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Weakly encoded memories due to acute sleep restriction can be rescued after one night of recovery sleep

Sleep is thought to play a complementary role in human memory processing: sleep loss impairs the formation of new memories during the following awake period and, conversely, normal sleep promotes the strengthening of the already encoded memories. However, whether sleep can strengthen deteriorated me...

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Autores principales: Baena, Daniel, Cantero, Jose L., Fuentemilla, Lluís, Atienza, Mercedes
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6989495/
https://www.ncbi.nlm.nih.gov/pubmed/31996775
http://dx.doi.org/10.1038/s41598-020-58496-4
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author Baena, Daniel
Cantero, Jose L.
Fuentemilla, Lluís
Atienza, Mercedes
author_facet Baena, Daniel
Cantero, Jose L.
Fuentemilla, Lluís
Atienza, Mercedes
author_sort Baena, Daniel
collection PubMed
description Sleep is thought to play a complementary role in human memory processing: sleep loss impairs the formation of new memories during the following awake period and, conversely, normal sleep promotes the strengthening of the already encoded memories. However, whether sleep can strengthen deteriorated memories caused by insufficient sleep remains unknown. Here, we showed that sleep restriction in a group of participants caused a reduction in the stability of EEG activity patterns across multiple encoding of the same event during awake, compared with a group of participants that got a full night’s sleep. The decrease of neural stability patterns in the sleep-restricted group was associated with higher slow oscillation-spindle coupling during a subsequent night of normal sleep duration, thereby suggesting the instantiation of restorative neural mechanisms adaptively supporting cognition and memory. Importantly, upon awaking, the two groups of participants showed equivalent retrieval accuracy supported by subtle differences in the reinstatement of encoding-related activity: it was longer lasting in sleep-restricted individuals than in controls. In addition, sustained reinstatement over time was associated with increased coupling between spindles and slow oscillations. Taken together, these results suggest that the strength of prior encoding might be an important moderator of memory consolidation during sleep. Supporting this view, spindles nesting in the slow oscillation increased the probability of correct recognition only for weakly encoded memories. Current results demonstrate the benefit that a full night’s sleep can induce to impaired memory traces caused by an inadequate amount of sleep.
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spelling pubmed-69894952020-02-05 Weakly encoded memories due to acute sleep restriction can be rescued after one night of recovery sleep Baena, Daniel Cantero, Jose L. Fuentemilla, Lluís Atienza, Mercedes Sci Rep Article Sleep is thought to play a complementary role in human memory processing: sleep loss impairs the formation of new memories during the following awake period and, conversely, normal sleep promotes the strengthening of the already encoded memories. However, whether sleep can strengthen deteriorated memories caused by insufficient sleep remains unknown. Here, we showed that sleep restriction in a group of participants caused a reduction in the stability of EEG activity patterns across multiple encoding of the same event during awake, compared with a group of participants that got a full night’s sleep. The decrease of neural stability patterns in the sleep-restricted group was associated with higher slow oscillation-spindle coupling during a subsequent night of normal sleep duration, thereby suggesting the instantiation of restorative neural mechanisms adaptively supporting cognition and memory. Importantly, upon awaking, the two groups of participants showed equivalent retrieval accuracy supported by subtle differences in the reinstatement of encoding-related activity: it was longer lasting in sleep-restricted individuals than in controls. In addition, sustained reinstatement over time was associated with increased coupling between spindles and slow oscillations. Taken together, these results suggest that the strength of prior encoding might be an important moderator of memory consolidation during sleep. Supporting this view, spindles nesting in the slow oscillation increased the probability of correct recognition only for weakly encoded memories. Current results demonstrate the benefit that a full night’s sleep can induce to impaired memory traces caused by an inadequate amount of sleep. Nature Publishing Group UK 2020-01-29 /pmc/articles/PMC6989495/ /pubmed/31996775 http://dx.doi.org/10.1038/s41598-020-58496-4 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Baena, Daniel
Cantero, Jose L.
Fuentemilla, Lluís
Atienza, Mercedes
Weakly encoded memories due to acute sleep restriction can be rescued after one night of recovery sleep
title Weakly encoded memories due to acute sleep restriction can be rescued after one night of recovery sleep
title_full Weakly encoded memories due to acute sleep restriction can be rescued after one night of recovery sleep
title_fullStr Weakly encoded memories due to acute sleep restriction can be rescued after one night of recovery sleep
title_full_unstemmed Weakly encoded memories due to acute sleep restriction can be rescued after one night of recovery sleep
title_short Weakly encoded memories due to acute sleep restriction can be rescued after one night of recovery sleep
title_sort weakly encoded memories due to acute sleep restriction can be rescued after one night of recovery sleep
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6989495/
https://www.ncbi.nlm.nih.gov/pubmed/31996775
http://dx.doi.org/10.1038/s41598-020-58496-4
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