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State-dependent pontine ensemble dynamics and interactions with cortex across sleep states

Tomomi Tsunematsu, Amisha A Patel, Arno Onken, View ORCID ProfileShuzo Sakata
doi: https://doi.org/10.1101/752683
Tomomi Tsunematsu
Strathclyde Institute of Pharmacy and Biomedical Sciences, University of Strathclyde, 161 Cathedral Street, Glasgow G4 0RE, UKSuper-network Brain Physiology, Graduate School of Life Sciences, Tohoku University, Sendai 980-8577, JapanPrecursory Research for Embryonic Science and Technology, Japan Science and Technology Agency, Kawaguchi 332-0012, Japan
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Amisha A Patel
Strathclyde Institute of Pharmacy and Biomedical Sciences, University of Strathclyde, 161 Cathedral Street, Glasgow G4 0RE, UK
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Arno Onken
School of Informatics, University of Edinburgh, 10 Crichton Street, Edinburgh EH8 9AB, UK
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Shuzo Sakata
Strathclyde Institute of Pharmacy and Biomedical Sciences, University of Strathclyde, 161 Cathedral Street, Glasgow G4 0RE, UK
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  • ORCID record for Shuzo Sakata
  • For correspondence: shuzo.sakata@strath.ac.uk
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Abstract

The pontine nuclei play a crucial role in sleep-wake regulation. However, pontine ensemble dynamics underlying sleep regulation remain poorly understood. By monitoring population activity in multiple pontine and adjacent brainstem areas, here we show slow, state-predictive pontine ensemble dynamics and state-dependent interactions between the pons and the cortex in mice. On a timescale of seconds to minutes, pontine populations exhibit diverse firing across vigilance states, with some of these dynamics being attributed to cell type-specific activity. Pontine population activity can predict pupil dilation and vigilance states: pontine neurons exhibit longer predictable power compared with hippocampal neurons. On a timescale of sub-seconds, pontine waves (P-waves) are observed as synchronous firing of pontine neurons primarily during rapid eye movement (REM) sleep, but also during non-REM (NREM) sleep. Crucially, P-waves functionally interact with cortical 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 hippocampal theta oscillations and are followed by burst firing in a subset of hippocampal neurons. Thus, the directionality of functional interactions between the hippocampus and pons changes depending on sleep states. This state-dependent global coordination between pontine and cortical regions implicates distinct functional roles of sleep.

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Posted September 02, 2019.
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State-dependent pontine ensemble dynamics and interactions with cortex across sleep states
Tomomi Tsunematsu, Amisha A Patel, Arno Onken, Shuzo Sakata
bioRxiv 752683; doi: https://doi.org/10.1101/752683
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State-dependent pontine ensemble dynamics and interactions with cortex across sleep states
Tomomi Tsunematsu, Amisha A Patel, Arno Onken, Shuzo Sakata
bioRxiv 752683; doi: https://doi.org/10.1101/752683

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