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Neural correlates of social exchanges during the Prisoner's Dilemma game in depression

Published online by Cambridge University Press:  14 January 2016

V. B. Gradin ,
A. Pérez ,
J. A. Macfarlane ,
I. Cavin ,
G. Waiter ,
E. B. Tone ,
B. Dritschel ,
A. Maiche  and
J. D. Steele
V. B. Gradin*
Affiliation:
Faculty of Psychology, CIBPsi, Universidad de la República, Montevideo, Uruguay
A. Pérez
Affiliation:
Faculty of Psychology, CIBPsi, Universidad de la República, Montevideo, Uruguay
J. A. Macfarlane
Affiliation:
Medical Physics, NHS Tayside, University of Dundee, Dundee, UK
I. Cavin
Affiliation:
Medical Physics, NHS Tayside, University of Dundee, Dundee, UK
G. Waiter
Affiliation:
Aberdeen Biomedical Imaging Centre, University of Aberdeen, Aberdeen, UK
E. B. Tone
Affiliation:
Department of Psychology, Georgia State University, Atlanta, GA, USA
B. Dritschel
Affiliation:
Department of Psychology, University of St Andrews, Fife, UK
A. Maiche
Affiliation:
Faculty of Psychology, CIBPsi, Universidad de la República, Montevideo, Uruguay
J. D. Steele
Affiliation:
School of Medicine (Neuroscience), University of Dundee, Ninewells Hospital and Medical School, Dundee, UK
*
*Address for correspondence: Dr V. Gradin, Faculty of Psychology, Center for Investigation of Basic Psychology (CIBPsi), Universidad de la República, Montevideo 11200, Uruguay. (Email: [email protected])
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Abstract

Background

Depression is a disabling disorder that significantly impacts on the interpersonal functioning of individuals. However, little is known about the neural substrates of such difficulties. In the last few years neuroeconomics, which combines imaging with multiplayer behavioural economic paradigms, has been used to study the neural substrates of normal and abnormal interpersonal interactions.

Method

This study used functional magnetic resonance imaging to investigate neural activity in unmedicated depressed participants (n = 25) and matched healthy controls (n = 25). During scanning, participants played a behavioural economic game, the Prisoner's Dilemma. In this game, the participant and a co-player independently choose either to cooperate or not cooperate with each other.

Results

Depressed participants reported higher levels of negative feelings (betrayal, guilt) during the game than did controls. Neural activation was compared between ‘imbalanced’ events [when one of the players cooperated and the other defected (‘CD’ and ‘DC’)] and ‘draw’ events [when both players either cooperated or defected (‘CC’ and ‘DD’)]. Participants preferentially activated the anterior insula and the dorsolateral prefrontal cortex (DLPFC), a region implicated in cognitive control and regulation of emotions. Importantly, compared to controls depressed participants showed reduced activation in the left DLPFC, with the extent of signal reduction correlating with increased self-report feelings of guilt associated with DC outcomes.

Conclusions

Our findings suggest that depression is associated with reduced activation of the DLPFC during social events that involve unreciprocated cooperation. This abnormality may underlie anomalies in cognitive control and top-down regulation of emotions during challenging social exchanges.

Keywords

DepressionfMRIneuroeconomicsPrisoner's Dilemma
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 6 , April 2016 , pp. 1289 - 1300
Copyright
Copyright © Cambridge University Press 2016 

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References

APA (2013). Diagnostic and Statistical Manual of Mental Disorders, 5th edn. Washington, DC: American Psychiatric Association.Google Scholar
Axelrod, R, Hamilton, WD (1981). The evolution of cooperation. Science 211, 1390–1396.CrossRefGoogle ScholarPubMed
Beck, AT (1979). Cognitive Theory of Depression. J. Wiley and Sons: New York.Google Scholar
Beck, AT, Epstein, N, Harrison, RP, Emery, G (1983). Development of the Sociotropy-Autonomy Scale: a Measure of Personality Factors in Psychopathology. Unpublished manuscript, University of Pennsylvania: Piladelphia.Google Scholar
Beck, AT, Ward, HC, Mendelson, M (1961). An inventory for measuring depression. Archives of General Psychiatry 4, 561–571.CrossRefGoogle ScholarPubMed
Bernstein, DP, Stein, JA, Newcomb, MD, Walker, E, Pogge, D, Ahluvalia, T, Stokes, J, Handelsman, L, Medrano, M, Desmond, D, Zule, W (2003). Development and validation of a brief screening version of the Childhood Trauma Questionnaire. Child Abuse and Neglect 27, 169–190.CrossRefGoogle ScholarPubMed
Billings, AG, Cronkite, RC, Moos, RH (1983). Social-environmental factors in unipolar depression: comparisons of depressed patients and nondepressed controls. Journal of Abnormal Psychology 92, 119–133.CrossRefGoogle ScholarPubMed
Crockett, MJ, Apergis-Schoute, A, Herrmann, B, Lieberman, MD, Muller, U, Robbins, TW, Clark, L (2013). Serotonin modulates striatal responses to fairness and retaliation in humans. Journal of Neuroscience 33, 3505–3513.Google Scholar
D'Esposito, M, Postle, BR (2015). The cognitive neuroscience of working memory. Annual Review of Psychology 66, 115–142.Google Scholar
Destoop, M, Schrijvers, D, De Grave, C, Sabbe, B, De Bruijn, ER (2012). Better to give than to take? Interactive social decision-making in severe major depressive disorder. Journal of Affective Disorders 137, 98–105.CrossRefGoogle ScholarPubMed
Disner, SG, Beevers, CG, Haigh, EA, Beck, AT (2011). Neural mechanisms of the cognitive model of depression. Nature Reviews Neuroscience 12, 467–477.Google Scholar
Emonds, G, Declerck, CH, Boone, C, Vandervliet, EJ, Parizel, PM (2012). The cognitive demands on cooperation in social dilemmas: an fMRI study. Social Neuroscience 7, 494–509.CrossRefGoogle ScholarPubMed
Eshel, N, Roiser, JP (2010). Reward and punishment processing in depression. Biological Psychiatry 68, 118–124.Google Scholar
Etkin, A, Schatzberg, AF (2011). Common abnormalities and disorder-specific compensation during implicit regulation of emotional processing in generalized anxiety and major depressive disorders. American Journal of Psychiatry 168, 968–978.CrossRefGoogle ScholarPubMed
Fales, CL, Barch, DM, Rundle, MM, Mintun, MA, Snyder, AZ, Cohen, JD, Mathews, J, Sheline, YI (2008). Altered emotional interference processing in affective and cognitive-control brain circuitry in major depression. Biological Psychiatry 63, 377–384.Google Scholar
Fredman, L, Weissman, MM, Leaf, PJ, Bruce, ML (1988). Social functioning in community residents with depression and other psychiatric disorders: results of the New Haven Epidemiologic Catchment Area Study. Journal of Affective Disorders 15, 103–112.Google Scholar
Frodl, T, Scheuerecker, J, Albrecht, J, Kleemann, AM, Muller-Schunk, S, Koutsouleris, N, Moller, HJ, Bruckmann, H, Wiesmann, M, Meisenzahl, E (2009). Neuronal correlates of emotional processing in patients with major depression. World Journal of Biological Psychiatry 10, 202–208.Google Scholar
Galynker, II, Cai, J, Ongseng, F, Finestone, H, Dutta, E, Serseni, D (1998). Hypofrontality and negative symptoms in major depressive disorder. Journal of Nuclear Medicine 39, 608–612.Google Scholar
Glimcher, PW, Rustichini, A (2004). Neuroeconomics: the consilience of brain and decision. Science 306, 447–452.Google Scholar
Gotlib, IH, Hamilton, JP (2008). Neuroimaging and Depression. Current Directions in Psychological Science 17, 159–163.Google Scholar
Gradin, VB, Kumar, P, Waiter, G, Ahearn, T, Stickle, C, Milders, M, Reid, I, Hall, J, Steele, JD (2011). Expected value and prediction error abnormalities in depression and schizophrenia. Brain 134, 1751–1764.Google Scholar
Gradin, VB, Perez, A, MacFarlane, JA, Cavin, I, Waiter, G, Engelmann, J, Dritschel, B, Pomi, A, Matthews, K, Steele, JD (2015). Abnormal brain responses to social fairness in depression: an fMRI study using the Ultimatum Game. Psychological Medicine 45, 1241–1251.Google Scholar
Hamilton, M (1959). The assessment of anxiety states by rating. British Journal of Medical Psychology 32, 50–55.Google Scholar
Hamilton, M (1960). Rating scale for depression. Journal of Neurology, Neurosurgery and Psychiatry 23, 56–62.Google Scholar
Harle, KM, Allen, JJ, Sanfey, AG (2010). The impact of depression on social economic decision making. Journal of Abnormal Psychology 119, 440–446.Google Scholar
Hasler, G (2011). Can the neuroeconomics revolution revolutionize psychiatry? Neuroscience and Biobehavioral Reviews 36, 64–78.Google Scholar
Hirschfeld, RM, Montgomery, SA, Keller, MB, Kasper, S, Schatzberg, AF, Moller, HJ, Healy, D, Baldwin, D, Humble, M, Versiani, M, Montenegro, R, Bourgeois, M (2000). Social functioning in depression: a review. Journal of Clinical Psychiatry 61, 268–275.CrossRefGoogle ScholarPubMed
Hokanson, JE, Sacco, WP, Blumberg, SR, Landrum, GC (1980). Interpersonal behavior of depressive individuals in a mixed-motive game. Journal of Abnormal Psychology 89, 320–332.CrossRefGoogle Scholar
Hooley, JM, Gruber, SA, Scott, LA, Hiller, JB, Yurgelun-Todd, DA (2005). Activation in dorsolateral prefrontal cortex in response to maternal criticism and praise in recovered depressed and healthy control participants. Biological Psychiatry 57, 809–812.CrossRefGoogle ScholarPubMed
Horowitz, LM, Rosenberg, SE, Bartholomew, K (1993). Interpersonal problems, attachment styles, and outcome in brief dynamic psychotherapy. Journal of Consulting and Clinical Psychology 61, 549–560.CrossRefGoogle ScholarPubMed
King-Casas, B, Chiu, PH (2012). Understanding interpersonal function in psychiatric illness through multiplayer economic games. Biological Psychiatry 72, 119–125.CrossRefGoogle ScholarPubMed
King-Casas, B, Sharp, C, Lomax-Bream, L, Lohrenz, T, Fonagy, P, Montague, PR (2008). The rupture and repair of cooperation in borderline personality disorder. Science 321, 806–810.Google Scholar
Koenigs, M, Huey, ED, Calamia, M, Raymont, V, Tranel, D, Grafman, J (2008). Distinct regions of prefrontal cortex mediate resistance and vulnerability to depression. Journal of Neuroscience 28, 12341–12348.CrossRefGoogle ScholarPubMed
Li, CT, Lin, CP, Chou, KH, Chen, IY, Hsieh, JC, Wu, CL, Lin, WC, Su, TP (2010). Structural and cognitive deficits in remitting and non-remitting recurrent depression: a voxel-based morphometric study. Neuroimage 50, 347–356.Google Scholar
Mayberg, HS, Liotti, M, Brannan, SK, McGinnis, S, Mahurin, RK, Jerabek, PA, Silva, JA, Tekell, JL, Martin, CC, Lancaster, JL, Fox, PT (1999). Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. American Journal of Psychiatry 156, 675–682.Google Scholar
McClure, EB, Parrish, JM, Nelson, EE, Easter, J, Thorne, JF, Rilling, JK, Ernst, M, Pine, DS (2007). Responses to conflict and cooperation in adolescents with anxiety and mood disorders. Journal of Abnormal Child Psychology 35, 567–577.CrossRefGoogle ScholarPubMed
McClure-Tone, EB, Nawa, NE, Nelson, EE, Detloff, AM, Fromm, SJ, Pine, DS, Ernst, M (2011). Preliminary findings: neural responses to feedback regarding betrayal and cooperation in adolescent anxiety disorders. Developmental Neuropsychology 36, 453–472.Google Scholar
Miller, EK, Cohen, JD (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience 24, 167–202.Google Scholar
Montgomery, SA, Asberg, M (1979). A new depression scale designed to be sensitive to change. British Journal of Psychiatry 134, 382–389.Google Scholar
Nelson, HE, Wilson, JR (1991). The Revised National Adult Reading Test – Test Manual. NFER-Wilson: Winsor.Google Scholar
Okon-Singer, H, Hendler, T, Pessoa, L, Shackman, AJ (2015). The neurobiology of emotion-cognition interactions: fundamental questions and strategies for future research. Frontiers in Human Neuroscience 9, 58.Google Scholar
Papakostas, GI, Petersen, T, Mahal, Y, Mischoulon, D, Nierenberg, AA, Fava, M (2004). Quality of life assessments in major depressive disorder: a review of the literature. General Hospital Psychiatry 26, 13–17.CrossRefGoogle ScholarPubMed
Pulcu, E, Elliott, R (2015). Neural origins of psychosocial functioning impairments in major depression. Lancet Psychiatry 2, 835–843.Google Scholar
Remijnse, PL, Nielen, MM, van Balkom, AJ, Hendriks, GJ, Hoogendijk, WJ, Uylings, HB, Veltman, DJ (2009). Differential frontal-striatal and paralimbic activity during reversal learning in major depressive disorder and obsessive-compulsive disorder. Psychological Medicine 39, 1503–1518.Google Scholar
Rilling, J, Gutman, D, Zeh, T, Pagnoni, G, Berns, G, Kilts, C (2002). A neural basis for social cooperation. Neuron 35, 395–405.Google Scholar
Rilling, JK, Glenn, AL, Jairam, MR, Pagnoni, G, Goldsmith, DR, Elfenbein, HA, Lilienfeld, SO (2007). Neural correlates of social cooperation and non-cooperation as a function of psychopathy. Biological Psychiatry 61, 1260–1271.CrossRefGoogle ScholarPubMed
Rilling, JK, Goldsmith, DR, Glenn, AL, Jairam, MR, Elfenbein, HA, Dagenais, JE, Murdock, CD, Pagnoni, G (2008). The neural correlates of the affective response to unreciprocated cooperation. Neuropsychologia 46, 1256–1266.Google Scholar
Rilling, JK, Sanfey, AG, Aronson, JA, Nystrom, LE, Cohen, JD (2004). Opposing BOLD responses to reciprocated and unreciprocated altruism in putative reward pathways. Neuroreport 15, 2539–2543.Google Scholar
Rive, MM, van Rooijen, G, Veltman, DJ, Phillips, ML, Schene, AH, Ruhe, HG (2013). Neural correlates of dysfunctional emotion regulation in major depressive disorder. A systematic review of neuroimaging studies. Neuroscience and Biobehavioral Reviews 37, 2529–2553.Google Scholar
Robins, CJ, Ladd, J, Welkowitz, J, Blaney, PH, Diaz, R, Kutcher, G (1994). The personal style inventory: preliminary validation studies of new measures of sociotropy and autonomy. Journal of Psychopathology and Behavioral Assessment 16, 277–300.CrossRefGoogle Scholar
Rosenberg, M (1965). Society and the Adolescent Self-Image. Princeton University Press: Princeton, NJ.CrossRefGoogle Scholar
Sanfey, AG, Rilling, JK, Aronson, JA, Nystrom, LE, Cohen, JD (2003). The neural basis of economic decision-making in the Ultimatum Game. Science 300, 1755–1758.Google Scholar
Scheele, D, Mihov, Y, Schwederski, O, Maier, W, Hurlemann, R (2013). A negative emotional and economic judgment bias in major depression. European Archives of Psychiatry and Clinical Neuroscience 263, 675–683.Google Scholar
Segrin, C (2000). Social skills deficits associated with depression. Clinical Psychology Review 20, 379–403.Google Scholar
Slotnick, SD, Moo, LR, Segal, JB, Hart, J Jr. (2003). Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. Cognitive Brain Research 17, 75–82.Google Scholar
Snaith, RP, Hamilton, M, Morley, S, Humayan, A, Hargreaves, D, Trigwell, P (1995). A scale for the assessment of hedonic tone the Snaith-Hamilton Pleasure Scale. British Journal of Psychiatry 167, 99–103.Google Scholar
Spielberger, CD (1983). State-Trait Anxiety Inventory for Adults, STAI Form Y-1. Mind Garden: Palo Alto.Google Scholar
Strigo, IA, Simmons, AN, Matthews, SC, Craig, AD, Paulus, MP (2008). Association of major depressive disorder with altered functional brain response during anticipation and processing of heat pain. Archives of General Psychiatry 65, 1275–1284.Google Scholar
Tabibnia, G, Satpute, AB, Lieberman, MD (2008). The sunny side of fairness: preference for fairness activates reward circuitry (and disregarding unfairness activates self-control circuitry). Psychological Science 19, 339–347.Google Scholar
Wang, Y, Yang, LQ, Li, S, Zhou, Y (2015). Game theory paradigm: a new tool for investigating social dysfunction in major depressive disorders. Frontiers in Psychiatry 6, 128.Google Scholar
Watson, D, Clark, LA, Tellegen, A (1988). Development and validation of brief measures of positive and negative affect: the PANAS scales. Journal of Personality and Social Psychology 54, 1063–1070.Google Scholar
Yoshida, W, Dolan, RJ, Friston, KJ (2008). Game theory of mind. PLOS Computational Biology 4, e1000254.Google Scholar
Yoshida, W, Seymour, B, Friston, KJ, Dolan, RJ (2010). Neural mechanisms of belief inference during cooperative games. Journal of Neuroscience 30, 10744–10751.Google Scholar
Zhang, WN, Chang, SH, Guo, LY, Zhang, KL, Wang, J (2013). The neural correlates of reward-related processing in major depressive disorder: a meta-analysis of functional magnetic resonance imaging studies. Journal of Affective Disorders 151, 531–539.CrossRefGoogle ScholarPubMed
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