD = 599.3).

ERP results

Ostracism outcome differences (i.e. value for exclusionrelative to inclusion outcomes) are reported for eachcomponent, measure, and region in Table 1 and illu-strated in Figure 4.

N2 amplitudeMultilevel models revealed a marginal main effect ofostracism outcome, such that the N2 amplitude was esti-mated to be larger (i.e. more negative) for exclusion com-pared to inclusion outcomes by 1.10 µV across medialcentral electrodes, F (1, 81) = 3.08, p = 0.083. Acrossmedialfrontal electrodes, the N2 was estimated to be largerfollowing physical compared to interpersonal decisionsby 0.51 µV, F (1, 81) = 4.71, p = 0.033. This was evident

Figure 3. Scalp topography for N2 and P3 components. Scalptopography for each of N2 and P3 components illustrate therelative voltage distribution averaged across 100 ms temporalwindows.

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only when the participant had been excluded [decisiondifference = 1.49 µV; t(81) = 2.29, p = 0.25], but not whenthe participant was included [decision difference = 0.51µV; t(81) = .78, p = 0.44]. There were no priming decisionor ostracism outcome condition differences across left orright frontal clusters.

N2 latencyAcross medial frontal electrodes, N2 latency was signifi-cantly faster following interpersonal (M = 162.2 ms,SE = 6.50) than physical priming decisions(M = 188.4 ms, SE = 6.76), F (1, 81) = 12.60, p = 0.0006.Pairwise comparisons indicated this pattern was evidentfor inclusion, [N2 difference = 34.2 ms; t(81) = 3.28,p = 0.002] more so than exclusion outcomes [marginalN2 difference = 18.2 ms; t(81) = 1.74, p = 0.085]. Multilevelmodels across medial central electrodes indicated a mar-ginal effect of ostracism outcome, F (1, 81) = 1.7 p = 0.093,indicating a faster N2 latency for exclusion (M = 167.3 ms,SE = 9.42) than inclusion outcomes (M = 147.7 ms,SE = 10.0) specifically following interpersonal, t(81) = 2.34, p = .022, but not physical priming decisions,t(81) = .07, p = .94.

P3 amplitudeMultilevel models revealed a marginal main effect ofostracism outcome indicating a larger P3 amplitude (i.e.more positive) for exclusion compared to inclusion out-comes across medial and right frontal, F (1, 81) = 4.44,p = 0.038, and F (1, 81) = 6.38, p = 0.014, respectively.Pairwise comparisons indicated that these effects werelarger following interpersonal (p’s < .064) compared tophysical priming decisions (p’s < .093). A marginal effectacross medial central electrodes, F (1, 81) = 2.78,p = 0.10, indicated the opposite pattern, such that the

P3 was larger for inclusion relative to exclusionoutcomes.

P3 latencyA main effect of ostracism outcome was evident acrossright frontal electrodes, F (1, 81) = 64.88, p = 0.03, suchthat P3 latency was slower for exclusion (M = 366.8 ms,SE = 12.02) compared to inclusion outcomes(M = 341.1ms, SE = 11.5). This effect was evident follow-ing physical, t(81) = 2.14, p = 0.036, but not interperso-nal priming decisions, t(81) = .99, p = 0.33.

Neural source results: temporal windows

Ostracism outcome differences (i.e. values for exclusionrelative to inclusion outcomes) are reported for eachtime window and region Table 2.

N2 source engagementSource estimation multilevel models indicated moresource engagement during exclusion compared toinclusion outcomes within the amygdala and ACC, F(1, 193) = 7.86, p = 0.0056, and F (1, 193) = 9.34,p = 0.0026, respectively. As indicated in Table 2, pair-wise comparisons were significant following interperso-nal decisions (p’s < .05) but marginally significantfollowing physical decisions (p’s < .07) for both theamygdala and ACC. There were also marginal maineffects of ostracism outcome within the insula and theSTG, F (1, 193) = 3.38, p = 0.068, and F (1, 193) = 3.08,p = 0.081, respectively. Ostracism discrimination of theSTG was only significant following interpersonal deci-sions. No regions exhibited significant main or interac-tive effects of priming decision.

Figure 4. ERP amplitude and latency results. Marginal amplitude (µV) and latency (ms) means are plotted for the N2 and P300components for left frontal (FRL), medial frontal (FRM), right frontal (FRR), and medial central (CEM). Ostracism outcomediscrimination between exclusion (red) and inclusion (blue) is denoted by asterisks (*, p < .05) and tildas (~, p < .1).

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P3 source engagementSimilar to the N2 time window, P3 multilevel modelsindicated more source engagement during exclusionscompared to inclusion outcomes within the amygdalaand ACC, F (1, 193) = 6.44, p = 0.012, and F (1,193) = 19.98, p = .0001, respectively. Two additionalregions were also sensitive to ostracism outcome inthis same pattern, including MFG and STG, F (1,193) = 11.22, p = 0.001, and F (1, 193) = 8.06,p = .005, respectively. Pairwise comparisons (seeTable 2) indicated that these main effects were drivenby interpersonal (p’s < .045) and not physical primingdecisions (p’s > .19) with one exception: the ACC exhib-ited a significant ostracism discrimination followingphysical decisions, although it was reduced comparedto interpersonal decisions.

The only region that was sensitive to priming deci-sion was the SPL, F (1, 193) = 4.02, p = .046, such thatmore source engagement was estimated following phy-sical (M = .51 nA, SE = .12) relative to interpersonaldecisions (M = .31 nA, SE = .04)

Neural source results: dynamics of sourceengagement

Here, three regions that were associated with ostracismoutcome for both temporal windows were targeted:ACC, amygdala, and STG (other regions illustrated in SIFigure 1). Periods of the waveform that indicate signifi-cant ostracism discrimination are illustrated in Figure 5.

ACC dynamicsMultilevel models revealed a significant effect of slope,F (1, 2613) = 70.76, p < .0001, such that ACC activationis estimated to increase from 150–400 ms post-feed-back onset. A significant interaction between ostracismoutcome and time bin, F (1, 2613) = 2.96, p = .0007,indicated that ACC engagement increases more rapidlyfor exclusion compared to inclusion outcomes. Therewas a significant interaction between ostracism out-come and priming decision, F (1, 2613) = 4.69,p = .031, such that there was greater ACC activationfor exclusion compared to inclusion following interper-sonal decisions between 250–600 ms (p’s < .0026). Incontrast, following physical decisions, ostracism discri-mination was evident between 350–600 ms (p’s < .043).

A main effect of priming decision, F (1, 2613) = 11.96,p = .0006, indicated that ACC activation was predictedto be greater (on average) following physical comparedto interpersonal decisions.

Amygdala dynamicsMultilevel models revealed a significant effect of slope,F (1, 2613) = 39.72, p < .0001, such that amygdalaactivation is estimated to increase from 200–550 mspost-feedback onset. There was a marginal interactionbetween ostracism outcome and priming decision, F (1,2613) = 3.15, p = .076, such that ostracism discrimina-tion was evident following interpersonal decisionsbetween 250–500 ms (p’s < .032), but there were noperiods of significant ostracism discrimination followingphysical decisions (p’s > .11).

Figure 5. Dynamic modulation of neural sources. Estimated neural source engagement is plotted over time for the anteriorcingulate cortex (ACC), amygdala, and superior temporal gyrus (STG). Box insets indicate the temporal period with significantostracism outcome discrimination between exclusion (red) and inclusion (blue) outcomes, specifically for interpersonal decisions(solid lines). The dashed black horizontal line indicates the temporal period in the ACC (350–600 ms) of ostracism outcomediscrimination for the physical priming decision condition.

SOCIAL NEUROSCIENCE 9

A main effect of priming decision, F (1, 2613) = 4.22,p= .04, indicated that amygdala activationwas predicted tobe greater (on average) following physical compared tointerpersonal decisions.

STG dynamicsMultilevel models revealed a significant effect of slope,F (1, 2613) = 50.11, p < .0001, such that STG activationwas estimated to increase from 150–400 ms post-feed-back onset. There was a significant interaction betweenostracism outcome and priming decision, F (1,2613) = 14.76, p = .0001, such that ostracism discrimi-nation was evident following interpersonal decisionsbetween 250–600 ms (p’s < .028), but there were noperiods of significant ostracism discrimination followingphysical decisions (p’s > .24).

Discussion

The goal of the current study was to evaluate neuralresponses to ostracism in a paradigm that controlled forlevel of participant engagement prior to the inclusion/exclusion outcomes. In the current experiment, ratherthan varying the target probability of being included ina social game as in the Cyberball paradigm, participantshad equal likelihood of being excluded every trialthroughout the experiment. As part of the Lunchroomtask, participants made an arbitrary decision and, subse-quently, were socially excluded or included, ostensiblybased upon that decision. In this way, potential involve-ment of an attention monitoring system (Cacioppo et al.,2013) was equalized across conditions to better specifyresponses to ostracism and social exclusion. In addition,the paradigm was intentionally designed with thehypothesis that arbitrary interpersonal decisions wouldprime the social brain network, resulting in an increasedostracism response, more so than physical decisions.

Fronto-central ERPs time-locked to the ostracismoutcome elicited an early N2 negative deflection (80–280 ms) and a mid-latency P3 positive deflection (200–550 ms). Aligned with our hypotheses and prior work(Crowley et al., 2010; Gutz et al., 2011; Themanson et al.,2015; Weschke & Niedeggen, 2013), the P3 was sensi-tive to ostracism, as indicated by larger amplitude toexclusion compared to inclusion outcomes. In contrast,the N2 amplitudes and latencies were more sensitive tothe priming decision than ostracism outcome. Sourceestimation indicated the amygdala, ACC, and STGregions were engaged and discriminated betweenostracism outcomes during the temporal windows forboth the N2 and P3, consistent with prior imaging work(Eisenberger, 2012b), particularly following interperso-nal decisions. Evaluation of the temporal dynamics of

this source engagement indicated that ostracism discri-mination effects were evident particularly between250–500 ms post-outcome onset, although activationfrom all three regions increased preceding this period.These findings delineate potential functional roles ofeach component and highlight the process by whichthese neural substrates are engaged in ostracismresponses.

N2 modulation by social priming

Unlike prior work that has found an increased N2response to social exclusion (Sreekrishnan et al., 2014;Themanson et al., 2013; Weschke & Niedeggen, 2013),our results revealed a sensitivity to social priming butnot ostracism. Specifically, our data indicated faster N2latencies and greater N2 amplitude (i.e. more negative)for interpersonal compared to physical decisions acrossmedial frontal electrodes. Of note, the N2 amplitudefinding was restricted to the exclusion outcome, indi-cating that while N2 latency was sensitive to socialpriming regardless of outcome, N2 amplitude only dis-criminated between priming in exclusion events. Thissuggests that the overall priming effect on the N2 mayinfluence the speed of processing more so than themagnitude, which may be selectively sensitive to ostra-cism. Generally speaking, the N2 is thought to reflecttop-down attentional control and conflict monitoring(Falkenstein, Hoormann, & Hohnsbein, 1999;Nieuwenhuis et al., 2003). An explanation may be that,as intended by our experimental design, the act ofdeciding between two social categories successfullyengaged the social brain prior to the outcome, subse-quently increasing the speed of the system for monitor-ing the subsequent social (ostracism) feedback, butonly modulating the capacity of this system in exclusionevents.

Alternatively, considering that the N2 amplitude onlydiscriminated between priming decisions in the exclu-sion condition, the N2 may reflect the engagement of areward-specific system more so than the social brain.One other study found a similar N2 amplitude differen-tiation of social context (i.e. computer-based versus liveCyberball players) that was unique to the exclusioncondition (Weschke & Niedeggen, 2013). In that study,the N2 amplitude was greater for participants interact-ing with live players relative to computer-based playersduring exclusion periods. The authors suggest the N2reflects the modulation of the reward system, such thatreceiving the ball equates to a social reward that ispotentially more valuable from a live player than froma computer-based player. Extending this to the currentstudy, it may be the case that participants are more

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hurt by exclusion following interpersonal decision. Thisis aligned with the perspective that neural responses toostracisms are reflective of social pain more so thanconflict monitoring (Eisenberger, 2012b).

P3 sensitivity to ostracism

As described above, this work supports prior reports ofthe P3 amplitude capturing the appraisal of ostracism. Itis proposed that in the context of the Cyberball para-digm the P3 is related specifically to the activation of anearly alarm system (Gutz et al., 2011; Kawamoto et al.,2013) that relates to a pre-attentive neural system trig-gered by ostracism (Williams, 2006). In contrast, otherresults challenge the role of the Cyberball P3 within aneural alarm system for social pain, considering equiva-lent responses between exclusion conditions and fre-quency violation (Niedeggen et al., 2014; Weschke &Niedeggen, 2016) and the lack of modulation basedupon whether the players are present or not (Weschke& Niedeggen, 2013). Considering that the Lunchroomparadigm was designed to control for frequency ofanticipation (outcomes were equiprobable) and con-sisted solely of simulated avatar “friends,” our resultssupport the notion that the frontal P3 amplitudereflects recruitment of the alarm system. Additionally,the ostracism effect was larger when the priming deci-sion was interpersonal, suggesting that social brainpriming was effective and resulted in increased sensi-tivity to ostracism.

Our paradigm was built in part to better isolateprocessing related to social inclusion by equalizingparticipant involvement across exclusion and inclu-sion conditions. Whereas the frontal P3 exhibited alarger response for exclusion, the medial central P3response indicated a potential marker for inclusion, asevident by increased amplitude. Previously,Niedeggen et al. (2014) suggested that the centraland parietal P3 response to inclusion relates to theparticipants’ expectation of social inclusion. In thatstudy and subsequent work (Niedeggen, Kerschreiter,Hirte, & Weschke, 2017; Weschke & Niedeggen,2015b), the P3 amplitude to inclusion events wasreduced as involvement in the Cyberball ball-tossinggame increased and corresponded to participants’self-reported proportion of time spent possessingthe ball. This notion that the P3 amplitude reflects aviolation of expectancy (aligned with visual probabil-ity P3 paradigms, (Polich & Bondurant, 1997; Stadler,Klimesch, Pouthas, & Ragot, 2006)) is inconsistent withour findings. Instead, our results suggest that whenparticipant involvement is controlled, the P3 may betopologically sensitive as both an ostracism and

inclusion marker. Although beyond the scope of thispaper, future work would benefit from a deeperexamination of the ERP topology in relation to inclu-sion events.

Engagement of neural sources

Our final objective was to bridge the gap between ERPand fMRI findings by using source estimation to specifythe sources generating the N2 and P3 components. Ofthe eight targeted key social brain regions, source esti-mation indicated that five regions were at least margin-ally more engaged in exclusion outcomes: ACC,amygdala, insula, MFG, and STG. Importantly, theseostracism effects were present following interpersonalbut not physical priming. In other words, there were noneural source differences from being excluded orincluded around the lunchroom table unless precededby making an arbitrary decision between people. Theone exception to this effect was the ACC, which dis-criminated between ostracism outcomes for both prim-ing conditions, emphasizing a potential dominant rolefor the ACC in ostracism processing, regardless ofcontext.

A critical innovation of this study was the implemen-tation of source dynamics to empirically evaluate therespective timing of neural sources immediately uponreceiving ostracism outcome feedback. Close inspectionof the three regions implicated in both N2 and P3 timewindows (ACC, amygdala, and STG) indicated sourceengagement increased approximately 150 ms post-out-come onset and began discriminating between ostra-cism conditions at 250 ms, as evident in the boxedportions of the source activation dynamics in Figure 5.For the ACC, these effects were driven in part by a morerapid slope for exclusion than inclusion outcomes, suchthat ACC increased in activity at a faster rate. The factthat all three regions are engaged and discriminatingbetween conditions during the same temporal period isreinforced by evidence of functional connectivity acrossthese regions during social perception (Bickart,Hollenbeck, Barrett, & Dickerson, 2012; Demenescuet al., 2013; Wu et al., 2016). For instance, in one studyof empathetic response, the amygdala was morestrongly connected to regions implicated in socialpain (including the ACC) when viewing self-causedrelative to other-caused pain (Akitsuki & Decety, 2009).Taken together, these results support a tightly con-nected network of brain regions responsible for encod-ing ostracism.

The SPL was the only brain region to be selectivelysensitive to priming decision, as indicated by greatersource engagement following physical relative to

SOCIAL NEUROSCIENCE 11

interpersonal decisions within the P3 time window. Aspart of the attention system, the SPL has been impli-cated in the top-down modulation of attention(Corbetta & Shulman, 2002), particularly in the contextof memory retrieval (Ciaramelli, Grady, & Moscovitch,2008; Koenigs, Barbey, Postle, & Grafman, 2009; Wagner,Shannon, Kahn, & Buckner, 2005). Thus, although theSPL was initially targeted due to its role in social atten-tion (Nummenmaa & Calder, 2009), these results sug-gest the SPL is more dedicated to attentional thansocial processes. One interpretation of this finding isthat subjects may require increased attentionalresources to parse meaning for outcomes followingphysical decisions, whereas interpersonal priming mayhold longer in short-term memory, requiring less mem-ory recall and/or attention reorienting.

Limitations

One of the limitations of the current study is that therewas no self-report of stress or other individual differ-ences related to changes in mood in order to confirmthe affective experience of being excluded. Forinstance, several studies have found that rejectionevents during the Cyberball task elicit slow-wave activ-ity across left and medial frontal electrodes that isrelated to self-reported distress (Crowley et al., 2009,2010; Sreekrishnan et al., 2014) and decreased quality ofparental attachment in youth (White et al., 2012).Although the current study did not evaluate slow-wave activity, it is possible that extended processingcontinues beyond our ERP time window and may relateto the affective experience of being socially excluded.Future work would benefit from objective measure-ments to better account for physiological reactions(i.e. breathing or heart rate changes) or facial affect(i.e. expression of positive versus negative emotions).

This study is described as exploratory in part due to thefact that the topography and timing of the ERP compo-nents are not entirely consistent with prior work. Forinstance, the N2 component is usually thought to startcloser to 120–130 ms, which is much later than the begin-ning negative deflection that starts ~ 80 ms observed inthis study. Similarly, the time window chosen for the P3(200–550 ms) is earlier than the common time windowsfor the P3, including the subcomponents of the P3 knownas the P3a (250–450 ms) and P3b (350–600 ms)(Comerchero & Polich, 1999). While it is possible that theLunchroom task elicits a much faster response due to thenature of the visual feedback, early N2 deflections areevident in the grand-averagedwaveforms in other studies(Sreekrishnan et al., 2014; Themanson et al., 2013;Weschke & Niedeggen, 2013), highlighting a need to

better understand this early processing. The P3 in thecurrent study was also unusual in frontal distributionrelative to prior work that identified a posterior P3(Crowley et al., 2010; Themanson et al., 2015) and centralP3 (Gutz et al., 2011). Here, we focused on the frontal P3 asthe most prominent component as evident in Figure 3.Yet, a prior study using the lunchroom framework (Kiatet al., 2017) indicated a stronger lateral central P3 inexclusion trials following a neutral more so than socially-meaningful (i.e. stereotyped) decision. In light of the ostra-cism effect reversal across central electrodes (i.e. greaterresponse to inclusion over exclusion) in the current study,it will be important to continue to evaluate posterior andcentral P3 contributions.

In addition, it is important to acknowledge the explora-tory nature of these analyses and subsequently cautionover-interpretation. Considering the novelty of the para-digm, we did not consider a priori hypotheses regardingthe ERP topography and neural source generation. Rather,as an exploratory study, we elected to test amplitude,latency, and source models across regions without omni-bus test correction. Considering that the posthoc compar-isons were significant with corrections, these results maybe considered a first step in understanding ostracismwhen active involvement is controlled across conditions.Second, the nature of the ERP waveform response to thisnovel paradigm should be replicated to confirm the earlytemporal window of the N2, the frontal topography of theP3, and the dependent relationships between adjacentcomponents. Lastly, although the paradigm did controlparticipant involvement during the activity, it is possiblethat the variability of physical stimulus characteristics (e.g,luminance, intensity) or auditory feedback anticipation forthemain contrast (i.e. exclusion versus inclusions) affectedthe neural response to ostracism. Taken together, futureresearch should extend this work by systematically mod-ifying the task to empirically assess task properties. Inaddition, continued work would benefit by implementa-tion of more sophisticated analytical (e.g. generalizedmixed models) (Lo & Andrews, 2015) and potentiallywaveform de-composition methods (e.g. temporal-spatialPCA or continuous ICA) (Delorme, Miyakoshi, Jung, &Makeig, 2015).

Conclusion

This study offers new insight into the dynamic and mod-ulatory nature of neural responses in the context of ostra-cism and social exclusion. By more clearly dissociatingactive task participation from the expression of ostracism,our results support prior work (Themanson et al., 2013;Weschke & Niedeggen, 2013), suggesting separable rolesof the N2 and P3 in modulation of social information and

12 C. M. HUDAC

sensitivity to ostracism outcomes, respectively. Further,social brain regions previously activated during functionalimaging, particularly within the amygdala, ACC, and STG(Eisenberger, 2003, 2012b; Masten et al., 2009, 2010; Mooret al., 2012; Williams et al., 2000), are also differentiallyengaged in response to ostracism outcomes. Critically,closer inspection of the temporal dynamics of thesebrain regions suggest a period of increased activationbetween 250–600 ms post-outcome onset, offering newevidence of the process by which these brain regions areengaged. These findings emphasize how daily (see-mingly) benign choices intensify the effects of ostracism.Considering the known impact of ostracism on behavior(Oaten, Williams, & Jones, 2008; Svetieva et al., 2016;Warburton, Williams, & Cairns, 2006), there may be poten-tial adverse consequences following arbitrary social deci-sions and how we subsequently interact with theenvironment. A deeper understanding of neural dynamicsof ostracism may lead to the discovery of possible protec-tive mechanisms in the brain that can be bolstered byinterventions (e.g. social supports and positive relation-ships; (Eisenberger, Taylor, Gable, Hilmert, & Lieberman,2007). Continued exploration of these processes may pro-vide essential clues to successfully strengthen healthysocial relationships and interactions at pivotal develop-mental periods.

Acknowledgments

Thank you to the individuals for their participation in this study.The author is grateful for assistance with data collection and inputon earlier drafts fromDr. Allison L. Skinner, aswell as beinggratefulfor feedback and suggestions from the anonymous reviewers andDr. Anne B. Arnett. This research did not receive any specific grantfrom funding agencies in the public, commercial, and not-for-profit sectors. The author would like to thank Dr. Dennis L.Molfese for supporting her graduate work.

Disclosure statement

No potential conflict of interest was reported by the author.

ORCID

Caitlin M. Hudac http://orcid.org/0000-0002-0478-440X

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