Journal article
Sleep loss diminishes hippocampal reactivation and replay
Nature (London), Vol.630(8018), pp.935-942
06/12/2024
DOI: 10.1038/s41586-024-07538-2
PMCID: PMC11472378
PMID: 38867049
Abstract
Memories benefit from sleep1, and the reactivation and replay of waking experiences during hippocampal sharp-wave ripples (SWRs) are considered to be crucial for this process2. However, little is known about how these patterns are impacted by sleep loss. Here we recorded CA1 neuronal activity over 12 h in rats across maze exploration, sleep and sleep deprivation, followed by recovery sleep. We found that SWRs showed sustained or higher rates during sleep deprivation but with lower power and higher frequency ripples. Pyramidal cells exhibited sustained firing during sleep deprivation and reduced firing during sleep, yet their firing rates were comparable during SWRs regardless of sleep state. Despite the robust firing and abundance of SWRs during sleep deprivation, we found that the reactivation and replay of neuronal firing patterns was diminished during these periods and, in some cases, completely abolished compared to ad libitum sleep. Reactivation partially rebounded after recovery sleep but failed to reach the levels found in natural sleep. These results delineate the adverse consequences of sleep loss on hippocampal function at the network level and reveal a dissociation between the many SWRs elicited during sleep deprivation and the few reactivations and replays that occur during these events.Memories benefit from sleep1, and the reactivation and replay of waking experiences during hippocampal sharp-wave ripples (SWRs) are considered to be crucial for this process2. However, little is known about how these patterns are impacted by sleep loss. Here we recorded CA1 neuronal activity over 12 h in rats across maze exploration, sleep and sleep deprivation, followed by recovery sleep. We found that SWRs showed sustained or higher rates during sleep deprivation but with lower power and higher frequency ripples. Pyramidal cells exhibited sustained firing during sleep deprivation and reduced firing during sleep, yet their firing rates were comparable during SWRs regardless of sleep state. Despite the robust firing and abundance of SWRs during sleep deprivation, we found that the reactivation and replay of neuronal firing patterns was diminished during these periods and, in some cases, completely abolished compared to ad libitum sleep. Reactivation partially rebounded after recovery sleep but failed to reach the levels found in natural sleep. These results delineate the adverse consequences of sleep loss on hippocampal function at the network level and reveal a dissociation between the many SWRs elicited during sleep deprivation and the few reactivations and replays that occur during these events.
Details
- Title: Subtitle
- Sleep loss diminishes hippocampal reactivation and replay
- Creators
- Bapun Giri - University of MichiganNathaniel Kinsky - University of MichiganUtku Kaya - University of MichiganKourosh Maboudi - University of MichiganTed Abel - University of IowaKamran Diba - University of Michigan
- Resource Type
- Journal article
- Publication Details
- Nature (London), Vol.630(8018), pp.935-942
- DOI
- 10.1038/s41586-024-07538-2
- PMID
- 38867049
- PMCID
- PMC11472378
- NLM abbreviation
- Nature
- ISSN
- 1476-4687
- eISSN
- 1476-4687
- Publisher
- Springer Science and Business Media LLC
- Language
- English
- Electronic publication date
- 06/12/2024
- Academic Unit
- Molecular Physiology and Biophysics; Psychiatry; Psychological and Brain Sciences; Iowa Neuroscience Institute; Neuroscience and Pharmacology; Biochemistry and Molecular Biology
- Record Identifier
- 9984642760002771
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