A midbrain GABAergic circuit constrains wakefulness in a mouse model of stress

Shuancheng Ren (), Cai Zhang, Faguo Yue, Jinxiang Tang, Wei Zhang, Yue Zheng, Yuanyuan Fang, Na Wang, Zhenbo Song, Zehui Zhang, Xiaolong Zhang, Han Qin, Yaling Wang, Jianxia Xia, Chenggang Jiang, Chao He (), Fenlan Luo () and Zhian Hu ()
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Shuancheng Ren: Army Medical University
Cai Zhang: Army Medical University
Faguo Yue: Army Medical University
Jinxiang Tang: Bishan Hospital of Chongqing Medical University
Wei Zhang: Army Medical University
Yue Zheng: Army Medical University
Yuanyuan Fang: Wuhan University
Na Wang: Army Medical University
Zhenbo Song: Army Medical University
Zehui Zhang: Jilin University
Xiaolong Zhang: Army Medical University
Han Qin: Guangyang Bay Laboratory
Yaling Wang: Army Medical University
Jianxia Xia: Army Medical University
Chenggang Jiang: Chongqing Health Center for Women and Children
Chao He: Army Medical University
Fenlan Luo: Army Medical University
Zhian Hu: Army Medical University

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract Enhancement of wakefulness is a prerequisite for adaptive behaviors to cope with acute stress, but hyperarousal is associated with impaired behavioral performance. Although the neural circuitries promoting wakefulness in acute stress conditions have been extensively identified, less is known about the circuit mechanisms constraining wakefulness to prevent hyperarousal. Here, we found that chemogenetic or optogenetic activation of GAD2-positive GABAergic neurons in the midbrain dorsal raphe nucleus (DRNGAD2) decreased wakefulness, while inhibition or ablation of these neurons produced an increase in wakefulness along with hyperactivity. Surprisingly, DRNGAD2 neurons were paradoxically wakefulness-active and were further activated by acute stress. Bidirectional manipulations revealed that DRNGAD2 neurons constrained the increase of wakefulness and arousal level in a mouse model of stress. Circuit-specific investigations demonstrated that DRNGAD2 neurons constrained wakefulness via inhibition of the wakefulness-promoting paraventricular thalamus. Therefore, the present study identified a wakefulness-constraining role DRNGAD2 neurons in acute stress conditions.

Date: 2024
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DOI: 10.1038/s41467-024-46707-9

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