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Serotonergic modulation of vigilance states in zebrafish and mice

Author

Listed:
  • Yang Zhao

    (Translational Research Institute of Brain and Brain-Like Intelligence, Shanghai Fourth People’s Hospital, School of Medicine, Tongji University
    Tongji University)

  • Chun-Xiao Huang

    (Translational Research Institute of Brain and Brain-Like Intelligence, Shanghai Fourth People’s Hospital, School of Medicine, Tongji University
    Tongji University)

  • Yiming Gu

    (Translational Research Institute of Brain and Brain-Like Intelligence, Shanghai Fourth People’s Hospital, School of Medicine, Tongji University
    Tongji University)

  • Yacong Zhao

    (Translational Research Institute of Brain and Brain-Like Intelligence, Shanghai Fourth People’s Hospital, School of Medicine, Tongji University
    Tongji University)

  • Wenjie Ren

    (Translational Research Institute of Brain and Brain-Like Intelligence, Shanghai Fourth People’s Hospital, School of Medicine, Tongji University
    Tongji University)

  • Yutong Wang

    (Translational Research Institute of Brain and Brain-Like Intelligence, Shanghai Fourth People’s Hospital, School of Medicine, Tongji University
    Tongji University)

  • Jinjin Chen

    (Translational Research Institute of Brain and Brain-Like Intelligence, Shanghai Fourth People’s Hospital, School of Medicine, Tongji University
    Tongji University)

  • Na N. Guan

    (Translational Research Institute of Brain and Brain-Like Intelligence, Shanghai Fourth People’s Hospital, School of Medicine, Tongji University
    Tongji University
    Tongji University
    Karolinska Institutet)

  • Jianren Song

    (Translational Research Institute of Brain and Brain-Like Intelligence, Shanghai Fourth People’s Hospital, School of Medicine, Tongji University
    Tongji University
    Tongji University
    Karolinska Institutet)

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.

Suggested Citation

  • Yang Zhao & Chun-Xiao Huang & Yiming Gu & Yacong Zhao & Wenjie Ren & Yutong Wang & Jinjin Chen & Na N. Guan & Jianren Song, 2024. "Serotonergic modulation of vigilance states in zebrafish and mice," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47021-0
    DOI: 10.1038/s41467-024-47021-0
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    References listed on IDEAS

    as
    1. Scott Creel & Paul Schuette & David Christianson, 2014. "Effects of predation risk on group size, vigilance, and foraging behavior in an African ungulate community," Behavioral Ecology, International Society for Behavioral Ecology, vol. 25(4), pages 773-784.
    2. Rong-wei Zhang & Xiao-quan Li & Koichi Kawakami & Jiu-lin Du, 2016. "Stereotyped initiation of retinal waves by bipolar cells via presynaptic NMDA autoreceptors," Nature Communications, Nature, vol. 7(1), pages 1-12, November.
    3. Catherine A. Marcinkiewcz & Christopher M. Mazzone & Giuseppe D’Agostino & Lindsay R. Halladay & J. Andrew Hardaway & Jeffrey F. DiBerto & Montserrat Navarro & Nathan Burnham & Claudia Cristiano & Cay, 2016. "Serotonin engages an anxiety and fear-promoting circuit in the extended amygdala," Nature, Nature, vol. 537(7618), pages 97-101, September.
    4. Chun-Xiao Huang & Yacong Zhao & Jie Mao & Zhen Wang & Lulu Xu & Jianwei Cheng & Na N. Guan & Jianren Song, 2021. "An injury-induced serotonergic neuron subpopulation contributes to axon regrowth and function restoration after spinal cord injury in zebrafish," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
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