Reduced cerebellar brain activity during reward processing in adolescent binge drinkers

Abstract

Due to ongoing development, adolescence may be a period of heightened vulnerability to the neurotoxic effects of alcohol. Binge drinking may alter reward-driven behavior and neurocircuitry, thereby increasing risk for escalating alcohol use. Therefore, we compared reward processing in adolescents with and without a history of recent binge drinking. At their baseline study visit, all participants (age=14.86 ± 0.88) were free of heavy alcohol use and completed a modified version of the Wheel of Fortune (WOF) functional magnetic resonance imaging task. Following this visit, 17 youth reported binge drinking on ≥3 occasions within a 90 day period and were matched to 17 youth who remained alcohol and substance-naïve. All participants repeated the WOF task during a second visit (age=16.83 ± 1.22). No significant effects were found in a region of interest analysis of the ventral striatum, but whole-brain analyses showed significant group differences in reward response at the second study visit in the left cerebellum, controlling for baseline visit brain activity (p/α<0.05), which was negatively correlated with mean number of drinks consumed/drinking day in the last 90 days. These findings suggest that binge drinking during adolescence may alter brain activity during reward processing in a dose-dependent manner.

Keywords: Adolescence; Alcohol; Binge; Cerebellum; Reward.

Fig. 1

Conjunction map of task-related brain activity during reward processing. Task-related activity maps for each group at each study visit (baseline and revisit) were voxel-thresholded at p < 0.05 and a conjunction map was created for Win > No Win brain response to determine areas commonly activated across participants regardless of group status or time of study visit. Occipital, superior parietal, dorsolateral prefrontal, caudate, and ventral striatal brain activity were seen in the Win > No Win contrast overlaid on AFNI's Talairach template brain in the axial view.

Fig. 2

Binge drinkers had reduced cerebellar brain activity during reward processing compared with controls. (A) Significantly reduced posterior cerebellar (lobule VIIa/crus I) activity during Win vs. No Win was seen in binge drinkers at the time of revisit, compared with controls, while accounting for baseline brain activity in this region. Results are displayed in the sagittal, coronal, and axial view overlaid on AFNI's Talairach template brain. (B) Bar graphs of percent signal change illustrating significant differences in brain activity in the contrast of interest (Win vs. No Win) and in simple effects are displayed for each visit. At revisit, binge drinkers had significantly reduced brain response during Win vs. No Win. Simple effects show this was attributed to reduced activity during Win vs. baseline in binge drinkers, compared with controls. While controls showed elevated brain response during Win vs. baseline compared with No Win vs. baseline, brain activity was not distinct in binge drinkers during reward receipt or absence. This is in contrast to brain response in this region at the baseline visit, when both groups showed more activity in response to Wins than No Wins. *p < 0.05.

Fig. 3

Drinks consumed/drinking day in the past 3 months was negatively related to cerebellar brain response in binge drinkers. Average drinks/drinking day was negatively associated with reward-related activity in binge drinkers. Win vs. baseline activity is plotted on the left y-axis, while No Win vs. baseline activity is plotted on the right y-axis.

Fig. S1

Cerebellar brain activity in binge drinkers and controls, divided by sex. A) No significant group, sex, or group-by-sex interactions in cerebellar response at the baseline visit. B) Two-way ANOVAs with group and sex as between-subjects factors indicate main effects of group and sex, such that binge drinkers had reduced cerebellar response compared with controls, and males had reduced cerebellar response compared with females, in the Win vs. No Win contrast. This was driven by main effects of group and sex during Win vs. baseline BOLD response. *p > 0.05