. 2023 Oct 18;111(20):3270-3287.e8.

doi: 10.1016/j.neuron.2023.07.007. Epub 2023 Aug 8.

A common thalamic hub for general and defensive arousal control

Yiwei Wang¹, Ling You¹, KaMun Tan¹, Meijie Li¹, Jingshan Zou², Zhifeng Zhao³, Wenxin Hu⁴, Tianyu Li¹, Fenghua Xie⁵, Caiqin Li¹, Ruizhi Yuan⁶, Kai Ding⁷, Lingwei Cao⁸, Fengyuan Xin¹, Congping Shang⁹, Miaomiao Liu¹⁰, Yixiao Gao¹¹, Liqiang Wei¹², Zhiwei You¹³, Xiaorong Gao¹⁴, Wei Xiong¹⁵, Peng Cao⁹, Minmin Luo¹⁶, Feng Chen¹⁷, Kun Li¹², Jiamin Wu³, Bo Hong¹⁸, Kexin Yuan¹⁹

Affiliations

¹ Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing 100084, China; IDG/McGovern Institute for Brain Research at Tsinghua, Beijing 100084, China.
² Hospital of Chengdu University of Traditional Chinese Medicine, Traditional Chinese Medicine Hospital of Sichuan Province, Chengdu 610036, China.
³ IDG/McGovern Institute for Brain Research at Tsinghua, Beijing 100084, China; Department of Automation, Tsinghua University, Beijing 100084, China.
⁴ School of Aerospace Engineering, Tsinghua University, Beijing 100084, China.
⁵ Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing 100084, China; Tsinghua Laboratory of Brain and Intelligence (THBI), Beijing 100084, China.
⁶ Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing 100084, China.
⁷ Department of Chemical Engineering, Tsinghua University, Beijing 100084, China.
⁸ Zhili College, Tsinghua University, Beijing 100084, China.
⁹ National Institute of Biological Sciences (NIBS), Beijing 102206, China.
¹⁰ Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing 100084, China; Laboratory Animal Resources Center, Tsinghua University, Beijing 100084, China.
¹¹ IDG/McGovern Institute for Brain Research at Tsinghua, Beijing 100084, China; Department of Basic Medical Sciences, School of Medicine, Tsinghua University, Beijing 100084, China; Tsinghua-Peking Joint Center for Life Sciences, Beijing 100084, China.
¹² IDG/McGovern Institute for Brain Research at Tsinghua, Beijing 100084, China; School of Life Sciences, Tsinghua University, Beijing 100084, China; Tsinghua-Peking Joint Center for Life Sciences, Beijing 100084, China.
¹³ Department of Basic Medical Sciences, School of Medicine, Tsinghua University, Beijing 100084, China; Tsinghua-Peking Joint Center for Life Sciences, Beijing 100084, China; Laboratory of Dynamic Immunobiology, Institute for Immunology, Tsinghua University, Beijing 100084, China.
¹⁴ Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing 100084, China; IDG/McGovern Institute for Brain Research at Tsinghua, Beijing 100084, China; Tsinghua Laboratory of Brain and Intelligence (THBI), Beijing 100084, China.
¹⁵ IDG/McGovern Institute for Brain Research at Tsinghua, Beijing 100084, China; School of Life Sciences, Tsinghua University, Beijing 100084, China; Chinese Institute for Brain Research, Beijing 102206, China.
¹⁶ National Institute of Biological Sciences (NIBS), Beijing 102206, China; Chinese Institute for Brain Research, Beijing 102206, China.
¹⁷ Department of Automation, Tsinghua University, Beijing 100084, China.
¹⁸ Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing 100084, China; Tsinghua Laboratory of Brain and Intelligence (THBI), Beijing 100084, China. Electronic address: hongbo@mail.tsinghua.edu.cn.
¹⁹ Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing 100084, China; IDG/McGovern Institute for Brain Research at Tsinghua, Beijing 100084, China; Tsinghua Laboratory of Brain and Intelligence (THBI), Beijing 100084, China. Electronic address: kexinyuan@mail.tsinghua.edu.cn.

PMID: 37557180
DOI: 10.1016/j.neuron.2023.07.007

A common thalamic hub for general and defensive arousal control

Yiwei Wang et al. Neuron. 2023.

. 2023 Oct 18;111(20):3270-3287.e8.

doi: 10.1016/j.neuron.2023.07.007. Epub 2023 Aug 8.

Authors

Affiliations

¹ Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing 100084, China; IDG/McGovern Institute for Brain Research at Tsinghua, Beijing 100084, China.
² Hospital of Chengdu University of Traditional Chinese Medicine, Traditional Chinese Medicine Hospital of Sichuan Province, Chengdu 610036, China.
³ IDG/McGovern Institute for Brain Research at Tsinghua, Beijing 100084, China; Department of Automation, Tsinghua University, Beijing 100084, China.
⁴ School of Aerospace Engineering, Tsinghua University, Beijing 100084, China.
⁵ Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing 100084, China; Tsinghua Laboratory of Brain and Intelligence (THBI), Beijing 100084, China.
⁶ Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing 100084, China.
⁷ Department of Chemical Engineering, Tsinghua University, Beijing 100084, China.
⁸ Zhili College, Tsinghua University, Beijing 100084, China.
⁹ National Institute of Biological Sciences (NIBS), Beijing 102206, China.
¹⁰ Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing 100084, China; Laboratory Animal Resources Center, Tsinghua University, Beijing 100084, China.
¹¹ IDG/McGovern Institute for Brain Research at Tsinghua, Beijing 100084, China; Department of Basic Medical Sciences, School of Medicine, Tsinghua University, Beijing 100084, China; Tsinghua-Peking Joint Center for Life Sciences, Beijing 100084, China.
¹² IDG/McGovern Institute for Brain Research at Tsinghua, Beijing 100084, China; School of Life Sciences, Tsinghua University, Beijing 100084, China; Tsinghua-Peking Joint Center for Life Sciences, Beijing 100084, China.
¹³ Department of Basic Medical Sciences, School of Medicine, Tsinghua University, Beijing 100084, China; Tsinghua-Peking Joint Center for Life Sciences, Beijing 100084, China; Laboratory of Dynamic Immunobiology, Institute for Immunology, Tsinghua University, Beijing 100084, China.
¹⁴ Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing 100084, China; IDG/McGovern Institute for Brain Research at Tsinghua, Beijing 100084, China; Tsinghua Laboratory of Brain and Intelligence (THBI), Beijing 100084, China.
¹⁵ IDG/McGovern Institute for Brain Research at Tsinghua, Beijing 100084, China; School of Life Sciences, Tsinghua University, Beijing 100084, China; Chinese Institute for Brain Research, Beijing 102206, China.
¹⁶ National Institute of Biological Sciences (NIBS), Beijing 102206, China; Chinese Institute for Brain Research, Beijing 102206, China.
¹⁷ Department of Automation, Tsinghua University, Beijing 100084, China.
¹⁸ Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing 100084, China; Tsinghua Laboratory of Brain and Intelligence (THBI), Beijing 100084, China. Electronic address: hongbo@mail.tsinghua.edu.cn.
¹⁹ Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing 100084, China; IDG/McGovern Institute for Brain Research at Tsinghua, Beijing 100084, China; Tsinghua Laboratory of Brain and Intelligence (THBI), Beijing 100084, China. Electronic address: kexinyuan@mail.tsinghua.edu.cn.

PMID: 37557180
DOI: 10.1016/j.neuron.2023.07.007

Abstract

The expression of defensive responses to alerting sensory cues requires both general arousal and a specific arousal state associated with defensive emotions. However, it remains unclear whether these two forms of arousal can be regulated by common brain regions. We discovered that the medial sector of the auditory thalamus (ATm) in mice is a thalamic hub controlling both general and defensive arousal. The spontaneous activity of VGluT2-expressing ATm (ATm^VGluT2+) neurons was correlated with and causally contributed to wakefulness. In sleeping mice, sustained ATm^VGluT2+ population responses were predictive of sensory-induced arousal, the likelihood of which was markedly decreased by inhibiting ATm^VGluT2+ neurons or multiple downstream pathways. In awake mice, ATm^VGluT2+ activation led to heightened arousal accompanied by excessive anxiety and avoidance behavior. Notably, blocking their neurotransmission abolished alerting stimuli-induced defensive behaviors. These findings may shed light on the comorbidity of sleep disturbances and abnormal sensory sensitivity in specific brain disorders.

Keywords: arousal; auditory thalamus; defensive behavior; sensory system; temporal association cortex; thalamocortical projection; two-photon microscopy; wakefulness.

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Conflict of interest statement

Declaration of interests The authors declare no competing interests.

Comment in

Several ways to wake you up by the thalamus.
Acsády L, Mátyás F. Acsády L, et al. Neuron. 2023 Oct 18;111(20):3140-3142. doi: 10.1016/j.neuron.2023.09.020. Neuron. 2023. PMID: 37857089

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A common thalamic hub for general and defensive arousal control

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A common thalamic hub for general and defensive arousal control

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