Temporal Irreversibility of Large-Scale Brain Dynamics in Alzheimer's Disease

Autores
Cruzat, Josephine; Herzog, Ruben; Prado, Pavel; Sanz Perl Hernandez, Yonatan; Gonzalez Gomez, Raul; Moguilner, Sebastian Gabriel; Kringelbach, Morten L.; Deco, Gustavo; Tagliazucchi, Enzo Rodolfo; Ibañez, Agustín
Año de publicación
2023
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Healthy brain dynamics can be understood as the emergence of a complex system far from thermodynamic equilibrium. Brain dynamics are temporally irreversible and thus establish a preferred direction in time (i.e., arrow of time). However, little is known about how the time-reversal symmetry of spontaneous brain activity is affected by Alzheimer's disease (AD). We hypothesized that the level of irreversibility would be compromised in AD, signaling a fundamental shift in the collective properties of brain activity toward equilibrium dynamics. We investigated the irreversibility from resting-state fMRI and EEG data in male and female human patients with AD and elderly healthy control subjects (HCs). We quantified the level of irreversibility and, thus, proximity to nonequilibrium dynamics by comparing forward and backward time series through time-shifted correlations. AD was associated with a breakdown of temporal irreversibility at the global, local, and network levels, and at multiple oscillatory frequency bands. At the local level, temporoparietal and frontal regions were affected by AD. The limbic, frontoparietal, default mode, and salience networks were the most compromised at the network level. The temporal reversibility was associated with cognitive decline in AD and gray matter volume in HCs. The irreversibility of brain dynamics provided higher accuracy and more distinctive information than classical neurocognitive measures when differentiating AD from control subjects. Findings were validated using an out-of-sample cohort. Present results offer new evidence regarding pathophysiological links between the entropy generation rate of brain dynamics and the clinical presentation of AD, opening new avenues for dementia characterization at different levels.
Fil: Cruzat, Josephine. Fundación Para El Estudio de la Conciencia Humana; Chile. Universidad Adolfo Ibañez; Chile
Fil: Herzog, Ruben. Fundación Para El Estudio de la Conciencia Humana; Chile. Universidad Adolfo Ibañez; Chile
Fil: Prado, Pavel. Fundación Para El Estudio de la Conciencia Humana; Chile. Universidad Adolfo Ibañez; Chile
Fil: Sanz Perl Hernandez, Yonatan. Universidad de Buenos Aires; Argentina. Universidad de San Andrés; Argentina. Universitat Pompeu Fabra; España. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Gonzalez Gomez, Raul. Universidad Adolfo Ibañez; Chile
Fil: Moguilner, Sebastian Gabriel. Universidad Adolfo Ibañez; Chile. Trinity College Dublin; Irlanda. University of California; Estados Unidos
Fil: Kringelbach, Morten L.. University Aarhus; Dinamarca. University of Oxford; Reino Unido
Fil: Deco, Gustavo. Universitat Pompeu Fabra; España. Monash University; Australia. Max Planck Institute For Human Cognitive And Brain Sciences; Alemania. Institució Catalana de Recerca I Estudis Avançats; España
Fil: Tagliazucchi, Enzo Rodolfo. Universidad de San Andrés; Argentina. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Adolfo Ibañez; Chile
Fil: Ibañez, Agustín. Trinity College Dublin; Irlanda. Universidad Adolfo Ibañez; Chile. Universidad de San Andrés; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. University of California; Estados Unidos
Materia
ALZHEIMER'S DISEASE
DYNAMIC NETWORKS
EEG
FMRI
IRREVERSIBILITY DYNAMICS
MACHINE LEARNING
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:11336/228444
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/228444
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Temporal Irreversibility of Large-Scale Brain Dynamics in Alzheimer's DiseaseCruzat, JosephineHerzog, RubenPrado, PavelSanz Perl Hernandez, YonatanGonzalez Gomez, RaulMoguilner, Sebastian GabrielKringelbach, Morten L.Deco, GustavoTagliazucchi, Enzo RodolfoIbañez, AgustínALZHEIMER'S DISEASEDYNAMIC NETWORKSEEGFMRIIRREVERSIBILITY DYNAMICSMACHINE LEARNINGhttps://purl.org/becyt/ford/1.3https://purl.org/becyt/ford/1Healthy brain dynamics can be understood as the emergence of a complex system far from thermodynamic equilibrium. Brain dynamics are temporally irreversible and thus establish a preferred direction in time (i.e., arrow of time). However, little is known about how the time-reversal symmetry of spontaneous brain activity is affected by Alzheimer's disease (AD). We hypothesized that the level of irreversibility would be compromised in AD, signaling a fundamental shift in the collective properties of brain activity toward equilibrium dynamics. We investigated the irreversibility from resting-state fMRI and EEG data in male and female human patients with AD and elderly healthy control subjects (HCs). We quantified the level of irreversibility and, thus, proximity to nonequilibrium dynamics by comparing forward and backward time series through time-shifted correlations. AD was associated with a breakdown of temporal irreversibility at the global, local, and network levels, and at multiple oscillatory frequency bands. At the local level, temporoparietal and frontal regions were affected by AD. The limbic, frontoparietal, default mode, and salience networks were the most compromised at the network level. The temporal reversibility was associated with cognitive decline in AD and gray matter volume in HCs. The irreversibility of brain dynamics provided higher accuracy and more distinctive information than classical neurocognitive measures when differentiating AD from control subjects. Findings were validated using an out-of-sample cohort. Present results offer new evidence regarding pathophysiological links between the entropy generation rate of brain dynamics and the clinical presentation of AD, opening new avenues for dementia characterization at different levels.Fil: Cruzat, Josephine. Fundación Para El Estudio de la Conciencia Humana; Chile. Universidad Adolfo Ibañez; ChileFil: Herzog, Ruben. Fundación Para El Estudio de la Conciencia Humana; Chile. Universidad Adolfo Ibañez; ChileFil: Prado, Pavel. Fundación Para El Estudio de la Conciencia Humana; Chile. Universidad Adolfo Ibañez; ChileFil: Sanz Perl Hernandez, Yonatan. Universidad de Buenos Aires; Argentina. Universidad de San Andrés; Argentina. Universitat Pompeu Fabra; España. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Gonzalez Gomez, Raul. Universidad Adolfo Ibañez; ChileFil: Moguilner, Sebastian Gabriel. Universidad Adolfo Ibañez; Chile. Trinity College Dublin; Irlanda. University of California; Estados UnidosFil: Kringelbach, Morten L.. University Aarhus; Dinamarca. University of Oxford; Reino UnidoFil: Deco, Gustavo. Universitat Pompeu Fabra; España. Monash University; Australia. Max Planck Institute For Human Cognitive And Brain Sciences; Alemania. Institució Catalana de Recerca I Estudis Avançats; EspañaFil: Tagliazucchi, Enzo Rodolfo. Universidad de San Andrés; Argentina. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Adolfo Ibañez; ChileFil: Ibañez, Agustín. Trinity College Dublin; Irlanda. Universidad Adolfo Ibañez; Chile. Universidad de San Andrés; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. University of California; Estados UnidosSociety for Neuroscience2023-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/228444Cruzat, Josephine; Herzog, Ruben; Prado, Pavel; Sanz Perl Hernandez, Yonatan; Gonzalez Gomez, Raul; et al.; Temporal Irreversibility of Large-Scale Brain Dynamics in Alzheimer's Disease; Society for Neuroscience; Journal of Neuroscience; 43; 9; 3-2023; 1643-16560270-64741529-2401CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1523/JNEUROSCI.1312-22.2022info:eu-repo/semantics/altIdentifier/url/https://www.jneurosci.org/content/43/9/1643info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-22T11:42:44Zoai:ri.conicet.gov.ar:11336/228444instacron: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:34982025-10-22 11:42:44.511CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Temporal Irreversibility of Large-Scale Brain Dynamics in Alzheimer's Disease
title Temporal Irreversibility of Large-Scale Brain Dynamics in Alzheimer's Disease
spellingShingle Temporal Irreversibility of Large-Scale Brain Dynamics in Alzheimer's Disease
Cruzat, Josephine
ALZHEIMER'S DISEASE
DYNAMIC NETWORKS
EEG
FMRI
IRREVERSIBILITY DYNAMICS
MACHINE LEARNING
title_short Temporal Irreversibility of Large-Scale Brain Dynamics in Alzheimer's Disease
title_full Temporal Irreversibility of Large-Scale Brain Dynamics in Alzheimer's Disease
title_fullStr Temporal Irreversibility of Large-Scale Brain Dynamics in Alzheimer's Disease
title_full_unstemmed Temporal Irreversibility of Large-Scale Brain Dynamics in Alzheimer's Disease
title_sort Temporal Irreversibility of Large-Scale Brain Dynamics in Alzheimer's Disease
dc.creator.none.fl_str_mv Cruzat, Josephine
Herzog, Ruben
Prado, Pavel
Sanz Perl Hernandez, Yonatan
Gonzalez Gomez, Raul
Moguilner, Sebastian Gabriel
Kringelbach, Morten L.
Deco, Gustavo
Tagliazucchi, Enzo Rodolfo
Ibañez, Agustín
author Cruzat, Josephine
author_facet Cruzat, Josephine
Herzog, Ruben
Prado, Pavel
Sanz Perl Hernandez, Yonatan
Gonzalez Gomez, Raul
Moguilner, Sebastian Gabriel
Kringelbach, Morten L.
Deco, Gustavo
Tagliazucchi, Enzo Rodolfo
Ibañez, Agustín
author_role author
author2 Herzog, Ruben
Prado, Pavel
Sanz Perl Hernandez, Yonatan
Gonzalez Gomez, Raul
Moguilner, Sebastian Gabriel
Kringelbach, Morten L.
Deco, Gustavo
Tagliazucchi, Enzo Rodolfo
Ibañez, Agustín
author2_role author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv ALZHEIMER'S DISEASE
DYNAMIC NETWORKS
EEG
FMRI
IRREVERSIBILITY DYNAMICS
MACHINE LEARNING
topic ALZHEIMER'S DISEASE
DYNAMIC NETWORKS
EEG
FMRI
IRREVERSIBILITY DYNAMICS
MACHINE LEARNING
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.3
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Healthy brain dynamics can be understood as the emergence of a complex system far from thermodynamic equilibrium. Brain dynamics are temporally irreversible and thus establish a preferred direction in time (i.e., arrow of time). However, little is known about how the time-reversal symmetry of spontaneous brain activity is affected by Alzheimer's disease (AD). We hypothesized that the level of irreversibility would be compromised in AD, signaling a fundamental shift in the collective properties of brain activity toward equilibrium dynamics. We investigated the irreversibility from resting-state fMRI and EEG data in male and female human patients with AD and elderly healthy control subjects (HCs). We quantified the level of irreversibility and, thus, proximity to nonequilibrium dynamics by comparing forward and backward time series through time-shifted correlations. AD was associated with a breakdown of temporal irreversibility at the global, local, and network levels, and at multiple oscillatory frequency bands. At the local level, temporoparietal and frontal regions were affected by AD. The limbic, frontoparietal, default mode, and salience networks were the most compromised at the network level. The temporal reversibility was associated with cognitive decline in AD and gray matter volume in HCs. The irreversibility of brain dynamics provided higher accuracy and more distinctive information than classical neurocognitive measures when differentiating AD from control subjects. Findings were validated using an out-of-sample cohort. Present results offer new evidence regarding pathophysiological links between the entropy generation rate of brain dynamics and the clinical presentation of AD, opening new avenues for dementia characterization at different levels.
Fil: Cruzat, Josephine. Fundación Para El Estudio de la Conciencia Humana; Chile. Universidad Adolfo Ibañez; Chile
Fil: Herzog, Ruben. Fundación Para El Estudio de la Conciencia Humana; Chile. Universidad Adolfo Ibañez; Chile
Fil: Prado, Pavel. Fundación Para El Estudio de la Conciencia Humana; Chile. Universidad Adolfo Ibañez; Chile
Fil: Sanz Perl Hernandez, Yonatan. Universidad de Buenos Aires; Argentina. Universidad de San Andrés; Argentina. Universitat Pompeu Fabra; España. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Gonzalez Gomez, Raul. Universidad Adolfo Ibañez; Chile
Fil: Moguilner, Sebastian Gabriel. Universidad Adolfo Ibañez; Chile. Trinity College Dublin; Irlanda. University of California; Estados Unidos
Fil: Kringelbach, Morten L.. University Aarhus; Dinamarca. University of Oxford; Reino Unido
Fil: Deco, Gustavo. Universitat Pompeu Fabra; España. Monash University; Australia. Max Planck Institute For Human Cognitive And Brain Sciences; Alemania. Institució Catalana de Recerca I Estudis Avançats; España
Fil: Tagliazucchi, Enzo Rodolfo. Universidad de San Andrés; Argentina. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Adolfo Ibañez; Chile
Fil: Ibañez, Agustín. Trinity College Dublin; Irlanda. Universidad Adolfo Ibañez; Chile. Universidad de San Andrés; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. University of California; Estados Unidos
description Healthy brain dynamics can be understood as the emergence of a complex system far from thermodynamic equilibrium. Brain dynamics are temporally irreversible and thus establish a preferred direction in time (i.e., arrow of time). However, little is known about how the time-reversal symmetry of spontaneous brain activity is affected by Alzheimer's disease (AD). We hypothesized that the level of irreversibility would be compromised in AD, signaling a fundamental shift in the collective properties of brain activity toward equilibrium dynamics. We investigated the irreversibility from resting-state fMRI and EEG data in male and female human patients with AD and elderly healthy control subjects (HCs). We quantified the level of irreversibility and, thus, proximity to nonequilibrium dynamics by comparing forward and backward time series through time-shifted correlations. AD was associated with a breakdown of temporal irreversibility at the global, local, and network levels, and at multiple oscillatory frequency bands. At the local level, temporoparietal and frontal regions were affected by AD. The limbic, frontoparietal, default mode, and salience networks were the most compromised at the network level. The temporal reversibility was associated with cognitive decline in AD and gray matter volume in HCs. The irreversibility of brain dynamics provided higher accuracy and more distinctive information than classical neurocognitive measures when differentiating AD from control subjects. Findings were validated using an out-of-sample cohort. Present results offer new evidence regarding pathophysiological links between the entropy generation rate of brain dynamics and the clinical presentation of AD, opening new avenues for dementia characterization at different levels.
publishDate 2023
dc.date.none.fl_str_mv 2023-03
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/11336/228444
Cruzat, Josephine; Herzog, Ruben; Prado, Pavel; Sanz Perl Hernandez, Yonatan; Gonzalez Gomez, Raul; et al.; Temporal Irreversibility of Large-Scale Brain Dynamics in Alzheimer's Disease; Society for Neuroscience; Journal of Neuroscience; 43; 9; 3-2023; 1643-1656
0270-6474
1529-2401
CONICET Digital
CONICET
url http://hdl.handle.net/11336/228444
identifier_str_mv Cruzat, Josephine; Herzog, Ruben; Prado, Pavel; Sanz Perl Hernandez, Yonatan; Gonzalez Gomez, Raul; et al.; Temporal Irreversibility of Large-Scale Brain Dynamics in Alzheimer's Disease; Society for Neuroscience; Journal of Neuroscience; 43; 9; 3-2023; 1643-1656
0270-6474
1529-2401
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1523/JNEUROSCI.1312-22.2022
info:eu-repo/semantics/altIdentifier/url/https://www.jneurosci.org/content/43/9/1643
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 Society for Neuroscience
publisher.none.fl_str_mv Society for Neuroscience
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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score 12.982451

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