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Feeling left out or just surprised? Neural correlates of social exclusion and overinclusion in adolescence

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.

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Acknowledgements

The authors wish to express gratitude to Rebecca Calcott for consultation on the analysis and to Danielle Cosme for scripts to process motion and to access brain parcellation maps. This work was supported by the grants P50 DA035763 (PIs: Chamberlain and Fisher) and R01 MH107418 (PI: Pfeifer). TWC was supported by National Center for Advancing Translational Sciences of the National Institutes of Health under award number TL1TR002371. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Open practices statement

None of the analyses were pre-registered. Statistical maps are available on NeuroVault (https://neurovault.org/collections/3794). Preprocessing scripts used for this analysis are available on GitHub at https://github.com/dsnlab/TDS_scripts/tree/cheng_cyb_main/fMRI/ppc/spm/tds2 (SPM scripts) and https://github.com/dsnlab/TDS_scripts/tree/cheng_cyb_main/fMRI/ppc/shell/schedule_spm_jobs/tds2 (shell scripts). High motion volumes were identified using an in-house automated script that is publicly available (Cosme et al., 2018). We refer interested readers to the most recent version (https://github.com/dsnlab/auto-motion), and the branch used in this analysis is available at https://github.com/dsnlab/TDS_scripts/tree/cheng_cyb_main/fMRI/fx/motion/auto-motion.

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Correspondence to Jennifer H. Pfeifer.

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Theresa W. Cheng and Nandita Vijayakumar share Co-first authorship

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Cheng, T.W., Vijayakumar, N., Flournoy, J.C. et al. Feeling left out or just surprised? Neural correlates of social exclusion and overinclusion in adolescence. Cogn Affect Behav Neurosci (2020). https://doi.org/10.3758/s13415-020-00772-x

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Keywords

  • Cyberball
  • Social exclusion
  • Functional MRI
  • Anterior cingulate cortex
  • Anterior insula