Pontine waves accompanied by short hippocampal sharp wave-ripples during non-rapid eye movement sleep

Pontine waves accompanied by short hippocampal sharp wave-ripples during non-rapid eye movement sleep
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非快动眼睡眠期间脑桥波伴有短海马尖波波纹

DOI:
10.1101/2022.06.03.494781
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发表时间:
2022
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通讯作者:
Tsunematsu T
Tsunematsu T
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作者:
Tsunematsu T

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脑桥-膝状体-枕(PGO)或脑桥(P)波长期以来被认为是快速眼动(REM)睡眠的电生理特征。然而,P波不仅可以在REM睡眠期间观察到,还可以在非REM(NREM)睡眠期间观察到。最近的研究发现,在NREM睡眠期间,P波与海马尖波纹(SWR)功能耦合。然而,目前还不清楚在何种程度上,P波在NREM睡眠期间共享他们的特点与P波在REM睡眠期间,以及如何功能耦合到P波调制SWR。在这里,我们通过在两种性别的小鼠中进行多种类型的电生理记录和纤维光度测定来解决这些问题。NREM睡眠期间的P波与REM睡眠期间的P波在短(~100 ms)时间尺度上共享其波形形状和局部神经系综动力学。然而,中桥脑胆碱能神经元的动力学在较长(~10 s)的时间尺度上是不同的:尽管P波伴随着胆碱能瞬变,但在NREM睡眠期间,胆碱能神经元的张力在P波发生之前逐渐降低。虽然P波在REM睡眠期间与海马θ节律耦合,但NREM睡眠期间的P波伴随着海马涟漪功率的快速减少。与P波耦合的SWR是短暂的,并且P波之后海马神经放电也减少。这些结果表明,P-波发挥独特的作用,在记忆巩固功能耦合与海马合奏在一个状态依赖marty.Significance StatementWhile睡眠状态可以定义基于不同的电生理标记,脑桥(P)波早已被公认为快速眼动(REM)睡眠的标志。尽管P波很突出,但与其他睡眠相关的神经事件相比,P波的研究较少。我们仍然对P波和其他睡眠状态下的神经事件之间的功能关系知之甚少。在本研究中,我们发现了一个意想不到的关系P波和海马尖波波纹(SWR)在非快速眼动(NREM)睡眠。虽然P波和驻波比是时间耦合的,但P波对驻波比的影响逐渐减小。因为已知SWR在记忆巩固中起关键作用,P波也可能在记忆巩固中起作用,但以睡眠状态依赖的方式。
Ponto-geniculo-occipital (PGO) 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 waveripples (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 ms) timescale with their REM sleep counterparts. However, the dynamics of mesopontine cholinergic neurons are distinct at a longer (~10 s) 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 suggest that P-waves play distinct roles in memory consolidation by functionally coupling with hippocampal ensembles in a state-dependent manner.Significance StatementWhile sleep states can be defined based on distinct electrophysiological markers, pontine (P) waves have long been recognized as a hallmark of rapid eye movement (REM) sleep. Despite their prominence, P-waves have been studied less compared to other sleep-related neural events. We still know little about the functional relationship between P-waves and other neural events across sleep states. In the present study, we discovered an unexpected relationship between P-waves and hippocampal sharp wave-ripples (SWRs) during non-REM (NREM) sleep. While P-waves and SWRs are temporally coupled, P-waves have a diminishing effect on SWRs. Because SWRs are known to play a critical role in memory consolidation, P-waves may also play a role in memory consolidation but in a sleep-state-dependent manner.