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Original Investigation
Meta-analysis
February 1, 2017

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

Author Affiliations
  • 1Behavioural Science Institute, Radboud University, Nijmegen, the Netherlands
  • 2Radboud University Medical Centre, Department of Psychiatry, Nijmegen Institute for Scientist Practitioners in Addiction, Nijmegen, the Netherlands
  • 3Department of Psychiatry and Psychotherapy, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
  • 4Department of Psychiatry, Academic Medical Center, Amsterdam, the Netherlands
  • 5Donders Institute for Brain, Cognition, and Behaviour, Radboud University, Nijmegen, the Netherlands
JAMA Psychiatry. Published online February 1, 2017. doi:10.1001/jamapsychiatry.2016.3084
Key Points

Question  What are the nature and direction of pathophysiologic reward-processing disruptions in the brain during anticipation and outcome notification of monetary rewards in individuals with addiction to substances and gambling?

Findings  In this image-based meta-analysis of neuroimaging studies, striatal activation during reward anticipation was decreased among individuals with addiction compared with those in control groups. During reward outcome, substance-addicted individuals showed increased activation in the ventral striatum, whereas gambling-addicted individuals showed decreased activation in the dorsal striatum, compared with controls.

Meaning  These findings provide evidence for both reward deficiency and learning-deficit theories in addiction.

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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