IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-47021-0.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-47021-0
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-47021-0?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Barman, Dipesh & Roy, Jyotirmoy & Alrabaiah, Hussam & Panja, Prabir & Mondal, Sankar Prasad & Alam, Shariful, 2021. "Impact of predator incited fear and prey refuge in a fractional order prey predator model," Chaos, Solitons & Fractals, Elsevier, vol. 142(C).
    2. Vishnu Muraleedharan Saraswathy & Lili Zhou & Mayssa H. Mokalled, 2024. "Single-cell analysis of innate spinal cord regeneration identifies intersecting modes of neuronal repair," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    3. Kumbhakar, Ruma & Hossain, Mainul & Pal, Nikhil, 2024. "Dynamics of a two-prey one-predator model with fear and group defense: A study in parameter planes," Chaos, Solitons & Fractals, Elsevier, vol. 179(C).
    4. M. E. Flanigan & O. J. Hon & S. D’Ambrosio & K. M. Boyt & L. Hassanein & M. Castle & H. L. Haun & M. M. Pina & T. L. Kash, 2023. "Subcortical serotonin 5HT2c receptor-containing neurons sex-specifically regulate binge-like alcohol consumption, social, and arousal behaviors in mice," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    5. Fangying Zhao & Jiangyong He & Jun Tang & Nianfei Cui & Yanyan Shi & Zhifan Li & Shengnan Liu & Yazhou Wang & Ming Ma & Congjian Zhao & Lingfei Luo & Li Li, 2022. "Brain milieu induces early microglial maturation through the BAX-Notch axis," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    6. Dániel L. Barabási & Gregor F. P. Schuhknecht & Florian Engert, 2024. "Functional neuronal circuits emerge in the absence of developmental activity," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. 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.
    8. Shachar Sherman & Irene Arnold-Ammer & Martin W. Schneider & Koichi Kawakami & Herwig Baier, 2023. "Retina-derived signals control pace of neurogenesis in visual brain areas but not circuit assembly," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. Hiro Taiyo Hamada & Yoshifumi Abe & Norio Takata & Masakazu Taira & Kenji F. Tanaka & Kenji Doya, 2024. "Optogenetic activation of dorsal raphe serotonin neurons induces brain-wide activation," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    10. Buddi S. Poudel & Peter G. Spooner & Alison Matthews, 2015. "Temporal shift in activity patterns of Himalayan marmots in relation to pastoralism," Behavioral Ecology, International Society for Behavioral Ecology, vol. 26(5), pages 1345-1351.
    11. Hossain, Mainul & Kumbhakar, Ruma & Pal, Nikhil, 2022. "Dynamics in the biparametric spaces of a three-species food chain model with vigilance," Chaos, Solitons & Fractals, Elsevier, vol. 162(C).

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47021-0. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.