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Ventral striatal islands of Calleja neurons bidirectionally mediate depression-like behaviors in mice

Author

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  • Yun-Feng Zhang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences
    University of Pennsylvania Perelman School of Medicine)

  • Jialiang Wu

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yingqi Wang

    (University of Pennsylvania Perelman School of Medicine)

  • Natalie L. Johnson

    (University of Florida)

  • Janardhan P. Bhattarai

    (University of Pennsylvania Perelman School of Medicine)

  • Guanqing Li

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences
    Hebei University)

  • Wenqiang Wang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences
    Hebei University)

  • Camilo Guevara

    (University of Pennsylvania Perelman School of Medicine)

  • Hannah Shoenhard

    (University of Pennsylvania Perelman School of Medicine)

  • Marc V. Fuccillo

    (University of Pennsylvania Perelman School of Medicine)

  • Daniel W. Wesson

    (University of Florida)

  • Minghong Ma

    (University of Pennsylvania Perelman School of Medicine)

Abstract

The ventral striatum is a reward center implicated in the pathophysiology of depression. It contains islands of Calleja, clusters of dopamine D3 receptor-expressing granule cells, predominantly in the olfactory tubercle (OT). These OT D3 neurons regulate self-grooming, a repetitive behavior manifested in affective disorders. Here we show that chronic restraint stress (CRS) induces robust depression-like behaviors in mice and decreases excitability of OT D3 neurons. Ablation or inhibition of these neurons leads to depression-like behaviors, whereas their activation ameliorates CRS-induced depression-like behaviors. Moreover, activation of OT D3 neurons has a rewarding effect, which diminishes when grooming is blocked. Finally, we propose a model that explains how OT D3 neurons may influence dopamine release via synaptic connections with OT spiny projection neurons (SPNs) that project to midbrain dopamine neurons. Our study reveals a crucial role of OT D3 neurons in bidirectionally mediating depression-like behaviors, suggesting a potential therapeutic target.

Suggested Citation

  • Yun-Feng Zhang & Jialiang Wu & Yingqi Wang & Natalie L. Johnson & Janardhan P. Bhattarai & Guanqing Li & Wenqiang Wang & Camilo Guevara & Hannah Shoenhard & Marc V. Fuccillo & Daniel W. Wesson & Mingh, 2023. "Ventral striatal islands of Calleja neurons bidirectionally mediate depression-like behaviors in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42662-z
    DOI: 10.1038/s41467-023-42662-z
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