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

Elife. 2020 Jan 14:9:e52244. doi: 10.7554/eLife.52244.

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.

Keywords: P/PGO waves; brain state; brainstem; mouse; neural ensemble dynamics; neural oscillations; neuroscience; sleep.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Stem / physiology*
  • Electroencephalography
  • Hippocampus / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Neurons / physiology*
  • Pons / physiology
  • Sleep / physiology*
  • Sleep Stages
  • Sleep, REM
  • Wakefulness / physiology*