Cited by 402Neurotransmitter Receptor Influence on BehaviorGambling Behavior and TreatmentsNeural and Behavioral Psychology Studies

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Disruption of Reward Processing in Addiction: An Image-Based Meta-analysis of Functional Magnetic Resonance Imaging Studies

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Luijten, Maartje, Schellekens, Arnt F., Kühn, Simone, Machielse, Marise W. J., Sescousse, Guillaume·2017·JAMA Psychiatry

DOI 10.1001/jamapsychiatry.2016.3084

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Abstract

IMPORTANCE: Disrupted reward processing, mainly driven by striatal dysfunction, is a key characteristic of addictive behaviors. However, functional magnetic resonance imaging (fMRI) studies have reported conflicting results, with both hypoactivations and hyperactivations during anticipation and outcome notification of monetary rewards in addiction. OBJECTIVE: To determine the nature and direction of reward-processing disruptions during anticipation and outcome notification of monetary rewards in individuals with addiction using image-based meta-analyses of fMRI studies. DATA SOURCES: Relevant publications were identified searching PubMed (inclusion until March 2015) using the following terms: reward, fMRI, substance use, cocaine, cannabis, opiates, alcohol, nicotine, smokers, gambling, gamblers, gaming, and gamers. Authors of included articles were contacted to obtain statistical fMRI maps. STUDY SELECTION: Inclusion criteria: reward task involving monetary reward anticipation and/or outcome; participants showing addictive behaviors; and healthy control group. Exclusion criteria: participants aged younger than 18 years; recreational substance use or gambling; participants at risk for addictive behaviors; and studies using the same patient data as other included studies. DATA EXTRACTION AND SYNTHESIS: Study procedures were conducted in accordance with the Meta-analysis of Observational Studies in Epidemiology guidelines. Using Seed-based d Mapping software, meta-analyses were performed using random-effect nonparametric statistics with group whole brain T-maps from individual studies as input. Analyses were performed across all addictions and for substance and gambling addictions separately. MAIN OUTCOMES AND MEASURES: Group differences (individuals with addiction vs control individuals) in reward-related brain activation during reward anticipation and outcome using fMRI (planned before data collection). RESULTS: Twenty-five studies were included in the meta-analysis, representing 643 individuals with addictive behaviors and 609 healthy control individuals. During reward anticipation, individuals with substance and gambling addictions showed decreased striatal activation compared with healthy control individuals. During reward outcome, individuals with substance addiction showed increased activation in the ventral striatum, whereas individuals with gambling addiction showed decreased activation in the dorsal striatum compared with healthy control individuals. CONCLUSIONS AND RELEVANCE: Striatal hypoactivation in individuals with addiction during reward anticipation and in individuals with gambling addiction during reward outcome is in line with the reward-deficiency theory of addiction. However, the combination of hypoactivation during reward anticipation and hyperactivation during reward outcome in the striatum of individuals with substance addiction may be explained using learning-deficit theory.

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Authors: Luijten, M., Schellekens, A. F., Kühn, S., Machielse, M. W. J., & Sescousse, G.
Affiliations: Radboud University Nijmegen (NL)
Radboud University Medical Center (NL)
University Medical Center Hamburg-Eppendorf (DE)
Amsterdam UMC Location University of Amsterdam (NL)
Corresponding author: Luijten, Maartje
ORCID: Luijten, Maartje
Schellekens, Arnt F.
Kühn, Simone
Sescousse, Guillaume
Venue: JAMA Psychiatry
Publisher: American Medical Association (AMA)
Published: 2017-04-01
Volume: 74
Issue: 4
Pages: 387
ISSN: 2168-622X (ISSN-L)
DOI: 10.1001/jamapsychiatry.2016.3084
OpenAlex: W2584830124
Cited by: 402
References: 81
Citations by year: 2026: 44 · 2025: 37 · 2024: 24 · 2023: 43 · 2022: 47 · 2021: 48 · 2020: 55 · 2019: 49 · 2018: 40 · 2017: 14
FWCI: 5.31
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: JAMA Psychiatry (publishedVersion)
PubMed (publishedVersion)
Radboud Repository (Radboud University) (submittedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Social Sciences › Psychology › Clinical Psychology › Gambling Behavior and Treatments
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: reward processing, addiction, striatal dysfunction, reward anticipation, reward outcome, monetary rewards, substance use disorders, gambling addiction, ventral striatum, dorsal striatum, brain activation
MeSH terms: Adult, Brain, Brain Mapping, Female, Gambling, Humans, Image Interpretation, Computer-Assisted, Magnetic Resonance Imaging, Male, Motivation, Reference Values, Reward, Software, Substance-Related Disorders, Anticipation, Psychological

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Disruption of Reward Processing in Addiction: An Image-Based Meta-analysis of Functional Magnetic Resonance Imaging Studies

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