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

• DOI: 10.1016/j.neuron.2020.05.008
• Publication Date: 2020-06-04T14:29:42Z
• Authors: 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 Sawamoto; Steven G. Kernie; Takeshi Sakurai; Thomas J. McHugh; Masanobu Kano; Masashi Yanagisawa; Masanori Sakaguchi
• Keywords: Neurons; 0303 health sciences; Electromyography; Neurogenesis; Sleep, REM; Electroencephalography; Fear; Hippocampus; Optogenetics; Mice; 03 medical and health sciences; Conditioning, Psychological; Dentate Gyrus; Animals; Learning; Calcium; Theta Rhythm; Memory Consolidation

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.