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State-dependent brainstem ensemble dynamics and their interactions with hippocampus across sleep states

  1. Tomomi Tsunematsu
  2. Amisha A Patel
  3. Arno Onken
  4. Shuzo Sakata  Is a corresponding author
  1. University of Strathclyde, United Kingdom
  2. University of Edinburgh, United Kingdom
Research Article
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Cite this article as: eLife 2020;9:e52244 doi: 10.7554/eLife.52244

Abstract

The brainstem plays a crucial role in sleep-wake regulation. However, their ensemble dynamics underlying sleep regulation remain poorly understood. Here we show slow, state-predictive brainstem ensemble dynamics and state-dependent interactions between the brainstem and the hippocampus in mice. On a timescale of seconds to minutes, brainstem populations can predict pupil dilation and vigilance states where they exhibit longer predictable power compared with hippocampal CA1 neurons. On a timescale of sub-seconds, pontine waves (P-waves) are accompanied by synchronous firing of brainstem neurons during both rapid eye movement (REM) and non-REM (NREM) sleep. Crucially, P-waves functionally interact with CA1 activity in a state-dependent manner: during NREM sleep, hippocampal sharp wave-ripples (SWRs) precede P-waves. On the other hand, P-waves during REM sleep are phase-locked with ongoing theta oscillations and are followed by burst firing of CA1 neurons. This state-dependent global coordination between the brainstem and hippocampus implicates distinct functional roles of sleep.

Article and author information

Author details

  1. Tomomi Tsunematsu

    Strathclyde Institute of Pharmacy and Biomedical Sciences, University of Strathclyde, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Amisha A Patel

    Strathclyde Institute of Pharmacy and Biomedical Sciences, University of Strathclyde, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Arno Onken

    School of Informatics, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7387-5535
  4. Shuzo Sakata

    Strathclyde Institute of Pharmacy and Biomedical Sciences, University of Strathclyde, Glasgow, United Kingdom
    For correspondence
    shuzo.sakata@strath.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6796-411X

Funding

Biotechnology and Biological Sciences Research Council (BB/M00905X/1)

  • Shuzo Sakata

Leverhulme Trust (RPG-2015-377)

  • Shuzo Sakata

Alzheimer's Research UK (ARUK-PPG2017B-005)

  • Shuzo Sakata

Action on Hearing Loss (S45)

  • Shuzo Sakata

Engineering and Physical Sciences Research Council (EP/S005692/1)

  • Arno Onken

Japan Society for the Promotion of Science

  • Tomomi Tsunematsu

Uehara Memorial Foundation

  • Tomomi Tsunematsu

Japan Science and Technology Agency (JPMJPR1887)

  • Tomomi Tsunematsu

Japan Society for the Promotion of Science (17H06520)

  • Tomomi Tsunematsu

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

Ethics

Animal experimentation: All experimental procedures were performed in accordance with the United Kingdom Animals (Scientific Procedures) Act of 1986 Home Office regulations and approved by the Home Office (PPL 70/8883).

Reviewing Editor

  1. Laura L Colgin, University of Texas at Austin, United States

Publication history

  1. Received: September 26, 2019
  2. Accepted: January 14, 2020
  3. Accepted Manuscript published: January 14, 2020 (version 1)

Copyright

© 2020, Tsunematsu 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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