Alcohol effects on globus pallidus connectivity: Role of impulsivity and binge drinking

Abstract

Despite the harm caused by binge drinking, the neural mechanisms leading to risky and disinhibited intoxication-related behaviors are not well understood. Evidence suggests that the globus pallidus externus (GPe), a substructure within the basal ganglia, participates in inhibitory control processes, as examined in stop-signaling tasks. In fact, studies in rodents have revealed that alcohol can change GPe activity by decreasing neuronal firing rates, suggesting that the GPe may have a central role in explaining impulsive behaviors and failures of inhibition that occur during binge drinking. In this study, twenty-five healthy volunteers underwent intravenous alcohol infusion to achieve a blood alcohol level of 0.08 g/dl, which is equivalent to a binge drinking episode. A resting state functional magnetic resonance imaging scan was collected prior to the infusion and at binge-level exposure. Functional connectivity analysis was used to investigate the association between alcohol-induced changes in GPe connectivity, drinking behaviors, and impulsivity traits. We found that individuals with greater number of drinks or heavy drinking days in the recent past had greater alcoholinduced deficits in GPe connectivity, particularly to the striatum. Our data also indicated an association between impulsivity and alcohol-induced deficits in GPe-frontal/precentral connectivity. Moreover, alcohol induced changes in GPe-amygdala circuitry suggested greater vulnerabilities to stress-related drinking in some individuals. Taken together, these findings suggest that alcohol may interact with impulsive personality traits and drinking patterns to drive alterations in GPe circuitry associated with behavioral inhibition, possibly indicating a neural mechanism by which binge drinking could lead to impulsive behaviors. Alcohol effects on globus pallidus connectivity PLOS ONE | https://doi.org/10.1371/journal.pone.0224906 March 26, 2020 3 / 19Fig 3. Effect of alcohol induced changes in GPe connectivity on the association between drinking and impulsivity. (As measured by the Alcohol Timeline Followback and UPPS-P, respectively). Cluster of Drinking Effect column: Brain images represent whole brain effects of drinks in past 30 days on alcohol induced change in functional connectivity (post-infusion connectivity > post-infusion connectivity). Warm colors indicate intoxication related increases in connectivity. Images shown at p < 0.005. Plots of Connectivity are scatter plots corresponding to individual connectivity at baseline in teal (estimated BAC: 0.0) and after infusion in salmon (BAC: 0.08); linear fit lines are also displayed for each timepoint. The y-axis for both plots is the same; the x-axis reflects the number of drinks in the last 30 days (center plot) and the number of drinks in the last 30 days multiplied by impulsivity score on the UPPS Negative Urgency scale (right plot). Abbreviations as follows: L. GPe-Left Globus Pallidus externus; Hipp./Amyg-Hippocampus/Amygdala cluster.Alcohol effects on globus pallidus connectivity PLOS ON...

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