Perturbation of whole-brain dynamics in silico reveals mechanistic differences between brain states

Detalhes bibliográficos
Autor(a) principal: Deco, Gustavo
Data de Publicação: 2018
Outros Autores: Cabral, Joana, Saenger, Victor M., Boly, Melanie, Tagliazucchi, Enzo, Laufs, Helmut, Van Someren, Eus, Jobst, Beatrice, Stevner, Angus, Kringelbach, Morten L.
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: https://hdl.handle.net/1822/57816
Resumo: Human neuroimaging research has revealed that wakefulness and sleep involve very different activity patterns. Yet, it is not clear why brain states differ in their dynamical complexity, e.g. in the level of integration and segregation across brain networks over time. Here, we investigate the mechanisms underlying the dynamical stability of brain states using a novel off-line in silico perturbation protocol. We first adjust a whole-brain computational model to the basal dynamics of wakefulness and deep sleep recorded with fMRI in two independent human fMRI datasets. Then, the models of sleep and awake brain states are perturbed using two distinct multifocal protocols either promoting or disrupting synchronization in randomly selected brain areas. Once perturbation is halted, we use a novel measure, the Perturbative Integration Latency Index (PILI), to evaluate the recovery back to baseline. We find a clear distinction between models, consistently showing larger PILI in wakefulness than in deep sleep, corroborating previous experimental findings. In the models, larger recoveries are associated to a critical slowing down induced by a shift in the model's operation point, indicating that the awake brain operates further from a stable equilibrium than deep sleep. This novel approach opens up for a new level of artificial perturbative studies unconstrained by ethical limitations allowing for a deeper investigation of the dynamical properties of different brain states.
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spelling Perturbation of whole-brain dynamics in silico reveals mechanistic differences between brain statesAdultBrainComputer SimulationElectroencephalographyFunctional NeuroimagingHumansMagnetic Resonance ImagingSleep StagesWakefulnessBrain stateSleepWhole brain modelingPerturbationScience & TechnologyHuman neuroimaging research has revealed that wakefulness and sleep involve very different activity patterns. Yet, it is not clear why brain states differ in their dynamical complexity, e.g. in the level of integration and segregation across brain networks over time. Here, we investigate the mechanisms underlying the dynamical stability of brain states using a novel off-line in silico perturbation protocol. We first adjust a whole-brain computational model to the basal dynamics of wakefulness and deep sleep recorded with fMRI in two independent human fMRI datasets. Then, the models of sleep and awake brain states are perturbed using two distinct multifocal protocols either promoting or disrupting synchronization in randomly selected brain areas. Once perturbation is halted, we use a novel measure, the Perturbative Integration Latency Index (PILI), to evaluate the recovery back to baseline. We find a clear distinction between models, consistently showing larger PILI in wakefulness than in deep sleep, corroborating previous experimental findings. In the models, larger recoveries are associated to a critical slowing down induced by a shift in the model's operation point, indicating that the awake brain operates further from a stable equilibrium than deep sleep. This novel approach opens up for a new level of artificial perturbative studies unconstrained by ethical limitations allowing for a deeper investigation of the dynamical properties of different brain states.GD was supported by the ERC Advanced Grant: DYSTRUCTURE (n. 295129), by the Spanish Research Project SAF2010-16085 and the FP7-ICT BrainScales. MLK and JC were supported by the ERC Consolidator Grant: CAREGIVING (n. 615539) and Center for Music in the Brain, funded by the Danish National Research Foundation (DNRF117). JC was supported under the project NORTE-01-0145-FEDER-000023, supported by the Northern Portugal Regional Operational Programme (NORTE 2020), under the Portugal 2020 Partnership Agreement, through the European Regional Development Fund (FEDER).info:eu-repo/semantics/publishedVersionElsevierUniversidade do MinhoDeco, GustavoCabral, JoanaSaenger, Victor M.Boly, MelanieTagliazucchi, EnzoLaufs, HelmutVan Someren, EusJobst, BeatriceStevner, AngusKringelbach, Morten L.2018-042018-04-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttps://hdl.handle.net/1822/57816engDeco, G., Cabral, J., Saenger, V. M., Boly, M., Tagliazucchi, E., Laufs, H., ... & Kringelbach, M. L. (2018). Perturbation of whole-brain dynamics in silico reveals mechanistic differences between brain states. NeuroImage, 169, 46-561053-81191095-957210.1016/j.neuroimage.2017.12.00929225066info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2023-09-30T01:28:18Zoai:repositorium.sdum.uminho.pt:1822/57816Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T19:15:40.001284Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse
dc.title.none.fl_str_mv Perturbation of whole-brain dynamics in silico reveals mechanistic differences between brain states
title Perturbation of whole-brain dynamics in silico reveals mechanistic differences between brain states
spellingShingle Perturbation of whole-brain dynamics in silico reveals mechanistic differences between brain states
Deco, Gustavo
Adult
Brain
Computer Simulation
Electroencephalography
Functional Neuroimaging
Humans
Magnetic Resonance Imaging
Sleep Stages
Wakefulness
Brain state
Sleep
Whole brain modeling
Perturbation
Science & Technology
title_short Perturbation of whole-brain dynamics in silico reveals mechanistic differences between brain states
title_full Perturbation of whole-brain dynamics in silico reveals mechanistic differences between brain states
title_fullStr Perturbation of whole-brain dynamics in silico reveals mechanistic differences between brain states
title_full_unstemmed Perturbation of whole-brain dynamics in silico reveals mechanistic differences between brain states
title_sort Perturbation of whole-brain dynamics in silico reveals mechanistic differences between brain states
author Deco, Gustavo
author_facet Deco, Gustavo
Cabral, Joana
Saenger, Victor M.
Boly, Melanie
Tagliazucchi, Enzo
Laufs, Helmut
Van Someren, Eus
Jobst, Beatrice
Stevner, Angus
Kringelbach, Morten L.
author_role author
author2 Cabral, Joana
Saenger, Victor M.
Boly, Melanie
Tagliazucchi, Enzo
Laufs, Helmut
Van Someren, Eus
Jobst, Beatrice
Stevner, Angus
Kringelbach, Morten L.
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Universidade do Minho
dc.contributor.author.fl_str_mv Deco, Gustavo
Cabral, Joana
Saenger, Victor M.
Boly, Melanie
Tagliazucchi, Enzo
Laufs, Helmut
Van Someren, Eus
Jobst, Beatrice
Stevner, Angus
Kringelbach, Morten L.
dc.subject.por.fl_str_mv Adult
Brain
Computer Simulation
Electroencephalography
Functional Neuroimaging
Humans
Magnetic Resonance Imaging
Sleep Stages
Wakefulness
Brain state
Sleep
Whole brain modeling
Perturbation
Science & Technology
topic Adult
Brain
Computer Simulation
Electroencephalography
Functional Neuroimaging
Humans
Magnetic Resonance Imaging
Sleep Stages
Wakefulness
Brain state
Sleep
Whole brain modeling
Perturbation
Science & Technology
description Human neuroimaging research has revealed that wakefulness and sleep involve very different activity patterns. Yet, it is not clear why brain states differ in their dynamical complexity, e.g. in the level of integration and segregation across brain networks over time. Here, we investigate the mechanisms underlying the dynamical stability of brain states using a novel off-line in silico perturbation protocol. We first adjust a whole-brain computational model to the basal dynamics of wakefulness and deep sleep recorded with fMRI in two independent human fMRI datasets. Then, the models of sleep and awake brain states are perturbed using two distinct multifocal protocols either promoting or disrupting synchronization in randomly selected brain areas. Once perturbation is halted, we use a novel measure, the Perturbative Integration Latency Index (PILI), to evaluate the recovery back to baseline. We find a clear distinction between models, consistently showing larger PILI in wakefulness than in deep sleep, corroborating previous experimental findings. In the models, larger recoveries are associated to a critical slowing down induced by a shift in the model's operation point, indicating that the awake brain operates further from a stable equilibrium than deep sleep. This novel approach opens up for a new level of artificial perturbative studies unconstrained by ethical limitations allowing for a deeper investigation of the dynamical properties of different brain states.
publishDate 2018
dc.date.none.fl_str_mv 2018-04
2018-04-01T00:00:00Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv https://hdl.handle.net/1822/57816
url https://hdl.handle.net/1822/57816
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Deco, G., Cabral, J., Saenger, V. M., Boly, M., Tagliazucchi, E., Laufs, H., ... & Kringelbach, M. L. (2018). Perturbation of whole-brain dynamics in silico reveals mechanistic differences between brain states. NeuroImage, 169, 46-56
1053-8119
1095-9572
10.1016/j.neuroimage.2017.12.009
29225066
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
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collection Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
repository.name.fl_str_mv Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
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