Dissociable brain mechanisms for processing social exclusion and rule 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.
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