Elsevier

NeuroImage

Volume 54, Issue 3, 1 February 2011, Pages 2462-2471
NeuroImage

Dissociable brain mechanisms for processing social exclusion and rule violation

https://doi.org/10.1016/j.neuroimage.2010.10.049Get rights and content

Abstract

Social exclusion inherently involves an element of expectancy violation, in that we expect other people to follow the unwritten rule to include us in social interactions. In this functional magnetic resonance imaging (fMRI) study, we employed a unique modification of an interactive virtual ball-tossing game called “Cyberball” (Williams et al., 2000) and a novel paradigm called “Cybershape,” in which rules are broken in the absence of social exclusion, to dissociate brain regions that process social exclusion from rule violations more generally. Our Cyberball game employed an alternating block design and removed evoked responses to events when the participant was throwing the ball in inclusion to make this condition comparable to exclusion, where participants did not throw. With these modifications, we replicated prior findings of ventral anterior cingulate cortex (vACC), insula, and posterior cingulate cortex activity evoked by social exclusion relative to inclusion. We also identified exclusion-evoked activity in the hippocampi, left ventrolateral prefrontal cortex, and left middle temporal gyrus. Comparing social exclusion and rule violation revealed a functional dissociation in the active neural systems as well as differential functional connectivity with vACC. Some overlap was observed in regions differentially modulated by social exclusion and rule violation, including the vACC and lateral parietal cortex. These overlapping brain regions showed different activation during social exclusion compared to rule violation, each relative to fair play. Comparing activation patterns to social exclusion and rule violation allowed for the dissociation of brain regions involved in the experience of exclusion versus expectancy violation.

Research Highlights

►Social exclusion activated vACC, PCC, hippocampus, and insula. ►Rule violation activated dorsal medial and lateral PFC and parietal cortex. ►vACC showed different patterns of functional connectivity in social exclusion and rule violation. ►Rule violation and Social exclusion showed a dorsal-ventral distinction in mPFC, respectively. ►Social exclusion and rule violation recruit distinct networks of brain activation.

Introduction

Ostracism, the exclusion of one member from a group, is a social phenomenon that threatens relationships, especially the security offered by friendships and peer networks. Williams et al. (2000) developed an experimental paradigm modeling social exclusion in an interactive computer-based program called Cyberball. In Cyberball, two other ostensibly real players may throw the ball with the participant, or only amongst themselves. Behavioral studies using Cyberball (Boyes and French, 2009, Masten et al., 2009, Sebastian et al., 2010, Zadro et al., 2004, Zadro et al., 2005) have found that exclusion elicits a more negative overall mood and decreased feelings of belongingness, control, meaningful existence, and self-esteem (Williams et al., 2000; Williams, 2007, Zadro et al., 2004). These effects occur even if participants know that the other players are computerized (Zadro et al., 2004).

Cyberball has been used in fMRI studies to investigate the brain response to social exclusion (Eisenberger et al., 2003, Masten et al., 2009, Onoda et al., 2009, Onoda et al., in press). Brain regions found active during exclusion versus fair play include ventrolateral prefrontal cortex (vlPFC) and anterior insula (Eisenberger et al., 2003, Masten et al., 2009), ventral anterior cingulate cortex (vACC, Masten et al., 2009, Onoda et al., 2009), dorsal anterior cingulate cortex (dACC, Eisenberger et al., 2003), and posterior cingulate cortex (Onoda et al., 2009). Several studies reported correlations between dACC activity during exclusion and self-reported social pain (Eisenberger et al., 2003, Onoda et al., 2009, Onoda et al., in press). However, the precise psychological correlates of these neural effects remain unclear. Exclusion in Cyberball potentially involves the emotional state of rejection, cognitive reactions to violated expectations of inclusion, and cognitive efforts to assess the situation. This complexity has likely contributed to inconsistent findings across fMRI studies.

We used two different virtual ball-toss games to functionally dissociate brain mechanisms involved in processing social exclusion and rule violation. Social exclusion was elicited by a modification of the original Cyberball paradigm. In prior studies, inclusion always preceded one period of exclusion. Our Cyberball design used alternating blocks of inclusion and exclusion to eliminate the potential confounds of scanner drift, changes in participant motion and attention, and fatigue occurring over the course of a scan session. In addition, the alternating block design decreases the likelihood of participant disengagement from the task in long periods of exclusion. The alternating blocks also model important aspects of naturally occurring ostracism, where exclusion can be transient and relatively ambiguous at times. Note that ambiguous ostracism, where the participant still occasionally receives the ball during periods of perceived exclusion, has been shown in past behavioral and imaging Cyberball studies to elicit strong feelings of exclusion (Boyes and French, 2009, Chernyak and Zayas, 2010; Onoda et al., 2009, Williams et al., 2000). As an additional methodological adjustment, we modeled and removed evoked responses to events when the participant was throwing the ball, to account for the potential confound that participants are actively playing during fair play but not exclusion.

Cyberball was compared to a new ball tossing game, “Cybershape,” in which the ball takes on a new shape on each toss, which specifies the player to whom the ball should be thrown. In Cybershape, one of the computerized players breaks the shape rule, eliciting a non-exclusive expectancy violation. Unlike social exclusion, however, rule violations do not threaten one's social relationships. A past study comparing rejection and expectancy violation found that dorsal and ventral ACC were recruited differentially by these two conditions (Somerville et al., 2006). Past Cyberball studies have found both dACC and vACC activation in exclusion, yet the psychological correlates of this activation remain unclear. Comparing patterns of activation during rule violation in Cybershape and social exclusion in Cyberball, two similar interactive, social paradigms, allowed for a functional dissociation of brain regions involved in the experiences of exclusion and expectancy violation more generally. Further, psychophysiological interaction analyses in the two games aimed to provide illumination of regional functional connectivity involved in the experience of social exclusion, as compared to connectivity in rule violation.

Section snippets

Participants

We studied a group of 26 healthy young adults (13 males, mean age = 24.15 years ± 4.07). Twenty-five of the participants played Cyberball and Cybershape consecutively in the same scanning session with a counterbalanced order (one participant played Cyberball only). All participants were asked upon completion of both games if they felt excluded during Cyberball, and if they noticed rules being broken in Cybershape. If the answer to either of these questions was no, the participant was excluded from

Results

The social exclusion questionnaire given to a subset of participants (n = 7) confirmed that Cyberball elicited feelings of distress following exclusion. The average response to each question was 2.89 (on a scale from 1 = “not at all” to 5 = “extremely”). The average total score on this questionnaire was 28.86 (± 2.64). This score was significantly greater than the minimum score of 10 reflecting no exclusion-related distress (t(6) = 7.14, p < 0.001). On the questionnaire consisting of ten different

Discussion

The present study demonstrated a functional dissociation in the neural responses to social exclusion and rule violation. The finding of statistically different regional activation between games (Fig. 3) supports the conclusion that the two games, though very similar in design, recruit dissociable neural systems as a function of the experience of social exclusion versus rule violation. Further, contrasting patterns of functional connectivity to the vACC were found between these two conditions.

Acknowledgments

The research presented herein was supported by grants from the National Institute of Mental Health, the John Merck Scholars Fund, and the Simons Foundation. Kevin Pelphrey was supported by a Career Development Award from the National Institutes of Health (NIMH Grant MH071284). Linda Mayes was also supported by a Career Development Award (NIDA K05 DA020091). Naomi Pitskel was supported by a grant from the Doris Duke Charitable Foundation to Yale University.

References (57)

  • M.D. Greicius et al.

    Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus

    Biol. Psychiatry

    (2007)
  • J. Levesque et al.

    Neural circuitry underlying voluntary suppression of sadness

    Biol. Psychiatry

    (2003)
  • M. Liotti et al.

    Differential limbic–cortical correlates of sadness and anxiety in healthy subjects: implications for affective disorders

    Biol. Psychiatry

    (2000)
  • R.J. Maddock

    The retrosplenial cortex and emotion: new insights from functional neuroimaging of the human brain

    Trends Neurosci.

    (1999)
  • K.L. Phan et al.

    Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI

    Neuroimage

    (2002)
  • K.L. Phan et al.

    Neural substrates for voluntary suppression of negative affect: a functional magnetic resonance imaging study

    Biol. Psychiatry

    (2005)
  • C. Sebastian et al.

    Social brain development and the affective consequences of ostracism in adolescence

    Brain Cogn.

    (2010)
  • K.M. Shafritz et al.

    The interaction of emotional and cognitive neural systems in emotionally guided response inhibition

    Neuroimage

    (2006)
  • J.D. Steele et al.

    Segregation of cognitive and emotional function in the prefrontal cortex: a stereotactic meta-analysis

    Neuroimage

    (2004)
  • J.N. Wood et al.

    Representation of attitudinal knowledge: role of prefrontal cortex, amygdala and parahippocampal gyrus

    Neuropsychologia

    (2005)
  • L. Zadro et al.

    How low can you go? Ostracism by a computer is sufficient to lower self-reported levels of belonging, control, self-esteem, and meaningful existence

    J. Exp. Soc. Psychol.

    (2004)
  • R. Zahn et al.

    Subgenual cingulate activity reflects individual differences in empathic concern

    Neurosci. Lett.

    (2009)
  • D.M. Amodio et al.

    Meeting of minds: the medial frontal cortex and social cognition

    Nat. Rev. Neurosci.

    (2006)
  • A.J. Blood et al.

    Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions

    Nat. Neurosci.

    (1999)
  • M. Brass et al.

    Decomposing components of task preparation with functional magnetic resonance imaging

    J. Cogn. Neurosci.

    (2004)
  • R.L. Buckner et al.

    The brain's default network: anatomy, function, and relevance to disease

    Ann. NY Acad. Sci.

    (2008)
  • S.A. Bunge

    How we use rules to select actions: a review of evidence from cognitive neuroscience

    Cogn. Affect. Behav. Neurosci.

    (2004)
  • S.A. Bunge et al.

    Neural circuitry underlying rule use in humans and nonhuman primates

    J. Neurosci.

    (2005)
  • Cited by (111)

    • Differential neural sensitivity to social inclusion and exclusion in adolescents in foster care

      2022, NeuroImage: Clinical
      Citation Excerpt :

      An additional zero-duration regressor of no interest marked when participants’ avatar “caught” the ball, signaling the participant’s turn to throw the ball. This regressor controlled for neural responses related to participants’ decision-making (and subsequent button-press) as used in previous studies with event related designs (Bolling et al., 2011). A final regressor modelled a “wait” period at the start of each run, where the screen displayed the words “Connecting to other players…” and a progress bar (lasting approximately 8 s).

    • Social exclusion reliably engages the default network: A meta-analysis of Cyberball

      2021, NeuroImage
      Citation Excerpt :

      An alternate predominant view of dACC activation for social exclusion may have motivated bias in subsequent reports to fit their results in the social pain framework. Indeed, some studies without whole brain dACC effects conduct additional region of interest analysis on the dACC (Asscheman et al., 2019) or lowered the statistical threshold for significance (Bollings et al., 2011b). Analyses investigating neural correlations with self-reported distress can more directly speak to the participant's neural response to the experience of social exclusion.

    View all citing articles on Scopus
    View full text