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Victory is its own reward: oxytocin increases costly competitive behavior in schizophrenia

Published online by Cambridge University Press:  04 April 2019

Ellen R. Bradley Open the ORCID record for Ellen R. Bradley [Opens in a new window] ,
Johanna Brustkern ,
Lize De Coster ,
Wouter van den Bos ,
Samuel M. McClure ,
Alison Seitz  and
Joshua D. Woolley
Ellen R. Bradley*
Affiliation:
Department of Psychiatry, University of California, San Francisco, CA94110, USA Mental Health Service, San Francisco Veterans Administration Medical Center, San Francisco, CA, USA
Johanna Brustkern
Affiliation:
Department of Psychology, University of Freiburg, Freiburg, Germany
Lize De Coster
Affiliation:
Department of Psychiatry, University of California, San Francisco, CA94110, USA Mental Health Service, San Francisco Veterans Administration Medical Center, San Francisco, CA, USA
Wouter van den Bos
Affiliation:
Center for Adaptive Rationality, Max Planck Institute for Human Development, Berlin, Germany
Samuel M. McClure
Affiliation:
Department of Psychology, Arizona State University, TempeAZ, USA
Alison Seitz
Affiliation:
Department of Psychiatry, University of California, San Francisco, CA94110, USA Mental Health Service, San Francisco Veterans Administration Medical Center, San Francisco, CA, USA
Joshua D. Woolley
Affiliation:
Department of Psychiatry, University of California, San Francisco, CA94110, USA Mental Health Service, San Francisco Veterans Administration Medical Center, San Francisco, CA, USA
*
Author for correspondence: Ellen Bradley, E-mail: [email protected]
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Abstract

Background

Aberrant sensitivity to social reward may be an important contributor to abnormal social behavior that is a core feature of schizophrenia. The neuropeptide oxytocin impacts the salience of social information across species, but its effect on social reward in schizophrenia is unknown.

Methods

We used a competitive economic game and computational modeling to examine behavioral dynamics and oxytocin effects on sensitivity to social reward among 39 men with schizophrenia and 54 matched healthy controls. In a randomized, double-blind study, participants received one dose of oxytocin (40 IU) or placebo and completed a 35-trial Auction Game that quantifies preferences for monetary v. social reward. We analyzed bidding behavior using multilevel linear mixed models and reinforcement learning models.

Results

Bidding was motivated by preferences for both monetary and social reward in both groups, but bidding dynamics differed: patients initially overbid less compared to controls, and across trials, controls decreased their bids while patients did not. Oxytocin administration was associated with sustained overbidding across trials, particularly in patients. This drug effect was driven by a stronger preference for winning the auction, regardless of monetary consequences. Learning rate and response variability did not differ between groups or drug condition, suggesting that differences in bidding derive primarily from differences in the subjective value of social rewards.

Conclusions

Our findings suggest that schizophrenia is associated with diminished motivation for social reward that may be increased by oxytocin administration.

Keywords

Auctionscomputational modelingdecision-makingoxytocinpsychosisreinforcement learningrewardschizophrenia
Type
Original Articles
Information
Psychological Medicine , Volume 50 , Issue 4 , March 2020 , pp. 674 - 682
Copyright
Copyright © Cambridge University Press 2019

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References

Andreasen, NC, Pressler, M, Nopoulos, P, Miller, D and Ho, B-C (2010) Antipsychotic dose equivalents and dose-years: a standardized method for comparing exposure to different drugs. Biological Psychiatry 67, 255–262.CrossRefGoogle ScholarPubMed
Ashenfelter, O and Genesove, D (1992) Testing for price anomalies in real estate auctions.CrossRefGoogle Scholar
Aydogan, G, Furtner, NC, Kern, B, Jobst, A, Müller, N and Kocher, MG (2017) Oxytocin promotes altruistic punishment. Social Cognitive and Affective Neuroscience 12, 1740–1747.CrossRefGoogle ScholarPubMed
Barch, DM, Carter, CS, Gold, JM, Johnson, SL, Kring, AM, MacDonald, AW, Pizzagalli, DA, Ragland, JD, Silverstein, SM and Strauss, ME (2017) Explicit and implicit reinforcement learning across the psychosis spectrum. Journal of Abnormal Psychology 126, 694–711.CrossRefGoogle ScholarPubMed
Bazerman, MH and Samuelson, WF (1983) I won the auction but don't want the prize. Journal of Conflict Resolution 27, 618–634.CrossRefGoogle Scholar
Bitsch, F, Berger, P, Nagels, A, Falkenberg, I and Straube, B (2018) Impaired right temporoparietal junction-hippocampus connectivity in schizophrenia and its relevance for generating representations of other minds. Schizophrenia Bulletin 16, 559.Google Scholar
Boccia, ML, Petrusz, P, Suzuki, K, Marson, L and Pedersen, CA (2013) Immunohistochemical localization of oxytocin receptors in human brain. Neuroscience 253, 155–164.CrossRefGoogle ScholarPubMed
Bora, E, Yücel, M and Allen, NB (2009) Neurobiology of human affiliative behaviour: implications for psychiatric disorders. Current Opinion in Psychiatry 22, 320–325.CrossRefGoogle ScholarPubMed
Bradley, ER and Woolley, JD (2017) Oxytocin effects in schizophrenia: reconciling mixed findings and moving forward. Neuroscience and Biobehavioral Reviews 80, 36–56.CrossRefGoogle ScholarPubMed
Burkner, P-C, Williams, DR, Simmons, TC and Woolley, JD (2017) Intranasal oxytocin may improve high-level social cognition in schizophrenia, but not social cognition or neurocognition in general: a multilevel Bayesian meta-analysis. Schizophrenia Bulletin 43, 1291–1303.CrossRefGoogle ScholarPubMed
Capen, EC, Clapp, RV and Campbell, WM (2013) Competitive bidding in high-risk situations. Journal of Petroleum Technology 23, 641–653.CrossRefGoogle Scholar
Carlsson, A (2006) The neurochemical circuitry of schizophrenia. Pharmacopsychiatry 39 (Suppl 1), S10–S14.CrossRefGoogle ScholarPubMed
Chang, SWC, Barter, JW, Ebitz, RB, Watson, KK and Platt, ML (2012) Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques (Macaca mulatta). Proceedings of the National Academy of Sciences of the United States of America 109, 959–964.CrossRefGoogle Scholar
Collins, AGE, Brown, JK, Gold, JM, Waltz, JA and Frank, MJ (2014) Working memory contributions to reinforcement learning impairments in schizophrenia. Journal of Neuroscience 34, 13747–13756.CrossRefGoogle Scholar
Couture, SM, Penn, DL and Roberts, DL (2006) The functional significance of social cognition in schizophrenia: a review. Schizophrenia Bulletin 32 (Suppl 1), S44–S63.CrossRefGoogle ScholarPubMed
Das, P, Lagopoulos, J, Coulston, CM, Henderson, AF and Malhi, GS (2012) Mentalizing impairment in schizophrenia: a functional MRI study. Schizophrenia Research 134, 158–164.CrossRefGoogle ScholarPubMed
Dölen, G, Darvishzadeh, A, Huang, KW and Malenka, RC (2013). Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 501, 179–184.CrossRefGoogle ScholarPubMed
Dumais, KM, Bredewold, R, Mayer, TE and Veenema, AH (2013). Sex differences in oxytocin receptor binding in forebrain regions: correlations with social interest in brain region- and sex-specific ways. Hormones and Behavior 64, 693–701.CrossRefGoogle ScholarPubMed
Dumais, KM, Kulkarni, PP, Ferris, CF and Veenema, AH (2017). Sex differences in neural activation following different routes of oxytocin administration in awake adult rats. Psychoneuroendocrinology 81, 52–62.CrossRefGoogle ScholarPubMed
Festinger, L (1954) A theory of social comparison processes.CrossRefGoogle Scholar
Fett, A-KJ, Shergill, SS, Joyce, DW, Riedl, A, Strobel, M, Gromann, PM and Krabbendam, L (2012) To trust or not to trust: the dynamics of social interaction in psychosis. Brain 135, 976–984.CrossRefGoogle ScholarPubMed
Fett, AKJ, Shergill, SS and Krabbendam, L (2015) Social neuroscience in psychiatry: unravelling the neural mechanisms of social dysfunction. Psychological Medicine 45, 1145–1165.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M and Williams, J (2002) Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research version, Non-Patient Edition (SCID-I/NP). New York: New York State Psychiatric Biometrics Research.Google Scholar
Freedman, R, Lewis, DA, Michels, R, Pine, DS, Schultz, SK, Tamminga, CA, Gabbard, GO, Gau, SS-F, Javitt, DC, Oquendo, MA, Shrout, PE, Vieta, E and Yager, J (2013) The initial field trials of DSM-5: new blooms and old thorns. American Journal of Psychiatry 170, 1–5.CrossRefGoogle ScholarPubMed
Fudenberg, D (2006) Advancing beyond advances in behavioral economics. Journal of Economic Literature 44, 694–711.CrossRefGoogle Scholar
Fulford, D, Campellone, T and Gard, DE (2018) Social motivation in schizophrenia: how research on basic reward processes informs and limits our understanding. Clinical Psychology Review 63, 12–24.CrossRefGoogle ScholarPubMed
Gard, DE, Kring, AM, Gard, MG, Horan, WP and Green, MF (2007) Anhedonia in schizophrenia: distinctions between anticipatory and consummatory pleasure. Schizophrenia Research 93, 253–260.CrossRefGoogle ScholarPubMed
Gold, JM, Waltz, JA, Prentice, KJ, Morris, SE and Heerey, EA (2008) Reward processing in schizophrenia: a deficit in the representation of value. Schizophrenia Bulletin 34, 835–847.CrossRefGoogle ScholarPubMed
Gold, JM, Strauss, GP, Waltz, JA, Robinson, BM, Brown, JK and Frank, MJ (2013) Negative symptoms of schizophrenia are associated with abnormal effort-cost computations. Biological Psychiatry 74, 130–136.CrossRefGoogle ScholarPubMed
Gordon, I, Jack, A, Pretzsch, CM, Vander Wyk, B, Leckman, JF, Feldman, R and Pelphrey, KA (2016) Intranasal oxytocin enhances connectivity in the neural circuitry supporting social motivation and social perception in children with autism. Scientific Reports 6, 35054.CrossRefGoogle ScholarPubMed
Green, MF, Horan, WP and Lee, J (2015) Social cognition in schizophrenia. Nature Reviews Neuroscience 16, 620–631.CrossRefGoogle ScholarPubMed
Groppe, SE, Gossen, A, Rademacher, L, Hahn, A, Westphal, L, Gründer, G and Spreckelmeyer, KN (2013) Oxytocin influences processing of socially relevant cues in the ventral tegmental area of the human brain. Biological Psychiatry 74, 172–179.CrossRefGoogle ScholarPubMed
Guastella, AJ, Hickie, IB, McGuinness, MM, Otis, M, Woods, EA, Disinger, HM, Chan, H-K, Chen, TF and Banati, RB (2013) Recommendations for the standardisation of oxytocin nasal administration and guidelines for its reporting in human research. Psychoneuroendocrinology 38, 612–625.CrossRefGoogle ScholarPubMed
Hampton, AN, Bossaerts, P and O'Doherty, JP (2008) Neural correlates of mentalizing-related computations during strategic interactions in humans. Proceedings of the National Academy of Sciences of the United States of America 105, 6741–6746.CrossRefGoogle ScholarPubMed
Holt-Lunstad, J, Smith, TB, Baker, M, Harris, T and Stephenson, D (2015) Loneliness and social isolation as risk factors for mortality: a meta-analytic review. Perspectives on Psychological Science 10, 227–237.CrossRefGoogle ScholarPubMed
Hu, J, Qi, S, Becker, B, Luo, L, Gao, S, Gong, Q, Hurlemann, R and Kendrick, KM (2015) Oxytocin selectively facilitates learning with social feedback and increases activity and functional connectivity in emotional memory and reward processing regions. Human Brain Mapping 36, 2132–2146.CrossRefGoogle ScholarPubMed
Huberman, BA, Loch, CH and Önçüler, A (2016) Status as a valued resource. Social Psychology Quarterly 67, 103–114.CrossRefGoogle Scholar
Hung, LW, Neuner, S, Polepalli, JS, Beier, KT, Wright, M, Walsh, JJ, Lewis, EM, Luo, L, Deisseroth, K, Dölen, G and Malenka, RC (2017) Gating of social reward by oxytocin in the ventral tegmental area. Science 357, 1406–1411.CrossRefGoogle ScholarPubMed
Kagel, JH and Levin, D (2009) Common Value Auctions and the Winner's Curse. Princeton, New Jersey: Princeton University Press.CrossRefGoogle Scholar
Kapur, S, Phillips, AG and Insel, TR (2012) Why has it taken so long for biological psychiatry to develop clinical tests and what to do about it? Molecular Psychiatry 17, 1174–1179.CrossRefGoogle Scholar
Kay, SR, Fiszbein, A and Opler, LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.CrossRefGoogle Scholar
Kim, H, Lee, D, Shin, Y-M and Chey, J (2007) Impaired strategic decision making in schizophrenia. Brain Research 1180, 90–100.Google Scholar
Kohli, S, King, MV, Williams, S, Edwards, A, Ballard, TM, Steward, LJ, Alberati, D and Fone, KCF (2018) Oxytocin attenuates phencyclidine hyperactivity and increases social interaction and nucleus accumben dopamine release in rats. Neuropsychopharmacology 53, 65.Google Scholar
Krach, S, Paulus, FM, Bodden, M and Kircher, T (2010) The rewarding nature of social interactions. Frontiers in Behavioral Neuroscience 4, 22. doi: 10.3389/fnbeh.2010.00022.Google ScholarPubMed
Kring, AM and Barch, DM (2014) The motivation and pleasure dimension of negative symptoms: neural substrates and behavioral outputs. European Neuropsychopharmacology 24, 725–736.CrossRefGoogle ScholarPubMed
Lambert, B, Declerck, CH, Boone, C and Parizel, PM (2017) A functional MRI study on how oxytocin affects decision making in social dilemmas: cooperate as long as it pays off, aggress only when you think you can win. Hormones and Behavior 94, 145–152.CrossRefGoogle Scholar
Lee, D (2013) Decision making: from neuroscience to psychiatry. Neuron 78, 233–248.CrossRefGoogle ScholarPubMed
Lee, J, Quintana, J, Nori, P and Green, MF (2011) Theory of mind in schizophrenia: exploring neural mechanisms of belief attribution. Social Neuroscience 6, 569–581.CrossRefGoogle ScholarPubMed
Lee, J, Jimenez, AM, Reavis, EA, Horan, WP, Wynn, JK and Green, MF (2018) Reduced neural sensitivity to social vs nonsocial reward in schizophrenia. Schizophrenia Bulletin 143, 332.Google Scholar
Liu, Z, Zheng, L, Li, L, Xu, J, Cheng, X, Guo, X, Mulcahy, J and Xu, M (2018) Social comparison modulates the neural responses to regret and subsequent risk-taking behavior. Social Cognitive and Affective Neuroscience 13, 1059–1070.CrossRefGoogle ScholarPubMed
Love, TM (2014) Oxytocin, motivation and the role of dopamine. Pharmacology, Biochemistry, and Behavior 119, 49–60.CrossRefGoogle ScholarPubMed
Macdonald, K and Macdonald, TM (2010) The peptide that binds: a systematic review of oxytocin and its prosocial effects in humans. Harvard Review of Psychiatry 18, 1–21.CrossRefGoogle ScholarPubMed
Messick, DM and McClintock, CG (1968) Motivational bases of choice in experimental games. Journal of Experimental Social Psychology 4, 1–25.CrossRefGoogle Scholar
Noritake, A, Ninomiya, T and Isoda, M (2018) Social reward monitoring and valuation in the macaque brain. Nature Neuroscience 64, 906.Google Scholar
Palaniyappan, L, Simmonite, M, White, TP, Liddle, EB and Liddle, PF (2013) Neural primacy of the salience processing system in schizophrenia. Neuron 79, 814–828.CrossRefGoogle Scholar
Paloyelis, Y, Doyle, OM, Zelaya, FO, Maltezos, S, Williams, SC, Fotopoulou, A and Howard, MA (2016) A spatiotemporal profile of in vivo cerebral blood flow changes following intranasal oxytocin in humans. Biological Psychiatry 79, 693–705.CrossRefGoogle ScholarPubMed
Parr, LA (2014) Intranasal oxytocin enhances socially-reinforced learning in rhesus monkeys. Frontiers in Behavioral Neuroscience 8, 278. doi: 10.3389/fnbeh.2014.00278.CrossRefGoogle Scholar
Paulus, MP, Geyer, MA and Braff, DL (1999) Long-range correlations in choice sequences of schizophrenic patients. Schizophrenia Research 35, 69–75.CrossRefGoogle ScholarPubMed
Peñagarikano, O, Lázaro, MT, Lu, X-H, Gordon, A, Dong, H, Lam, HA, Peles, E, Maidment, NT, Murphy, NP and Yang, XW (2015) Exogenous and evoked oxytocin restores social behavior in the Cntnap2 mouse model of autism. Science Translational Medicine 7, 271ra8–271ra8.CrossRefGoogle ScholarPubMed
Pinheiro, J, Bates, D, DebRoy, S, Sarkar, D and EISPACK, HS (2016) R Development Core Team (2016) Nlme: linear and nonlinear mixed effects models. R package version (Version 3.1–128).Google Scholar
Premkumar, P, Fannon, D, Kuipers, E, Simmons, A, Frangou, S and Kumari, V (2008) Emotional decision-making and its dissociable components in schizophrenia and schizoaffective disorder: a behavioural and MRI investigation. Neuropsychologia 46, 2002–2012.CrossRefGoogle ScholarPubMed
Qi, J, Yang, J-Y, Song, M, Li, Y, Wang, F and Wu, C-F (2008) Inhibition by oxytocin of methamphetamine-induced hyperactivity related to dopamine turnover in the mesolimbic region in mice. Naunyn-Schmiedebergs Archives of Pharmacology 376, 441–448.CrossRefGoogle ScholarPubMed
Quintana, DS and Woolley, JD (2016) Intranasal oxytocin mechanisms can be better understood, but its effects on social cognition and behavior are not to be sniffed at. Biological Psychiatry 79, e49–e50.CrossRefGoogle ScholarPubMed
R Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing.Google Scholar
Resnick, SM (1992) Matching for education in studies of schizophrenia. Archives of General Psychiatry 49, 246.CrossRefGoogle ScholarPubMed
Scheele, D, Wille, A, Kendrick, KM, Stoffel-Wagner, B, Becker, B, Güntürkün, O, Maier, W and Hurlemann, R (2013) Oxytocin enhances brain reward system responses in men viewing the face of their female partner. Proceedings of the National Academy of Sciences of the United States of America 110, 20308–20313.CrossRefGoogle ScholarPubMed
Schultz, W (2016) Dopamine reward prediction-error signalling: a two-component response. Nature Reviews Neuroscience 17, 183–195.CrossRefGoogle ScholarPubMed
Shahrokh, DK, Zhang, T-Y, Diorio, J, Gratton, A and Meaney, MJ (2010) Oxytocin–dopamine interactions mediate variations in maternal behavior in the rat. Endocrinology 151, 2276–2286.CrossRefGoogle ScholarPubMed
Shamay-Tsoory, S and Young, LJ (2016) Understanding the oxytocin system and Its relevance to psychiatry. Biological Psychiatry 79, 150–152.CrossRefGoogle ScholarPubMed
Sheremeta, RM (2013) Overbidding and heterogeneous behavior in contest experiments. SSRN Electronic Journal, Available at https://ssrn.comabstract=2197151.CrossRefGoogle Scholar
Slovic, P (1966) Risk-Taking in children: age and Sex differences. Child Development 37, 169.CrossRefGoogle Scholar
Song, Z, Larkin, TE, Malley, MO and Albers, HE (2016) Oxytocin (OT) and arginine-vasopressin (AVP) act on OT receptors and not AVP V1a receptors to enhance social recognition in adult Syrian hamsters (Mesocricetus auratus). Hormones and Behavior 81, 20–27.CrossRefGoogle Scholar
Strathearn, L, Fonagy, P, Amico, J and Montague, PR (2009) Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology 34, 2655–2666.CrossRefGoogle ScholarPubMed
Striepens, N, Kendrick, KM, Hanking, V, Landgraf, R, Wüllner, U, Maier, W and Hurlemann, R (2013) Elevated cerebrospinal fluid and blood concentrations of oxytocin following its intranasal administration in humans. Scientific Reports 3, 3440.CrossRefGoogle ScholarPubMed
Striepens, N, Matusch, A, Kendrick, KM, Mihov, Y, Elmenhorst, D, Becker, B, Lang, M, Coenen, HH, Maier, W, Hurlemann, R and Bauer, A (2014) Oxytocin enhances attractiveness of unfamiliar female faces independent of the dopamine reward system. Psychoneuroendocrinology 39, 74–87.CrossRefGoogle ScholarPubMed
Trezza, V, Campolongo, P and Vanderschuren, LJMJ (2011) Evaluating the rewarding nature of social interactions in laboratory animals. Developmental Cognitive Neuroscience 1, 444–458.CrossRefGoogle ScholarPubMed
Uvnäs-Moberg, K, Alster, P and Svensson, TH (1992) Amperozide and clozapine but not haloperidol or raclopride increase the secretion of oxytocin in rats. Psychopharmacology 109, 473–476.CrossRefGoogle ScholarPubMed
van den Bos, W, Li, J, Lau, T, Maskin, E, Cohen, JD, Montague, PR and McClure, SM (2008) The value of victory: social origins of the winner's curse in common value auctions. Judgment and Decision Making 3, 483–492.Google ScholarPubMed
van den Bos, W, Golka, PJM, Effelsberg, D and McClure, SM (2013 a) Pyrrhic victories: the need for social status drives costly competitive behavior. Frontiers in Neuroscience 7, 189.CrossRefGoogle ScholarPubMed
van den Bos, W, Talwar, A and McClure, SM (2013 b) Neural correlates of reinforcement learning and social preferences in competitive bidding. The Journal of Neuroscience 33, 2137–2146.CrossRefGoogle ScholarPubMed
Waltz, JA, Frank, MJ, Robinson, BM and Gold, JM (2007) Selective reinforcement learning deficits in schizophrenia support predictions from computational models of striatal-cortical dysfunction. Biological Psychiatry 62, 756–764.CrossRefGoogle ScholarPubMed
Young, LJ and Wang, Z (2004) The neurobiology of pair bonding. Nature Neuroscience 7, 1048–1054.CrossRefGoogle ScholarPubMed
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