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Disruption of NREM sleep and sleep-related spatial memory consolidation in mice lacking adult hippocampal neurogenesis

Cellular plasticity at the structural level and sleep at the behavioural level are both essential for memory formation. The link between the two is not well understood. A functional connection between adult neurogenesis and hippocampus-dependent memory consolidation during NREM sleep has been hypoth...

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Autores principales: Sippel, D., Schwabedal, J., Snyder, J. C., Oyanedel, C. N., Bernas, S. N., Garthe, A., Tröndle, A., Storch, A., Kempermann, G., Brandt, M. D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7536189/
https://www.ncbi.nlm.nih.gov/pubmed/33020501
http://dx.doi.org/10.1038/s41598-020-72362-3
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author Sippel, D.
Schwabedal, J.
Snyder, J. C.
Oyanedel, C. N.
Bernas, S. N.
Garthe, A.
Tröndle, A.
Storch, A.
Kempermann, G.
Brandt, M. D.
author_facet Sippel, D.
Schwabedal, J.
Snyder, J. C.
Oyanedel, C. N.
Bernas, S. N.
Garthe, A.
Tröndle, A.
Storch, A.
Kempermann, G.
Brandt, M. D.
author_sort Sippel, D.
collection PubMed
description Cellular plasticity at the structural level and sleep at the behavioural level are both essential for memory formation. The link between the two is not well understood. A functional connection between adult neurogenesis and hippocampus-dependent memory consolidation during NREM sleep has been hypothesized but not experimentally shown. Here, we present evidence that during a three-day learning session in the Morris water maze task a genetic knockout model of adult neurogenesis (Cyclin D2(−/−)) showed changes in sleep macro- and microstructure. Sleep EEG analyses revealed a lower total sleep time and NREM fraction in Cyclin D2(−/−) mice as well as an impairment of sleep specific neuronal oscillations that are associated with memory consolidation. Better performance in the memory task was associated with specific sleep parameters in wild-type, but not in Cyclin D2(−/−) mice. In wild-type animals the number of proliferating cells correlated with the amount of NREM sleep. The lack of adult neurogenesis led to changes in sleep architecture and oscillations that represent the dialog between hippocampus and neocortex during sleep. We suggest that adult neurogenesis—as a key event of hippocampal plasticity—might play an important role for sleep-dependent memory consolidation and modulates learning-induced changes of sleep macro- and microstructure.
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spelling pubmed-75361892020-10-06 Disruption of NREM sleep and sleep-related spatial memory consolidation in mice lacking adult hippocampal neurogenesis Sippel, D. Schwabedal, J. Snyder, J. C. Oyanedel, C. N. Bernas, S. N. Garthe, A. Tröndle, A. Storch, A. Kempermann, G. Brandt, M. D. Sci Rep Article Cellular plasticity at the structural level and sleep at the behavioural level are both essential for memory formation. The link between the two is not well understood. A functional connection between adult neurogenesis and hippocampus-dependent memory consolidation during NREM sleep has been hypothesized but not experimentally shown. Here, we present evidence that during a three-day learning session in the Morris water maze task a genetic knockout model of adult neurogenesis (Cyclin D2(−/−)) showed changes in sleep macro- and microstructure. Sleep EEG analyses revealed a lower total sleep time and NREM fraction in Cyclin D2(−/−) mice as well as an impairment of sleep specific neuronal oscillations that are associated with memory consolidation. Better performance in the memory task was associated with specific sleep parameters in wild-type, but not in Cyclin D2(−/−) mice. In wild-type animals the number of proliferating cells correlated with the amount of NREM sleep. The lack of adult neurogenesis led to changes in sleep architecture and oscillations that represent the dialog between hippocampus and neocortex during sleep. We suggest that adult neurogenesis—as a key event of hippocampal plasticity—might play an important role for sleep-dependent memory consolidation and modulates learning-induced changes of sleep macro- and microstructure. Nature Publishing Group UK 2020-10-05 /pmc/articles/PMC7536189/ /pubmed/33020501 http://dx.doi.org/10.1038/s41598-020-72362-3 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Sippel, D.
Schwabedal, J.
Snyder, J. C.
Oyanedel, C. N.
Bernas, S. N.
Garthe, A.
Tröndle, A.
Storch, A.
Kempermann, G.
Brandt, M. D.
Disruption of NREM sleep and sleep-related spatial memory consolidation in mice lacking adult hippocampal neurogenesis
title Disruption of NREM sleep and sleep-related spatial memory consolidation in mice lacking adult hippocampal neurogenesis
title_full Disruption of NREM sleep and sleep-related spatial memory consolidation in mice lacking adult hippocampal neurogenesis
title_fullStr Disruption of NREM sleep and sleep-related spatial memory consolidation in mice lacking adult hippocampal neurogenesis
title_full_unstemmed Disruption of NREM sleep and sleep-related spatial memory consolidation in mice lacking adult hippocampal neurogenesis
title_short Disruption of NREM sleep and sleep-related spatial memory consolidation in mice lacking adult hippocampal neurogenesis
title_sort disruption of nrem sleep and sleep-related spatial memory consolidation in mice lacking adult hippocampal neurogenesis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7536189/
https://www.ncbi.nlm.nih.gov/pubmed/33020501
http://dx.doi.org/10.1038/s41598-020-72362-3
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