Preliminary Evidence for Disrupted Nucleus Accumbens Reactivity and Connectivity to Reward in Binge Drinkers

Abstract

Aims: Dysfunctional brain reward circuitry, particularly in the nucleus accumbens (NAcc), has been proposed as a risk factor for alcohol use disorder (AUD). This risk factor may be evident in binge drinkers (BD), who are at high risk for developing AUD. We examined whole-brain and NAcc reactivity to reward in BD compared to non-binge drinkers (NBD), hypothesizing that groups would differ in their neural reactivity and connectivity.

Methods: Healthy BD (N = 27) and NBD (N = 23)-none meeting AUD criteria-completed a reward-guessing game, the 'Doors' task, during functional magnetic resonance imaging. We conducted an exploratory whole-brain search for group differences, but given our a priori hypotheses, we also extracted activation from the NAcc to examine reactivity during reward (Win > Loss) and functional connectivity (FC) to the prefrontal cortex.

Results: Compared to NBD, BD exhibited greater activation in both the right and left NAcc during reward relative to loss. Additionally, NBD drinkers exhibited positive FC between the NAcc and dorsal anterior cingulate (dACC) whereas the BD showed negative FC between these regions. Furthermore, less NAcc-dACC FC was related to more past month alcohol use.

Conclusions: Our results provide preliminary evidence that BD exhibit greater NAcc activation during reward receipt relative to loss. This is consistent with the broader AUD literature and suggests aberrant neural reactivity may precede disorder onset. In addition, BD exhibited less NAcc-dACC FC, perhaps reflecting deficient regulation of activation to rewards compared to losses. This profile of reward brain circuitry could represent neural correlates of vulnerability for AUD.

Short summary: Healthy binge drinkers, at risk for alcohol use disorder, exhibited greater nucleus accumbens activation during reward relative to loss. In addition, binge drinkers exhibited reduced connectivity between the nucleus accumbens and dorsal anterior cingulate, which was associated with more past month alcohol use.

Fig. 1.

Whole-brain task activation during reward. Whole-brain task activation (P < 0.05, corrected) for all subjects to reward (Win > Loss trials).

Fig. 2.

Group differences in region-of-interest (ROI) NAcc BOLD reward reactivity. (A) Left and right NAcc ROI used (B) Extracted response (in β-weights/parameter estimates of activation) for each group from the left and right NAcc activation to reward (Win > Loss).

Fig. 3.

Group differences in NAcc–dACC functional connectivity during reward. (A and D) Activation in the dACC, where Binge drinkers displayed negative right NAcc to bilateral dACC functional connectivity (A) and negative left NAcc to bilateral dACC functional connectivity (D), while non-binge drinkers showed positive connectivity between these regions (P < 0.05, corrected). (B) Group differences in extracted right NAcc to dACC BOLD functional connectivity. (E) Group differences in extracted left NAcc to dACC BOLD functional connectivity. (C and F) The relationship between past month drinking and right and left NAcc–dACC BOLD functional connectivity, respectively.