Brain Advance Access originally published online on July 11, 2007
Brain 2007 130(9):2412-2424; doi:10.1093/brain/awm147
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Ageing and early-stage Parkinson's disease affect separable neural mechanisms of mesolimbic reward processing
1Leibniz-Institute for Neurobiology, Brenneckestr. 6, Magdeburg 39118 2Department of Neurology II and Center for Advanced Imaging, Otto von Guericke University, Magdeburg, Germany 3Wellcome Department of Imaging Neuroscience, Institute of Neurology, University College London and 4Institute of Cognitive Neuroscience, University College London, London, UK
Correspondence to: Emrah Düzel, Institute of Cognitive Neuroscience, University College London, Alexandra House, Queen Square, London, UK E-mail: e.duzel{at}icn.ucl.ac.uk
The ability to learn stimulus-reward associations on the basis of reward prediction errors critically depends on the mesolimbic dopaminergic system including the dopaminergic midbrain and the ventral striatum. It is known that healthy elderly and patients with Parkinson's disease are less proficient than healthy young adults in learning stimulus-reward contingencies, but it is unclear whether this is due to dysfunctional mesolimbic reward prediction or due to deficiency in processing the rewards per se. We used a well-established event-related fMRI reward-prediction paradigm to address this question. Young adults showed the well-replicated pattern of midbrain and ventral striatal activation for stimuli that predicted monetary reward when compared with stimuli that predicted neutral feedback. Also, as expected, the predicted reward feedback itself did not elicit a mesolimbic response. Healthy elderly subjects and unmedicated early-stage idiopathic Parkinson's disease patients showed the opposite pattern with an absent mesolimbic reward prediction response, but mesolimbic activation to the reward feedback itself. This suggests that the healthy elderly and Parkinson's disease patients were less proficient in learning the predictive value of the reward cues despite preserved mesolimbic processing of reward prediction errors. Parkinson's disease patients additionally displayed a relatively increased response of the anterior cingulate during reward feedback processing and diminished functional connectivity of the midbrain and ventral striatum. Our results are compatible with existing behavioural evidence that both groups exhibit a particularly pronounced deficit in learning from positive feedback and support the view that a tendency to underestimate expected values of reward cues might underlie this deficit. Furthermore, alterations in reward processing in Parkinson's disease extend beyond accelerated ageing effects and include altered connectivity within the mesolimbic system.
Key Words: ageing; Parkinson's disease; reward; expected value; accumbens; fMRI; functional connectivity
Abbreviations: CS+, conditioned (i.e. reward-predicting) stimulus; DA, dopamine; NAcc, nucleus accumbens; PD, Parkinson's disease; PFC, prefrontal cortex; SN, substantia nigra; VTA, ventral tegmental area
Received January 8, 2007. Revised April 29, 2007. Accepted May 30, 2007.
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