Sleep-dependent upscaled excitability, saturated neuroplasticity, and modulated cognition in the human brain

  1. Mohammad Ali Salehinejad
  2. Elham Ghanavati
  3. Jörg Reinders
  4. Jan G Hengstler
  5. Min-Fang Kuo
  6. Michael A Nitsche  Is a corresponding author
  1. Leibniz Research Centre for Working Environment and Human Factors, Germany

Abstract

Sleep strongly affects synaptic strength, making it critical for cognition, especially learning, and memory formation. Whether and how sleep deprivation modulates human brain physiology and cognition is not well understood. Here we examined how overnight sleep deprivation vs overnight sufficient sleep affects (a) cortical excitability, measured by transcranial magnetic stimulation (TMS), (b) inducibility of LTP- and-LTD-like plasticity via transcranial direct current stimulation (tDCS), and (c) learning, memory and attention. The results suggest that sleep deprivation upscales cortical excitability due to enhanced glutamate-related cortical facilitation and decreased and/or reversed GABAergic cortical inhibition. Furthermore, tDCS-induced LTP-like plasticity abolishes while the inhibitory LTD-like plasticity converts to excitatory LTP-like plasticity under sleep deprivation. This is associated with increased EEG theta oscillations due to sleep pressure. Finally, we show that learning and memory formation, behavioral counterparts of plasticity, and working memory and attention, which rely on cortical excitability, are impaired during sleep deprivation. Our data suggest that upscaled brain excitability, and altered plasticity, due to sleep deprivation, are associated with impaired cognitive performance.

Data availability

The data files generated in this study are publicly available at https://osf.io/kve6d via Open Science Foundation (OSF).

Article and author information

Author details

  1. Mohammad Ali Salehinejad

    Department of Psychology and Neurosciences, Leibniz Research Centre for Working Environment and Human Factors, Dortmund, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1913-4677
  2. Elham Ghanavati

    Department of Psychology and Neurosciences, Leibniz Research Centre for Working Environment and Human Factors, Dortmund, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5944-8123
  3. Jörg Reinders

    Department of Toxicology, Leibniz Research Centre for Working Environment and Human Factors, Dortmund, Germany
    Competing interests
    No competing interests declared.
  4. Jan G Hengstler

    Department of Toxicology, Leibniz Research Centre for Working Environment and Human Factors, Dortmund, Germany
    Competing interests
    No competing interests declared.
  5. Min-Fang Kuo

    Department of Psychology and Neurosciences, Leibniz Research Centre for Working Environment and Human Factors, Dortmund, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9955-0237
  6. Michael A Nitsche

    Department of Psychology and Neurosciences, Leibniz Research Centre for Working Environment and Human Factors, Dortmund, Germany
    For correspondence
    nitsche@ifado.de
    Competing interests
    Michael A Nitsche, is a member of the Scientific Advisory Boards of Neuroelectrics and NeuroDevice.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2207-5965

Funding

No external funding was received for this work

Ethics

Human subjects: This study conformed to the Declaration of Helsinki guidelines and was approved by the Institutional Review Board (ethics code: 99). Participants gave informed consent and received monetary compensation.

Reviewing Editor

  1. Martin Dresler, Radboud University Medical Centre, Netherlands

Version history

  1. Received: April 11, 2021
  2. Preprint posted: April 30, 2021 (view preprint)
  3. Accepted: June 1, 2022
  4. Accepted Manuscript published: June 6, 2022 (version 1)
  5. Version of Record published: June 23, 2022 (version 2)

Copyright

© 2022, Salehinejad 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. Mohammad Ali Salehinejad
  2. Elham Ghanavati
  3. Jörg Reinders
  4. Jan G Hengstler
  5. Min-Fang Kuo
  6. Michael A Nitsche
(2022)
Sleep-dependent upscaled excitability, saturated neuroplasticity, and modulated cognition in the human brain
eLife 11:e69308.
https://doi.org/10.7554/eLife.69308

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https://doi.org/10.7554/eLife.69308

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