Sleep disrupts complex spiking dynamics in the neocortex and hippocampus

Detalhes bibliográficos
Autor(a) principal: González, Joaquín
Data de Publicação: 2023
Outros Autores: Cavelli, Matias, Tort, Adriano Bretanha Lopes, Torterolo, Pablo, Rubido, Nicolás
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UFRN
Texto Completo: https://repositorio.ufrn.br/handle/123456789/54971
Resumo: Neuronal interactions give rise to complex dynamics in cortical networks, often described in terms of the diversity of activity patterns observed in a neural signal. Interestingly, the complexity of spontaneous electroencephalographic signals decreases during slow-wave sleep (SWS); however, the underlying neural mechanisms remain elusive. Here, we analyse in-vivo recordings from neocortical and hippocampal neuronal populations in rats and show that the complexity decrease is due to the emergence of synchronous neuronal DOWN states. Namely, we find that DOWN states during SWS force the population activity to be more recurrent, deterministic, and less random than during REM sleep or wakefulness, which, in turn, leads to less complex field recordings. Importantly, when we exclude DOWN states from the analysis, the recordings during wakefulness and sleep become indistinguishable: the spiking activity in all the states collapses to a common scaling. We complement these results by implementing a critical branching model of the cortex, which shows that inducing DOWN states to only a percentage of neurons is enough to generate a decrease in complexity that replicates SWS
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spelling González, JoaquínCavelli, MatiasTort, Adriano Bretanha LopesTorterolo, PabloRubido, Nicolás2023-10-11T17:30:20Z2023-10-11T17:30:20Z2023-08GONZÁLEZ, Joaquín; CAVELLI, Matias; TORT, Adriano B. L.; TORTEROLO, Pablo; RUBIDO, Nicolás. Sleep disrupts complex spiking dynamics in the neocortex and hippocampus. Plos One, [S. l.], v. 18, n. 8, p. e0290146, ago. 2023. Doi: http://dx.doi.org/10.1371/journal.pone.0290146. Disponível em: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0290146. Acesso em: 11 out. 2023https://repositorio.ufrn.br/handle/123456789/5497110.1371/journal.pone.0290146Public Library of Science (PLoS)Attribution 3.0 Brazilhttp://creativecommons.org/licenses/by/3.0/br/info:eu-repo/semantics/openAccessSleep - NeocortexSleep - HippocampusSpontaneous electroencephalographic signals - Slow-wave sleep (SWS)Neuronal DOWN statesNeuronal modellingIn-vivo neuronal populationsSleep disrupts complex spiking dynamics in the neocortex and hippocampusinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleNeuronal interactions give rise to complex dynamics in cortical networks, often described in terms of the diversity of activity patterns observed in a neural signal. Interestingly, the complexity of spontaneous electroencephalographic signals decreases during slow-wave sleep (SWS); however, the underlying neural mechanisms remain elusive. Here, we analyse in-vivo recordings from neocortical and hippocampal neuronal populations in rats and show that the complexity decrease is due to the emergence of synchronous neuronal DOWN states. Namely, we find that DOWN states during SWS force the population activity to be more recurrent, deterministic, and less random than during REM sleep or wakefulness, which, in turn, leads to less complex field recordings. Importantly, when we exclude DOWN states from the analysis, the recordings during wakefulness and sleep become indistinguishable: the spiking activity in all the states collapses to a common scaling. We complement these results by implementing a critical branching model of the cortex, which shows that inducing DOWN states to only a percentage of neurons is enough to generate a decrease in complexity that replicates SWSengreponame:Repositório Institucional da UFRNinstname:Universidade Federal do Rio Grande do Norte (UFRN)instacron:UFRNORIGINALSleepDisruptsComplex_Tort_2023.pdfSleepDisruptsComplex_Tort_2023.pdfSleepDisruptsComplex_Tort_2023application/pdf3185741https://repositorio.ufrn.br/bitstream/123456789/54971/1/SleepDisruptsComplex_Tort_2023.pdfbd104fa19a4afc334b4b4a8bac3ee452MD51CC-LICENSElicense_rdflicense_rdfapplication/rdf+xml; charset=utf-8914https://repositorio.ufrn.br/bitstream/123456789/54971/2/license_rdf4d2950bda3d176f570a9f8b328dfbbefMD52LICENSElicense.txtlicense.txttext/plain; charset=utf-81484https://repositorio.ufrn.br/bitstream/123456789/54971/3/license.txte9597aa2854d128fd968be5edc8a28d9MD53123456789/549712023-10-11 14:30:20.809oai:https://repositorio.ufrn.br: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Repositório de PublicaçõesPUBhttp://repositorio.ufrn.br/oai/opendoar:2023-10-11T17:30:20Repositório Institucional da UFRN - Universidade Federal do Rio Grande do Norte (UFRN)false
dc.title.pt_BR.fl_str_mv Sleep disrupts complex spiking dynamics in the neocortex and hippocampus
title Sleep disrupts complex spiking dynamics in the neocortex and hippocampus
spellingShingle Sleep disrupts complex spiking dynamics in the neocortex and hippocampus
González, Joaquín
Sleep - Neocortex
Sleep - Hippocampus
Spontaneous electroencephalographic signals - Slow-wave sleep (SWS)
Neuronal DOWN states
Neuronal modelling
In-vivo neuronal populations
title_short Sleep disrupts complex spiking dynamics in the neocortex and hippocampus
title_full Sleep disrupts complex spiking dynamics in the neocortex and hippocampus
title_fullStr Sleep disrupts complex spiking dynamics in the neocortex and hippocampus
title_full_unstemmed Sleep disrupts complex spiking dynamics in the neocortex and hippocampus
title_sort Sleep disrupts complex spiking dynamics in the neocortex and hippocampus
author González, Joaquín
author_facet González, Joaquín
Cavelli, Matias
Tort, Adriano Bretanha Lopes
Torterolo, Pablo
Rubido, Nicolás
author_role author
author2 Cavelli, Matias
Tort, Adriano Bretanha Lopes
Torterolo, Pablo
Rubido, Nicolás
author2_role author
author
author
author
dc.contributor.author.fl_str_mv González, Joaquín
Cavelli, Matias
Tort, Adriano Bretanha Lopes
Torterolo, Pablo
Rubido, Nicolás
dc.subject.por.fl_str_mv Sleep - Neocortex
Sleep - Hippocampus
Spontaneous electroencephalographic signals - Slow-wave sleep (SWS)
Neuronal DOWN states
Neuronal modelling
In-vivo neuronal populations
topic Sleep - Neocortex
Sleep - Hippocampus
Spontaneous electroencephalographic signals - Slow-wave sleep (SWS)
Neuronal DOWN states
Neuronal modelling
In-vivo neuronal populations
description Neuronal interactions give rise to complex dynamics in cortical networks, often described in terms of the diversity of activity patterns observed in a neural signal. Interestingly, the complexity of spontaneous electroencephalographic signals decreases during slow-wave sleep (SWS); however, the underlying neural mechanisms remain elusive. Here, we analyse in-vivo recordings from neocortical and hippocampal neuronal populations in rats and show that the complexity decrease is due to the emergence of synchronous neuronal DOWN states. Namely, we find that DOWN states during SWS force the population activity to be more recurrent, deterministic, and less random than during REM sleep or wakefulness, which, in turn, leads to less complex field recordings. Importantly, when we exclude DOWN states from the analysis, the recordings during wakefulness and sleep become indistinguishable: the spiking activity in all the states collapses to a common scaling. We complement these results by implementing a critical branching model of the cortex, which shows that inducing DOWN states to only a percentage of neurons is enough to generate a decrease in complexity that replicates SWS
publishDate 2023
dc.date.accessioned.fl_str_mv 2023-10-11T17:30:20Z
dc.date.available.fl_str_mv 2023-10-11T17:30:20Z
dc.date.issued.fl_str_mv 2023-08
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
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status_str publishedVersion
dc.identifier.citation.fl_str_mv GONZÁLEZ, Joaquín; CAVELLI, Matias; TORT, Adriano B. L.; TORTEROLO, Pablo; RUBIDO, Nicolás. Sleep disrupts complex spiking dynamics in the neocortex and hippocampus. Plos One, [S. l.], v. 18, n. 8, p. e0290146, ago. 2023. Doi: http://dx.doi.org/10.1371/journal.pone.0290146. Disponível em: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0290146. Acesso em: 11 out. 2023
dc.identifier.uri.fl_str_mv https://repositorio.ufrn.br/handle/123456789/54971
dc.identifier.doi.none.fl_str_mv 10.1371/journal.pone.0290146
identifier_str_mv GONZÁLEZ, Joaquín; CAVELLI, Matias; TORT, Adriano B. L.; TORTEROLO, Pablo; RUBIDO, Nicolás. Sleep disrupts complex spiking dynamics in the neocortex and hippocampus. Plos One, [S. l.], v. 18, n. 8, p. e0290146, ago. 2023. Doi: http://dx.doi.org/10.1371/journal.pone.0290146. Disponível em: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0290146. Acesso em: 11 out. 2023
10.1371/journal.pone.0290146
url https://repositorio.ufrn.br/handle/123456789/54971
dc.language.iso.fl_str_mv eng
language eng
dc.rights.driver.fl_str_mv Attribution 3.0 Brazil
http://creativecommons.org/licenses/by/3.0/br/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv Attribution 3.0 Brazil
http://creativecommons.org/licenses/by/3.0/br/
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Public Library of Science (PLoS)
publisher.none.fl_str_mv Public Library of Science (PLoS)
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