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Loss and frontal striatal reactivities characterize alcohol use severity and rule-breaking behavior in young adult drinkers

  • Guangfei Li
    Affiliations
    Department of Biomedical engineering, School of Life Sciences, Beijing Institute of technology, Beijing, China
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  • Yu Chen
    Affiliations
    Department of Psychiatry, Yale University School of Medicine, New Haven, CT
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  • Shefali Chaudhary
    Affiliations
    Department of Psychiatry, Yale University School of Medicine, New Haven, CT
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  • Xiaoying Tang
    Correspondence
    Address correspondence to: Xiaoying Tang, 715-3 Teaching Building No.5, Beijing Institute of technology, 5 South Zhongguancun Road, Haidian District, Beijing 100081, China, Phone: +86 010-68915998
    Affiliations
    Department of Biomedical engineering, School of Life Sciences, Beijing Institute of technology, Beijing, China
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  • Chiang-Shan R. Li
    Correspondence
    Address correspondence to: C.-S. Ray Li, Connecticut Mental Health Center S112, 34 Park Street, New Haven, CT 06519-1109, U.S.A, Phone: +1 203-974-7354
    Affiliations
    Department of Psychiatry, Yale University School of Medicine, New Haven, CT

    Department of Neuroscience, Yale University School of Medicine, New Haven, CT

    Interdepartmental Neuroscience Program, Yale University School of Medicine, New Haven, CT

    Wu Tsai Institute, Yale University, New Haven, CT
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      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 influences alcohol use severity and rule-breaking behavior in young adult drinkers.

      Methods

      We curated the data of the Human Connectome Project and identified 181 binge (132 men) and 288 non-binge (97 men) drinkers performing a gambling task during brain imaging. Alcohol use severity was quantified by the first principal component (PC1) of principal component analysis of all drinking measures. We analyzed the imaging data with published routines and evaluated the results at a corrected threshold. We examined the inter-relationship between imaging and clinical metrics with mediation and path analyses.

      Results

      Bingers vs. non-bingers showed more severe rule-breaking behavior and responded significantly faster during post-loss than post-win trials. Bingers vs. non-bingers demonstrated greater inferior/middle frontal gyrus (IFG/MFG) and cerebellum activations in loss-predominating blocks but no differences in regional responses to win-predominating blocks, relative to an inter-block baseline. The right caudate body showed loss reactivity in positive correlation with rule-breaking score. No regional responses to wins were significantly correlated with rule-breaking score. Mediation and path analysis demonstrated significant models with IFG/MFG and caudate reactivity to loss inter-relating rule-breaking and alcohol use severity.

      Conclusions

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

      Keywords

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