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The Journal of Neuroscience, October 15, 2008, 28(42):10509-10516; doi:10.1523/JNEUROSCI.2807-08.2008

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Behavioral/Systems/Cognitive
Blocking Central Opiate Function Modulates Hedonic Impact and Anterior Cingulate Response to Rewards and Losses

Predrag Petrovic,^1,2 Burkhard Pleger,¹ Ben Seymour,¹ Stefan Klöppel,¹ Benedetto De Martino,¹ Hugo Critchley,¹ and Raymond J. Dolan¹

¹Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3BG, United Kingdom, and ²Department of Clinical Neuroscience, Karolinska Institute, 17176 Stockholm, Sweden

Correspondence should be addressed to Predrag Petrovic, Cognitive Neurophysiology, MR Research Center, Department of Clinical Neuroscience, N-8, Karolinska Hospital, 17176 Stockholm, Sweden. Email: predrag.petrovic{at}ki.se

Reward processing is linked to specific neuromodulatory systems with a dopaminergic contribution to reward learning and motivational drive being well established. Neuromodulatory influences on hedonic responses to actual receipt of reward, or punishment, referred to as experienced utility are less well characterized, although a link to the endogenous opioid system is suggested. Here, in a combined functional magnetic resonance imaging–psychopharmacological investigation, we used naloxone to block central opioid function while subjects performed a gambling task associated with rewards and losses of different magnitudes, in which the mean expected value was always zero. A graded influence of naloxone on reward outcome was evident in an attenuation of pleasure ratings for larger reward outcomes, an effect mirrored in attenuation of brain activity to increasing reward magnitude in rostral anterior cingulate cortex. A more striking effect was seen for losses such that under naloxone all levels of negative outcome were rated as more unpleasant. This hedonic effect was associated with enhanced activity in anterior insula and caudal anterior cingulate cortex, areas implicated in aversive processing. Our data indicate that a central opioid system contributes to both reward and loss processing in humans and directly modulates the hedonic experience of outcomes.

Key words: naloxone; opioid; reward; fMRI; cingulate; insula; human

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Received June 18, 2008; revised July 12, 2008; accepted July 28, 2008.

Correspondence should be addressed to Predrag Petrovic, Cognitive Neurophysiology, MR Research Center, Department of Clinical Neuroscience, N-8, Karolinska Hospital, 17176 Stockholm, Sweden. Email: predrag.petrovic{at}ki.se

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