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Chronic alcohol intake abolishes the relationship between dopamine synthesis capacity and learning signals in the ventral striatum

  • Drugs of abuse elicit dopamine release in the ventral striatum, possibly biasing dopamine-driven reinforcement learning towards drug-related reward at the expense of non-drug-related reward. Indeed, in alcohol-dependent patients, reactivity in dopaminergic target areas is shifted from non-drug-related stimuli towards drug-related stimuli. Such hijacked' dopamine signals may impair flexible learning from non-drug-related rewards, and thus promote craving for the drug of abuse. Here, we used functional magnetic resonance imaging to measure ventral striatal activation by reward prediction errors (RPEs) during a probabilistic reversal learning task in recently detoxified alcohol-dependent patients and healthy controls (N=27). All participants also underwent 6-[F-18]fluoro-DOPA positron emission tomography to assess ventral striatal dopamine synthesis capacity. Neither ventral striatal activation by RPEs nor striatal dopamine synthesis capacity differed between groups. However, ventral striatal coding of RPEs correlated inversely withDrugs of abuse elicit dopamine release in the ventral striatum, possibly biasing dopamine-driven reinforcement learning towards drug-related reward at the expense of non-drug-related reward. Indeed, in alcohol-dependent patients, reactivity in dopaminergic target areas is shifted from non-drug-related stimuli towards drug-related stimuli. Such hijacked' dopamine signals may impair flexible learning from non-drug-related rewards, and thus promote craving for the drug of abuse. Here, we used functional magnetic resonance imaging to measure ventral striatal activation by reward prediction errors (RPEs) during a probabilistic reversal learning task in recently detoxified alcohol-dependent patients and healthy controls (N=27). All participants also underwent 6-[F-18]fluoro-DOPA positron emission tomography to assess ventral striatal dopamine synthesis capacity. Neither ventral striatal activation by RPEs nor striatal dopamine synthesis capacity differed between groups. However, ventral striatal coding of RPEs correlated inversely with craving in patients. Furthermore, we found a negative correlation between ventral striatal coding of RPEs and dopamine synthesis capacity in healthy controls, but not in alcohol-dependent patients. Moderator analyses showed that the magnitude of the association between dopamine synthesis capacity and RPE coding depended on the amount of chronic, habitual alcohol intake. Despite the relatively small sample size, a power analysis supports the reported results. Using a multimodal imaging approach, this study suggests that dopaminergic modulation of neural learning signals is disrupted in alcohol dependence in proportion to long-term alcohol intake of patients. Alcohol intake may perpetuate itself by interfering with dopaminergic modulation of neural learning signals in the ventral striatum, thus increasing craving for habitual drug intake.show moreshow less

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Metadaten
Author:Lorenz Deserno, Anne Beck, Quentin J. M. Huys, Robert C. Lorenz, Ralph Buchert, Hans-Georg Buchholz, Michail Plotkin, Yoshitaka Kumakara, Paul Cumming, Hans-Jochen Heinze, Anthony A. Grace, Michael Armin RappORCiDGND, Florian Schlagenhauf, Andreas Heinz
DOI:https://doi.org/10.1111/ejn.12802
ISSN:0953-816X (print)
ISSN:1460-9568 (online)
Pubmed Id:http://www.ncbi.nlm.nih.gov/pubmed?term=25546072
Parent Title (English):European journal of neuroscience
Publisher:Wiley-Blackwell
Place of publication:Hoboken
Document Type:Article
Language:English
Year of first Publication:2015
Year of Completion:2015
Release Date:2017/03/27
Tag:PET; alcohol addiction; dopamine; fMRI; prediction error
Volume:41
Issue:4
Pagenumber:10
First Page:477
Last Page:486
Funder:German Research Foundation [DFG HE2597/4-3, DFG HE2597/7-3, DFG Exc 257, DFG HE2597/14-1, DFG FOR 1617, DFG SCHL 1968/1-1]; German Ministry for Education and Research [BMBF 01QG87164, 01GS08159, 01ZX1311E]
Organizational units:Humanwissenschaftliche Fakultät / Institut für Sportwissenschaft
Peer Review:Referiert