Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-19T04:14:28.430Z Has data issue: false hasContentIssue false

Intact striatal dopaminergic modulation of reward learning and daily-life reward-oriented behavior in first-degree relatives of individuals with psychotic disorder

Published online by Cambridge University Press:  13 December 2017

Zuzana Kasanova*
Affiliation:
Center for Contextual Psychiatry, Department of Neurosciences, KU Leuven – Leuven University, Leuven, Belgium
Jenny Ceccarini
Affiliation:
Division of Nuclear Medicine and Molecular Imaging, Department of Imaging & Pathology, University Hospitals Leuven, Leuven, Belgium
Michael J. Frank
Affiliation:
Department of Cognitive, Linguistic and Psychological Sciences, Brown University, Providence, USA
Thérèse van Amelsvoort
Affiliation:
Department of Psychiatry and Neuropsychology, Maastricht University, Maastricht, The Netherlands
Jan Booij
Affiliation:
Department of Nuclear Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
Esther van Duin
Affiliation:
Department of Psychiatry and Neuropsychology, Maastricht University, Maastricht, The Netherlands
Henrietta Steinhart
Affiliation:
Center for Contextual Psychiatry, Department of Neurosciences, KU Leuven – Leuven University, Leuven, Belgium Department of Psychiatry and Neuropsychology, Maastricht University, Maastricht, The Netherlands
Thomas Vaessen
Affiliation:
Center for Contextual Psychiatry, Department of Neurosciences, KU Leuven – Leuven University, Leuven, Belgium Department of Psychiatry and Neuropsychology, Maastricht University, Maastricht, The Netherlands
Alexander Heinzel
Affiliation:
Department of Nuclear Medicine, University Hospital RWTH Aachen University, Aachen, Germany
Felix Mottaghy
Affiliation:
Department of Nuclear Medicine, University Hospital RWTH Aachen University, Aachen, Germany
Inez Myin-Germeys
Affiliation:
Center for Contextual Psychiatry, Department of Neurosciences, KU Leuven – Leuven University, Leuven, Belgium
*
Author for correspondence: Zuzana Kasanova, E-mail: zuzana.kasanova@kuleuven.be

Abstract

Background

Abnormalities in reward learning in psychotic disorders have been proposed to be linked to dysregulated subcortical dopaminergic (DA) neurotransmission, which in turn is a suspected mechanism for predisposition to psychosis. We therefore explored the striatal dopaminergic modulation of reward processing and its behavioral correlates in individuals at familial risk for psychosis.

Methods

We performed a DA D2/3 receptor [18F]fallypride positron emission tomography scan during a probabilistic reinforcement learning task in 16 healthy first-degree relatives of patients with psychosis and 16 healthy volunteers, followed by a 6-day ecological momentary assessment study capturing reward-oriented behavior in the everyday life.

Results

We detected significant reward-induced DA release in bilateral caudate, putamen and ventral striatum of both groups, with no group differences in its magnitude nor spatial extent. In both groups alike, greater extent of reward-induced DA release in all regions of interest was associated with better performance in the task, as well as in greater tendency to be engaged in reward-oriented behavior in the daily life.

Conclusions

These findings suggest intact striatal dopaminergic modulation of reinforcement learning and reward-oriented behavior in individuals with familial predisposition to psychosis. Furthermore, this study points towards a key link between striatal reward-related DA release and pursuit of ecologically relevant rewards.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2017 

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

Bigdeli, TB, Ripke, S, Bacanu, SA, Lee, SH, Wray, NR, Gejman, PV et al. (2016) Genome-wide association study reveals greater polygenic loading for schizophrenia in cases with a family history of illness. American Journal of Medical Genetics. Part B: Neuropsychiatric Genetics 171B, 276289.Google Scholar
Boehme, R, Deserno, L, Gleich, T, Katthagen, T, Pankow, A, Behr, J et al. (2015) Aberrant salience is related to reduced reinforcement learning signals and elevated dopamine synthesis capacity in healthy adults. Journal of Neuroscience 35, 1010310111.Google Scholar
Ceccarini, J, Vrieze, E, Koole, M, Muylle, T, Bormans, G, Claes, S et al. (2012) Optimized in vivo detection of dopamine release using 18F-fallypride PET. Journal of Nuclear Medicine 53, 15651572.Google Scholar
Christian, BT, Lehrer, DS, Shi, B, Narayanan, TK, Strohmeyer, PS, Buchsbaum, MS et al. (2006) Measuring dopamine neuromodulation in the thalamus: using [F-18]fallypride PET to study dopamine release during a spatial attention task. NeuroImage 31, 139152.Google Scholar
Decker, JH, Otto, AR, Daw, ND, and Hartley, CA (2016) From creatures of habit to goal-directed learners: tracking the developmental emergence of model-based reinforcement learning. Psychological Science 27, 848858.Google Scholar
de Leeuw, M, Kahn, RS, and Vink, M (2015) Fronto-striatal dysfunction during reward processing in unaffected siblings of schizophrenia patients. Schizophrenia Bulletin 41, 94103.Google Scholar
Deserno, L, Huys, QJ, Boehme, R, Buchert, R, Heinze, HJ, Grace, AA et al. (2015) Ventral striatal dopamine reflects behavioral and neural signatures of model-based control during sequential decision making. Proceedings of the National Academy of Sciences of the USA 112, 15951600.Google Scholar
Frank, MJ, Seeberger, LC, and O'Reilly, RC (2004) By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science 306, 19401943.Google Scholar
Gold, JM, Waltz, JA, Matveeva, TM, Kasanova, Z, Strauss, GP, Herbener, ES et al. (2012) Negative symptoms and the failure to represent the expected reward value of actions: behavioral and computational modeling evidence. Archives of General Psychiatry 69, 129138.Google Scholar
Grimm, O, Heinz, A, Walter, H, Kirsch, P, Erk, S, Haddad, L et al. (2014) Striatal response to reward anticipation: evidence for a systems-level intermediate phenotype for schizophrenia. JAMA Psychiatry 71, 531539.Google Scholar
Hanssen, E, van der Velde, J, Gromann, PM, Shergill, SS, de Haan, L, Bruggeman, R et al. (2015) Neural correlates of reward processing in healthy siblings of patients with schizophrenia. Frontiers in Human Neuroscience 9, 504.Google Scholar
Hernaus, D, Collip, D, Kasanova, Z, Winz, O, Heinzel, A, van Amelsvoort, T et al. (2015) No evidence for attenuated stress-induced extrastriatal dopamine signaling in psychotic disorder. Translational Psychiatry 5, e547.Google Scholar
Huttunen, J, Heinimaa, M, Svirskis, T, Nyman, M, Kajander, J, Forsback, S et al. (2008) Striatal dopamine synthesis in first-degree relatives of patients with schizophrenia. Biological Psychiatry 63, 114117.Google Scholar
Kasanova, Z, Ceccarini, J, Frank, MJ, Amelsvoort, TV, Booij, J, Heinzel, A et al. (2017) Striatal dopaminergic modulation of reinforcement learning predicts reward-oriented behavior in daily life. Biological Psychology 127, 19.Google Scholar
Kuepper, R, Ceccarini, J, Lataster, J, van Os, J, van Kroonenburgh, M, van Gerven, JM et al. (2013) Delta-9-tetrahydrocannabinol-induced dopamine release as a function of psychosis risk: 18F-fallypride positron emission tomography study. PLoS ONE 8, e70378.Google Scholar
Lancaster, TM, Ihssen, N, Brindley, LM, Tansey, KE, Mantripragada, K, O'Donovan, MC et al. (2016) Associations between polygenic risk for schizophrenia and brain function during probabilistic learning in healthy individuals. Human Brain Mapping 37, 491500.Google Scholar
Lataster, J, Collip, D, Ceccarini, J, Haas, D, Booij, L, van Os, J et al. (2011) Psychosocial stress is associated with in vivo dopamine release in human ventromedial prefrontal cortex: a positron emission tomography study using [(1)(8)F]fallypride. NeuroImage 58, 10811089.Google Scholar
Myin-Germeys, I, Birchwood, M, and Kwapil, T (2011) From environment to therapy in psychosis: a real-world momentary assessment approach. Schizophrenia Bulletin 37, 244247.Google Scholar
Nurnberger, JI, Blehar, MC, Kaufmann, CA, York-Cooler, C, Simpson, SG, Harkavy-Friedman, J et al. (1994) Diagnostic interview for genetic studies. Rationale, unique features, and training. NIMH Genetics Initiative. Archives of General Psychiatry 51, 849859; discussion 863–864.Google Scholar
Pessiglione, M, Seymour, B, Flandin, G, Dolan, RJ, and Frith, CD (2006) Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 442, 10421045.Google Scholar
Poline, JB, Worsley, KJ, Evans, AC, and Friston, KJ (1997) Combining spatial extent and peak intensity to test for activations in functional imaging. NeuroImage 5, 8396.Google Scholar
Schultz, W (2010) Dopamine signals for reward value and risk: basic and recent data. Behavioral and Brain Functions 6, 24.Google Scholar
Schultz, W (2016) Dopamine reward prediction-error signalling: a two-component response. Nature Reviews: Neuroscience 17, 183195.Google Scholar
Schultz, W, Dayan, P, and Montague, PR (1997) A neural substrate of prediction and reward. Science 275, 15931599.Google Scholar
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E et al. (1998) The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59(Suppl. 20), 2233; quiz 34–57.Google Scholar
Shotbolt, P, Stokes, PR, Owens, SF, Toulopoulou, T, Picchioni, MM, Bose, SK et al. (2011) Striatal dopamine synthesis capacity in twins discordant for schizophrenia. Psychological Medicine 41, 23312338.Google Scholar
Strauss, GP, Frank, MJ, Waltz, JA, Kasanova, Z, Herbener, ES, and Gold, JM (2011) Deficits in positive reinforcement learning and uncertainty-driven exploration are associated with distinct aspects of negative symptoms in schizophrenia. Biological Psychiatry 69, 424431.Google Scholar
Strauss, GP, Waltz, JA, and Gold, JM (2014) A review of reward processing and motivational impairment in schizophrenia. Schizophrenia Bulletin 40(Suppl. 2), S107S116.Google Scholar
Vrieze, E, Ceccarini, J, Pizzagalli, DA, Bormans, G, Vandenbulcke, M, Demyttenaere, K et al. (2013) Measuring extrastriatal dopamine release during a reward learning task. Human Brain Mapping 34, 575586.Google Scholar