The temporal asymmetry of cortical dynamics as a signature of brain states

The brain is a complex non-equilibrium system capable of expressing many different dynamics as well as the transitions between them. We hypothesized that the level of non-equilibrium can serve as a signature of a given brain state, which was quantified using the arrow of time (the level of irreversi...

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Autores: Camassa, Alessandra, Torao-Angosto, Melody, Manasanch, Arnau, Kringelbach, Morten L., Deco, Gustavo, Sanchez-Vives, Maria V.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10230/72741
Acceso en línea:https://hdl.handle.net/10230/72741
http://dx.doi.org/10.1038/s41598-024-74649-1
Access Level:acceso abierto
Palabra clave:Cerebral cortex
Synchronization
Oscillations
Cortical dynamics
Anesthesia
Slow waves
Sleep
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spelling The temporal asymmetry of cortical dynamics as a signature of brain statesCamassa, AlessandraTorao-Angosto, MelodyManasanch, ArnauKringelbach, Morten L.Deco, GustavoSanchez-Vives, Maria V.Cerebral cortexSynchronizationOscillationsCortical dynamicsAnesthesiaSlow wavesSleepThe brain is a complex non-equilibrium system capable of expressing many different dynamics as well as the transitions between them. We hypothesized that the level of non-equilibrium can serve as a signature of a given brain state, which was quantified using the arrow of time (the level of irreversibility). Using this thermodynamic framework, the irreversibility of emergent cortical activity was quantified from local field potential recordings in male Lister-hooded rats at different anesthesia levels and during the sleep-wake cycle. This measure was carried out on five distinct brain states: slow-wave sleep, awake, deep anesthesia'slow waves, light anesthesia'slow waves, and microarousals. Low levels of irreversibility were associated with synchronous activity found both in deep anesthesia and slow-wave sleep states, suggesting that slow waves were the state closest to the thermodynamic equilibrium (maximum symmetry), thus requiring minimum energy. Higher levels of irreversibility were found when brain dynamics became more asynchronous, for example, in wakefulness. These changes were also reflected in the hierarchy of cortical dynamics across different cortical areas. The neural dynamics associated with different brain states were characterized by different degrees of irreversibility and hierarchy, also acting as markers of brain state transitions. This could open new routes to monitoring, controlling, and even changing brain states in health and disease.This work has received funding from the European Union's Horizon 2020 Framework Programme for Research and Innovation under the Specific Grant Agreement No. 945539 (Human Brain Project SGA3) to MVSV and GD. It has also been funded by the Spanish Ministry of Science and Innovation through the MICIN/AEI under grant PID2020-112947RB-I00 to MVSV. The authors thank Tony Donegan for language editing.Nature Research2026202620242026info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttps://hdl.handle.net/10230/72741http://dx.doi.org/10.1038/s41598-024-74649-1https://hdl.handle.net/10230/72741reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésScientific Reports. 2024 Oct 16;14(1):24271info:eu-repo/grantAgreement/EC/H2020/945539info:eu-repo/grantAgreement/ES/2PE/PID2020-112947RB-I00This 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/.http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:recercat.cat:10230/727412026-05-29T05:05:01Z
dc.title.none.fl_str_mv The temporal asymmetry of cortical dynamics as a signature of brain states
title The temporal asymmetry of cortical dynamics as a signature of brain states
spellingShingle The temporal asymmetry of cortical dynamics as a signature of brain states
Camassa, Alessandra
Cerebral cortex
Synchronization
Oscillations
Cortical dynamics
Anesthesia
Slow waves
Sleep
title_short The temporal asymmetry of cortical dynamics as a signature of brain states
title_full The temporal asymmetry of cortical dynamics as a signature of brain states
title_fullStr The temporal asymmetry of cortical dynamics as a signature of brain states
title_full_unstemmed The temporal asymmetry of cortical dynamics as a signature of brain states
title_sort The temporal asymmetry of cortical dynamics as a signature of brain states
dc.creator.none.fl_str_mv Camassa, Alessandra
Torao-Angosto, Melody
Manasanch, Arnau
Kringelbach, Morten L.
Deco, Gustavo
Sanchez-Vives, Maria V.
author Camassa, Alessandra
author_facet Camassa, Alessandra
Torao-Angosto, Melody
Manasanch, Arnau
Kringelbach, Morten L.
Deco, Gustavo
Sanchez-Vives, Maria V.
author_role author
author2 Torao-Angosto, Melody
Manasanch, Arnau
Kringelbach, Morten L.
Deco, Gustavo
Sanchez-Vives, Maria V.
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv Cerebral cortex
Synchronization
Oscillations
Cortical dynamics
Anesthesia
Slow waves
Sleep
topic Cerebral cortex
Synchronization
Oscillations
Cortical dynamics
Anesthesia
Slow waves
Sleep
description The brain is a complex non-equilibrium system capable of expressing many different dynamics as well as the transitions between them. We hypothesized that the level of non-equilibrium can serve as a signature of a given brain state, which was quantified using the arrow of time (the level of irreversibility). Using this thermodynamic framework, the irreversibility of emergent cortical activity was quantified from local field potential recordings in male Lister-hooded rats at different anesthesia levels and during the sleep-wake cycle. This measure was carried out on five distinct brain states: slow-wave sleep, awake, deep anesthesia'slow waves, light anesthesia'slow waves, and microarousals. Low levels of irreversibility were associated with synchronous activity found both in deep anesthesia and slow-wave sleep states, suggesting that slow waves were the state closest to the thermodynamic equilibrium (maximum symmetry), thus requiring minimum energy. Higher levels of irreversibility were found when brain dynamics became more asynchronous, for example, in wakefulness. These changes were also reflected in the hierarchy of cortical dynamics across different cortical areas. The neural dynamics associated with different brain states were characterized by different degrees of irreversibility and hierarchy, also acting as markers of brain state transitions. This could open new routes to monitoring, controlling, and even changing brain states in health and disease.
publishDate 2024
dc.date.none.fl_str_mv 2024
2026
2026
2026
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/10230/72741
http://dx.doi.org/10.1038/s41598-024-74649-1
https://hdl.handle.net/10230/72741
url https://hdl.handle.net/10230/72741
http://dx.doi.org/10.1038/s41598-024-74649-1
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Scientific Reports. 2024 Oct 16;14(1):24271
info:eu-repo/grantAgreement/EC/H2020/945539
info:eu-repo/grantAgreement/ES/2PE/PID2020-112947RB-I00
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Nature Research
publisher.none.fl_str_mv Nature Research
dc.source.none.fl_str_mv reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
repository.name.fl_str_mv
repository.mail.fl_str_mv
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