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
- Institución
- Consejo Nacional de Investigaciones Científicas y Técnicas
- OAI Identificador
- oai:ri.conicet.gov.ar:11336/228444
Ver los metadatos del registro completo
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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 Técnicas2025-09-29T10:12:51Zoai: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:34982025-09-29 10:12:51.342CONICET 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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1844614039245684736 |
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13.070432 |