Transient reactivation of small ensembles of adult-born neurons during REM sleep supports memory consolidation in mice

Abstract While memory consolidation is widely believed to require memory reactivation synchronized with theta oscillations during REM sleep, direct causal evidence linking specific neuronal ensembles to this process has been lacking. Strong theta oscillations arise in the hippocampal dentate gyrus,...

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Main Authors: Sakthivel Srinivasan, Iyo Koyanagi, Pablo Vergara, Yuteng Wang, Akinobu Ohba, Toshie Naoi, Kaspar E. Vogt, Yoan Chérasse, Noriki Kutsumura, Takeshi Sakurai, Taro Tezuka, Masanori Sakaguchi
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Language:English
Published: Nature Portfolio 2025-08-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-62554-8
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author Sakthivel Srinivasan
Iyo Koyanagi
Pablo Vergara
Yuteng Wang
Akinobu Ohba
Toshie Naoi
Kaspar E. Vogt
Yoan Chérasse
Noriki Kutsumura
Takeshi Sakurai
Taro Tezuka
Masanori Sakaguchi
author_facet Sakthivel Srinivasan
Iyo Koyanagi
Pablo Vergara
Yuteng Wang
Akinobu Ohba
Toshie Naoi
Kaspar E. Vogt
Yoan Chérasse
Noriki Kutsumura
Takeshi Sakurai
Taro Tezuka
Masanori Sakaguchi
author_sort Sakthivel Srinivasan
collection DOAJ
description Abstract While memory consolidation is widely believed to require memory reactivation synchronized with theta oscillations during REM sleep, direct causal evidence linking specific neuronal ensembles to this process has been lacking. Strong theta oscillations arise in the hippocampal dentate gyrus, where a small population of principal neurons is continuously generated throughout adulthood. Although these adult-born neurons (ABNs) are known to modulate hippocampal circuits for memory, the causality between their specific information content and memory-related behavior was unknown. Here, we show that REM sleep reactivation of memory ensembles comprising as few as ~3 ABNs is necessary for fear memory consolidation. Crucially, we found that the synchronization of ABN activity with a specific theta phase is essential for associative memory consolidation. Our findings thus provide causal evidence that consolidation critically depends on both the reactivation of minimal neuronal populations and precise neuronal coordination within theta-defined temporal windows.
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publishDate 2025-08-01
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series Nature Communications
spelling doaj-art-bcdce99f65ed4d10a10b2d99a14a960e2025-08-20T03:43:03ZengNature PortfolioNature Communications2041-17232025-08-0116111110.1038/s41467-025-62554-8Transient reactivation of small ensembles of adult-born neurons during REM sleep supports memory consolidation in miceSakthivel Srinivasan0Iyo Koyanagi1Pablo Vergara2Yuteng Wang3Akinobu Ohba4Toshie Naoi5Kaspar E. Vogt6Yoan Chérasse7Noriki Kutsumura8Takeshi Sakurai9Taro Tezuka10Masanori Sakaguchi11International Institute for Integrative Sleep Medicine (WPI-IIIS), University of TsukubaInternational Institute for Integrative Sleep Medicine (WPI-IIIS), University of TsukubaInternational Institute for Integrative Sleep Medicine (WPI-IIIS), University of TsukubaInternational Institute for Integrative Sleep Medicine (WPI-IIIS), University of TsukubaInternational Institute for Integrative Sleep Medicine (WPI-IIIS), University of TsukubaInternational Institute for Integrative Sleep Medicine (WPI-IIIS), University of TsukubaInternational Institute for Integrative Sleep Medicine (WPI-IIIS), University of TsukubaInternational Institute for Integrative Sleep Medicine (WPI-IIIS), University of TsukubaInternational Institute for Integrative Sleep Medicine (WPI-IIIS), University of TsukubaInternational Institute for Integrative Sleep Medicine (WPI-IIIS), University of TsukubaInstitute of Systems and Information Engineering, University of TsukubaInternational Institute for Integrative Sleep Medicine (WPI-IIIS), University of TsukubaAbstract While memory consolidation is widely believed to require memory reactivation synchronized with theta oscillations during REM sleep, direct causal evidence linking specific neuronal ensembles to this process has been lacking. Strong theta oscillations arise in the hippocampal dentate gyrus, where a small population of principal neurons is continuously generated throughout adulthood. Although these adult-born neurons (ABNs) are known to modulate hippocampal circuits for memory, the causality between their specific information content and memory-related behavior was unknown. Here, we show that REM sleep reactivation of memory ensembles comprising as few as ~3 ABNs is necessary for fear memory consolidation. Crucially, we found that the synchronization of ABN activity with a specific theta phase is essential for associative memory consolidation. Our findings thus provide causal evidence that consolidation critically depends on both the reactivation of minimal neuronal populations and precise neuronal coordination within theta-defined temporal windows.https://doi.org/10.1038/s41467-025-62554-8
spellingShingle Sakthivel Srinivasan
Iyo Koyanagi
Pablo Vergara
Yuteng Wang
Akinobu Ohba
Toshie Naoi
Kaspar E. Vogt
Yoan Chérasse
Noriki Kutsumura
Takeshi Sakurai
Taro Tezuka
Masanori Sakaguchi
Transient reactivation of small ensembles of adult-born neurons during REM sleep supports memory consolidation in mice
Nature Communications
title Transient reactivation of small ensembles of adult-born neurons during REM sleep supports memory consolidation in mice
title_full Transient reactivation of small ensembles of adult-born neurons during REM sleep supports memory consolidation in mice
title_fullStr Transient reactivation of small ensembles of adult-born neurons during REM sleep supports memory consolidation in mice
title_full_unstemmed Transient reactivation of small ensembles of adult-born neurons during REM sleep supports memory consolidation in mice
title_short Transient reactivation of small ensembles of adult-born neurons during REM sleep supports memory consolidation in mice
title_sort transient reactivation of small ensembles of adult born neurons during rem sleep supports memory consolidation in mice
url https://doi.org/10.1038/s41467-025-62554-8
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