Cortical excitability signatures for the degree of sleepiness in human

  1. Chin-Hsuan Chia
  2. Xin-Wei Tang
  3. Yue Cao
  4. Hua-Teng Cao
  5. Wei Zhang
  6. Jun-Fa Wu
  7. Yu-Lian Zhu
  8. Ying Chen
  9. Yi Lin
  10. Yi Wu
  11. Zhe Zhang  Is a corresponding author
  12. Ti-Fei Yuan  Is a corresponding author
  13. Rui-Ping Hu  Is a corresponding author
  1. Huashan hospital, Fudan University, China
  2. Institute of Neuroscience, China
  3. Institute of Brain Science, Fudan University, China
  4. Nantong University, China

Abstract

Sleep is essential in maintaining physiological homeostasis in the brain. While the underlying mechanism is not fully understood, a 'synaptic homeostasis' theory has been proposed that synapses continue to strengthen during awake, and undergo downscaling during sleep. This theory predicts that brain excitability increases with sleepiness. Here, we collected transcranial magnetic stimulation (TMS) measurements in 38 subjects in a 34-hour program, and decoded the relationship between cortical excitability and self-report sleepiness using advanced statistical methods. By utilizing a combination of partial least squares (PLS) regression and mixed-effect models, we identified a robust pattern of excitability changes, which can quantitatively predict the degree of sleepiness. Moreover, we found that synaptic strengthen occurred in both excitatory and inhibitory connections after sleep deprivation. In sum, our study provides supportive evidence for the synaptic homeostasis theory in human sleep and clarifies the process of synaptic strength modulation during sleepiness.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Chin-Hsuan Chia

    rehabilitation medicine, Huashan hospital, Fudan University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Xin-Wei Tang

    rehabilitation medicine, Huashan hospital, Fudan University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Yue Cao

    rehabilitation medicine, Huashan hospital, Fudan University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Hua-Teng Cao

    CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Neuroscience, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Wei Zhang

    Brain Science, Institute of Brain Science, Fudan University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Jun-Fa Wu

    rehabilitation medicine, Huashan hospital, Fudan University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Yu-Lian Zhu

    rehabilitation medicine, Huashan hospital, Fudan University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Ying Chen

    rehabilitation medicine, Huashan hospital, Fudan University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Yi Lin

    rehabilitation medicine, Huashan hospital, Fudan University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Yi Wu

    rehabilitation medicine, Huashan hospital, Fudan University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Zhe Zhang

    CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Neuroscience, Shanghai, China
    For correspondence
    zhezhang@ion.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0899-8077
  12. Ti-Fei Yuan

    Psychology, Nantong University, Nantong, China
    For correspondence
    ytf0707@126.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0510-715X
  13. Rui-Ping Hu

    rehabilitation medicine, Huashan hospital, Fudan University, shanghai city, China
    For correspondence
    wuyi4000@163.com
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Key Research and Development Program of China (2018YFC2001700)

  • Yi Wu

the Key Projects of Shanghai Science and Technology on Biomedicine (18411962300)

  • Rui-Ping Hu

Shanghai Health and Family Planning Commission project (201840225)

  • Yu-Lian Zhu

Shanghai Municipal Key Clinical Specialty (s.shslczdzk02702)

  • Yi Wu

the Key Projects of Shanghai Science and Technology on Biomedicine (20412420200)

  • Yi Wu

Natural Science Foundation of China grant (32071010)

  • Zhe Zhang

Shanghai Pujiang Program (20PJ1415000)

  • Zhe Zhang

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: 1. That informed consent, and consent to publish, was obtained2. This study was designed as a prospective self-controlled study. The Ethics Committee of Huashan Hospital approved the study (2017-410) and was registered on the Chinese Clinical Trial Registry (ChiCTR1800016771).

Reviewing Editor

  1. Laura Dugué, Uni­ver­sité de Paris, France

Version history

  1. Received: November 22, 2020
  2. Accepted: July 26, 2021
  3. Accepted Manuscript published: July 27, 2021 (version 1)
  4. Version of Record published: August 18, 2021 (version 2)

Copyright

© 2021, Chia et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Chin-Hsuan Chia
  2. Xin-Wei Tang
  3. Yue Cao
  4. Hua-Teng Cao
  5. Wei Zhang
  6. Jun-Fa Wu
  7. Yu-Lian Zhu
  8. Ying Chen
  9. Yi Lin
  10. Yi Wu
  11. Zhe Zhang
  12. Ti-Fei Yuan
  13. Rui-Ping Hu
(2021)
Cortical excitability signatures for the degree of sleepiness in human
eLife 10:e65099.
https://doi.org/10.7554/eLife.65099

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