Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-10T06:11:10.084Z Has data issue: false hasContentIssue false
  • English
  • Français

Neural substrates of expectancy violation associated with social feedback in individuals with subthreshold depression

Published online by Cambridge University Press:  28 October 2020

Zhenhong He ,
Xiang Ao ,
Nils Muhlert ,
Rebecca Elliott  and
Dandan Zhang
Zhenhong He
Affiliation:
Division of Neuroscience and Experimental Psychology, School of Biological Science, University of Manchester, Manchester, M13 9PL, UK School of Psychology, Shenzhen University, Shenzhen, 518060, China
Xiang Ao
Affiliation:
School of Psychology, Shenzhen University, Shenzhen, 518060, China
Nils Muhlert
Affiliation:
Division of Neuroscience and Experimental Psychology, School of Biological Science, University of Manchester, Manchester, M13 9PL, UK
Rebecca Elliott
Affiliation:
Division of Neuroscience and Experimental Psychology, School of Biological Science, University of Manchester, Manchester, M13 9PL, UK
Dandan Zhang*
Affiliation:
School of Psychology, Shenzhen University, Shenzhen, 518060, China Shenzhen Institute of Neuroscience, Shenzhen 518060, China
*
Author for correspondence: Dandan Zhang, E-mail: zhangdd05@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Abnormal processing of social feedback is an important contributor to social dysfunction in depression, however the exact mechanisms remain unclear. One important factor may be the extent to which social processing depends on expectations, in particular whether social feedback confirms or violates expectations.

Methods

To answer this question, we studied behavioral and brain responses during the evaluative processing of social feedback in 25 individuals with subthreshold depression (SD) and 25 healthy controls (HCs). Participants completed a Social Judgment Task in which they first indicated expectation about whether a peer would like them or not, and then received peer's feedback indicating acceptance or rejection.

Results

Individuals with SD who reported greater depressive symptoms gave fewer positive expectations. Compared to HCs, individuals with SD showed reduced activation in the medial prefrontal cortex when expecting positive feedback. They also exhibited increased dorsal anterior cingulate cortex after receipt of unexpected social rejection, and reduced ventral striatum activity after receipt of unexpected social acceptance.

Conclusions

The observed alternations are specific to unexpected social feedback processing and highlight an important role of expectancy violation in the brain dysfunction of social feedback perception and evaluation in individuals at risk for depression.

Keywords

Depressiondorsal anterior cingulate cortexexpectancy violationmedial prefrontal cortexsocial feedbackventral striatum
Type
Original Article
Information
Psychological Medicine , Volume 52 , Issue 11 , August 2022 , pp. 2043 - 2051
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amodio, D. M., & Frith, C. D. (2006). Meeting of minds: The medial frontal cortex and social cognition. Nature Reviews Neuroscience, 7(4), 268–277.CrossRefGoogle ScholarPubMed
Atzil, S., Gao, W., Fradkin, I., & Barrett, L. F. (2018). Growing a social brain. Nature Human Behaviour, 2(9), 624–636.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Beck, A. T., Steer, R. A., & Brown, G. K. (1996). Beck depression inventory-second edition manual. San Antonio, TX: The Psychological Corporation.Google Scholar
Behrens, TE, Hunt, LT, & Rushworth, MF. (2009). The computation of social behavior. Science, 324(5931), 1160–1164.CrossRefGoogle ScholarPubMed
Bora, E., & Berk, M. (2016). Theory of mind in major depressive disorder: A meta-analysis. Journal of Affective Disorders, 191, 49–55.CrossRefGoogle ScholarPubMed
Cusi, A. M., Nazarov, A., Holshausen, K., Macqueen, G. M., & McKinnon, M. C. (2012). Systematic review of the neural basis of social cognition in patients with mood disorders. Journal of Psychiatry & Neuroscience, 37(3), 154–169.CrossRefGoogle ScholarPubMed
Dekkers, L. M., van der Molen, M. J., Gunther, M. B., van der Veen, F. M., & van der Molen, M. W. (2015). Cardiac and electro-cortical concomitants of social feedback processing in women. Social Cognitive and Affective Neuroscience, 10(11), 1506–1514.CrossRefGoogle ScholarPubMed
Dombrovski, A. Y., Szanto, K., Clark, L., Reynolds, C. F., & Siegle, G. J. (2013). Reward signals, attempted suicide, and impulsivity in late-life depression. JAMA Psychiatry, 70(10), 1.CrossRefGoogle ScholarPubMed
Dreher, J. C., Schmidt, P. J., Kohn, P., Furman, D., Rubinow, D., & Berman, K. F. (2007). Menstrual cycle phase modulates reward-related neural function in women. Proceedings of the National Academy of Sciences of the United States of America, 104(7), 2465–2470.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
First, M. B., Gibbon, M., Spitzer, R. L., & Williams, J. B. (2002). Structured clinical interview for DSM-IV-TR axis I disorders, research version, Non-patient edition (SCID-I/NP). New York: Biometrics Research Department. New York State Psychiatric Institute.Google Scholar
Frey, A. L., & McCabe, C. (2020). Impaired social learning predicts reduced real-life motivation in individuals with depression: A computational fMRI study. Journal of Affective Disorders, 263, 698–706.CrossRefGoogle ScholarPubMed
Gotlib, I. H., Hamilton, J. P., Cooney, R. E., Singh, M. K., Henry, M. L., & Joormann, J. (2010). Neural processing of reward and loss in girls at risk for major depression. Archives of General Psychiatry, 67(4), 380–387.CrossRefGoogle ScholarPubMed
Gradin, V. B., Kumar, P., Waiter, G., Ahearn, T., Stickle, C., Milders, M., … Steele, J. D. (2011). Expected value and prediction error abnormalities in depression and schizophrenia. Brain, 134(Pt 6), 1751–1764.CrossRefGoogle ScholarPubMed
Gunther, M. B., Crone, E. A., & van der Molen, M. W. (2010). The heartbrake of social rejection: Heart rate deceleration in response to unexpected peer rejection. Psychological Science, 21(9), 1326–1333.CrossRefGoogle Scholar
Gunther Moor, B., van Leijenhorst, L., Rombouts, S. A., Crone, E. A., & Van der Molen, M. W. (2010). Do you like me? Neural correlates of social evaluation and developmental trajectories. Social Neuroscience, 5–6(5), 461–482.CrossRefGoogle Scholar
Hames, J. L., Hagan, C. R., & Joiner, T. E. (2013). Interpersonal processes in depression. Annual Review of Clinical Psychology, 9, 355–377.CrossRefGoogle ScholarPubMed
Hammen, C. (2005). Stress and depression. Annual Review of Clinical Psychology, 1, 293–319.CrossRefGoogle ScholarPubMed
Hasin, D. S., Sarvet, A. L., Meyers, J. L., Saha, T. D., Ruan, W. J., & Stohl, M. (2018). Epidemiology of adult DSM-5 major depressive disorder and its specifiers in the United States. JAMA Psychiatry, 75(4), 336–346.CrossRefGoogle ScholarPubMed
He, Z., Zhang, D., Muhlert, N., & Elliott, R. (2019). Neural substrates for anticipation and consumption of social and monetary incentives in depression. Social Cognitive and Affective Neuroscience, 14(8), 815–826.CrossRefGoogle ScholarPubMed
Hirschfeld, R. M., Montgomery, S. A., Keller, M. B., Kasper, S., Schatzberg, A. F., Moller, H. J., … Bourgeois, M. (2000). Social functioning in depression: A review. Journal of Clinical Psychiatry, 61(4), 268–275.CrossRefGoogle ScholarPubMed
Horwitz, A. G., Berona, J., Czyz, E. K., Yeguez, C. E., & King, C. A. (2017). Positive and negative expectations of hopelessness as longitudinal predictors of depression, suicidal ideation, and suicidal behavior in high-risk adolescents. Suicide and Life-Threatening Behavior, 47(2), 168–176.CrossRefGoogle ScholarPubMed
Jankowski, K. F., Batres, J., Scott, H., Smyda, G., Pfeifer, J. H., & Quevedo, K. (2018). Feeling left out: Depressed adolescents may atypically recruit emotional salience and regulation networks during social exclusion. Social Cognitive and Affective Neuroscience, 13(8), 863–876.CrossRefGoogle ScholarPubMed
Jonsson, U., Bohman, H., von Knorring, L., Olsson, G., Paaren, A., & von Knorring, A. L. (2011). Mental health outcome of long-term and episodic adolescent depression: 15-year follow-up of a community sample. Journal of Affective Disorders, 130(3), 395–404.CrossRefGoogle ScholarPubMed
Keren, H., O'Callaghan, G., Vidal-Ribas, P., Buzzell, G. A., Brotman, M. A., Leibenluft, E., … Stringaris, A. (2018). Reward processing in depression: A conceptual and meta-analytic review across fMRI and EEG studies. American Journal of Psychiatry, 175(11), 1111–1120.CrossRefGoogle ScholarPubMed
Knorr, F. G., Neukam, P. T., Fröhner, J. H., Mohr, H., & Marxen, M. (2020). A comparison of fMRI and behavioral models for predicting inter-temporal choices. NeuroImage, 211, 116634.CrossRefGoogle ScholarPubMed
Korn, C. W., Sharot, T., Walter, H., Heekeren, H. R., & Dolan, R. J. (2014). Depression is related to an absence of optimistically biased belief updating about future life events. Psychological Medicine, 44(3), 579–592.CrossRefGoogle Scholar
Kube, T., Rief, W., & Glombiewski, J. A. (2017). On the maintenance of expectations in Major depression - investigating a neglected phenomenon. Frontiers in Psychology, 8, 9.CrossRefGoogle ScholarPubMed
Kube, T., Rief, W., Gollwitzer, M., Gartner, T., & Glombiewski, J. A. (2019). Why dysfunctional expectations in depression persist - results from two experimental studies investigating cognitive immunization. Psychological Medicine, 49(9), 1532–1544.CrossRefGoogle ScholarPubMed
Kube, T., Schwarting, R., Rozenkrantz, L., Glombiewski, J. A., & Rief, W. (2020). Distorted cognitive processes in Major depression: A predictive processing perspective. Biological Psychiatry, 87(5), 388–398.CrossRefGoogle ScholarPubMed
Kumar, P., Waiter, G., Ahearn, T., Milders, M., Reid, I., & Steele, J. D. (2008). Abnormal temporal difference reward-learning signals in major depression. Brain, 131(Pt 8), 2084–2093.CrossRefGoogle ScholarPubMed
Kumar, P., Waiter, G. D., Dubois, M., Milders, M., Reid, I., & Steele, J. D. (2017). Increased neural response to social rejection in major depression. Depression and Anxiety, 34(11), 1049–1056.CrossRefGoogle ScholarPubMed
Kupferberg, A., Bicks, L., & Hasler, G. (2016). Social functioning in major depressive disorder. Neuroscience & Biobehavioral Reviews, 69, 313–332.CrossRefGoogle ScholarPubMed
Lewis, C. A., Kimmig, A. S., Zsido, R. G., Jank, A., Derntl, B., & Sacher, J. (2019). Effects of hormonal contraceptives on mood: A focus on emotion recognition and reactivity, reward processing, and stress response. Current Psychiatry Reports, 21(11), 115.CrossRefGoogle ScholarPubMed
Liknaitzky, P., Smillie, L. D., & Allen, N. B. (2017). Out-of-the-Blue: Depressive symptoms are associated with deficits in processing inferential expectancy-violations using a novel cognitive rigidity task. Cognitive Therapy and Research, 41(5), 757–776.CrossRefGoogle Scholar
Matthew, B., Jean-Luc, A., Romain, V., & Jean-Baptiste, P. (2002). Region of interest analysis using the MarsBar toolbox for SPM 99. NeuroImage, 16(2), S497.Google Scholar
Pizzagalli, D. A., Holmes, A. J., Dillon, D. G., Goetz, E. L., Birk, J. L., Bogdan, R., … Fava, M. (2009). Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder. American Journal of Psychiatry, 166(6), 702–710.CrossRefGoogle ScholarPubMed
Porcelli, S., Van der Wee, N., van der Werff, S., Aghajani, M., Glennon, J. C., van Heukelum, S., … Serretti, A. (2019). Social brain, social dysfunction and social withdrawal. Neuroscience & Biobehavioral Reviews, 97(SI), 10–33.CrossRefGoogle ScholarPubMed
Powers, K. E., Somerville, L. H., Kelley, W. M., & Heatherton, T. F. (2013). Rejection sensitivity polarizes striatal-medial prefrontal activity when anticipating social feedback. Journal of Cognitive Neuroscience, 25(11), 1887–1895.CrossRefGoogle ScholarPubMed
Pulcu, E., & Elliott, R. (2015). Neural origins of psychosocial functioning impairments in major depression. The Lancet. Psychiatry, 2(9), 835–843.CrossRefGoogle ScholarPubMed
Rhebergen, D., Beekman, A. T., de Graaf, R., Nolen, W. A., Spijker, J., Hoogendijk, W. J., … Penninx, B. W. (2010). Trajectories of recovery of social and physical functioning in major depression, dysthymic disorder and double depression: A 3-year follow-up. Journal of Affective Disorders, 124(1–2), 148–156.CrossRefGoogle ScholarPubMed
Robinson, O. J., Cools, R., Carlisi, C. O., Sahakian, B. J., & Drevets, W. C. (2012). Ventral striatum response during reward and punishment reversal learning in unmedicated major depressive disorder. American Journal of Psychiatry, 169(2), 152–159.CrossRefGoogle ScholarPubMed
Rothkirch, M., Tonn, J., Kohler, S., & Sterzer, P. (2017). Neural mechanisms of reinforcement learning in unmedicated patients with major depressive disorder. Brain, 140(4), 1147–1157.CrossRefGoogle ScholarPubMed
Rottenberg, J., & Gotlib, I. H.. (2004). Socioemotional functioning in depression. In M, Power (Ed.), Mood disorders: A handbook of science and practice (pp. 61–77). New York: Wiley.CrossRefGoogle Scholar
Schultz, W., Dayan, P., & Montague, P. R. (1997). A neural substrate of prediction and reward. Science (New York, N.Y.), 275(5306), 1593–1599.CrossRefGoogle ScholarPubMed
Schurz, M., Radua, J., Aichhorn, M., Richlan, F., & Perner, J. (2014). Fractionating theory of mind: A meta-analysis of functional brain imaging studies. Neuroscience & Biobehavioral Reviews, 42, 9–34.CrossRefGoogle ScholarPubMed
Segarra, N., Metastasio, A., Ziauddeen, H., Spencer, J., Reinders, N. R., Dudas, R. B., … Murray, G. K. (2016). Abnormal frontostriatal activity during unexpected reward receipt in depression and schizophrenia: Relationship to anhedonia. Neuropsychopharmacology, 41(8), 2001–2010.CrossRefGoogle ScholarPubMed
Segrin, C. (2000). Social skills deficits associated with depression. Clinical Psychology Review, 20(3), 379–403.CrossRefGoogle ScholarPubMed
Silk, J. S., Siegle, G. J., Lee, K. H., Nelson, E. E., Stroud, L. R., & Dahl, R. E. (2014). Increased neural response to peer rejection associated with adolescent depression and pubertal development. Social Cognitive and Affective Neuroscience, 9(11), 1798–1807.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Somerville, L. H., Kelley, W. M., & Heatherton, T. F. (2010). Self-esteem modulates medial prefrontal cortical responses to evaluative social feedback. Cerebral Cortex, 20(12), 3005–3013.CrossRefGoogle ScholarPubMed
Spielberger, C. D., Gorsuch, R. L., Lushene, R. E., Vagg, P. R., & Jacobs, G. A. (1983). Manual for the state-trait anxiety inventory. Palo Alto, CA: Consulting Psychologists Press.Google Scholar
Stoodley, C. J., Valera, E. M., & Schmahmann, J. D. (2012). Functional topography of the cerebellum for motor and cognitive tasks: An fMRI study. NeuroImage, 59(2), 1560–1570.CrossRefGoogle Scholar
Torrubia, R., Avila, C., Molto, J., & Caseras, X. (2001). The Sensitivity to Punishment and Sensitivity to Reward Questionnaire (SPSRQ) as a measure of Gray's anxiety and impulsivity dimensions. Personality and Individual Differences, 31(6), 837–862.CrossRefGoogle Scholar
Ubl, B., Kuehner, C., Kirsch, P., Ruttorf, M., Diener, C., & Flor, H. (2015). Altered neural reward and loss processing and prediction error signalling in depression. Social Cognitive and Affective Neuroscience, 10(8), 1102–1112.CrossRefGoogle ScholarPubMed
Uekermann, J., Channon, S., Lehmkamper, C., Abdel-Hamid, M., Vollmoeller, W., & Daum, I. (2008). Executive function, mentalizing and humor in major depression. Journal of the International Neuropsychological Society, 14(1), 55–62.CrossRefGoogle ScholarPubMed
van der Molen, M., Dekkers, L., Westenberg, P. M., van der Veen, F. M., & van der Molen, M. W. (2017). Why don't you like me? Midfrontal theta power in response to unexpected peer rejection feedback. NeuroImage, 146, 474–483.CrossRefGoogle ScholarPubMed
van der Veen, F. M., van der Molen, M. W., Sahibdin, P. P., & Franken, I. H. (2014). The heart-break of social rejection versus the brain wave of social acceptance. Social Cognitive and Affective Neuroscience, 9(9), 1346–1351.CrossRefGoogle ScholarPubMed
Vossen, S., Ham, J., & Midden, C. (2010). What makes social feedback from a robot work? Disentangling the effect of speech, physical appearance and evaluation. In Ploug, T., Hasle, P., & Oinas-Kukkonen, H. (Eds.), PERSUASIVE: 5th international conference on persuasive technology (pp. 52–57). Berlin, Heidelberg: Springer.CrossRefGoogle Scholar
Weightman, M. J., Air, T. M., & Baune, B. T. (2014). A review of the role of social cognition in major depressive disorder. Frontiers in Psychiatry, 5, 179.CrossRefGoogle ScholarPubMed
Wesselmann, E. D., Wirth, J. H., & Bernstein, M. J. (2017). Expectations of social inclusion and exclusion. Frontiers in Psychology, 8, 112.CrossRefGoogle ScholarPubMed
Wesselmann, E. D., Wirth, J. H., Pryor, J. B., Reeder, G. D., & Williams, K. D. (2012). When do we ostracize? Social Psychological and Personality Science, 4(1), 108–115.CrossRefGoogle Scholar
Xie, H., Jiang, D., & Zhang, D. (2018). Individuals with depressive tendencies experience difficulty in forgetting negative material: Two mechanisms revealed by ERP data in the directed forgetting paradigm. Scientific Reports, 8(1), 1113.CrossRefGoogle ScholarPubMed
Zhang, S., Mano, H., Ganesh, G., Robbins, T., & Seymour, B. (2016). Dissociable learning processes underlie human pain conditioning. Current Biology, 26(1), 52–58.CrossRefGoogle ScholarPubMed
Zung, W. W., Richards, C. B., & Short, M. J. (1965). Self-rating depression scale in an outpatient clinic. Further validation of the SDS. Archives Of General Psychiatry, 13(6), 508–515.CrossRefGoogle Scholar
Supplementary material: File

He et al. supplementary material

He et al. supplementary material

Download He et al. supplementary material(File)
File 37.6 KB