Neurovascular coupling and bilateral connectivity during NREM and REM sleep

  1. Kevin L Turner
  2. Kyle W Gheres
  3. Elizabeth A Proctor
  4. Patrick J Drew  Is a corresponding author
  1. Pennsylvania State University, United States

Abstract

To understand how arousal state impacts cerebral hemodynamics and neurovascular coupling, we monitored neural activity, behavior, and hemodynamic signals in un-anesthetized, head-fixed mice. Mice frequently fell asleep during imaging, and these sleep events were interspersed with periods of wake. During both NREM and REM sleep, mice showed large increases in cerebral blood volume ([HbT]) and arteriole diameter relative to the awake state, two to five times larger than those evoked by sensory stimulation. During NREM, the amplitude of bilateral low-frequency oscillations in [HbT] increased markedly, and coherency between neural activity and hemodynamic signals was higher than the awake resting and REM states. Bilateral correlations in neural activity and [HbT] were highest during NREM, and lowest in the awake state. Hemodynamic signals in the cortex are strongly modulated by arousal state, and changes during sleep are substantially larger than sensory-evoked responses.

Data availability

Source data and code for generation of all figures can be found here:Code repository location: https://github.com/DrewLab/Turner_Gheres_Proctor_Drew_eLife2020Data repository location: https://doi.org/10.5061/dryad.6hdr7sqz5

The following data sets were generated

Article and author information

Author details

  1. Kevin L Turner

    Biomedical Engineering, Pennsylvania State University, University Park, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3044-7079
  2. Kyle W Gheres

    Molecular Cellular and Integrative Biosciences program, Pennsylvania State University, University Park, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7568-9023
  3. Elizabeth A Proctor

    Pharmacology, Biomedical Engineering, and Engineering Science & Mechanics, Pennsylvania State University, Hershey, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Patrick J Drew

    Engineering Science and Mechanics, Biomedical Engineering, and Neurosurgery, Pennsylvania State University, University Park, United States
    For correspondence
    PJD17@PSU.EDU
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7483-7378

Funding

National Institutes of Health (R01NS078168)

  • Patrick J Drew

National Institutes of Health (R01NS079737)

  • Patrick J Drew

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

Ethics

Animal experimentation: This study was performed in accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All procedures were performed in accordance with protocols approved by the Institutional Animal Care and Use Committee (IACUC) of Pennsylvania State University (protocol # 201042827).

Reviewing Editor

  1. Adrien Peyrache, McGill University, Canada

Publication history

  1. Received: August 12, 2020
  2. Accepted: October 28, 2020
  3. Accepted Manuscript published: October 29, 2020 (version 1)
  4. Version of Record published: December 23, 2020 (version 2)
  5. Version of Record updated: November 22, 2021 (version 3)

Copyright

© 2020, Turner 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. Kevin L Turner
  2. Kyle W Gheres
  3. Elizabeth A Proctor
  4. Patrick J Drew
(2020)
Neurovascular coupling and bilateral connectivity during NREM and REM sleep
eLife 9:e62071.
https://doi.org/10.7554/eLife.62071

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