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

Tsunematsu, Tomomi and Patel, Amisha A and Onken, Arno and Sakata, Shuzo (2020) State-dependent brainstem ensemble dynamics and their interactions with hippocampus across sleep states. eLife, 9. e52244. ISSN 2050-084X

[img]
Preview
Text (Tsunematsu-etal-eLife-2020-State-dependent-brainstem-ensemble-dynamics-and-their-interactions)
Tsunematsu_etal_eLife_2020_State_dependent_brainstem_ensemble_dynamics_and_their_interactions.pdf
Final Published Version
License: Creative Commons Attribution 4.0 logo

Download (3MB)| Preview

    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.