Loss and Frontal Striatal Reactivities Characterize Alcohol Use Severity and Rule-Breaking Behavior in Young Adult Drinkers

Guangfei Li; Yu Chen; Shefali Chaudhary; Xiaoying Tang; Chiang-Shan R Li

doi:10.1016/j.bpsc.2022.06.001

Loss and Frontal Striatal Reactivities Characterize Alcohol Use Severity and Rule-Breaking Behavior in Young Adult Drinkers

Biol Psychiatry Cogn Neurosci Neuroimaging. 2022 Oct;7(10):1007-1016. doi: 10.1016/j.bpsc.2022.06.001. Epub 2022 Jun 13.

Authors

Guangfei Li¹, Yu Chen², Shefali Chaudhary², Xiaoying Tang³, Chiang-Shan R Li⁴

Affiliations

¹ Department of Biomedical Engineering, Faculty of Environment and Life Sciences, Beijing University of Technology, Beijing, China; Department of Biomedical Engineering, School of Life Sciences, Beijing Institute of Technology, Beijing, China.
² Department of Psychiatry, Yale University School of Medicine, New Haven, Connecticut.
³ Department of Biomedical Engineering, School of Life Sciences, Beijing Institute of Technology, Beijing, China. Electronic address: xiaoying@bit.edu.cn.
⁴ Department of Psychiatry, Yale University School of Medicine, New Haven, Connecticut; Department of Neuroscience, Yale University School of Medicine, New Haven, Connecticut; Interdepartmental Neuroscience Program, Yale University School of Medicine, New Haven, Connecticut; Wu Tsai Institute, Yale University, New Haven, Connecticut. Electronic address: chiang-shan.li@yale.edu.

Abstract

Background: Alcohol misuse is associated with externalizing behaviors, including rule breaking. Studies have implicated altered reward processing in externalizing behaviors and alcohol misuse. Here, we investigated whether reward or punishment reactivity more significantly influenced alcohol use severity and rule-breaking behavior in young adult drinkers.

Methods: We curated data from the Human Connectome Project and identified 181 binge (132 men) and 288 nonbinge (97 men) drinkers performing a gambling task during brain imaging. Alcohol use severity was quantified by the first principal component of principal-component analysis of all drinking measures. We analyzed the imaging data using published routines and evaluated the results at a corrected threshold. We examined the interrelationship between imaging and clinical metrics with mediation and path analyses.

Results: Compared with nonbingers, bingers showed more severe rule-breaking behavior and responded significantly faster during post-loss than during post-win trials. Compared with nonbingers, bingers demonstrated greater inferior/middle frontal gyrus and cerebellum activations in loss-predominating blocks but no differences in regional responses to win-predominating blocks, relative to an interblock baseline. The right caudate body showed loss reactivity that was positively correlated with the rule-breaking score. No regional responses to wins were significantly correlated with the rule-breaking score. Mediation and path analyses demonstrated significant models with inferior/middle frontal gyrus and caudate reactivity to loss interrelating rule breaking and alcohol use severity.

Conclusions: Punishment rather than reward reactivity was associated with alcohol use severity and rule breaking in young adults. The findings highlight the roles of negative emotions in psychological models of externalizing behaviors and alcohol misuse.

Keywords: Alcohol use disorder (AUD); Binge drinking; Punishment; Reward; Rule breaking; fMRI.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Alcohol Drinking / psychology
Alcoholism* / psychology
Brain / physiology
Ethanol
Humans
Magnetic Resonance Imaging / methods
Male
Reward
Young Adult

Substances

Ethanol

Abstract

Publication types

MeSH terms

Substances

Grants and funding