Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-29T02:04:09.709Z Has data issue: false hasContentIssue false
  • English
  • Français

Reduced brain reward response during cooperation in first-degree relatives of patients with psychosis: an fMRI study

Published online by Cambridge University Press:  09 April 2014

P. M. Gromann ,
S. S. Shergill ,
L. de Haan ,
D. G. J. Meewis ,
A.-K. J. Fett ,
N. Korver-Nieberg  and
L. Krabbendam
P. M. Gromann
Affiliation:
Department of Educational Neuroscience, Faculty of Psychology and Education, VU University Amsterdam, The Netherlands CSI Laboratory, Department of Psychosis Studies, Institute of Psychiatry, King's College London, UK
S. S. Shergill
Affiliation:
CSI Laboratory, Department of Psychosis Studies, Institute of Psychiatry, King's College London, UK
L. de Haan
Affiliation:
Department of Early Psychosis, AMC, Academic Psychiatric Centre, Amsterdam, The Netherlands
D. G. J. Meewis
Affiliation:
Department of Educational Neuroscience, Faculty of Psychology and Education, VU University Amsterdam, The Netherlands
A.-K. J. Fett*
Affiliation:
Department of Educational Neuroscience, Faculty of Psychology and Education, VU University Amsterdam, The Netherlands CSI Laboratory, Department of Psychosis Studies, Institute of Psychiatry, King's College London, UK
N. Korver-Nieberg
Affiliation:
Department of Early Psychosis, AMC, Academic Psychiatric Centre, Amsterdam, The Netherlands
L. Krabbendam
Affiliation:
Department of Educational Neuroscience, Faculty of Psychology and Education, VU University Amsterdam, The Netherlands
*
*Address for correspondence: A.-K. J. Fett, Department of Educational Neuroscience, Faculty of Psychology and Education, VU University Amsterdam, Van der Boechorststraat 1, 1081 BT Amsterdam, The Netherlands. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background.

Psychosis is characterized by a profound lack of trust and disturbed social interactions. Investigating the neural basis of these deficits is difficult because of medication effects but first-degree relatives show qualitatively similar abnormalities to patients with psychosis on various tasks. This study aimed to investigate neural activation in siblings of patients in response to an interactive task. We hypothesized that, compared to controls, siblings would show (i) less basic trust at the beginning of the task and (ii) reduced activation of the brain reward and mentalizing systems.

Method.

Functional magnetic resonance imaging (fMRI) data were acquired on 50 healthy siblings of patients with psychosis and 33 healthy controls during a multi-round trust game with a cooperative counterpart. An a priori region-of-interest (ROI) analysis of the caudate, temporoparietal junction (TPJ), superior temporal sulcus (STS), insula and medial prefrontal cortex (mPFC) was performed focusing on the investment and repayment phases. An exploratory whole-brain analysis was run to test for group-wise differences outside these ROIs.

Results.

The siblings’ behaviour during the trust game did not differ significantly from that of the controls. At the neural level, siblings showed reduced activation of the right caudate during investments, and the left insula during repayments. In addition, the whole-brain analysis revealed reduced putamen activation in siblings during investments.

Conclusions.

The findings suggest that siblings show aberrant functioning of regions traditionally involved in reward processing in response to cooperation, which may be associated with the social reward deficits observed in psychosis.

Keywords

Caudatefunctional MRIpsychosisrewardsiblingstrust
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 16 , December 2014 , pp. 3445 - 3454
Copyright
Copyright © Cambridge University Press 2014 

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

Adolphs, R (2009). The social brain: neural basis of social knowledge. Annual Review of Psychology 60, 693–716.Google Scholar
Anselmetti, S, Bechi, M, Bosia, M, Quarticelli, C, Ermoli, E, Smeraldi, E, Cavallaro, R (2009). ‘Theory’ of mind impairment in patients affected by schizophrenia and in their parents. Schizophrenia Research 115, 278–285.Google Scholar
Baas, D, van't Wout, M, Aleman, A, Kahn, RS (2008). Social judgment in clinically stable patients with schizophrenia and healthy relatives: behavioural evidence of social brain dysfunction. Psychological Medicine 38, 747–754.Google Scholar
Baumgartner, T, Heinrichs, M, Vonlanthen, A, Fischbacher, U, Fehr, E (2008). Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 58, 639–650.Google Scholar
Berg, J, Dickhaut, J, McCabe, K (1995). Trust, reciprocity and social history. Games and Economic Behavior 10, 122–142.Google Scholar
Bora, E, Pantelis, C (2013). Theory of mind impairments in first-episode psychosis, individuals at ultra-high risk for psychosis and in first-degree relatives of schizophrenia: systematic review and meta-analysis. Schizophrenia Research 144, 31–36.Google Scholar
Braff, DL, Freedman, R, Schork, NJ, Gottesman, II (2007). Deconstructing schizophrenia: an overview of the use of endophenotypes in order to understand a complex disorder. Schizophrenia Bulletin 33, 21–32.Google Scholar
Camerer, CF (2003). Psychology and economics. Strategizing in the brain. Science 300, 1673–1675.Google Scholar
Chau, DT, Roth, RM, Green, AI (2004). The neural circuitry of reward and its relevance to psychiatric disorders. Current Psychiatry Reports 6, 391–399.Google Scholar
Croson, R, Buchan, N (1999). Gender and culture: international experimental evidence from trust games. American Economic Review 89, 386–391.CrossRefGoogle Scholar
Delgado, MR, Frank, RH, Phelps, EA (2005). Perceptions of moral character modulate the neural systems of reward during the trust game. Nature Neuroscience 8, 1611–1618.Google Scholar
Eckel, CC, Wilson, RK (2004). Is trust a risky decision? Journal of Economic Behavior and Organization 55, 447–465.Google Scholar
Fehr, E (2009). On the economics and biology of trust. Journal of the European Economic Association 7, 235–266.Google Scholar
Fett, AK, Shergill, SS, Gromann, PM, Dumontheil, I, Blakemore, S-J, Yakub, F, Krabbendam, L (2014). Trust and social reciprocity in adolescence – a matter of perspective-taking. Journal of Adolescence 37, 175–184.CrossRefGoogle ScholarPubMed
Fett, AK, Shergill, SS, Joyce, DW, Riedl, A, Strobel, M, Gromann, PM, Krabbendam, L (2012). To trust or not to trust: the dynamics of social interaction in psychosis. Brain 135, 976–984.CrossRefGoogle ScholarPubMed
Fett, AK, Viechtbauer, W, Dominguez, MD, Penn, DL, van Os, J, Krabbendam, L (2011). The relationship between neurocognition and social cognition with functional outcomes in schizophrenia: a meta-analysis. Neuroscience and Biobehavioral Reviews 35, 573–588.CrossRefGoogle ScholarPubMed
Frith, U, Frith, CD (2003). Development and neurophysiology of mentalizing. Philosophical Transactions of the Royal Society. Series B, Biological Sciences 358, 459–473.Google Scholar
Gallagher, HL, Frith, CD (2003). Functional imaging of ‘theory of mind’. Trends in Cognitive Sciences 7, 77–83.Google Scholar
Glaeser, E, Laibson, D, Scheinkman, J, Soutter, C (2000). Measuring trust. Quarterly Journal of Economics 115, 811–846.Google Scholar
Gottesman, II, Gould, TD (2003). The endophenotype concept in psychiatry: etymology and strategic intentions. American Journal of Psychiatry 160, 636–645.Google Scholar
Greenwood, TA, Braff, DL, Light, GA, Cadenhead, KS, Calkins, ME, Dobie, DJ, Freedman, R, Green, MF, Gur, RE, Gur, RC, Mintz, J, Nuechterlein, KH, Olincy, A, Radant, AD, Seidman, LJ, Siever, LJ, Silverman, JM, Stone, WS, Swerdlow, NR, Tsuang, DW, Tsuang, MT, Turetsky, BI, Schork, NJ (2007). Initial heritability analyses of endophenotypic measures for schizophrenia: the Consortium on the Genetics of Schizophrenia. Archives of General Psychiatry 64, 1242–1250.Google Scholar
Gromann, PM, Shergill, SS, Heslenfeld, D, Fett, AK, Krabbendam, L (2013). Trust versus paranoia: abnormal response to social reward in psychotic illness. Brain 136, 1968–1975.Google Scholar
Hamani, C, Mayberg, H, Stone, S, Laxton, A, Haber, S, Lozano, AM (2011). The subcallosal cingulate gyrus in the context of major depression. Biological Psychiatry 69, 301–308.Google Scholar
Hampton, AN, Bossaerts, P, O'Doherty, JP (2008). Neural correlates of mentalizing-related computations during strategic interactions in humans. Proceedings of the National Academy of Sciences USA 105, 6741–6746.Google Scholar
Harbaugh, WT, Mayr, U, Burghart, DR (2007). Neural responses to taxation and voluntary giving reveal motives for charitable donations. Science 316, 1622–1625.Google Scholar
Harford, T, Solomon, L (1969). Effects of a ‘reformed sinner’ and a ‘lapsed saint’ strategy upon trust formation in paranoid and non-paranoid schizophrenic patients. Journal of Abnormal Psychology 74, 498–504.Google Scholar
Helenius, D, Munk-Jørgensen, P, Steinhausen, HC (2012). Family load estimates of schizophrenia and associated risk factors in a nation-wide population study of former child and adolescent patients up to forty years of age. Schizophrenia Research 139, 183–188.Google Scholar
Houser, D, Schunk, D, Winter, J (2010). Distinguishing trust from risk: an anatomy of the investment game. Journal of Economic Behavior and Organization 74, 72–81.Google Scholar
Irani, F, Platek, SM, Panyavin, IS, Calkins, ME, Kohler, C, Siegel, SJ, Schachter, M, Gur, RE, Gur, RC (2006). Self-face recognition and theory of mind in patients with schizophrenia and first-degree relatives. Schizophrenia Research 88, 151–160.Google Scholar
Johns, LC, van Os, J (2001). The continuity of psychotic experiences in the general population. Clinical Psychology Review 21, 1125–1141.CrossRefGoogle ScholarPubMed
Juckel, G, Schlagenhauf, F, Koslowski, M, Filonov, D, Wüstenberg, T, Villringer, A, Knutson, B, Kienast, T, Gallinat, J, Wrase, J, Heinz, A (2006). Dysfunction of ventral striatal reward prediction in schizophrenic patients treated with typical, not atypical, neuroleptics. Psychopharmacology 187, 222–228.CrossRefGoogle Scholar
Karlan, DS (2005). Using experimental economics to measure social capital and predict financial decisions. American Economic Review 95, 1688–1699.Google Scholar
Keshavan, MS, Kulkarni, S, Bhojraj, T, Francis, A, Diwadkar, V, Montrose, DM, Seidman, LJ, Sweeney, J (2010). Premorbid cognitive deficits in young relatives of schizophrenia patients. Frontiers in Human Neuroscience 3, 1–14.Google Scholar
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
King-Casas, B, Tomlin, D, Anen, C, Camerer, CF, Quartz, SR, Montague, PR (2005). Getting to know you: reputation and trust in a two-person economic exchange. Science 308, 78–83.Google Scholar
Knutson, B, Fong, GW, Adams, CM, Varner, JL, Hommer, D (2001). Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport 12, 3683–3687.Google Scholar
Korver, N, Quee, PJ, Boos, HBM, Simons, CJP, de Haan, L (2012). Genetic Risk and Outcome of Psychosis (GROUP), a multi-site longitudinal cohort study focused on gene-environment interaction: objectives, sample characteristics, recruitment and assessment methods. International Journal of Methods in Psychiatric Research 21, 205–221.Google Scholar
Kosfeld, M, Heinrichs, M, Zak, PJ, Fischbacher, U, Fehr, E (2005). Oxytocin increases trust in humans. Nature 435, 673–676.CrossRefGoogle ScholarPubMed
Krabbendam, L, Myin-Germeys, I, de Graaf, R (2004). Dimensions of depression, mania and psychosis in the general population. Psychological Medicine 34, 1177–1186.Google Scholar
Krabbendam, L, Myin-Germeys, I, Hanssen, M, van Os, J (2005). Familial covariation of the subclinical psychosis phenotype and verbal fluency in the general population. Schizophrenia Research 74, 37–41.Google Scholar
Lavoie, M-A, Plana, I, Bédard Lacroix, J, Godmaire-Duhaime, F, Jackson, PL, Achim, AM (2013). Social cognition in first-degree relatives of people with schizophrenia: a meta-analysis. Psychiatry Research 209, 129–135.Google Scholar
Lichtermann, D, Karbe, E, Maier, W (2000). The genetic epidemiology of schizophrenia and of schizophrenia spectrum disorders. European Archives of Psychiatry and Clinical Neurosciences 250, 304–310.Google Scholar
Mazza, M, Di Michele, V, Pollice, R, Casacchia, M, Roncone, R (2008). Pragmatic language and theory of mind deficits in people with schizophrenia and their relatives. Psychopathology 41, 254–263.Google Scholar
Menon, V, Uddin, LQ (2010). Saliency, switching, attention and control: a network model of insula function. Brain Structure and Function 214, 655–667.Google Scholar
Murray, GK, Corlett, PR, Clark, L, Pessiglione, M, Blackwell, AD, Honey, G, Jones, PB, Bullmore, ET, Robbins, TW, Fletcher, PC (2008). Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Molecular Psychiatry 13, 239–276.CrossRefGoogle ScholarPubMed
Phan, KL, Sripada, CS, Angstadt, M, McCabe, K (2010). Reputation for reciprocity engages the brain reward center. Proceedings of the National Academy of Sciences USA 107, 13 099–13 104.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
Sanfey, AG (2007). Social decision-making: insights from game theory and neuroscience. Science 318, 598–602.Google Scholar
Saxe, R, Kanwisher, N (2003). People thinking about people: the role of the temporoparietal junction in ‘theory of mind’. NeuroImage 19, 1835–1842.Google Scholar
Scharleman, J, Eckel, C, Kacelnik, A, Wilson, R (2001). The value of a smile: game theory with a human face. Journal of Economic Psychology 22, 617–640.Google Scholar
Schlagenhauf, F, Juckel, G, Koslowski, M, Kahnt, T, Knutson, B, Dembler, T, Kienast, T, Gallinat, J, Wrase, J, Heinz, A (2008). Reward system activation in schizophrenic patients switched from typical neuroleptics to olanzapine. Psychopharmacology 196, 673–684.Google Scholar
Seeley, WW, Menon, V, Schatzberg, AF, Keller, J, Glover, GH, Kenna, H, Reiss, AL, Greicius, MD (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. Journal of Neuroscience 27, 2349–2356.Google Scholar
Simons, CJ, Jacobs, N, Jolles, J, van Os, J, Krabbendam, L (2007). Subclinical psychotic experiences and cognitive functioning as a bivariate phenotype for genetic studies in the general population. Schizophrenia Research 92, 24–31.CrossRefGoogle ScholarPubMed
Singer, T, Kiebel, SJ, Winston, JS, Dolan, RJ, Frith, CD (2004). Brain responses to the acquired moral status of faces. Neuron 41, 653–662.CrossRefGoogle 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. Brain Research. Cognitive Brain Research 17, 75–82.Google Scholar
Sripada, CS, Angstadt, M, Banks, S, Nathan, PJ, Liberzon, I, Phan, KL (2009). Deciding who to trust: functional neuroimaging of mentalizing during the trust game in social anxiety disorder. Neuroreport 20, 984–989.CrossRefGoogle Scholar
Stefanis, NC, Hanssen, M, Smirnis, NK, Avramopoulos, DA, Evdokimidis, IK, Stefanis, CN, Verdoux, H, van Os, J (2002). Evidence that three dimensions of psychosis have a distribution in the general population. Psychological Medicine 32, 347–358.Google Scholar
Tankersley, D, Stowe, CJ, Huettel, SA (2007). Altruism is associated with an increased neural response to agency. Nature Neuroscience 10, 150–151.CrossRefGoogle ScholarPubMed
Tsuang, MT, Stone, WS, Faraone, SV (1999). Schizophrenia: a review of genetic studies. Harvard Review of Psychiatry 7, 185–207.Google Scholar
van den Bos, W, van Dijk, E, Westenberg, M, Rombouts, SA, Crone, EA (2009). What motivates repayment? Neural correlates of reciprocity in the Trust Game. Social Cognitive and Affective Neuroscience 4, 294–304.Google Scholar
van den Bos, W, Westenberg, M, Van Dijk, E, Crone, EA (2010). Development of trust and reciprocity in adolescence. Cognitive Development 25, 90–102.Google Scholar
Versmissen, D, Janssen, I, Myin-Germeys, I, Mengelers, R, Campo, JA, van Os, J, Krabbendam, L (2008). Evidence for a relationship between mentalising deficits and paranoia over the psychosis continuum. Schizophrenia Research 99, 103–110.CrossRefGoogle ScholarPubMed
Supplementary material: File

Gromann Supplementary Material

Supplementary Material

Download Gromann Supplementary Material(File)
File 76.3 KB