Abstract

Social belonging is an important human drive that influences mood and behavior. Neural responses to social exclusion are well-characterized, but the specificity of these responses to processing rejection-related affective distress is unknown. The present study compares neural responses to exclusion and overinclusion, a condition that similarly violates fairness expectations but does not involve rejection, with a focus on implications for models of dorsal anterior cingulate cortex (dACC) and anterior insula (AI) function. In an fMRI adaptation of the Cyberball paradigm with adolescents aged 11.1-17.7 years (N = 69), we employed parametric modulators to examine scaling of neural signal with cumulative exclusion and inclusion events, an approach that overcomes arbitrary definitions of condition onsets/offsets imposed on fluid, continuous gameplay. We identified positive scaling of dACC and posterior insula response with cumulative exclusion events, but these same regions exhibited trending signal decreases with cumulative inclusion events. Furthermore, areas within the dACC and insula also responded to context incongruency (throws to the participant in the exclusion run; throws between computer players in the overinclusion run). These findings caution against interpretations that responses in these regions uniquely reflect the affective distress of exclusion within social interaction paradigms. We further identified that the left ventrolateral PFC, rostromedial PFC, and left intraparietal sulcus responded similarly to cumulative exclusion and inclusion. These findings shed light on which neural regions exhibit patterns of differential sensitivity to exclusion or overinclusion, as well as those that are more broadly engaged by both types of social interaction.

Highlights

  • From the earliest fMRI studies on social rejection, it has been proposed that the dorsal anterior cingulate cortex and anterior insula (AI) process the affective distress underlyingTheresa W

  • L middle frontal gyrus dACC, dorsal anterior cingulate cortex; BA, Brodmann area; Context Congruent: events which match the context, i.e., inclusion throws in the inclusion round and exclusion throws in the exclusion round; Context Incongruent: events which do not match the context, i.e., inclusion throws in the exclusion round and exclusion throws in the inclusion round

  • We used parametric modulators to examine the specificity of neural responses to social exclusion as compared to overinclusion during Cyberball

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Summary

Introduction

From the earliest fMRI studies on social rejection, it has been proposed that the dorsal anterior cingulate cortex (dACC) and anterior insula (AI) process the affective distress underlyingTheresa W. While recent studies suggest that pain and social rejection have distinct representations in the dACC and AI (Woo et al, 2014; Kragel et al, 2018), many perspectives maintain a role for these regions in processing rejection-related affective distress This hypothesis can be evaluated by considering whether a brain region’s responses are specific to social rejection compared with social overinclusion. Cyberball (Williams, Cheung, & Choi, 2000) is a virtual ball-tossing game commonly used to simulate social exclusion in neuroimaging studies (for review and meta-analysis, see Vijayakumar, Cheng, & Pfeifer, 2017) Such studies often compare social exclusion to a condition referred to as “social inclusion” that resembles fair play (i.e., Cogn Affect Behav Neurosci (2020) 20:340–355 roughly equal participation by all players). Few human neuroimaging studies compare social exclusion to overinclusion

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