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.

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.

Metrics

  • 3,687
    views
  • 740
    downloads
  • 35
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

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

Further reading

    1. Neuroscience
    Eleni Hackwell, Sharon R Ladyman ... David R Grattan
    Research Article

    The specific role that prolactin plays in lactational infertility, as distinct from other suckling or metabolic cues, remains unresolved. Here, deletion of the prolactin receptor (Prlr) from forebrain neurons or arcuate kisspeptin neurons resulted in failure to maintain normal lactation-induced suppression of estrous cycles. Kisspeptin immunoreactivity and pulsatile LH secretion were increased in these mice, even in the presence of ongoing suckling stimulation and lactation. GCaMP fibre photometry of arcuate kisspeptin neurons revealed that the normal episodic activity of these neurons is rapidly suppressed in pregnancy and this was maintained throughout early lactation. Deletion of Prlr from arcuate kisspeptin neurons resulted in early reactivation of episodic activity of kisspeptin neurons prior to a premature return of reproductive cycles in early lactation. These observations show dynamic variation in arcuate kisspeptin neuronal activity associated with the hormonal changes of pregnancy and lactation, and provide direct evidence that prolactin action on arcuate kisspeptin neurons is necessary for suppressing fertility during lactation in mice.

    1. Neuroscience
    Choongheon Lee, Mohammad Shokrian ... Jong-Hoon Nam
    Research Article

    We hypothesized that active outer hair cells drive cochlear fluid circulation. The hypothesis was tested by delivering the neurotoxin, kainic acid, to the intact round window of young gerbil cochleae while monitoring auditory responses in the cochlear nucleus. Sounds presented at a modest level significantly expedited kainic acid delivery. When outer-hair-cell motility was suppressed by salicylate, the facilitation effect was compromised. A low-frequency tone was more effective than broadband noise, especially for drug delivery to apical locations. Computational model simulations provided the physical basis for our observation, which incorporated solute diffusion, fluid advection, fluid–structure interaction, and outer-hair-cell motility. Active outer hair cells deformed the organ of Corti like a peristaltic tube to generate apically streaming flows along the tunnel of Corti and basally streaming flows along the scala tympani. Our measurements and simulations coherently suggest that active outer hair cells in the tail region of cochlear traveling waves drive cochlear fluid circulation.