State-dependent brainstem ensemble dynamics and their interactions with hippocampus across sleep states
- University of Strathclyde, United Kingdom
- University of Edinburgh, United Kingdom
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.
Data availability
The source data files are available online (https://doi.org/10.15129/4f81777a-7b88-48f3-af4d-da484706fa5d).
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Data for: State-dependent brainstem ensemble dynamics and their interactions with hippocampus across sleep statesUniversity of Strathclyde, 10.15129/4f81777a-7b88-48f3-af4d-da484706fa5d.
Article and author information
Author details
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).
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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State-dependent brainstem ensemble dynamics and their interactions with hippocampus across sleep states
eLife 9:e52244.
https://doi.org/10.7554/eLife.52244
