Abnormal Striatal BOLD Responses to Reward Anticipation and Reward Delivery in ADHD

Abstract

Altered reward processing has been proposed to contribute to the symptoms of attention deficit hyperactivity disorder (ADHD). The neurobiological mechanism underlying this alteration remains unclear. We hypothesize that the transfer of dopamine release from reward to reward-predicting cues, as normally observed in animal studies, may be deficient in ADHD. Functional magnetic resonance imaging (fMRI) was used to investigate striatal responses to reward-predicting cues and reward delivery in a classical conditioning paradigm. Data from 14 high-functioning and stimulant-naïve young adults with elevated lifetime symptoms of ADHD (8 males, 6 females) and 15 well-matched controls (8 males, 7 females) were included in the analyses. During reward anticipation, increased blood-oxygen-level-dependent (BOLD) responses in the right ventral and left dorsal striatum were observed in controls, but not in the ADHD group. The opposite pattern was observed in response to reward delivery; the ADHD group demonstrated significantly greater BOLD responses in the ventral striatum bilaterally and the left dorsal striatum relative to controls. In the ADHD group, the number of current hyperactivity/impulsivity symptoms was inversely related to ventral striatal responses during reward anticipation and positively associated with responses to reward. The BOLD response patterns observed in the striatum are consistent with impaired predictive dopamine signaling in ADHD, which may explain altered reward-contingent behaviors and symptoms of ADHD.

Ventral striatal hyperconnectivity during rewarded interference control in adolescents with ADHD

“…Although our finding differed from the frequently reported VS hyporesponsivity to reward anticipation in adults with ADHD (Plichta & Scheres, 2014), it is in line with recent studies demonstrating VS hyperresponsivity in individuals with ADHD during reward receipt (Furukawa et al, 2014;von Rhein et al, 2015). The divergent results may be explained by differences in the reward processing phase: anticipation, target, or receipt (Tripp & Wickens, 2009).…”

Neuroanatomic and cognitive abnormalities in attention-deficit/hyperactivity disorder in the era of ‘high definition’ neuroimaging

“…Showing a similar discontinuity, an fMRI study of neurotypical young adults showed activation in the right ventral and left dorsal striatum during reward anticipation in a classical conditioning paradigm, but no significant effects in the ADHD group. Conversely, upon receipt of rewards, never-medicated adults with ADHD demonstrated significantly greater responses in the ventral striatum bilaterally and in left dorsal striatum relative to controls [25]. Recently emerging resting-state functional MRI (fMRI) methods [26] have also been used to examine ventral striatal functional connectivity.…”

Reward-Related Ventral Striatum Activity Links Polygenic Risk for Attention-Deficit/Hyperactivity Disorder to Problematic Alcohol Use in Young Adulthood

“…ADHD symptoms and diagnosis, in contrast, have been predominantly characterized by lower VS responsiveness to reward-predicting cues (see 13 for meta-analysis and review, but see also 12 and subsequent commentary in 49 and 50). Neural activation to reward outcome has been less systematically studied in ADHD, with some evidence of relative hyper-responsiveness (12, 51, and 52, but see also 53 and 54). This discrepancy in relative VS activation to reward anticipation versus outcome may reflect impaired reward learning (51), consistent with evidence of impaired behavioral modification based on prior reinforcement history in ADHD (55).…”

“…Neural activation to reward outcome has been less systematically studied in ADHD, with some evidence of relative hyper-responsiveness (12, 51, and 52, but see also 53 and 54). This discrepancy in relative VS activation to reward anticipation versus outcome may reflect impaired reward learning (51), consistent with evidence of impaired behavioral modification based on prior reinforcement history in ADHD (55). Given the design of our functional paradigm, in which we compared mean VS activation across positive versus negative feedback blocks (with non-valence-specific cues), our results may more appropriately reflect emergent data linking ADHD to increased VS response to reward outcomes.…”