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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Addis, D. R., Wong, A. T., & Schacter, D. L. (2007). Remembering the past and imagining the future: common and distinct neural substrates during event construction and elaboration. Neuropsychologia, 45(7), 1363–1377. https://doi.org/10.1016/j.neuropsychologia.2006.10.016
Ames, D. L., Jenkins, A. C., Banaji, M. R., & Mitchell, J. P. (2008). Taking Another Person’s Perspective Increases Self-Referential Neural Processing. Psychological Science, 19(7), 642–644. https://doi.org/10.1111/j.1467-9280.2008.02135.x
Anderson, M., & Jiang, J. (2018). Teens, Social Media & Technology 2018. Pew Research Center.
Ardila, A., Bernal, B., & Rosselli, M. (2017). Should Broca’s area include Brodmann area 47? Psicothema, 29(1), 73–77. https://doi.org/10.7334/psicothema2016.11
Barron, H. C., Garvert, M. M., & Behrens, T. E. J. (2016). Repetition suppression: A means to index neural representations using BOLD? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 371(1705). https://doi.org/10.1098/rstb.2015.0355
Baumeister, R. F., & Leary, M. R. (1995). The need to belong: Desire for interpersonal attachments as a fundamental human motivation. Psychological Bulletin, 117(3), 497–529. https://doi.org/10.1037/0033-2909.117.3.497
Benjamini, Y., & Hochberg, Y. (1995). Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society. Series B (Methodological), 57(1), 289–300. Retrieved from JSTOR.
Berthoz, S., Armony, J. L., Blair, R. J. R., Dolan, R. J. (2002). An fMRI study of intentional and unintentional (embarrassing) violations of social norms. Brain, 125, 1696–1708.
Blakemore, S.-J., & Mills, K. L. (2014). Is adolescence a sensitive period for sociocultural processing? Annual Review of Psychology, 65(August 2013), 187–207. https://doi.org/10.1146/annurev-psych-010213-115202
Bolling, D. Z., Pelphrey, K. A., & Wyk, B. C. V. (2016). Unlike adults, children and adolescents show predominantly increased neural activation to social exclusion by members of the opposite gender. Social Neuroscience, 11(5), 475–486. https://doi.org/10.1080/17470919.2015.1117019
Bolling, D. Z., Pitskel, N. B., Deen, B., Crowley, M. J., Mayes, L. C., & Pelphrey, K. A. (2011). Development of neural systems for processing social exclusion from childhood to adolescence. Developmental Science, 14(6), 1431–1444. https://doi.org/10.1111/j.1467-7687.2011.01087.x
Bolling, D. Z., Pitskel, N. B., Deen, B., Crowley, M. J., McPartland, J. C., Mayes, L. C., & Pelphrey, K. A. (2011a). Dissociable brain mechanisms for processing social exclusion and rule violation. NeuroImage, 54(3), 2462–2471. https://doi.org/10.1016/j.neuroimage.2010.10.049
Brunet, E., Sarfati, Y., Hardy-Baylé, M-C., & Decety, J. (2000). A PET investigation of the attribution of intentions with a nonverbal task. NeuroImage, 11(2), 157–166.
Bush, G., Luu, P., & Posner, M. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences, 4(6), 215–222. https://doi.org/10.1016/S1364-6613(00)01483-2
Cacioppo, S., Frum, C., Asp, E., Weiss, R. M., Lewis, J. W., & Cacioppo, J. T. (2013). A Quantitative Meta-Analysis of Rejection. Nature Scientific Reports, 10–12. https://doi.org/10.1038/srep02027
Cosme, D., Flournoy, J. C., & Vijayakumar, N. (2018). auto-motion-fmriprep: A tool for automated assessment of motion artifacts. https://doi.org/10.5281/zenodo.1412131
Craddock, R. C., James, G. A., Holtzheimer, P. E., Hu, X. P., & Mayberg, H. S. (2012). A whole brain fMRI atlas generated via spatially constrained spectral clustering. Human Brain Mapping, 33(8), 1914–1928.
Csikszentmihalyi, M., & Larson, R. (1984). Being Adolescent: Conflict and Growth in the Teenage Years. New York: Basic Books.
de Water, E., Mies, G. W., Ma, I., Mennes, M., Cillessen, A. H. N., & Scheres, A. (2017). Neural responses to social exclusion in adolescents: Effects of peer status. Cortex, 92, 32–43. https://doi.org/10.1016/j.cortex.2017.02.018
Dalgleish, T., Walsh, N. D., Mobbs, D., Schweizer, S., Harmelen, A.-L. van, Dunn, B., … Stretton, J. (2017). Social pain and social gain in the adolescent brain: A common neural circuitry underlying both positive and negative social evaluation. Scientific Reports, 7, 42010. https://doi.org/10.1038/srep42010
Eisenberger, N. I. (2012). Broken Hearts and Broken Bones A Neural Perspective on the Similarities Between Social and Physical Pain. Current Directions in Psychological Science, 21(1), 42–47. https://doi.org/10.1177/0963721411429455
Eisenberger, N. I. (2015). Social pain and the brain: Controversies, Questions, and Where to Go from Here. Annual Review of Psychology, 66(1), 601–629.
Eisenberger, N. I., Jarcho, J. M., Lieberman, M. D., & Naliboff, B. D. (2006). An experimental study of shared sensitivity to physical pain and social rejection. Pain, 126(1), 132–138. https://doi.org/10.1016/j.pain.2006.06.024
Eisenberger, N. I., Lieberman, M. D., & Williams, K. D. (2003). Does rejection hurt? An FMRI study of social exclusion. Science (New York, N.Y.), 302(5643), 290–292. https://doi.org/10.1126/science.1089134
Eklund, A., Nichols, T. E., & Knutsson, H. (2016). Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences, 113(28), 7900–7905. https://doi.org/10.1073/pnas.1602413113
Falk, E. B., Cascio, C. N., Brook O’Donnell, M., Carp, J., Tinney, F. J., Bingham, C. R., … Simons-Morton, B. G. (2014). Neural Responses to Exclusion Predict Susceptibility to Social Influence. Journal of Adolescent Health, 54(5), S22–S31. https://doi.org/10.1016/j.jadohealth.2013.12.035
Gardner, M., & Steinberg, L. (2005). Peer Influence on Risk Taking, Risk Preference, and Risky Decision Making in Adolescence and Adulthood: An Experimental Study. Developmental Psychology, 41(4), 625–635. https://doi.org/10.1037/0012-16188.8.131.525
Gerber, J. P., Chang, S.-H., & Reimel, H. (2017). Construct validity of Williams’ ostracism needs threat scale. Personality and Individual Differences, 115, 50–53. https://doi.org/10.1016/j.paid.2016.07.008
Gunther Moor, B., Leijenhorst, L. van, Rombouts, S. A. R. B., Crone, E. A., & Molen, M. W. V. der. (2010). Do you like me? Neural correlates of social evaluation and developmental trajectories. Social Neuroscience, 5(5–6), 461–482. https://doi.org/10.1080/17470910903526155
Gunther Moor B, Güroğlu B, Op de Macks ZA, Rombouts SARB, Van der Molen MW, Crone EA (2012) Social exclusion and punishment of excluders: Neural correlates and developmental trajectories. NeuroImage 59:708–717.
Jenkins, A. C., Macrae, C. N., & Mitchell, J. P. (2008). Repetition suppression of ventromedial prefrontal activity during judgments of self and others. Proceedings of the National Academy of Sciences of the United States of America, 105(11), 4507–4512. https://doi.org/10.1073/pnas.0708785105
Jensen, J., McIntosh, A. R., Crawley, A. P., Mikulis, D. J., Remington, G., & Kapur, S. (2003). Direct activation of the ventral striatum in anticipation of aversive stimuli. Neuron, 40(6), 1251–1257.
Kawamoto, T., Onoda, K., Nakashima, K., Nittono, H., Yamaguchi, S., & Ura, M. (2012). Is dorsal anterior cingulate cortex activation in response to social exclusion due to expectancy violation ? An fMRI study. Frontiers in Evolutionary Neuroscience, 4(July), 1–10. https://doi.org/10.3389/fnevo.2012.00011
Knutson, B., Westdorp, A., Kaiser, E., & Hommer, D. (2000). FMRI visualization of brain activity during a monetary incentive delay task. NeuroImage, 12(1), 20–27. https://doi.org/10.1006/nimg.2000.0593
Kragel, P. A., Kano, M., Oudenhove, L. V., Ly, H. G., Dupont, P., Rubio, A., … Wager, T. D. (2018). Generalizable representations of pain, cognitive control, and negative emotion in medial frontal cortex. Nature Neuroscience, 21(2), 283–289. https://doi.org/10.1038/s41593-017-0051-7
Lau, T., & Cikara, M. (2017). FMRI Repetition Suppression During Generalized Social Categorization. Scientific Reports, 7(1), 4262. https://doi.org/10.1038/s41598-017-04115-8
Levita, L., Hare, T. A., Voss, H. U., Glover, G., Ballon, D. J., & Casey, B. J. (2009). The bivalent side of the nucleus accumbens. NeuroImage, 44(3), 1178–1187. https://doi.org/10.1016/j.neuroimage.2008.09.039
Lieberman, M. D., & Eisenberger, N. I. (2015). The dorsal anterior cingulate cortex is selective for pain: Results from large-scale reverse inference. Proceedings of the National Academy of Sciences, 112(49), 15250–15255.
Lindquist, K. A., Satpute, A. B., Wager, T. D., Weber, J., & Feldman Barrett, L. (2016). The brain basis of positive and negative affect: Evidence from a meta-analysis of the human neuroimaging literature. Cerebral Cortex.
Masten, C. L., Eisenberger, N. I., Borofsky, L. A., Pfeifer, J. H., McNealy, K., Mazziotta, J. C., & Dapretto, M. (2009). Neural correlates of social exclusion during adolescence: understanding the distress of peer rejection. Social Cognitive and Affective Neuroscience, 4(2), 143–157. https://doi.org/10.1093/scan/nsp007
Modinos, G., Ormel, J., & Aleman, A. (2009). Activation of Anterior Insula during Self-Reflection. PLoS ONE, 4(2), 1–8. https://doi.org/10.1371/journal.pone.0004618
Morelli, S. A., & Lieberman, M. D. (2013). The role of automaticity and attention in neural processes underlying empathy for happiness, sadness, and anxiety. Frontiers in Human Neuroscience, 7. https://doi.org/10.3389/fnhum.2013.00160
Op de Macks, Z. A., Flannery, J. E., Peake, S. J., Flournoy, J. C., Mobasser, A., Alberti, S. L., … Pfeifer, J. H. (2018). Novel insights from the Yellow Light Game: Safe and risky decisions differentially impact adolescent outcome-related brain function. NeuroImage, 181, 568–581. https://doi.org/10.1016/j.neuroimage.2018.06.058
Peake, S. J., Dishion, T. J., Stormshak, E. A., Moore, W. E., & Pfeifer, J. H. (2013). Risk-taking and social exclusion in adolescence: neural mechanisms underlying peer influences on decision-making. NeuroImage, 82, 23–34. https://doi.org/10.1016/j.neuroimage.2013.05.061
Petrides, M. (2016). The ventrolateral frontal region. In Neurobiology of Language (pp. 25–33). https://doi.org/10.1016/B978-0-12-407794-2.00003-1
Pfeifer, J. H., Masten, C. L., Moore, W. E., Oswald, T. M., Mazziotta, J. C., Iacoboni, M., & Dapretto, M. (2011). Entering Adolescence: Resistance to Peer Influence, Risky Behavior, and Neural Changes in Emotion Reactivity. Neuron, 69(5), 1029–1036. https://doi.org/10.1016/j.neuron.2011.02.019
Rodman, A. M., Powers, K. E., & Somerville, L. H. (2017). Development of self-protective biases in response to social evaluative feedback. Proceedings of the National Academy of Sciences, 114(50), 13158–13163. https://doi.org/10.1073/pnas.1712398114
Rotge, J.-Y., Lemogne, C., Hinfray, S., Huguet, P., Grynszpan, O., Tartour, E., … Fossati, P. (2015). A meta-analysis of the anterior cingulate contribution to social pain. Social Cognitive and Affective Neuroscience, 10(1), 19–27. https://doi.org/10.1093/scan/nsu110
Sebastian, C. L., Tan, G. C. Y., Roiser, J. P., Viding, E., Dumontheil, I., & Blakemore, S.-J. (2011). Developmental influences on the neural bases of responses to social rejection: Implications of social neuroscience for education. NeuroImage, 57(3), 686–694. https://doi.org/10.1016/j.neuroimage.2010.09.063
Sebastian, C., Viding, E., Williams, K. D., & Blakemore, S.-J. (2010). Social brain development and the affective consequences of ostracism in adolescence. Brain and Cognition, 72(1), 134–145. https://doi.org/10.1016/j.bandc.2009.06.008
Sescousse, G., Caldú, X., Segura, B., & Dreher, J.-C. (2013). Processing of primary and secondary rewards: A quantitative meta-analysis and review of human functional neuroimaging studies. Neuroscience & Biobehavioral Reviews, 37(4), 681–696. https://doi.org/10.1016/j.neubiorev.2013.02.002
Silverman, M. H., Jedd, K., & Luciana, M. (2015). Neural Networks Involved in Adolescent Reward Processing: An Activation Likelihood Estimation Meta-Analysis of Functional Neuroimaging Studies. NeuroImage, 122, 427–439. https://doi.org/10.1016/j.neuroimage.2015.07.083
Smith, J. (2011). MRIConvert. Eugene, OR: The Lewis Center for Neuroimaging, University of Oregon.
Somerville, L. H. (2013). The Teenage Brain: Sensitivity to Social Evaluation. Current Directions in Psychological Science, 22, 121–127. https://doi.org/10.1177/0963721413476512
Somerville, Leah H., Heatherton, T. F., & Kelley, W. M. (2006). Anterior cingulate cortex responds differentially to expectancy violation and social rejection. Nature Neuroscience, 9(8), 1007–1008. https://doi.org/10.1038/nn1728
Spitzer, M., Fischbacher, U., Herrnberger, B., Grön, G., & Fehr, E. (2007). The Neural Signature of Social Norm Compliance. Neuron, 56(1), 185–196. https://doi.org/10.1016/j.neuron.2007.09.011
Vijayakumar, N., Cheng, T. W., & Pfeifer, J. H. (2017). Neural correlates of social exclusion across ages: A coordinate-based meta-analysis of functional MRI studies. NeuroImage, 153, 359–368. https://doi.org/10.1016/j.neuroimage.2017.02.050
Wager, T. D., Davidson, M. L., Hughes, B. L., Lindquist, M. A., & Ochsner, K. N. (2008). Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron, 59(6), 1037–1050.
Wechsler, D. (1999). Wechsler Abbreviated Scale of Intelligence. San Antonio, TX: The Psychological Corporation.
White, L. O., Wu, J., Borelli, J. L., Mayes, L. C., & Crowley, M. J. (2013). Play it again: neural responses to reunion with excluders predicted by attachment patterns. Developmental Science, n/a-n/a. https://doi.org/10.1111/desc.12035
Will G-J, van Lier PAC, Crone EA, Güroğlu B (2016) Chronic Childhood Peer Rejection is Associated with Heightened Neural Responses to Social Exclusion During Adolescence. J Abnorm Child Psychol 44:43–55.
Williams, K. D., Cheung, C. K., & Choi, W. (2000). Cyberostracism: effects of being ignored over the Internet. Journal of Personality and Social Psychology, 79(5), 748–762.
Woo, C.-W., Koban, L., Kross, E., Lindquist, M. A., Banich, M. T., Ruzic, L., … Wager, T. D. (2014). Separate neural representations for physical pain and social rejection. Nature Communications, 5, 5380. https://doi.org/10.1038/ncomms6380
Zadro, L., Williams, K. D., & Richardson, R. (2004). How low can you go? Ostracism by a computer is sufficient to lower self-reported levels of belonging, control, self-esteem, and meaningful existence. Journal of Experimental Social Psychology, 40(4), 560–567. https://doi.org/10.1016/j.jesp.2003.11.006
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.
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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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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
- Social exclusion
- Functional MRI
- Anterior cingulate cortex
- Anterior insula