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

Tomomi Tsunematsu,Shuzo Sakata,Arno Onken,Amisha A Patel

doi:10.7554/elife.52244

Tomomi Tsunematsu, Shuzo Sakata + Show 2 more

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https://doi.org/10.7554/elife.52244

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Abstract

The brainstem plays a crucial role in sleep-wake regulation. However, the 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 and exhibit longer prediction power than 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.

Highlights

The sleep-wake cycle is a fundamental homeostatic process across animal species (Siegel, 2005, Anafi et al, 2019, Aulsebrook et al, 2016)
Cortical slow oscillations, sleep spindles and hippocampal sharp wave-ripples (SWRs) are prominent neural events during non-rapid eye movement (NREM) sleep whereas theta oscillations and ponto-geniculo-occipital (PGO) or pontine (P) waves are seen during rapid eye movement (REM) sleep (Steriade, 2006, Montgomery et al, 2008, Buzsaki, 2015, Buzsaki, 2002, Jouvet, 1969, Steriade et al, 1993b, Callaway et al, 1987, Datta, 1997, Rasch and Born, 2013, Bizzi and Brooks, 1963)
Whereas NREM sleep was characterized by higher power of slow oscillations (Figure 1C) and a wider dynamic range of pupil diameter (Figure 1F)

Summary

Introduction

The sleep-wake cycle is a fundamental homeostatic process across animal species (Siegel, 2005, Anafi et al, 2019, Aulsebrook et al, 2016). Cortical slow oscillations, sleep spindles and hippocampal sharp wave-ripples (SWRs) are prominent neural events during NREM sleep whereas theta oscillations and ponto-geniculo-occipital (PGO) or pontine (P) waves are seen during REM sleep (Steriade, 2006, Montgomery et al, 2008, Buzsaki, 2015, Buzsaki, 2002, Jouvet, 1969, Steriade et al, 1993b, Callaway et al, 1987, Datta, 1997, Rasch and Born, 2013, Bizzi and Brooks, 1963). Toward a better understanding of functional roles of sleep states, it is essential to characterize state-dependent changes in brainstem network activity and their functional interactions with cortical regions across sleep states

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