Pontine waves accompanied by short hippocampal sharp wave-ripples during non-rapid eye movement sleep : P-waves during NREM and REM sleep

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Tsunematsu, Tomomi and Matsumoto, Sumire and Merkler, Mirna and Sakata, Shuzo (2023) Pontine waves accompanied by short hippocampal sharp wave-ripples during non-rapid eye movement sleep : P-waves during NREM and REM sleep. SLEEP, 46 (9). zsad193. ISSN 1550-9109 (https://doi.org/10.1093/sleep/zsad193)

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Abstract

Ponto-geniculo-occipital or pontine (P) waves have long been recognized as an electrophysiological signature of rapid eye movement (REM) sleep. However, P-waves can be observed not just during REM sleep, but also during non-REM (NREM) sleep. Recent studies have uncovered that P-waves are functionally coupled with hippocampal sharp wave ripples (SWRs) during NREM sleep. However, it remains unclear to what extent P-waves during NREM sleep share their characteristics with P-waves during REM sleep and how the functional coupling to P-waves modulates SWRs. Here, we address these issues by performing multiple types of electrophysiological recordings and fiber photometry in both sexes of mice. P-waves during NREM sleep share their waveform shapes and local neural ensemble dynamics at a short (~100 milliseconds) timescale with their REM sleep counterparts. However, the dynamics of mesopontine cholinergic neurons are distinct at a longer (~10 seconds) timescale: although P-waves are accompanied by cholinergic transients, the cholinergic tone gradually reduces before P-wave genesis during NREM sleep. While P-waves are coupled to hippocampal theta rhythms during REM sleep, P-waves during NREM sleep are accompanied by a rapid reduction in hippocampal ripple power. SWRs coupled with P-waves are short-lived and hippocampal neural firing is also reduced after P-waves. These results demonstrate that P-waves are part of coordinated sleep-related activity by functionally coupling with hippocampal ensembles in a state-dependent manner.

ORCID iDs

Tsunematsu, Tomomi, Matsumoto, Sumire, Merkler, Mirna and Sakata, Shuzo ORCID logoORCID: https://orcid.org/0000-0001-6796-411X;
CORE (COnnecting REpositories)