Binge drinking impacts dorsal striatal response during decision making in adolescents

Abstract

Adolescence is a time of both increased risk taking and increased vulnerability to the neurotoxic effects of alcohol. However, it is unclear whether brain functioning abnormalities in adolescent binge drinkers are a result of alcohol use itself or whether they represent premorbid risk characteristics. The current study addresses this question by using a modified version of the Wheel of Fortune (WOF) task, during functional magnetic resonance imaging (fMRI), at both baseline, while all subjects were alcohol-naïve, and revisit, when half of the subjects had emerged into regular binge drinking (n=13) and half remained alcohol and substance-naïve (n=13). Region of interest (ROI) analysis revealed that during decision making, there was a significant binge-drinking related reduction in brain activation in the dorsal striatum, an effect associated with degree of recent use. Furthermore, whole-brain analysis revealed a decrease in fronto-parietal brain activation prior to initiation of alcohol use, in adolescents who went on to binge drink. Additionally, there were numerous regions, both cortical and subcortical, in which there was a significant time-related developmental change, across groups. These results demonstrate how abnormalities in decision-making related circuitry might both lead to and perpetuate alcohol drinking behavior. These findings help aid in our ability to disentangle consequences of binge drinking from potential risk markers for future binge drinking, and may help guide future prevention and intervention strategies.

Keywords: Adolescence; Alcohol; Binge; Decision making; Dorsal striatum.

Figure 1. Task activation map

Regions of the brain in which there is a significant risky vs. safe contrast, in binge-drinking adolescents or controls at either baseline or revisit.

Figure 2. Group-by-time interaction in the left dorsal caudate

(a) Percent signal change (mean ± SEM) in risky vs. safe brain activation at baseline and revisit. *Binge-drinking adolescents showed decreased risky vs. safe brain activation at revisit compared to baseline. ^#At revisit, binge-drinking adolescents showed decreased risky vs. safe brain activation compared to controls. (b) Drinking days in the past 3 months, and (c) heavy drinking days in the past 3 months, were negatively related to the change in risky vs. safe percent signal change, between revisit and baseline, in binge-drinking adolescents.

Figure 3. Main effect of group

Significant main effect of group in risky vs safe brain activation in the left inferior parietal lobule, left inferior frontal gyrus, left middle temporal gyrus and right superior temporal gyrus. Percent signal change (mean ± SEM) during risky vs. safe selection in both groups is collapsed across time. *Controls had higher risky vs. safe selection response than binge-drinking adolescents.

Figure 4. Main effect of time

Significant main effect of time in risky vs safe brain activation in the left cerebellum, right superior frontal gyrus, left postcentral gyrus, bilateral anterior cingulate, right middle occipital gyrus, and left thalamus. Percent signal change (mean ± SEM) during risky vs. safe selection at baseline and revisit is collapsed across group. *Risky vs. safe selection response was higher at baseline than revisit.