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Contextual exclusion processing: an fMRI study of rejection in a performance-related context

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Abstract

Social stress has a major detrimental impact on subjective well-being. Previous research mainly focused on two methods to induce and measure social stress: social exclusion and performance evaluation. For social exclusion researchers frequently focused on the Cyberball task, which in contrast to many psychosocial stress paradigms does not include a performance component. The aim of the current study was to establish an optimized psychosocial stress paradigm by combining both, social exclusion as well as performance evaluation within a single fMRI paradigm. We implemented a modification of the Cyberball task including a performance game (with exclusion and inclusion periods) in addition to the already established exclusion and inclusion periods. This indeed resulted in increased subjective stress in the performance game. Hence, the modified Cyberball version seems to be superior in mapping relevant neural social stress correlates more pronounced and reliably. Exclusion within the performance-related context contrasted to the unmodified exclusion was associated with higher activation in the dorsal anterior cingulate cortex and the anterior insula. Moreover, the modified exclusion reflected greater social processing in the precuneus, several temporo-parietal and medial prefrontal areas, as suggested by the additional task aspects of social evaluation and social perspective taking. The findings emphasize that public negative evaluation is effective in substantially enlarging and potentiating the distressing effect of exclusion on a subjective as well as on a neural level. This may have a great potential for further experimental research on social stress.

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References

  • Bass, E. C., Stednitz, S. J., Simonson, K., Shen, T., & Gahtan, E. (2014). Physiological stress reactivity and empathy following social exclusion: a test of the defensive emotional analgesia hypothesis. Social Neuroscience, 9(5), 504–513. doi:10.1080/17470919.2014.929533.

    Article  PubMed  Google Scholar 

  • Bastian, B., & Haslam, N. (2010). Excluded from humanity: the dehumanizing effects of social ostracism. Journal of Experimental Social Psychology, 46(1), 107–113. doi:10.1016/j.jesp.2009.06.022.

    Article  Google Scholar 

  • Baumeister, R. F., DeWall, C. N., Ciarocco, N. J., & Twenge, J. M. (2005). Social exclusion impairs self-regulation. Journal of Personality and Social Psychology, 88(4), 589–604.

    Article  PubMed  Google Scholar 

  • Beekman, J. B., Stock, M. L., & Marcus, T. (2015). Need to belong, not rejection sensitivity, moderates cortisol response, self-reported stress, and negative affect following social exclusion. The Journal of Social Psychology, 156(2), 131–138. doi:10.1080/00224545.2015.1071767.

    Article  PubMed  Google Scholar 

  • Bernstein, M. J., & Claypool, H. M. (2012). Not all social exclusions are created equal: emotional distress following social exclusion is moderated by exclusion paradigm. Social Influence, 7(2), 113–130. doi:10.1080/15534510.2012.664326.

    Article  Google Scholar 

  • Blackhart, G. C., Eckel, L. a., & Tice, D. M. (2007). Salivary cortisol in response to acute social rejection and acceptance by peers. Biological Psychology, 75(3), 267–276. doi:10.1016/j.biopsycho.2007.03.005.

    Article  PubMed  Google Scholar 

  • Blackhart, G. C., Nelson, B. C., Knowles, M. L., & Baumeister, R. F. (2009). Rejection elicits emotional reactions but neither causes immediate distress nor lowers self-esteem: a meta-analytic review of 192 studies on social exclusion. Personality and Social Psychology Review, 13(4), 269–309. doi:10.1177/1088868309346065.

    Article  PubMed  Google Scholar 

  • Bolling, D. Z., Pitskel, N. B., Deen, B., Crowley, M. J., McPartland, J. C., Mayes, L. C., et al. (2011). Dissociable brain mechanisms for processing social exclusion and rule violation. NeuroImage, 54(3), 2462–2471. doi:10.1016/j.neuroimage.2010.10.049.

    Article  PubMed  Google Scholar 

  • Cacioppo, S., Frum, C., Asp, E., Weiss, R. M., Lewis, J. W., & Cacioppo, J. T. (2013). A quantitative meta-analysis of functional imaging studies of social rejection. Scientific Reports, 3, 2027. doi:10.1038/srep02027.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chiong, W., Wilson, S. M., D’Esposito, M., Kayser, A. S., Grossman, S. N., Poorzand, P., et al. (2013). The salience network causally influences default mode network activity during moral reasoning. Brain, 136(6), 1929–1941. doi:10.1093/brain/awt066.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chow, R. M., Tiedens, L. Z., & Govan, C. L. (2008). Excluded emotions: the role of anger in antisocial responses to ostracism. Journal of Experimental Social Psychology, 44(3), 896–903. doi:10.1016/j.jesp.2007.09.004.

    Article  Google Scholar 

  • Dedovic, K., Renwick, R., Mahani, N. K., Engert, V., Lupien, S. J., & Pruessner, J. C. (2005). The Montreal imaging stress task: using functional imaging to investigate the effects of perceiving and processing psychosocial stress in the human brain. Journal of Psychiatry & Neuroscience: JPN, 30(5), 319–325.

    Google Scholar 

  • Dedovic, K., Duchesne, A., Engert, V., Lue, S. D., Andrews, J., Efanov, S. I., et al. (2014). Psychological, endocrine and neural responses to social evaluation in subclinical depression. Social Cognitive and Affective Neuroscience, 9(10), 1632–1644. doi:10.1093/scan/nst151.

    Article  PubMed  Google Scholar 

  • DeWall, C. N., Masten, C. L., Powell, C., Combs, D., Schurtz, D. R., & Eisenberger, N. I. (2012). Do neural responses to rejection depend on attachment style? An fMRI study. Social Cognitive and Affective Neuroscience, 7(2), 184–192. doi:10.1093/scan/nsq107.

    Article  PubMed  Google Scholar 

  • Dickerson, S. S., & Kemeny, M. E. (2004). Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130(3), 355–91. doi:10.1037/0033-2909.130.3.355.

  • Eisenberger, N. I., & Lieberman, M. D. (2004). Why rejection hurts: a common neural alarm system for physical and social pain. Trends in Cognitive Sciences, 8(7), 294–300. doi:10.1016/j.tics.2004.05.010.

    Article  PubMed  Google Scholar 

  • 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. doi:10.1126/science.1089134.

    Article  CAS  Google Scholar 

  • Ford, M. B., & Collins, N. L. (2010). Self-esteem moderates neuroendocrine and psychological responses to interpersonal rejection. Journal of Personality and Social Psychology, 98(3), 405–419.

    Article  PubMed  Google Scholar 

  • Goldin, P. R., McRae, K., Ramel, W., & Gross, J. J. (2008). The neural bases of emotion regulation: reappraisal and suppression of negative emotion. Biological Psychiatry, 63(6), 577–586. doi:10.1016/j.biopsych.2007.05.031.

    Article  PubMed  Google Scholar 

  • Goodwin, S. A., Williams, K. D., & Carter-Sowell, A. R. (2010). The psychological sting of stigma: the costs of attributing ostracism to racism. Journal of Experimental Social Psychology, 46(4), 612–618. doi:10.1016/j.jesp.2010.02.002.

    Article  Google Scholar 

  • Gradin, V. B., Waiter, G., Kumar, P., Stickle, C., Milders, M., Matthews, K., et al. (2012). Abnormal neural responses to social exclusion in schizophrenia. PloS One, 7(8), e42608. doi:10.1371/journal.pone.0042608.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gruenewald, T. L., Dickerson, S. S., & Kemeny, M. E. (2007). A social function for self-conscious emotions: The social self preservation theory. New York.

  • Hartgerink, C. H. J., van Beest, I., Wicherts, J. M., & Williams, K. D. (2015). The ordinal effects of ostracism: a meta-analysis of 120 Cyberball studies. PloS One, 10(5), e0127002. doi:10.1371/journal.pone.0127002.

    Article  PubMed  PubMed Central  Google Scholar 

  • Karremans, J. C., Heslenfeld, D. J., van Dillen, L. F., & Van Lange, P. A. M. (2011). Secure attachment partners attenuate neural responses to social exclusion: an fMRI investigation. International Journal of Psychophysiology: Official Journal of the International Organization of Psychophysiology, 81(1), 44–50. doi:10.1016/j.ijpsycho.2011.04.003.

    Article  Google Scholar 

  • 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), 11. doi:10.3389/fnevo.2012.00011.

    PubMed  PubMed Central  Google Scholar 

  • Kawamoto, T., Ura, M., & Nittono, H. (2015). Intrapersonal and interpersonal processes of social exclusion. Frontiers in Neuroscience, 9, 62. doi:10.3389/fnins.2015.00062.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kirschbaum, C., Pirke, K.-M., & Hellhammer, D. H. (1993). The’Trier social Sress Test' - a tool for investigating psychobiological stress responses in a laboratory setting. Neurobiology, 28, 76–81.

    CAS  Google Scholar 

  • Kogler, L., Mueller, V. I., Chang, A., Eickhoff, S. B., Fox, P. T., Gur, R. C., et al. (2015). Psychosocial versus physiological stress – meta-analyses on deactivations and activations of the neural correlates of stress reactions. NeuroImage, 119, 235–251. doi:10.1016/j.neuroimage.2015.06.059.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kohn, N., Eickhoff, S. B., Scheller, M., Laird, A. R., Fox, P. T., & Habel, U. (2014). Neural network of cognitive emotion regulation - an ALE meta-analysis and MACM analysis. NeuroImage, 87, 345–355. doi:10.1016/j.neuroimage.2013.11.001.

    Article  CAS  PubMed  Google Scholar 

  • Kross, E., Berman, M. G., Mischel, W., Smith, E. E., & Wager, T. D. (2011). Social rejection shares somatosensory representations with physical pain. Proceedings of the National Academy of Sciences of the United States of America, 108(15), 6270–6275. doi:10.1073/pnas.1102693108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehrl, S., Triebig, G., & Fischer, B. (1995). Multiple choice vocabulary test MWT as a valid and short test to estimate premorbid intelligence. Acta Neurologica Scandinavica, 91(5), 335–345. doi:10.1111/j.1600-0404.1995.tb07018.x.

    Article  CAS  PubMed  Google Scholar 

  • Masten, C. L., Eisenberger, N. I., Borofsky, L. a., Pfeifer, J. H., McNealy, K., Mazziotta, J. C., et al. (2009). Neural correlates of social exclusion during adolescence: understanding the distress of peer rejection. Social Cognitive and Affective Neuroscience, 4(2), 143–157. doi:10.1093/scan/nsp007.

    Article  PubMed  PubMed Central  Google Scholar 

  • Masten, C. L., Morelli, S. A., & Eisenberger, N. I. (2011a). An fMRI investigation of empathy for “social pain” and subsequent prosocial behavior. NeuroImage, 55(1), 381–388. doi:10.1016/j.neuroimage.2010.11.060.

    Article  PubMed  Google Scholar 

  • Masten, C. L., Telzer, E. H., & Eisenberger, N. I. (2011b). An FMRI investigation of attributing negative social treatment to racial discrimination. Journal of Cognitive Neuroscience, 23(5), 1042–1051. doi:10.1162/jocn.2010.21520.

    Article  PubMed  Google Scholar 

  • Moor, B. G., Güroğlu, B., Op de Macks, Z. A., Rombouts, S. a R. B., Van der Molen, M. W., & Crone, E. A. (2012). Social exclusion and punishment of excluders: neural correlates and developmental trajectories. NeuroImage, 59(1), 708–717. doi:10.1016/j.neuroimage.2011.07.028.

  • Nepon, T., Flett, G. L., Hewitt, P. L., & Molnar, D. S. (2011). Perfectionism, negative social feedback, and interpersonal rumination in depression and social anxiety. Canadian Journal of Behavioural Science, 43(4), 297–308.

    Article  Google Scholar 

  • Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9(1), 97–113. doi:10.1016/0028-3932(71)90067-4.

    Article  CAS  PubMed  Google Scholar 

  • Onoda, K., Okamoto, Y., Nakashima, K., Nittono, H., Ura, M., & Yamawaki, S. (2009). Decreased ventral anterior cingulate cortex activity is associated with reduced social pain during emotional support. Social Neuroscience, 4(5), 443–454. doi:10.1080/17470910902955884.

    Article  PubMed  Google Scholar 

  • Reitan, R. M. (1956). Trail making test. Manual for administration, scoring, and interpretation. Indianapolis: Indiana University Press.

    Google Scholar 

  • Rotge, J.-Y., Lemogne, C., Hinfray, S., Huguet, P., Grynszpan, O., Tartour, E., et al. (2014). A meta-analysis of the anterior cingulate contribution to social pain. Social Cognitive and Affective Neuroscience, 10(1), 19–27. doi:10.1093/scan/nsu110.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schurz, M., Radua, J., Aichhorn, M., Richlan, F., & Perner, J. (2014). Fractionating theory of mind: a meta-analysis of functional brain imaging studies. Neuroscience and Biobehavioral Reviews, 42, 9–34. doi:10.1016/j.neubiorev.2014.01.009.

    Article  PubMed  Google Scholar 

  • 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. doi:10.1016/j.neuroimage.2010.09.063.

    Article  PubMed  Google Scholar 

  • Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., et al. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 27(9), 2349–2356. doi:10.1523/JNEUROSCI.5587-06.2007.

    Article  CAS  Google Scholar 

  • Seidel, E. M., Silani, G., Metzler, H., Thaler, H., Lamm, C., Gur, R. C., et al. (2013). The impact of social exclusion vs. inclusion on subjective and hormonal reactions in females and males. Psychoneuroendocrinology, 38(12), 2925–2932. doi:10.1016/j.psyneuen.2013.07.021.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith, A., & Williams, K. D. (2004). R U there? Ostracism by cell phone text messages. Group Dynamics: Theory, Research, and Practice, 8(4), 291–301.

    Article  Google Scholar 

  • Somerville, L. 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. doi:10.1038/nn1728.

  • Stroud, L. R., Salovey, P., & Epel, E. S. (2002). Sex differences in stress responses: social rejection versus achievement stress. Biological Psychiatry, 52(4), 318–327. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/12208639

  • Taylor, K. S., Seminowicz, D. A., & Davis, K. D. (2009). Two systems of resting state connectivity between the insula and cingulate cortex. Human Brain Mapping, 30(9), 2731–2745. doi:10.1002/hbm.20705.

    Article  PubMed  Google Scholar 

  • Tossani, E. (2013). The concept of mental pain. Psychotherapy and Psychosomatics, 82(2), 67–73 http://doi.org/10.1159/000343003.

    Article  PubMed  Google Scholar 

  • Vogt, B. A. (2005). Pain and emotion interactions in subregions of the cingulate gyrus. Nature Reviews. Neuroscience, 6(7), 533–544. doi:10.1038/nrn1704.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Von Aster, M., Neubauer, A. C., & Horn, R. (2006). Hamburg-Wechsler-Intelligenz-test für Erwachsene III. Frankfurt.

  • Will, G.-J., van Lier, P. A. C., Crone, E. A., & Güroğlu, B. (2016). Chronic childhood peer rejection is associated with heightened neural responses to social exclusion during adolescence. Journal of Abnormal Child Psychology, 44(1), 43–55. doi:10.1007/s10802-015-9983-0.

    Article  PubMed  Google Scholar 

  • Williams, K. D. (2007a). Ostracism. Annual Review of Psychology, 58, 425–452. doi:10.1146/annurev.psych.58.110405.085641.

    Article  PubMed  Google Scholar 

  • Williams, K. D. (2007b). Ostracism: the kiss of social death. Social and Personality Psychology Compass, 1(1), 236–247. doi:10.1111/j.1751-9004.2007.00004.x.

    Article  Google Scholar 

  • Williams, K. D., & Nida, S. A. (2011). Ostracism: consequences and coping. Current Directions in Psychological Science, 20(2), 71–75. doi:10.1177/0963721411402480.

    Article  Google Scholar 

  • Williams, K. D., Cheung, C. K. T., & Choi, W. (2000). Cyberostracism: effects of being ignored over the internet. Journal of Personality and Social Psychology, 79(5), 748–762. doi:10.1037//0022-3514.79.5.748.

    Article  CAS  PubMed  Google Scholar 

  • Wirth, J. H., & Williams, K. D. (2009). `They Don’t like our kind': consequences of being ostracized while possessing a group membership. Group Processes & Intergroup Relations, 12(1), 111–127. doi:10.1177/1368430208098780.

    Article  Google Scholar 

  • Wudarczyk, O. A., Kohn, N., Bergs, R., Gur, R. E., Turetsky, B., Schneider, F., et al. (2015). Chemosensory anxiety cues moderate the experience of social exclusion - an fMRI investigation with Cyberball. Frontiers in Psychology, 6, 1475. doi:10.3389/fpsyg.2015.01475.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 http://doi.org/10.1016/j.jesp.2003.11.006.

    Article  Google Scholar 

  • Zöller, C., Maroof, P., Weik, U., & Deinzer, R. (2010). No effect of social exclusion on salivary cortisol secretion in women in a randomized controlled study. Psychoneuroendocrinology, 35(9), 1294–1298. doi:10.1016/j.psyneuen.2010.02.019.

    Article  PubMed  Google Scholar 

  • Zwolinski, J. (2012). Psychological and neuroendocrine reactivity to ostracism. Aggressive Behavior, 38(2), 108–125. doi:10.1002/ab.21411.

    CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the State of North Rhine-Westphalia (NRW, Germany), the European Union through the ‘NRW Ziel2 Program’ as a part of the European Fund for Regional Development and by the German Research Foundation (DFG, IRTG 1328). The authors thank Andre Schueppen, from the Brain Imaging Facility of the Interdisciplinary Centre for Clinical Research at the RWTH Aachen University and the radiographers Cordula Kemper and Maria Peters, for their assistance with data acquisition. Furthermore, the authors thank Monica Bell and Katharina Görlich for their assistance in editing the manuscript.

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Fig. 3 Significant clusters for the contrast of exclusion > inclusion (Ex > IN) are indicated in red (left part) and significant clusters for the contrast of performance context > free game context (PG > FG) are indicated in yellow (right part). A voxel level threshold of p < .05 FWE corrected was used for all clusters. (GIF 38 kb)

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Wagels, L., Bergs, R., Clemens, B. et al. Contextual exclusion processing: an fMRI study of rejection in a performance-related context. Brain Imaging and Behavior 11, 874–886 (2017). https://doi.org/10.1007/s11682-016-9561-2

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