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Influence of Dopaminergically Mediated Reward on Somatosensory Decision-Making

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  • Burkhard Pleger
  • Christian C Ruff
  • Felix Blankenburg
  • Stefan Klöppel
  • Jon Driver
  • Raymond J Dolan

Abstract

This pharmacological fMRI study shows that during reward-based sensory decision-making, dopamine is crucially involved in reward-related modulation of human primary sensory cortex.Reward-related dopaminergic influences on learning and overt behaviour are well established, but any influence on sensory decision-making is largely unknown. We used functional magnetic resonance imaging (fMRI) while participants judged electric somatosensory stimuli on one hand or other, before being rewarded for correct performance at trial end via a visual signal, at one of four anticipated financial levels. Prior to the procedure, participants received either placebo (saline), a dopamine agonist (levodopa), or an antagonist (haloperidol). Principal findings: higher anticipated reward improved tactile decisions. Visually signalled reward reactivated primary somatosensory cortex for the judged hand, more strongly for higher reward. After receiving a higher reward on one trial, somatosensory activations and decisions were enhanced on the next trial. These behavioural and neural effects were all enhanced by levodopa and attenuated by haloperidol, indicating dopaminergic dependency. Dopaminergic reward-related influences extend even to early somatosensory cortex and sensory decision-making.Author Summary: The rewards one receives during decision-making has a profound impact on learning. Much recent interest has focused on the role of the neurotransmitter dopamine in the basal ganglia for influencing learning and behaviour. Here, we ask whether reward can influence low-level sensory processing, for instance in primary sensory cortex, and how dopamine mediates this process. We show in humans that dopamine level, as manipulated with a dopamine agonist and antagonist in a double-blind placebo-controlled design, is involved in reward modulation of primary somatosensory cortex. Higher anticipated reward improved tactile decisions, and receipt of visual reward signals reactivated primary somatosensory cortex for the judged hand as measured using functional neuroimaging. After receiving a higher reward on one trial, somatosensory activations and decisions were enhanced on the next trial, suggesting that reward outcome provides a form of teaching signal that may be fed back to task-relevant sensory cortex. All these behavioural and neural effects of reward on somatosensory decision-making were strongly modulated by the availability of dopamine as the mediating neurotransmitter. These findings raise the tantalising new possibility that reward manipulations in conjunction with dopaminergic drugs might be used to enhance pathologically deficient or lapsed sensory processes, analogous to how rewards can be used to shape or correct behaviour.

Suggested Citation

  • Burkhard Pleger & Christian C Ruff & Felix Blankenburg & Stefan Klöppel & Jon Driver & Raymond J Dolan, 2009. "Influence of Dopaminergically Mediated Reward on Somatosensory Decision-Making," PLOS Biology, Public Library of Science, vol. 7(7), pages 1-10, July.
  • Handle: RePEc:plo:pbio00:1000164
    DOI: 10.1371/journal.pbio.1000164
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    References listed on IDEAS

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    1. Pascale Waelti & Anthony Dickinson & Wolfram Schultz, 2001. "Dopamine responses comply with basic assumptions of formal learning theory," Nature, Nature, vol. 412(6842), pages 43-48, July.
    2. Michael L. Platt & Paul W. Glimcher, 1999. "Neural correlates of decision variables in parietal cortex," Nature, Nature, vol. 400(6741), pages 233-238, July.
    3. P. Read Montague & Steven E. Hyman & Jonathan D. Cohen, 2004. "Computational roles for dopamine in behavioural control," Nature, Nature, vol. 431(7010), pages 760-767, October.
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    1. Mkael Symmonds & Nicholas D Wright & Elizabeth Fagan & Raymond J Dolan, 2013. "Assaying the Effect of Levodopa on the Evaluation of Risk in Healthy Humans," PLOS ONE, Public Library of Science, vol. 8(7), pages 1-10, July.

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