Ventral-striatal responsiveness during reward anticipation in ADHD and its relation to trait impulsivity in the healthy population: a meta-analytic review of the fMRI literature

Abstract

A review of the existing functional magnetic resonance imaging (fMRI) studies on reward anticipation in patients with attention-deficit/hyperactivity disorder (ADHD) is provided. Meta-analysis showed a significant medium effect size (Cohen's d=0.48-0.58) in terms of ventral-striatal (VS)-hyporesponsiveness in ADHD. Studies on VS-responsiveness and trait impulsivity in the healthy population demonstrate the opposite relationship, i.e. impulsivity-scores positively correlated with VS activation during reward processing. Against the background that ADHD may represent an extreme on a continuum of normal variability, the question arises as to how these contrasting findings can be integrated. We discuss three theoretical approaches, each of which integrates the opposing findings: (1) an inverted-u-shape model; (2) a (genetic) moderator model; and (3) the "unrelated model". We conclude that at the present stage the number of existing studies in the healthy population as well as in ADHD groups is too small for a final answer. Therefore, our presented integrative approaches should be understood as an attempt to frame future research directions by generating testable hypotheses and giving practical suggestions for future studies.

Keywords: ADHD; Hyporesponsiveness; Impulsivity; Reward; Ventral striatum; Ventral–striatal hypoactivation.

Fig. 1

Panel A shows the anatomical area of interest, i.e. the ventral-striatum (VS) including nucleus caudate (CAU), putamen (PUT) and the nucleus accumbens (NAcc). The right hemisphere is indicated by an “R”. Panel B is a 3-D representation of the striatum showing the peak-voxels by means of coloured dots of each single study on reward anticipation in ADHD. Panel C shows the data and results of the meta-analysis including a forest plot of effect sizes for VS-responsiveness during reward anticipation in ADHD. The diamond symbol represents the pooled estimate across all studies and indicates a medium effect (ES = 0.48; P < 0.001) in terms of VS-hyporesponsiveness in ADHD. Notes: ^aEffect size estimates were set to zero because these studies did not find significant VS effects and therefore did not report exact t/P-values. ^bThe averaged effect-size was calculated from the separate effect-size estimates (ES = 0 for ADHD-combined type; ES = 1.126 for ADHD-inattentive type). Panel B was visualized with the BrainNet Viewer (http://www.nitrc.org/projects/bnv/).

Fig. 2

Three hypothetical approaches that integrate the findings on correlations between impulsivity and VS-activity in healthy individuals and patients with ADHD. Panel A shows the inverted u-shape model. Low-medium to high impulsive groups in the healthy population (blue boxes) and patients with ADHD (red boxes) are highlighted to show that VS group differences can depend on sample selection. Panel B shows the moderator model which assumes a third background variable determining the correlation direction (e.g. dopamine bioavailability). Panel C represents the “unrelated model” which states that it is ADHD-specific symptoms and not impulsivity that is negatively related to VS-response. See text for further details.

Fig. 3

Left panel shows that an initially hyper-responsive VS-system might increase the probability to behave impulsively in multiple ways (positive correlation in the healthy population). In some individuals, putatively those with additional (genetic) risk factors, such repeated VS-overstimulation triggered by impulsive behaviour might lead to a subsequent down-regulation of the reward system (middle panel). The degree of down-regulation is presumably positively correlated with the degree of impulsivity and therefore a negative correlation of symptom severity and VS-response results (right panel).