Serotonergic modulation of vigilance states in zebrafish and mice

Yang Zhao; Chun-Xiao Huang; Yiming Gu; Yacong Zhao; Wenjie Ren; Yutong Wang; Jinjin Chen; Na N Guan; Jianren Song

doi:10.1038/s41467-024-47021-0

Serotonergic modulation of vigilance states in zebrafish and mice

Nat Commun. 2024 Mar 22;15(1):2596. doi: 10.1038/s41467-024-47021-0.

Authors

Yang Zhao^#^{1

2}, Chun-Xiao Huang^#^{1

2}, Yiming Gu^{1

2}, Yacong Zhao^{1

2}, Wenjie Ren^{1

2}, Yutong Wang^{1

2}, Jinjin Chen^{1

2}, Na N Guan^{3

4

5

6}, Jianren Song^{7

8

9

10}

Affiliations

¹ Shanghai Key Laboratory of Anesthesiology and Brain Functional Modulation, Clinical Research Center for Anesthesiology and Perioperative Medicine, Translational Research Institute of Brain and Brain-Like Intelligence, Shanghai Fourth People's Hospital, School of Medicine, Tongji University, Shanghai, 200434, China.
² Clinical Center for Brain and Spinal Cord Research, Tongji University, 200092, Shanghai, China.
³ Shanghai Key Laboratory of Anesthesiology and Brain Functional Modulation, Clinical Research Center for Anesthesiology and Perioperative Medicine, Translational Research Institute of Brain and Brain-Like Intelligence, Shanghai Fourth People's Hospital, School of Medicine, Tongji University, Shanghai, 200434, China. [email protected].
⁴ Clinical Center for Brain and Spinal Cord Research, Tongji University, 200092, Shanghai, China. [email protected].
⁵ Frontiers Science Center for Intelligent Autonomous Systems, Tongji University, Shanghai, China. [email protected].
⁶ Department of Neuroscience, Karolinska Institutet, 171 77, Stockholm, Sweden. [email protected].
⁷ Shanghai Key Laboratory of Anesthesiology and Brain Functional Modulation, Clinical Research Center for Anesthesiology and Perioperative Medicine, Translational Research Institute of Brain and Brain-Like Intelligence, Shanghai Fourth People's Hospital, School of Medicine, Tongji University, Shanghai, 200434, China. [email protected].
⁸ Clinical Center for Brain and Spinal Cord Research, Tongji University, 200092, Shanghai, China. [email protected].
⁹ Frontiers Science Center for Intelligent Autonomous Systems, Tongji University, Shanghai, China. [email protected].
¹⁰ Department of Neuroscience, Karolinska Institutet, 171 77, Stockholm, Sweden. [email protected].

^# Contributed equally.

Abstract

Vigilance refers to being alertly watchful or paying sustained attention to avoid potential threats. Animals in vigilance states reduce locomotion and have an enhanced sensitivity to aversive stimuli so as to react quickly to dangers. Here we report that an unconventional 5-HT driven mechanism operating at neural circuit level which shapes the internal state underlying vigilance behavior in zebrafish and male mice. The neural signature of internal vigilance state was characterized by persistent low-frequency high-amplitude neuronal synchrony in zebrafish dorsal pallium and mice prefrontal cortex. The neuronal synchronization underlying vigilance was dependent on intense release of 5-HT induced by persistent activation of either DRN 5-HT neuron or local 5-HT axon terminals in related brain regions via activation of 5-HTR7. Thus, we identify a mechanism of vigilance behavior across species that illustrates the interplay between neuromodulators and neural circuits necessary to shape behavior states.

MeSH terms

Animals
Brain
Male
Mice
Neurons / physiology
Serotonergic Neurons / physiology
Serotonin* / physiology
Wakefulness / physiology
Zebrafish*

Substances

Serotonin