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Persistent ventral anterior cingulate cortex and resolved amygdala hyper-responses to negative outcomes after depression remission: a combined cross-sectional and longitudinal study

  • Xiaocui Zhang
    Correspondence
    Corresponding authors: Xiaocui Zhang, MD, Medical Psychological Institute, Central South University, Changsha, China,
    Affiliations
    Medical Psychological Center, The Second Xiangya Hospital, Central South University, Changsha, China

    Medical Psychological Institute of Central South University, Changsha, China

    National Clinical Research Center for Mental Disorders, Changsha, China

    Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA
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  • Xiang Wang
    Affiliations
    Medical Psychological Center, The Second Xiangya Hospital, Central South University, Changsha, China

    Medical Psychological Institute of Central South University, Changsha, China

    National Clinical Research Center for Mental Disorders, Changsha, China
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  • Daifeng Dong
    Affiliations
    Medical Psychological Center, The Second Xiangya Hospital, Central South University, Changsha, China

    Medical Psychological Institute of Central South University, Changsha, China
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  • Xiaoqiang Sun
    Affiliations
    Medical Psychological Center, The Second Xiangya Hospital, Central South University, Changsha, China

    Medical Psychological Institute of Central South University, Changsha, China
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  • Xue Zhong
    Affiliations
    Medical Psychological Center, The Second Xiangya Hospital, Central South University, Changsha, China

    Medical Psychological Institute of Central South University, Changsha, China
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  • Ge Xiong
    Affiliations
    Medical Psychological Center, The Second Xiangya Hospital, Central South University, Changsha, China

    Medical Psychological Institute of Central South University, Changsha, China
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  • Chang Cheng
    Affiliations
    Medical Psychological Center, The Second Xiangya Hospital, Central South University, Changsha, China

    Medical Psychological Institute of Central South University, Changsha, China
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  • Hui Lei
    Affiliations
    College of Education, Hunan Agricultural University, Changsha, Hunan, China

    Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA
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  • Ya Chai
    Affiliations
    Key Laboratory of Applied Brain and Cognitive Sciences, Shanghai International Studies University, Shanghai, China

    Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA
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  • Meichen Yu
    Affiliations
    Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA

    Department of Psychiatry, University of Pennsylvania, Philadelphia, PA, USA
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  • Peng Quan
    Affiliations
    Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA

    Research Center for Quality of Life and Applied Psychology, Guangdong Medical University, Dongguan, China
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  • Philip R. Gehrman
    Affiliations
    Department of Psychiatry, University of Pennsylvania, Philadelphia, PA, USA
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  • John A. Detre
    Affiliations
    Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA
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  • Shuqiao Yao
    Correspondence
    Corresponding authors: Shuqiao Yao, MD, Medical Psychological Institute, Central South University, Changsha, China,
    Affiliations
    Medical Psychological Center, The Second Xiangya Hospital, Central South University, Changsha, China

    Medical Psychological Institute of Central South University, Changsha, China

    National Clinical Research Center for Mental Disorders, Changsha, China
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  • Hengyi Rao
    Correspondence
    Corresponding authors: Hengyi Rao, PhD. Center for Functional Neuroimaging & Department of Neurology, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, 19104, USA,
    Affiliations
    Key Laboratory of Applied Brain and Cognitive Sciences, Shanghai International Studies University, Shanghai, China

    Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA

    Department of Psychiatry, University of Pennsylvania, Philadelphia, PA, USA
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Published:September 07, 2022DOI:https://doi.org/10.1016/j.biopsych.2022.09.003

      Abstract

      Objective

      Major depressive disorder (MDD) is a highly prevalent mood disorder affecting over 300 million people worldwide. Biased processing of negative information and neural hyper-responses to negative events are hallmarks of depression. The present study combined cross-sectional and longitudinal experiments to explore both persistent and resolved neural hyper-responses to negative outcomes from risky decision-making in current and remitted MDD patients.

      Methods

      A total of 264 subjects participated in the cross-sectional study, including 117 patients with medication-naive first-episode current depression, 45 remitted patients with only one episode of depression, and 102 healthy controls. Participants completed a modified balloon analog risk task during functional MRI. In the longitudinal arm of the study, 42 current MDD patients were followed up and 26 remitted patients were studied again after 8-week of antidepressant treatment.

      Results

      Current MDD patients showed hyper-responses to loss outcomes in multiple limbic regions including the amygdala and ventral anterior cingulate cortex (vACC). Amygdala but not vACC hyperactivity correlated with depression scores in current MDD patients. Furthermore, amygdala hyperactivity resolved while vACC hyperactivity persisted in remitted MDD patients in both cross-sectional and longitudinal studies.

      Conclusions

      These findings provide consistent evidence supporting differential patterns of the amygdala and vACC hyper-responses to negative outcomes during depression remission. Amygdala hyperactivity may be a symptomatic and state-dependent marker of depressive neural responses, while vACC hyperactivity may reflect a persistent and state-independent effect of depression on brain function. These findings offer new insights into the neural underpinnings of depression remission and prevention of depression recurrence.

      Keywords

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