Allostatic-Interoceptive Overload in Frontotemporal Dementia

Autores
Birba, Agustina; Santamaría García, Hernando; Prado, Pavel; Cruzat, Josefina; Sainz Ballesteros, Agustín; Legaz, Agustina; Fittipaldi, Sol; Duran Aniotz, Claudia; Slachevsky, Andrea; Santibañez, Rodrigo; Sigman, Mariano; García, Adolfo Martín; Whelan, Robert; Moguilner, Sebastian Gabriel; Ibañez, Agustin Mariano
Año de publicación
2022
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
BACKGROUND: The predictive coding theory of allostatic-interoceptive load states that brain networks mediating autonomic regulation and interoceptive-exteroceptive balance regulate the internal milieu to anticipate future needs and environmental demands. These functions seem to be distinctly compromised in behavioral variant frontotemporal dementia (bvFTD), including alterations of the allostatic-interoceptive network (AIN). Here, we hypothesize that bvFTD is typified by an allostatic-interoceptive overload. METHODS: We assessed resting-state heartbeat evoked potential (rsHEP) modulation as well as its behavioral and multimodal neuroimaging correlates in patients with bvFTD relative to healthy control subjects and patients with Alzheimer’s disease (N = 94). We measured 1) resting-state electroencephalography (to assess the rsHEP, prompted by visceral inputs and modulated by internal body sensing), 2) associations between rsHEP and its neural generators (source location), 3) cognitive disturbances (cognitive state, executive functions, facial emotion recognition), 4) brain atrophy, and 5) resting-state functional magnetic resonance imaging functional connectivity (AIN vs. control networks). RESULTS: Relative to healthy control subjects and patients with Alzheimer’s disease, patients with bvFTD presented more negative rsHEP amplitudes with sources in critical hubs of the AIN (insula, amygdala, somatosensory cortex, hippocampus, anterior cingulate cortex). This exacerbated rsHEP modulation selectively predicted the patients’ cognitive profile (including cognitive decline, executive dysfunction, and emotional impairments). In addition, increased rsHEP modulation in bvFTD was associated with decreased brain volume and connectivity of the AIN. Machine learning results confirmed AIN specificity in predicting the bvFTD group. CONCLUSIONS: Altogether, these results suggest that bvFTD may be characterized by an allostatic-interoceptive overload manifested in ongoing electrophysiological markers, brain atrophy, functional networks, and cognition.
Fil: Birba, Agustina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Adolfo Ibañez; Chile. Universidad de San Andrés; Argentina
Fil: Santamaría García, Hernando. Pontificia Universidad Javeriana; Colombia
Fil: Prado, Pavel. Universidad Adolfo Ibañez; Chile
Fil: Cruzat, Josefina. Universidad Adolfo Ibañez; Chile
Fil: Sainz Ballesteros, Agustín. Universidad Adolfo Ibañez; Chile
Fil: Legaz, Agustina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Adolfo Ibañez; Chile
Fil: Fittipaldi, Sol. Universidad Adolfo Ibañez; Chile
Fil: Duran Aniotz, Claudia. Universidad Adolfo Ibañez; Chile
Fil: Slachevsky, Andrea. Universidad de Chile. Facultad de Medicina.; Chile
Fil: Santibañez, Rodrigo. Pontificia Universidad Católica de Chile; Chile
Fil: Sigman, Mariano. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: García, Adolfo Martín. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Santiago de Chile; Chile. Universidad Adolfo Ibañez; Chile
Fil: Whelan, Robert. University of California; Estados Unidos
Fil: Moguilner, Sebastian Gabriel. Universidad de San Andrés; Argentina. University of California; Estados Unidos. Universidad Adolfo Ibañez; Chile
Fil: Ibañez, Agustin Mariano. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de San Andrés; Argentina. Universidad Adolfo Ibañez; Chile
Materia
ALLOSTASIS
ALLOSTATIC-INTEROCEPTIVE NETWORK
FRONTOTEMPORAL DEMENTIA
HEP
INTEROCEPTION
MULTIMODAL IMAGING
PREDICTIVE CODING
rsHEP
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:11336/234392

id CONICETDig_e9061ddf5396afb2e77a929c4e584e66
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network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Allostatic-Interoceptive Overload in Frontotemporal DementiaBirba, AgustinaSantamaría García, HernandoPrado, PavelCruzat, JosefinaSainz Ballesteros, AgustínLegaz, AgustinaFittipaldi, SolDuran Aniotz, ClaudiaSlachevsky, AndreaSantibañez, RodrigoSigman, MarianoGarcía, Adolfo MartínWhelan, RobertMoguilner, Sebastian GabrielIbañez, Agustin MarianoALLOSTASISALLOSTATIC-INTEROCEPTIVE NETWORKFRONTOTEMPORAL DEMENTIAHEPINTEROCEPTIONMULTIMODAL IMAGINGPREDICTIVE CODINGrsHEPhttps://purl.org/becyt/ford/3.1https://purl.org/becyt/ford/3BACKGROUND: The predictive coding theory of allostatic-interoceptive load states that brain networks mediating autonomic regulation and interoceptive-exteroceptive balance regulate the internal milieu to anticipate future needs and environmental demands. These functions seem to be distinctly compromised in behavioral variant frontotemporal dementia (bvFTD), including alterations of the allostatic-interoceptive network (AIN). Here, we hypothesize that bvFTD is typified by an allostatic-interoceptive overload. METHODS: We assessed resting-state heartbeat evoked potential (rsHEP) modulation as well as its behavioral and multimodal neuroimaging correlates in patients with bvFTD relative to healthy control subjects and patients with Alzheimer’s disease (N = 94). We measured 1) resting-state electroencephalography (to assess the rsHEP, prompted by visceral inputs and modulated by internal body sensing), 2) associations between rsHEP and its neural generators (source location), 3) cognitive disturbances (cognitive state, executive functions, facial emotion recognition), 4) brain atrophy, and 5) resting-state functional magnetic resonance imaging functional connectivity (AIN vs. control networks). RESULTS: Relative to healthy control subjects and patients with Alzheimer’s disease, patients with bvFTD presented more negative rsHEP amplitudes with sources in critical hubs of the AIN (insula, amygdala, somatosensory cortex, hippocampus, anterior cingulate cortex). This exacerbated rsHEP modulation selectively predicted the patients’ cognitive profile (including cognitive decline, executive dysfunction, and emotional impairments). In addition, increased rsHEP modulation in bvFTD was associated with decreased brain volume and connectivity of the AIN. Machine learning results confirmed AIN specificity in predicting the bvFTD group. CONCLUSIONS: Altogether, these results suggest that bvFTD may be characterized by an allostatic-interoceptive overload manifested in ongoing electrophysiological markers, brain atrophy, functional networks, and cognition.Fil: Birba, Agustina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Adolfo Ibañez; Chile. Universidad de San Andrés; ArgentinaFil: Santamaría García, Hernando. Pontificia Universidad Javeriana; ColombiaFil: Prado, Pavel. Universidad Adolfo Ibañez; ChileFil: Cruzat, Josefina. Universidad Adolfo Ibañez; ChileFil: Sainz Ballesteros, Agustín. Universidad Adolfo Ibañez; ChileFil: Legaz, Agustina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Adolfo Ibañez; ChileFil: Fittipaldi, Sol. Universidad Adolfo Ibañez; ChileFil: Duran Aniotz, Claudia. Universidad Adolfo Ibañez; ChileFil: Slachevsky, Andrea. Universidad de Chile. Facultad de Medicina.; ChileFil: Santibañez, Rodrigo. Pontificia Universidad Católica de Chile; ChileFil: Sigman, Mariano. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: García, Adolfo Martín. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Santiago de Chile; Chile. Universidad Adolfo Ibañez; ChileFil: Whelan, Robert. University of California; Estados UnidosFil: Moguilner, Sebastian Gabriel. Universidad de San Andrés; Argentina. University of California; Estados Unidos. Universidad Adolfo Ibañez; ChileFil: Ibañez, Agustin Mariano. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de San Andrés; Argentina. Universidad Adolfo Ibañez; ChileElsevier Science Inc.2022-05info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/234392Birba, Agustina; Santamaría García, Hernando; Prado, Pavel; Cruzat, Josefina; Sainz Ballesteros, Agustín; et al.; Allostatic-Interoceptive Overload in Frontotemporal Dementia; Elsevier Science Inc.; Biological Psychiatry; 92; 1; 5-2022; 54-670006-32231873-2402CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.biologicalpsychiatryjournal.com/article/S0006-3223(22)01042-3/fulltextinfo:eu-repo/semantics/altIdentifier/doi/10.1016/j.biopsych.2022.02.955info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-15T14:25:44Zoai:ri.conicet.gov.ar:11336/234392instacron: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 14:25:44.734CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Allostatic-Interoceptive Overload in Frontotemporal Dementia
title Allostatic-Interoceptive Overload in Frontotemporal Dementia
spellingShingle Allostatic-Interoceptive Overload in Frontotemporal Dementia
Birba, Agustina
ALLOSTASIS
ALLOSTATIC-INTEROCEPTIVE NETWORK
FRONTOTEMPORAL DEMENTIA
HEP
INTEROCEPTION
MULTIMODAL IMAGING
PREDICTIVE CODING
rsHEP
title_short Allostatic-Interoceptive Overload in Frontotemporal Dementia
title_full Allostatic-Interoceptive Overload in Frontotemporal Dementia
title_fullStr Allostatic-Interoceptive Overload in Frontotemporal Dementia
title_full_unstemmed Allostatic-Interoceptive Overload in Frontotemporal Dementia
title_sort Allostatic-Interoceptive Overload in Frontotemporal Dementia
dc.creator.none.fl_str_mv Birba, Agustina
Santamaría García, Hernando
Prado, Pavel
Cruzat, Josefina
Sainz Ballesteros, Agustín
Legaz, Agustina
Fittipaldi, Sol
Duran Aniotz, Claudia
Slachevsky, Andrea
Santibañez, Rodrigo
Sigman, Mariano
García, Adolfo Martín
Whelan, Robert
Moguilner, Sebastian Gabriel
Ibañez, Agustin Mariano
author Birba, Agustina
author_facet Birba, Agustina
Santamaría García, Hernando
Prado, Pavel
Cruzat, Josefina
Sainz Ballesteros, Agustín
Legaz, Agustina
Fittipaldi, Sol
Duran Aniotz, Claudia
Slachevsky, Andrea
Santibañez, Rodrigo
Sigman, Mariano
García, Adolfo Martín
Whelan, Robert
Moguilner, Sebastian Gabriel
Ibañez, Agustin Mariano
author_role author
author2 Santamaría García, Hernando
Prado, Pavel
Cruzat, Josefina
Sainz Ballesteros, Agustín
Legaz, Agustina
Fittipaldi, Sol
Duran Aniotz, Claudia
Slachevsky, Andrea
Santibañez, Rodrigo
Sigman, Mariano
García, Adolfo Martín
Whelan, Robert
Moguilner, Sebastian Gabriel
Ibañez, Agustin Mariano
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv ALLOSTASIS
ALLOSTATIC-INTEROCEPTIVE NETWORK
FRONTOTEMPORAL DEMENTIA
HEP
INTEROCEPTION
MULTIMODAL IMAGING
PREDICTIVE CODING
rsHEP
topic ALLOSTASIS
ALLOSTATIC-INTEROCEPTIVE NETWORK
FRONTOTEMPORAL DEMENTIA
HEP
INTEROCEPTION
MULTIMODAL IMAGING
PREDICTIVE CODING
rsHEP
purl_subject.fl_str_mv https://purl.org/becyt/ford/3.1
https://purl.org/becyt/ford/3
dc.description.none.fl_txt_mv BACKGROUND: The predictive coding theory of allostatic-interoceptive load states that brain networks mediating autonomic regulation and interoceptive-exteroceptive balance regulate the internal milieu to anticipate future needs and environmental demands. These functions seem to be distinctly compromised in behavioral variant frontotemporal dementia (bvFTD), including alterations of the allostatic-interoceptive network (AIN). Here, we hypothesize that bvFTD is typified by an allostatic-interoceptive overload. METHODS: We assessed resting-state heartbeat evoked potential (rsHEP) modulation as well as its behavioral and multimodal neuroimaging correlates in patients with bvFTD relative to healthy control subjects and patients with Alzheimer’s disease (N = 94). We measured 1) resting-state electroencephalography (to assess the rsHEP, prompted by visceral inputs and modulated by internal body sensing), 2) associations between rsHEP and its neural generators (source location), 3) cognitive disturbances (cognitive state, executive functions, facial emotion recognition), 4) brain atrophy, and 5) resting-state functional magnetic resonance imaging functional connectivity (AIN vs. control networks). RESULTS: Relative to healthy control subjects and patients with Alzheimer’s disease, patients with bvFTD presented more negative rsHEP amplitudes with sources in critical hubs of the AIN (insula, amygdala, somatosensory cortex, hippocampus, anterior cingulate cortex). This exacerbated rsHEP modulation selectively predicted the patients’ cognitive profile (including cognitive decline, executive dysfunction, and emotional impairments). In addition, increased rsHEP modulation in bvFTD was associated with decreased brain volume and connectivity of the AIN. Machine learning results confirmed AIN specificity in predicting the bvFTD group. CONCLUSIONS: Altogether, these results suggest that bvFTD may be characterized by an allostatic-interoceptive overload manifested in ongoing electrophysiological markers, brain atrophy, functional networks, and cognition.
Fil: Birba, Agustina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Adolfo Ibañez; Chile. Universidad de San Andrés; Argentina
Fil: Santamaría García, Hernando. Pontificia Universidad Javeriana; Colombia
Fil: Prado, Pavel. Universidad Adolfo Ibañez; Chile
Fil: Cruzat, Josefina. Universidad Adolfo Ibañez; Chile
Fil: Sainz Ballesteros, Agustín. Universidad Adolfo Ibañez; Chile
Fil: Legaz, Agustina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Adolfo Ibañez; Chile
Fil: Fittipaldi, Sol. Universidad Adolfo Ibañez; Chile
Fil: Duran Aniotz, Claudia. Universidad Adolfo Ibañez; Chile
Fil: Slachevsky, Andrea. Universidad de Chile. Facultad de Medicina.; Chile
Fil: Santibañez, Rodrigo. Pontificia Universidad Católica de Chile; Chile
Fil: Sigman, Mariano. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: García, Adolfo Martín. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Santiago de Chile; Chile. Universidad Adolfo Ibañez; Chile
Fil: Whelan, Robert. University of California; Estados Unidos
Fil: Moguilner, Sebastian Gabriel. Universidad de San Andrés; Argentina. University of California; Estados Unidos. Universidad Adolfo Ibañez; Chile
Fil: Ibañez, Agustin Mariano. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de San Andrés; Argentina. Universidad Adolfo Ibañez; Chile
description BACKGROUND: The predictive coding theory of allostatic-interoceptive load states that brain networks mediating autonomic regulation and interoceptive-exteroceptive balance regulate the internal milieu to anticipate future needs and environmental demands. These functions seem to be distinctly compromised in behavioral variant frontotemporal dementia (bvFTD), including alterations of the allostatic-interoceptive network (AIN). Here, we hypothesize that bvFTD is typified by an allostatic-interoceptive overload. METHODS: We assessed resting-state heartbeat evoked potential (rsHEP) modulation as well as its behavioral and multimodal neuroimaging correlates in patients with bvFTD relative to healthy control subjects and patients with Alzheimer’s disease (N = 94). We measured 1) resting-state electroencephalography (to assess the rsHEP, prompted by visceral inputs and modulated by internal body sensing), 2) associations between rsHEP and its neural generators (source location), 3) cognitive disturbances (cognitive state, executive functions, facial emotion recognition), 4) brain atrophy, and 5) resting-state functional magnetic resonance imaging functional connectivity (AIN vs. control networks). RESULTS: Relative to healthy control subjects and patients with Alzheimer’s disease, patients with bvFTD presented more negative rsHEP amplitudes with sources in critical hubs of the AIN (insula, amygdala, somatosensory cortex, hippocampus, anterior cingulate cortex). This exacerbated rsHEP modulation selectively predicted the patients’ cognitive profile (including cognitive decline, executive dysfunction, and emotional impairments). In addition, increased rsHEP modulation in bvFTD was associated with decreased brain volume and connectivity of the AIN. Machine learning results confirmed AIN specificity in predicting the bvFTD group. CONCLUSIONS: Altogether, these results suggest that bvFTD may be characterized by an allostatic-interoceptive overload manifested in ongoing electrophysiological markers, brain atrophy, functional networks, and cognition.
publishDate 2022
dc.date.none.fl_str_mv 2022-05
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/11336/234392
Birba, Agustina; Santamaría García, Hernando; Prado, Pavel; Cruzat, Josefina; Sainz Ballesteros, Agustín; et al.; Allostatic-Interoceptive Overload in Frontotemporal Dementia; Elsevier Science Inc.; Biological Psychiatry; 92; 1; 5-2022; 54-67
0006-3223
1873-2402
CONICET Digital
CONICET
url http://hdl.handle.net/11336/234392
identifier_str_mv Birba, Agustina; Santamaría García, Hernando; Prado, Pavel; Cruzat, Josefina; Sainz Ballesteros, Agustín; et al.; Allostatic-Interoceptive Overload in Frontotemporal Dementia; Elsevier Science Inc.; Biological Psychiatry; 92; 1; 5-2022; 54-67
0006-3223
1873-2402
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
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info:eu-repo/semantics/altIdentifier/doi/10.1016/j.biopsych.2022.02.955
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/
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application/pdf
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