Modeling regional changes in dynamic stability during sleep and wakefulness

Autores
Perez Ipiña, Ignacio Martin; Donnelly Kehoe, Patricio Andres; Kringelbach, Morten; Laufs, Helmut; Ibañez, Agustin; Deco, Gustavo; Sanz Perl Hernandez, Yonatan; Tagliazucchi, Enzo Rodolfo
Año de publicación
2020
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Global brain states are frequently placed within a unidimensional continuum by correlational studies, ranging from states of deep unconsciousness to ordinary wakefulness. An alternative is their multidimensional and mechanistic characterization in terms of different cognitive capacities, using computational models to reproduce the underlying neural dynamics. We explore this alternative by introducing a semi-empirical model linking regional activation and long-range functional connectivity in the different brain states visited during the natural wake-sleep cycle. Our model combines functional magnetic resonance imaging (fMRI) data, in vivo estimates of structural connectivity, and anatomically-informed priors to constrain the independent variation of regional activation. The best fit to empirical data was achieved using priors based on functionally coherent networks, with the resulting model parameters dividing the cortex into regions presenting opposite dynamical behavior. Frontoparietal regions approached a bifurcation from dynamics at a fixed point governed by noise, while sensorimotor regions approached a bifurcation from oscillatory dynamics. In agreement with human electrophysiological experiments, sleep onset induced subcortical deactivation with low correlation, which was subsequently reversed for deeper stages. Finally, we introduced periodic forcing of variable intensity to simulate external perturbations, and identified the key regions relevant for the recovery of wakefulness from deep sleep. Our model represents sleep as a state with diminished perceptual gating and the latent capacity for global accessibility that is required for rapid arousals. To the extent that the qualitative characterization of local dynamics is exhausted by the dichotomy between unstable and stable behavior, our work highlights how expanding the model parameter space can describe states of consciousness in terms of multiple dimensions with interpretations given by the choice of anatomically-informed priors.
Fil: Perez Ipiña, Ignacio Martin. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Física; Argentina
Fil: Donnelly Kehoe, Patricio Andres. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Centro Internacional Franco Argentino de Ciencias de la Información y de Sistemas. Universidad Nacional de Rosario. Centro Internacional Franco Argentino de Ciencias de la Información y de Sistemas; Argentina
Fil: Kringelbach, Morten. University of Oxford; Reino Unido. University Aarhus; Dinamarca
Fil: Laufs, Helmut. University of Kiel; Alemania
Fil: Ibañez, Agustin. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Neurociencia Cognitiva. Fundación Favaloro. Instituto de Neurociencia Cognitiva; Argentina. Universidad de San Andrés; Argentina. Australian Research Council; Australia. Universidad Adolfo Ibañez; Chile. Universidad Autónoma del Caribe; Colombia
Fil: Deco, Gustavo. Universitat Pompeu Fabra; España
Fil: Sanz Perl Hernandez, Yonatan. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de San Andrés; Argentina
Fil: Tagliazucchi, Enzo Rodolfo. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Física; Argentina
Materia
Whole-Brain Models
Neuroscience
Non-linear dynamics
Human Sleep Stages
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/140103

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network_name_str CONICET Digital (CONICET)
spelling Modeling regional changes in dynamic stability during sleep and wakefulnessPerez Ipiña, Ignacio MartinDonnelly Kehoe, Patricio AndresKringelbach, MortenLaufs, HelmutIbañez, AgustinDeco, GustavoSanz Perl Hernandez, YonatanTagliazucchi, Enzo RodolfoWhole-Brain ModelsNeuroscienceNon-linear dynamicsHuman Sleep Stageshttps://purl.org/becyt/ford/3.3https://purl.org/becyt/ford/3Global brain states are frequently placed within a unidimensional continuum by correlational studies, ranging from states of deep unconsciousness to ordinary wakefulness. An alternative is their multidimensional and mechanistic characterization in terms of different cognitive capacities, using computational models to reproduce the underlying neural dynamics. We explore this alternative by introducing a semi-empirical model linking regional activation and long-range functional connectivity in the different brain states visited during the natural wake-sleep cycle. Our model combines functional magnetic resonance imaging (fMRI) data, in vivo estimates of structural connectivity, and anatomically-informed priors to constrain the independent variation of regional activation. The best fit to empirical data was achieved using priors based on functionally coherent networks, with the resulting model parameters dividing the cortex into regions presenting opposite dynamical behavior. Frontoparietal regions approached a bifurcation from dynamics at a fixed point governed by noise, while sensorimotor regions approached a bifurcation from oscillatory dynamics. In agreement with human electrophysiological experiments, sleep onset induced subcortical deactivation with low correlation, which was subsequently reversed for deeper stages. Finally, we introduced periodic forcing of variable intensity to simulate external perturbations, and identified the key regions relevant for the recovery of wakefulness from deep sleep. Our model represents sleep as a state with diminished perceptual gating and the latent capacity for global accessibility that is required for rapid arousals. To the extent that the qualitative characterization of local dynamics is exhausted by the dichotomy between unstable and stable behavior, our work highlights how expanding the model parameter space can describe states of consciousness in terms of multiple dimensions with interpretations given by the choice of anatomically-informed priors.Fil: Perez Ipiña, Ignacio Martin. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Física; ArgentinaFil: Donnelly Kehoe, Patricio Andres. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Centro Internacional Franco Argentino de Ciencias de la Información y de Sistemas. Universidad Nacional de Rosario. Centro Internacional Franco Argentino de Ciencias de la Información y de Sistemas; ArgentinaFil: Kringelbach, Morten. University of Oxford; Reino Unido. University Aarhus; DinamarcaFil: Laufs, Helmut. University of Kiel; AlemaniaFil: Ibañez, Agustin. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Neurociencia Cognitiva. Fundación Favaloro. Instituto de Neurociencia Cognitiva; Argentina. Universidad de San Andrés; Argentina. Australian Research Council; Australia. Universidad Adolfo Ibañez; Chile. Universidad Autónoma del Caribe; ColombiaFil: Deco, Gustavo. Universitat Pompeu Fabra; EspañaFil: Sanz Perl Hernandez, Yonatan. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de San Andrés; ArgentinaFil: Tagliazucchi, Enzo Rodolfo. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Física; ArgentinaElsevier2020-07-15info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/140103Perez Ipiña, Ignacio Martin; Donnelly Kehoe, Patricio Andres; Kringelbach, Morten; Laufs, Helmut; Ibañez, Agustin; et al.; Modeling regional changes in dynamic stability during sleep and wakefulness; Elsevier; Journal Neuroimag; 215; 116833; 15-7-2020; 1-131053-8119CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://linkinghub.elsevier.com/retrieve/pii/S1053811920303207info:eu-repo/semantics/altIdentifier/doi/10.1016/j.neuroimage.2020.116833info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-15T14:40:31Zoai:ri.conicet.gov.ar:11336/140103instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-10-15 14:40:31.441CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Modeling regional changes in dynamic stability during sleep and wakefulness
title Modeling regional changes in dynamic stability during sleep and wakefulness
spellingShingle Modeling regional changes in dynamic stability during sleep and wakefulness
Perez Ipiña, Ignacio Martin
Whole-Brain Models
Neuroscience
Non-linear dynamics
Human Sleep Stages
title_short Modeling regional changes in dynamic stability during sleep and wakefulness
title_full Modeling regional changes in dynamic stability during sleep and wakefulness
title_fullStr Modeling regional changes in dynamic stability during sleep and wakefulness
title_full_unstemmed Modeling regional changes in dynamic stability during sleep and wakefulness
title_sort Modeling regional changes in dynamic stability during sleep and wakefulness
dc.creator.none.fl_str_mv Perez Ipiña, Ignacio Martin
Donnelly Kehoe, Patricio Andres
Kringelbach, Morten
Laufs, Helmut
Ibañez, Agustin
Deco, Gustavo
Sanz Perl Hernandez, Yonatan
Tagliazucchi, Enzo Rodolfo
author Perez Ipiña, Ignacio Martin
author_facet Perez Ipiña, Ignacio Martin
Donnelly Kehoe, Patricio Andres
Kringelbach, Morten
Laufs, Helmut
Ibañez, Agustin
Deco, Gustavo
Sanz Perl Hernandez, Yonatan
Tagliazucchi, Enzo Rodolfo
author_role author
author2 Donnelly Kehoe, Patricio Andres
Kringelbach, Morten
Laufs, Helmut
Ibañez, Agustin
Deco, Gustavo
Sanz Perl Hernandez, Yonatan
Tagliazucchi, Enzo Rodolfo
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Whole-Brain Models
Neuroscience
Non-linear dynamics
Human Sleep Stages
topic Whole-Brain Models
Neuroscience
Non-linear dynamics
Human Sleep Stages
purl_subject.fl_str_mv https://purl.org/becyt/ford/3.3
https://purl.org/becyt/ford/3
dc.description.none.fl_txt_mv Global brain states are frequently placed within a unidimensional continuum by correlational studies, ranging from states of deep unconsciousness to ordinary wakefulness. An alternative is their multidimensional and mechanistic characterization in terms of different cognitive capacities, using computational models to reproduce the underlying neural dynamics. We explore this alternative by introducing a semi-empirical model linking regional activation and long-range functional connectivity in the different brain states visited during the natural wake-sleep cycle. Our model combines functional magnetic resonance imaging (fMRI) data, in vivo estimates of structural connectivity, and anatomically-informed priors to constrain the independent variation of regional activation. The best fit to empirical data was achieved using priors based on functionally coherent networks, with the resulting model parameters dividing the cortex into regions presenting opposite dynamical behavior. Frontoparietal regions approached a bifurcation from dynamics at a fixed point governed by noise, while sensorimotor regions approached a bifurcation from oscillatory dynamics. In agreement with human electrophysiological experiments, sleep onset induced subcortical deactivation with low correlation, which was subsequently reversed for deeper stages. Finally, we introduced periodic forcing of variable intensity to simulate external perturbations, and identified the key regions relevant for the recovery of wakefulness from deep sleep. Our model represents sleep as a state with diminished perceptual gating and the latent capacity for global accessibility that is required for rapid arousals. To the extent that the qualitative characterization of local dynamics is exhausted by the dichotomy between unstable and stable behavior, our work highlights how expanding the model parameter space can describe states of consciousness in terms of multiple dimensions with interpretations given by the choice of anatomically-informed priors.
Fil: Perez Ipiña, Ignacio Martin. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Física; Argentina
Fil: Donnelly Kehoe, Patricio Andres. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Centro Internacional Franco Argentino de Ciencias de la Información y de Sistemas. Universidad Nacional de Rosario. Centro Internacional Franco Argentino de Ciencias de la Información y de Sistemas; Argentina
Fil: Kringelbach, Morten. University of Oxford; Reino Unido. University Aarhus; Dinamarca
Fil: Laufs, Helmut. University of Kiel; Alemania
Fil: Ibañez, Agustin. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Neurociencia Cognitiva. Fundación Favaloro. Instituto de Neurociencia Cognitiva; Argentina. Universidad de San Andrés; Argentina. Australian Research Council; Australia. Universidad Adolfo Ibañez; Chile. Universidad Autónoma del Caribe; Colombia
Fil: Deco, Gustavo. Universitat Pompeu Fabra; España
Fil: Sanz Perl Hernandez, Yonatan. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de San Andrés; Argentina
Fil: Tagliazucchi, Enzo Rodolfo. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Física; Argentina
description Global brain states are frequently placed within a unidimensional continuum by correlational studies, ranging from states of deep unconsciousness to ordinary wakefulness. An alternative is their multidimensional and mechanistic characterization in terms of different cognitive capacities, using computational models to reproduce the underlying neural dynamics. We explore this alternative by introducing a semi-empirical model linking regional activation and long-range functional connectivity in the different brain states visited during the natural wake-sleep cycle. Our model combines functional magnetic resonance imaging (fMRI) data, in vivo estimates of structural connectivity, and anatomically-informed priors to constrain the independent variation of regional activation. The best fit to empirical data was achieved using priors based on functionally coherent networks, with the resulting model parameters dividing the cortex into regions presenting opposite dynamical behavior. Frontoparietal regions approached a bifurcation from dynamics at a fixed point governed by noise, while sensorimotor regions approached a bifurcation from oscillatory dynamics. In agreement with human electrophysiological experiments, sleep onset induced subcortical deactivation with low correlation, which was subsequently reversed for deeper stages. Finally, we introduced periodic forcing of variable intensity to simulate external perturbations, and identified the key regions relevant for the recovery of wakefulness from deep sleep. Our model represents sleep as a state with diminished perceptual gating and the latent capacity for global accessibility that is required for rapid arousals. To the extent that the qualitative characterization of local dynamics is exhausted by the dichotomy between unstable and stable behavior, our work highlights how expanding the model parameter space can describe states of consciousness in terms of multiple dimensions with interpretations given by the choice of anatomically-informed priors.
publishDate 2020
dc.date.none.fl_str_mv 2020-07-15
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/140103
Perez Ipiña, Ignacio Martin; Donnelly Kehoe, Patricio Andres; Kringelbach, Morten; Laufs, Helmut; Ibañez, Agustin; et al.; Modeling regional changes in dynamic stability during sleep and wakefulness; Elsevier; Journal Neuroimag; 215; 116833; 15-7-2020; 1-13
1053-8119
CONICET Digital
CONICET
url http://hdl.handle.net/11336/140103
identifier_str_mv Perez Ipiña, Ignacio Martin; Donnelly Kehoe, Patricio Andres; Kringelbach, Morten; Laufs, Helmut; Ibañez, Agustin; et al.; Modeling regional changes in dynamic stability during sleep and wakefulness; Elsevier; Journal Neuroimag; 215; 116833; 15-7-2020; 1-13
1053-8119
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://linkinghub.elsevier.com/retrieve/pii/S1053811920303207
info:eu-repo/semantics/altIdentifier/doi/10.1016/j.neuroimage.2020.116833
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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