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Neuroimaging Meta-Analyses Reveal Convergence of Interoception, Emotion, and Social Cognition Across Neurodegenerative Diseases
Indexado
WoS WOS:001504547700008
Scopus SCOPUS_ID:85213050044
DOI 10.1016/J.BIOPSYCH.2024.10.013
Año 2025
Tipo artículo de investigación

Citas Totales

Autores Afiliación Chile

Instituciones Chile

% Participación
Internacional

Autores
Afiliación Extranjera

Instituciones
Extranjeras


Abstract



Background: Simultaneous interoceptive, emotional, and social cognition deficits are observed across neurodegenerative diseases. Indirect evidence suggests shared neurobiological bases underlying these impairments, termed the allostatic-interoceptive network (AIN). However, no study has yet explored the convergence of these deficits in neurodegenerative diseases or examined how structural and functional changes contribute to cross-domain impairments. Methods: A Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) activated likelihood estimate meta-analysis encompassed studies that met the following inclusion criteria: interoception, emotion, or social cognition tasks; neurodegenerative diseases (behavioral variant frontotemporal dementia, primary progressive aphasias, Alzheimer's disease, Parkinson's disease, multiple sclerosis); and neuroimaging (structural: magnetic resonance imaging voxel-based morphometry; functional: magnetic resonance imaging and fluorodeoxyglucose–positron emission tomography). Results: Of 20,593 studies, 170 met inclusion criteria (58 interoception, 65 emotion, and 47 social cognition) involving 7032 participants (4963 patients and 2069 healthy control participants). In all participants combined, conjunction analyses revealed AIN involvement of the insula, amygdala, orbitofrontal cortex, anterior cingulate, striatum, thalamus, and hippocampus across domains. In behavioral variant frontotemporal dementia, this conjunction was replicated across domains, with further involvement of the temporal pole, temporal fusiform cortex, and angular gyrus. A convergence of interoception and emotion in the striatum, thalamus, and hippocampus in Parkinson's disease and the posterior insula in primary progressive aphasias was also observed. In Alzheimer's disease and multiple sclerosis, disruptions in the AIN were observed during interoception, but no convergence with emotion was identified. Conclusions: Neurodegeneration induces dysfunctional AIN across atrophy, connectivity, and metabolism, more accentuated in behavioral variant frontotemporal dementia. Findings bolster the predictive coding theories of large-scale AIN, calling for more synergistic approaches to understanding interoception, emotion, and social cognition impairments in neurodegeneration.

Revista



Revista ISSN
Biological Psychiatry 0006-3223

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Disciplinas de Investigación



WOS
Neurosciences
Psychiatry
Scopus
Biological Psychiatry
SciELO
Sin Disciplinas

Muestra la distribución de disciplinas para esta publicación.

Publicaciones WoS (Ediciones: ISSHP, ISTP, AHCI, SSCI, SCI), Scopus, SciELO Chile.

Colaboración Institucional



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Autores - Afiliación



Ord. Autor Género Institución - País
1 Hazelton, Jessica L. - Universidad Adolfo Ibáñez - Chile
Universidad de San Andrés - Argentina
The University of Sydney - Australia
Univ San Andres - Argentina
UNIV SYDNEY - Australia
2 Carneiro, Fábio - Universidade do Porto - Portugal
Faculdade de Medicina da Universidade do Porto (FMUP) - Portugal
Unidade Local de Saúde do Alto Ave - Portugal
Univ Porto - Portugal
Unidade Local Saude Alto Ave - Portugal
3 Maito, Marcelo - Universidad Adolfo Ibáñez - Chile
Universidad de San Andrés - Argentina
Univ San Andres - Argentina
4 Richter, Fabian - Deutsches Herzzentrum Berlin - Alemania
Charité – Universitätsmedizin Berlin - Alemania
Deutsch Herzzentrumder Charite - Alemania
Charite Univ Med Berlin - Alemania
FREE UNIV BERLIN - Alemania
Humboldt Univ - Alemania
5 LEGAZ, AGUSTINA Mujer Universidad Adolfo Ibáñez - Chile
Universidad de San Andrés - Argentina
Univ San Andres - Argentina
6 Altschuler, Florencia - Universidad de San Andrés - Argentina
Univ San Andres - Argentina
7 Cubillos-Pinilla, Leidy - Technische Universität München - Alemania
TECH UNIV MUNICH - Alemania
8 Chen, Yu - UCSF School of Medicine - Estados Unidos
UNIV CALIF SAN FRANCISCO - Estados Unidos
University of California, San Francisco - Estados Unidos
9 Doherty, Colin P. - Trinity College Dublin - Irlanda
University of California, San Francisco - Estados Unidos
Trinity Coll Dublin - Irlanda
UNIV CALIF SAN FRANCISCO - Estados Unidos
10 Baez, Sandra - Trinity College Dublin - Irlanda
University of California, San Francisco - Estados Unidos
Universidad de Los Andes, Colombia - Colombia
Trinity Coll Dublin - Irlanda
UNIV CALIF SAN FRANCISCO - Estados Unidos
Universidad de Los Andes, Chile - Colombia
11 Ibáñez, Agustín - Universidad Adolfo Ibáñez - Chile
Universidad de San Andrés - Argentina
Trinity College Dublin - Irlanda
University of California, San Francisco - Estados Unidos
Univ San Andres - Argentina
Trinity Coll Dublin - Irlanda
UNIV CALIF SAN FRANCISCO - Estados Unidos

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Financiamiento



Fuente
Consejo Nacional de Investigaciones Científicas y Técnicas
CONICET
Fondef
Fundação para a Ciência e a Tecnologia
Fondo Nacional de Desarrollo Científico y Tecnológico
Fogarty International Center
National Institutes of Health
Fondo de Fomento al Desarrollo Científico y Tecnológico
Alzheimer's Association
National Institute on Aging
Takeda
Global Brain Health Institute
Agencia Nacional de Investigación y Desarrollo
Rainwater Charitable Foundation
ANID/FONDECYT Regular
CARDS-NIH
Alz-heimer's Association
Portuguese Foundation for Sci-ence and Technology
Rainwater Charitable Foundation-The Bluefield project
Fogarty International Center, National Institutes of Health, National Institutes of Aging

Muestra la fuente de financiamiento declarada en la publicación.

Agradecimientos



Agradecimiento
JLH is supported by a postdoctoral fellowship granted by the multipartner consortium to expand dementia research in Latin America (ReDLat). FC is supported by a Ph.D. grant funded by the Portuguese Foundation for Science and Technology (Reference No. 2023.00362.BD). AI is supported by grants from CONICET ; ANID/FONDECYT Regular (Grant Nos. 1210195, 1210176, and 1220995); ANID/FONDAP/15150012; ANID/PIA/ANILLOS (Grant No. ACT210096); FONDEF (Grant Nos. ID20I10152 and ID22I10029); ANID/FONDAP (Grant No. 15150012); Takeda (Grant No. CW2680521); and the ReDLat , supported by Fogarty International Center, National Institutes of Health , National Institutes of Aging (Grant Nos. R01 AG057234, R01 AG075775, R01 AG083799), CARDS-National Institutes of Health , Alzheimer's Association (Grant No. SG-20\u2013725707), Rainwater Charitable Foundation\u2014The Bluefield project to cure FTD, and Global Brain Health Institute .
JLH is supported by a postdoctoral fellowship granted by the multi-partner consortium to expand dementia research in Latin America (ReDLat). FC is supported by a PhD grant funded by the Portuguese Foundation for Science and Technology with reference 2023.00362.BD. AI is supported by grants from CONICET; ANID/FONDECYT Regular (1210195 and 1210176 and 1220995); ANID/FONDAP/15150012; ANID/PIA/ANILLOS ACT210096; FONDEF ID20I10152, ID22I10029; ANID/FONDAP 15150012; Takeda CW2680521 and the MULTI-PARTNER CONSORTIUM TO EXPAND DEMENTIA RESEARCH IN LATIN AMERICA [ReDLat, supported by Fogarty International Center (FIC), National Institutes of Health, National Institutes of Aging (R01 AG057234, R01 AG075775, R01 AG=21051, R01 AG083799, CARDS-NIH), Alzheimer's Association (SG-20\u2013725707), Rainwater Charitable Foundation \u2013 The Bluefield project to cure FTD, and Global Brain Health Institute)].
JLH is supported by a postdoctoral fellowship granted by the multipartner consortium to expand dementia research in Latin America (ReDLat) . FC is supported by a Ph.D. grant funded by the Portuguese Foundation for Sci-ence and Technology (Reference No. 2023.00362.BD) . AI is supported by grants from CONICET; ANID/FONDECYT Regular (Grant Nos. 1210195, 1210176, and 1220995) ; ANID/FONDAP/15150012; ANID/PIA/ANILLOS (Grant No. ACT210096) ; FONDEF (Grant Nos. ID20I10152 and ID22I10029) ; ANID/FONDAP (Grant No. 15150012) ; Takeda (Grant No. CW2680521) ; and the ReDLat, supported by Fogarty International Center, National Institutes of Health, National Institutes of Aging (Grant Nos. R01 AG057234, R01 AG075775, R01 AG083799) , CARDS-National Institutes of Health, Alz-heimer's Association (Grant No. SG-20-725707) , Rainwater Charitable Foundation-The Bluefield project to cure FTD, and Global Brain Health Institute. We thank the authors of studies included in this meta-analysis for their kind assistance in providing information when required. We also thank all the participants and their families for participating in the studies included in this meta-analysis. JLH, FC, and AI were responsible for conceptualization. JLH, MM, and FA were responsible for methodology. JLH and MM were responsible for formal analysis and data curation. JLH and FC were responsible for inves-tigation. JLH was responsible for writing the original draft of the manuscript, JLH, AL, and FA were responsible for visualization. MM and FR were responsible for software. FR and YC were responsible for methodology. AI was responsible for resources, supervision, and funding acquisition. All authors contributed to reviewing/editing and final approval of the manuscript. The authors report no biomedical financial interests or potential conflicts of interest.

Muestra la fuente de financiamiento declarada en la publicación.