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The Journal of Neuroscience, February 4, 2009, 29(5):1538-1543; doi:10.1523/JNEUROSCI.4467-08.2009

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Behavioral/Systems/Cognitive
Striatal Dopamine Predicts Outcome-Specific Reversal Learning and Its Sensitivity to Dopaminergic Drug Administration

Roshan Cools,¹ Michael J. Frank,^3,4 Sasha E. Gibbs,^2,5 Asako Miyakawa,² William Jagust,^2,6 and Mark D'Esposito²

¹Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen Medical Centre, 6500 HB Nijmegen, The Netherlands, ²Helen Wills Neuroscience Institute, University of California, Berkeley, California 94720-3192, Departments of ³Cognitive and Linguistic Sciences and ⁴Psychology, Brown University, Providence, Rhode Island 02912, ⁵Department of Psychology, Stanford University, Stanford, California 94305, and ⁶Lawrence Berkeley National Laboratory, Berkeley, California 94720

Correspondence should be addressed to Roshan Cools, Donders Centre for Cognitive Neuroimaging, Kapittelweg 29, 6500 HB Nijmegen, The Netherlands. Email: roshan.cools{at}donders.ru.nl

Individual variability in reward-based learning has been ascribed to quantitative variation in baseline levels of striatal dopamine. However, direct evidence for this pervasive hypothesis has hitherto been unavailable. We demonstrate that individual differences in reward-based reversal learning reflect variation in baseline striatal dopamine synthesis capacity, as measured with neurochemical positron emission tomography. Subjects with high baseline dopamine synthesis in the striatum showed relatively better reversal learning from unexpected rewards than from unexpected punishments, whereas subjects with low baseline dopamine synthesis in the striatum showed the reverse pattern. In addition, baseline dopamine synthesis predicted the direction of dopaminergic drug effects. The D₂ receptor agonist bromocriptine improved reward-based relative to punishment-based reversal learning in subjects with low baseline dopamine synthesis capacity, while impairing it in subjects with high baseline dopamine synthesis capacity in the striatum. Finally, this pattern of drug effects was outcome-specific, and driven primarily by drug effects on punishment-, but not reward-based reversal learning. These data demonstrate that the effects of D₂ receptor stimulation on reversal learning in humans depend on task demands and baseline striatal dopamine synthesis capacity.

Key words: dopamine; reward; punishment; striatum; PET; learning

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Received Sept. 18, 2008; revised Jan. 7, 2009; accepted Jan. 8, 2009.

Correspondence should be addressed to Roshan Cools, Donders Centre for Cognitive Neuroimaging, Kapittelweg 29, 6500 HB Nijmegen, The Netherlands. Email: roshan.cools{at}donders.ru.nl

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