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

Reviewing Editor

  1. Martin Dresler, Radboud University Medical Centre, Netherlands

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.

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.

Metrics

  • 2,812
    Page views
  • 619
    Downloads
  • 17
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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
    Kiwamu Kudo, Kamalini G Ranasinghe ... Srikantan S Nagarajan
    Research Article

    Alzheimer’s disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive neurodegeneration and cognitive decline. Altered neural oscillations have been consistently demonstrated in AD. However, the trajectories of abnormal neural oscillations in AD progression and their relationship to neurodegeneration and cognitive decline are unknown. Here, we deployed robust event-based sequencing models (EBMs) to investigate the trajectories of long-range and local neural synchrony across AD stages, estimated from resting-state magnetoencephalography. The increases in neural synchrony in the delta-theta band and the decreases in the alpha and beta bands showed progressive changes throughout the stages of the EBM. Decreases in alpha and beta band synchrony preceded both neurodegeneration and cognitive decline, indicating that frequency-specific neuronal synchrony abnormalities are early manifestations of AD pathophysiology. The long-range synchrony effects were greater than the local synchrony, indicating a greater sensitivity of connectivity metrics involving multiple regions of the brain. These results demonstrate the evolution of functional neuronal deficits along the sequence of AD progression.

    1. Cell Biology
    2. Neuroscience
    Zhenyong Wu, Grant F Kusick ... Shigeki Watanabe
    Research Article

    Despite decades of intense study, the molecular basis of asynchronous neurotransmitter release remains enigmatic. Synaptotagmin (syt) 7 and Doc2 have both been proposed as Ca2+ sensors that trigger this mode of exocytosis, but conflicting findings have led to controversy. Here, we demonstrate that at excitatory mouse hippocampal synapses, Doc2α is the major Ca2+ sensor for asynchronous release, while syt7 supports this process through activity-dependent docking of synaptic vesicles. In synapses lacking Doc2α, asynchronous release after single action potentials is strongly reduced, while deleting syt7 has no effect. However, in the absence of syt7, docked vesicles cannot be replenished on millisecond timescales. Consequently, both synchronous and asynchronous release depress from the second pulse onward during repetitive activity. By contrast, synapses lacking Doc2α have normal activity-dependent docking, but continue to exhibit decreased asynchronous release after multiple stimuli. Moreover, disruption of both Ca2+ sensors is non-additive. These findings result in a new model whereby syt7 drives activity-dependent docking, thus providing synaptic vesicles for synchronous (syt1) and asynchronous (Doc2 and other unidentified sensors) release during ongoing transmission.