Sparse Activity of Hippocampal Adult-Born Neurons during REM Sleep Is Necessary for Memory Consolidation

Deependra Kumar, Iyo Koyanagi, Alvaro Carrier-Ruiz, Pablo Vergara, Sakthivel Srinivasan, Yuki Sugaya, Masatoshi Kasuya, Tzong Shiue Yu, Kaspar E. Vogt, Masafumi Muratani, Takaaki Ohnishi, Sima Singh, Catia M. Teixeira, Yoan Chérasse, Toshie Naoi, Szu Han Wang, Pimpimon Nondhalee, Boran A.H. Osman, Naoko Kaneko, Kazunobu SawamotoSteven G. Kernie, Takeshi Sakurai, Thomas J. McHugh, Masanobu Kano, Masashi Yanagisawa, Masanori Sakaguchi

Research output: Contribution to journalArticlepeer-review

10 Scopus citations

Abstract

The occurrence of dreaming during rapid eye movement (REM) sleep prompts interest in the role of REM sleep in hippocampal-dependent episodic memory. Within the mammalian hippocampus, the dentate gyrus (DG) has the unique characteristic of exhibiting neurogenesis persisting into adulthood. Despite their small numbers and sparse activity, adult-born neurons (ABNs) in the DG play critical roles in memory; however, their memory function during sleep is unknown. Here, we investigate whether young ABN activity contributes to memory consolidation during sleep using Ca2+ imaging in freely moving mice. We found that contextual fear learning recruits a population of young ABNs that are reactivated during subsequent REM sleep against a backdrop of overall reduced ABN activity. Optogenetic silencing of this sparse ABN activity during REM sleep alters the structural remodeling of spines on ABN dendrites and impairs memory consolidation. These findings provide a causal link between ABN activity during REM sleep and memory consolidation.

Original languageEnglish (US)
Pages (from-to)552-565.e10
JournalNeuron
Volume107
Issue number3
DOIs
StatePublished - Aug 5 2020
Externally publishedYes

Keywords

  • REM sleep
  • adult neurogenesis
  • calcium imaging
  • memory consolidation
  • miniaturized microscope
  • optogenetics

ASJC Scopus subject areas

  • Neuroscience(all)

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