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


METHODS
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.


METHODS
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.


METHODS
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.


METHODS
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
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.
Behavioural Science Institute, Radboud University, Nijmegen, the Netherlands.
Maartje
M
Luijten
Radboud University Medical Centre, Department of Psychiatry, Nijmegen Institute for Scientist Practitioners in Addiction, Nijmegen, the Netherlands.
Arnt F
AF
Schellekens
Department of Psychiatry and Psychotherapy, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
Simone
S
Kühn
Department of Psychiatry, Academic Medical Center, Amsterdam, the Netherlands.
Marise W J
MW
Machielse
Donders Institute for Brain, Cognition, and Behaviour, Radboud University, Nijmegen, the Netherlands.
Guillaume
G
Sescousse
D000328:Adult; D059031:Anticipation, Psychological / Q000502:physiology*; D001921:Brain / Q000000981:diagnostic imaging* / Q000503:physiopathology*; D001931:Brain Mapping; D005260:Female; D005715:Gambling / Q000000981:diagnostic imaging* / Q000503:physiopathology* / Q000523:psychology; D006801:Humans; D007090:Image Interpretation, Computer-Assisted; D008279:Magnetic Resonance Imaging; D008297:Male; D009042:Motivation / Q000502:physiology; D012016:Reference Values; D012201:Reward; D012984:Software; D019966:Substance-Related Disorders / Q000000981:diagnostic imaging* / Q000503:physiopathology* / Q000523:psychology