Predicting attentional focus: Heartbeat-evoked responses and brain dynamics during interoceptive and exteroceptive processing

Autores
Fló, Emilia; Belloli, Laouen Mayal Louan; Cabana, Álvaro; Ruyant Belabbas, Alessia; Jodaitis, Lise; Valente, Melanie; Rohaut, Benjamin; Naccache, Lionel; Rosanova, Mario; Comanducci, Angela; Andrillon, Thomas; Sitt, Jacobo
Año de publicación
2024
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Attention shapes our consciousness content and perception by increasing the probability of becoming aware and/or better encoding a selection of the incoming inner or outer sensory world. Engaging interoceptive and exteroceptive attention should elicit distinctive neural responses to visceral and external stimuli and could be useful in detecting covert command-following in unresponsive patients. We designed a task to engage healthy participants’ attention toward their heartbeats or auditory stimuli and investigated whether brain dynamics and the heartbeat-evoked potential (HEP) distinguished covert interoceptive–exteroceptive attention. Exteroceptive attention yielded an overall flattening of the power spectral density (PSD), whereas during interoception, there was a decrease in complexity, an increase in frontal connectivity and theta oscillations, and a modulation of the HEP. Subject-level classifiers based on HEP features classified the attentional state of 17/20 participants. Kolmogorov complexity, permutation entropy, and weighted symbolic mutual information showed comparable accuracy in classifying covert attention and exhibited a synergic behavior with the HEP features. PSD features demonstrated exceptional performance (20/20). Command-following was assessed in five brain-injured patients with a modified version of the task. An unresponsive wakefulness syndrome/vegetative state patient and a locked-in syndrome patient demonstrated a willful modulation of the HEP and together with the explored brain markers suggest that patients were complying with task instructions. Our findings underscore the importance of attentional mechanisms in shaping interoceptive and exteroceptive sensory processing and expand the framework of heart–brain interactions employed for diagnostic purposes in patients with disorders of consciousness.
Fil: Fló, Emilia. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
Fil: Belloli, Laouen Mayal Louan. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Investigación en Ciencias de la Computación. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Investigación en Ciencias de la Computación; Argentina
Fil: Cabana, Álvaro. Universidad de la Republica. Facultad de Psicologia.; Uruguay
Fil: Ruyant Belabbas, Alessia. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
Fil: Jodaitis, Lise. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
Fil: Valente, Melanie. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
Fil: Rohaut, Benjamin. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
Fil: Naccache, Lionel. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
Fil: Rosanova, Mario. Università degli Studi di Milano; Italia
Fil: Comanducci, Angela. Università degli Studi di Milano; Italia
Fil: Andrillon, Thomas. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
Fil: Sitt, Jacobo. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
Materia
interoception
HEP
exteroception
attention
disorders of consciousness
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:11336/265801
Acceder
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repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Predicting attentional focus: Heartbeat-evoked responses and brain dynamics during interoceptive and exteroceptive processingFló, EmiliaBelloli, Laouen Mayal LouanCabana, ÁlvaroRuyant Belabbas, AlessiaJodaitis, LiseValente, MelanieRohaut, BenjaminNaccache, LionelRosanova, MarioComanducci, AngelaAndrillon, ThomasSitt, JacobointeroceptionHEPexteroceptionattentiondisorders of consciousnesshttps://purl.org/becyt/ford/3.1https://purl.org/becyt/ford/3Attention shapes our consciousness content and perception by increasing the probability of becoming aware and/or better encoding a selection of the incoming inner or outer sensory world. Engaging interoceptive and exteroceptive attention should elicit distinctive neural responses to visceral and external stimuli and could be useful in detecting covert command-following in unresponsive patients. We designed a task to engage healthy participants’ attention toward their heartbeats or auditory stimuli and investigated whether brain dynamics and the heartbeat-evoked potential (HEP) distinguished covert interoceptive–exteroceptive attention. Exteroceptive attention yielded an overall flattening of the power spectral density (PSD), whereas during interoception, there was a decrease in complexity, an increase in frontal connectivity and theta oscillations, and a modulation of the HEP. Subject-level classifiers based on HEP features classified the attentional state of 17/20 participants. Kolmogorov complexity, permutation entropy, and weighted symbolic mutual information showed comparable accuracy in classifying covert attention and exhibited a synergic behavior with the HEP features. PSD features demonstrated exceptional performance (20/20). Command-following was assessed in five brain-injured patients with a modified version of the task. An unresponsive wakefulness syndrome/vegetative state patient and a locked-in syndrome patient demonstrated a willful modulation of the HEP and together with the explored brain markers suggest that patients were complying with task instructions. Our findings underscore the importance of attentional mechanisms in shaping interoceptive and exteroceptive sensory processing and expand the framework of heart–brain interactions employed for diagnostic purposes in patients with disorders of consciousness.Fil: Fló, Emilia. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; FranciaFil: Belloli, Laouen Mayal Louan. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Investigación en Ciencias de la Computación. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Investigación en Ciencias de la Computación; ArgentinaFil: Cabana, Álvaro. Universidad de la Republica. Facultad de Psicologia.; UruguayFil: Ruyant Belabbas, Alessia. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; FranciaFil: Jodaitis, Lise. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; FranciaFil: Valente, Melanie. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; FranciaFil: Rohaut, Benjamin. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; FranciaFil: Naccache, Lionel. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; FranciaFil: Rosanova, Mario. Università degli Studi di Milano; ItaliaFil: Comanducci, Angela. Università degli Studi di Milano; ItaliaFil: Andrillon, Thomas. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; FranciaFil: Sitt, Jacobo. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; FranciaOxford University Press2024-12info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/265801Fló, Emilia; Belloli, Laouen Mayal Louan; Cabana, Álvaro; Ruyant Belabbas, Alessia; Jodaitis, Lise; et al.; Predicting attentional focus: Heartbeat-evoked responses and brain dynamics during interoceptive and exteroceptive processing; Oxford University Press; PNAS Nexus; 3; 12; 12-2024; 1-152752-6542CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/pnasnexus/article/doi/10.1093/pnasnexus/pgae531/7908286info:eu-repo/semantics/altIdentifier/doi/10.1093/pnasnexus/pgae531info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:51:32Zoai:ri.conicet.gov.ar:11336/265801instacron: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:34982025-09-03 09:51:32.75CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Predicting attentional focus: Heartbeat-evoked responses and brain dynamics during interoceptive and exteroceptive processing
title Predicting attentional focus: Heartbeat-evoked responses and brain dynamics during interoceptive and exteroceptive processing
spellingShingle Predicting attentional focus: Heartbeat-evoked responses and brain dynamics during interoceptive and exteroceptive processing
Fló, Emilia
interoception
HEP
exteroception
attention
disorders of consciousness
title_short Predicting attentional focus: Heartbeat-evoked responses and brain dynamics during interoceptive and exteroceptive processing
title_full Predicting attentional focus: Heartbeat-evoked responses and brain dynamics during interoceptive and exteroceptive processing
title_fullStr Predicting attentional focus: Heartbeat-evoked responses and brain dynamics during interoceptive and exteroceptive processing
title_full_unstemmed Predicting attentional focus: Heartbeat-evoked responses and brain dynamics during interoceptive and exteroceptive processing
title_sort Predicting attentional focus: Heartbeat-evoked responses and brain dynamics during interoceptive and exteroceptive processing
dc.creator.none.fl_str_mv Fló, Emilia
Belloli, Laouen Mayal Louan
Cabana, Álvaro
Ruyant Belabbas, Alessia
Jodaitis, Lise
Valente, Melanie
Rohaut, Benjamin
Naccache, Lionel
Rosanova, Mario
Comanducci, Angela
Andrillon, Thomas
Sitt, Jacobo
author Fló, Emilia
author_facet Fló, Emilia
Belloli, Laouen Mayal Louan
Cabana, Álvaro
Ruyant Belabbas, Alessia
Jodaitis, Lise
Valente, Melanie
Rohaut, Benjamin
Naccache, Lionel
Rosanova, Mario
Comanducci, Angela
Andrillon, Thomas
Sitt, Jacobo
author_role author
author2 Belloli, Laouen Mayal Louan
Cabana, Álvaro
Ruyant Belabbas, Alessia
Jodaitis, Lise
Valente, Melanie
Rohaut, Benjamin
Naccache, Lionel
Rosanova, Mario
Comanducci, Angela
Andrillon, Thomas
Sitt, Jacobo
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv interoception
HEP
exteroception
attention
disorders of consciousness
topic interoception
HEP
exteroception
attention
disorders of consciousness
purl_subject.fl_str_mv https://purl.org/becyt/ford/3.1
https://purl.org/becyt/ford/3
dc.description.none.fl_txt_mv Attention shapes our consciousness content and perception by increasing the probability of becoming aware and/or better encoding a selection of the incoming inner or outer sensory world. Engaging interoceptive and exteroceptive attention should elicit distinctive neural responses to visceral and external stimuli and could be useful in detecting covert command-following in unresponsive patients. We designed a task to engage healthy participants’ attention toward their heartbeats or auditory stimuli and investigated whether brain dynamics and the heartbeat-evoked potential (HEP) distinguished covert interoceptive–exteroceptive attention. Exteroceptive attention yielded an overall flattening of the power spectral density (PSD), whereas during interoception, there was a decrease in complexity, an increase in frontal connectivity and theta oscillations, and a modulation of the HEP. Subject-level classifiers based on HEP features classified the attentional state of 17/20 participants. Kolmogorov complexity, permutation entropy, and weighted symbolic mutual information showed comparable accuracy in classifying covert attention and exhibited a synergic behavior with the HEP features. PSD features demonstrated exceptional performance (20/20). Command-following was assessed in five brain-injured patients with a modified version of the task. An unresponsive wakefulness syndrome/vegetative state patient and a locked-in syndrome patient demonstrated a willful modulation of the HEP and together with the explored brain markers suggest that patients were complying with task instructions. Our findings underscore the importance of attentional mechanisms in shaping interoceptive and exteroceptive sensory processing and expand the framework of heart–brain interactions employed for diagnostic purposes in patients with disorders of consciousness.
Fil: Fló, Emilia. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
Fil: Belloli, Laouen Mayal Louan. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Investigación en Ciencias de la Computación. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Investigación en Ciencias de la Computación; Argentina
Fil: Cabana, Álvaro. Universidad de la Republica. Facultad de Psicologia.; Uruguay
Fil: Ruyant Belabbas, Alessia. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
Fil: Jodaitis, Lise. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
Fil: Valente, Melanie. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
Fil: Rohaut, Benjamin. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
Fil: Naccache, Lionel. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
Fil: Rosanova, Mario. Università degli Studi di Milano; Italia
Fil: Comanducci, Angela. Università degli Studi di Milano; Italia
Fil: Andrillon, Thomas. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
Fil: Sitt, Jacobo. Centre de Recherche de I'Institut du Cerveau et de la Moelle Epinière; Francia
description Attention shapes our consciousness content and perception by increasing the probability of becoming aware and/or better encoding a selection of the incoming inner or outer sensory world. Engaging interoceptive and exteroceptive attention should elicit distinctive neural responses to visceral and external stimuli and could be useful in detecting covert command-following in unresponsive patients. We designed a task to engage healthy participants’ attention toward their heartbeats or auditory stimuli and investigated whether brain dynamics and the heartbeat-evoked potential (HEP) distinguished covert interoceptive–exteroceptive attention. Exteroceptive attention yielded an overall flattening of the power spectral density (PSD), whereas during interoception, there was a decrease in complexity, an increase in frontal connectivity and theta oscillations, and a modulation of the HEP. Subject-level classifiers based on HEP features classified the attentional state of 17/20 participants. Kolmogorov complexity, permutation entropy, and weighted symbolic mutual information showed comparable accuracy in classifying covert attention and exhibited a synergic behavior with the HEP features. PSD features demonstrated exceptional performance (20/20). Command-following was assessed in five brain-injured patients with a modified version of the task. An unresponsive wakefulness syndrome/vegetative state patient and a locked-in syndrome patient demonstrated a willful modulation of the HEP and together with the explored brain markers suggest that patients were complying with task instructions. Our findings underscore the importance of attentional mechanisms in shaping interoceptive and exteroceptive sensory processing and expand the framework of heart–brain interactions employed for diagnostic purposes in patients with disorders of consciousness.
publishDate 2024
dc.date.none.fl_str_mv 2024-12
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/11336/265801
Fló, Emilia; Belloli, Laouen Mayal Louan; Cabana, Álvaro; Ruyant Belabbas, Alessia; Jodaitis, Lise; et al.; Predicting attentional focus: Heartbeat-evoked responses and brain dynamics during interoceptive and exteroceptive processing; Oxford University Press; PNAS Nexus; 3; 12; 12-2024; 1-15
2752-6542
CONICET Digital
CONICET
url http://hdl.handle.net/11336/265801
identifier_str_mv Fló, Emilia; Belloli, Laouen Mayal Louan; Cabana, Álvaro; Ruyant Belabbas, Alessia; Jodaitis, Lise; et al.; Predicting attentional focus: Heartbeat-evoked responses and brain dynamics during interoceptive and exteroceptive processing; Oxford University Press; PNAS Nexus; 3; 12; 12-2024; 1-15
2752-6542
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://academic.oup.com/pnasnexus/article/doi/10.1093/pnasnexus/pgae531/7908286
info:eu-repo/semantics/altIdentifier/doi/10.1093/pnasnexus/pgae531
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 Oxford University Press
publisher.none.fl_str_mv Oxford University Press
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 13.13397

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