Multimodal mechanisms of human socially reinforced learning across neurodegenerative diseases

Autores
Legaz, Agustina; Abrevaya, Sofia; Dottori, Martín; Campo, Cecilia González; Birba, Agustina; Martorell Caro, Miguel Angel; Aguirre, María Julieta; Slachevsky, Andrea; Aranguiz, Rafael; Serrano, Cecilia Mariela; Gillan, Claire M.; Leroi, Iracema; García, Adolfo Martín; Fittipaldi, Sol; Ibañez, Agustin Mariano
Año de publicación
2021
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Social feedback can selectively enhance learning in diverse domains. Relevant neurocognitive mechanisms have been studied mainly in healthy persons, yielding correlational findings. Neurodegenerative lesion models, coupled with multimodal brain measures, can complement standard approaches by revealing direct multidimensional correlates of the phenomenon. To this end, we assessed socially reinforced and non-socially reinforced learning in 40 healthy participants as well as persons with behavioural variant frontotemporal dementia (n = 21), Parkinson's disease (n = 31) and Alzheimer's disease (n = 20). These conditions are typified by predominant deficits in social cognition, feedback-based learning and associative learning, respectively, although all three domains may be partly compromised in the other conditions. We combined a validated behavioural task with ongoing EEG signatures of implicit learning (medial frontal negativity) and offline MRI measures (voxel-based morphometry). In healthy participants, learning was facilitated by social feedback relative to non-social feedback. In comparison with controls, this effect was specifically impaired in behavioural variant frontotemporal dementia and Parkinson's disease, while unspecific learning deficits (across social and non-social conditions) were observed in Alzheimer's disease. EEG results showed increased medial frontal negativity in healthy controls during social feedback and learning. Such a modulation was selectively disrupted in behavioural variant frontotemporal dementia. Neuroanatomical results revealed extended temporo-parietal and fronto-limbic correlates of socially reinforced learning, with specific temporo-parietal associations in behavioural variant frontotemporal dementia and predominantly fronto-limbic regions in Alzheimer's disease. In contrast, non-socially reinforced learning was consistently linked to medial temporal/hippocampal regions. No associations with cortical volume were found in Parkinson's disease. Results are consistent with core social deficits in behavioural variant frontotemporal dementia, subtle disruptions in ongoing feedback-mechanisms and social processes in Parkinson's disease and generalized learning alterations in Alzheimer's disease. This multimodal approach highlights the impact of different neurodegenerative profiles on learning and social feedback. Our findings inform a promising theoretical and clinical agenda in the fields of social learning, socially reinforced learning and neurodegeneration.
Fil: Legaz, Agustina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Neurociencia Cognitiva. Fundación Favaloro. Instituto de Neurociencia Cognitiva; Argentina. Universidad Nacional de Córdoba; Argentina
Fil: Abrevaya, Sofia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Neurociencia Cognitiva. Fundación Favaloro. Instituto de Neurociencia Cognitiva; Argentina
Fil: Dottori, Martín. Universidad de San Andrés; Argentina
Fil: Campo, Cecilia González. Universidad de San Andrés; Argentina
Fil: Birba, Agustina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de San Andrés; Argentina
Fil: Martorell Caro, Miguel Angel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Neurociencia Cognitiva. Fundación Favaloro. Instituto de Neurociencia Cognitiva; Argentina
Fil: Aguirre, María Julieta. Universidad Nacional de Córdoba. Instituto de Investigaciones Psicológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Investigaciones Psicológicas; Argentina
Fil: Slachevsky, Andrea. Universidad de Chile.; Chile
Fil: Aranguiz, Rafael. Instituto Nacional de Geriatría; Chile
Fil: Serrano, Cecilia Mariela. Unidad Asistencial "Dr. César Milstein"; Argentina
Fil: Gillan, Claire M.. University of California; Estados Unidos
Fil: Leroi, Iracema. University of California; Estados Unidos
Fil: García, Adolfo Martín. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de San Andrés; Argentina. University of California; Estados Unidos. Trinity College; Estados Unidos. Universidad Nacional de Cuyo; Argentina. Universidad de Santiago de Chile; Chile
Fil: Fittipaldi, Sol. Universidad de San Andrés; Argentina
Fil: Ibañez, Agustin Mariano. Universidad de San Andrés; Argentina. University of California; Estados Unidos. Trinity College; Estados Unidos. Universidad Adolfo Ibañez; Chile. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Materia
ALZHEIMER'S DISEASE
BEHAVIOURAL VARIANT FRONTOTEMPORAL DEMENTIA
LEARNING
PARKINSON'S DISEASE
SOCIAL REINFORCEMENT
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:11336/171513
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/171513
network_acronym_str CONICETDig
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network_name_str CONICET Digital (CONICET)
spelling Multimodal mechanisms of human socially reinforced learning across neurodegenerative diseasesLegaz, AgustinaAbrevaya, SofiaDottori, MartínCampo, Cecilia GonzálezBirba, AgustinaMartorell Caro, Miguel AngelAguirre, María JulietaSlachevsky, AndreaAranguiz, RafaelSerrano, Cecilia MarielaGillan, Claire M.Leroi, IracemaGarcía, Adolfo MartínFittipaldi, SolIbañez, Agustin MarianoALZHEIMER'S DISEASEBEHAVIOURAL VARIANT FRONTOTEMPORAL DEMENTIALEARNINGPARKINSON'S DISEASESOCIAL REINFORCEMENThttps://purl.org/becyt/ford/3.1https://purl.org/becyt/ford/3Social feedback can selectively enhance learning in diverse domains. Relevant neurocognitive mechanisms have been studied mainly in healthy persons, yielding correlational findings. Neurodegenerative lesion models, coupled with multimodal brain measures, can complement standard approaches by revealing direct multidimensional correlates of the phenomenon. To this end, we assessed socially reinforced and non-socially reinforced learning in 40 healthy participants as well as persons with behavioural variant frontotemporal dementia (n = 21), Parkinson's disease (n = 31) and Alzheimer's disease (n = 20). These conditions are typified by predominant deficits in social cognition, feedback-based learning and associative learning, respectively, although all three domains may be partly compromised in the other conditions. We combined a validated behavioural task with ongoing EEG signatures of implicit learning (medial frontal negativity) and offline MRI measures (voxel-based morphometry). In healthy participants, learning was facilitated by social feedback relative to non-social feedback. In comparison with controls, this effect was specifically impaired in behavioural variant frontotemporal dementia and Parkinson's disease, while unspecific learning deficits (across social and non-social conditions) were observed in Alzheimer's disease. EEG results showed increased medial frontal negativity in healthy controls during social feedback and learning. Such a modulation was selectively disrupted in behavioural variant frontotemporal dementia. Neuroanatomical results revealed extended temporo-parietal and fronto-limbic correlates of socially reinforced learning, with specific temporo-parietal associations in behavioural variant frontotemporal dementia and predominantly fronto-limbic regions in Alzheimer's disease. In contrast, non-socially reinforced learning was consistently linked to medial temporal/hippocampal regions. No associations with cortical volume were found in Parkinson's disease. Results are consistent with core social deficits in behavioural variant frontotemporal dementia, subtle disruptions in ongoing feedback-mechanisms and social processes in Parkinson's disease and generalized learning alterations in Alzheimer's disease. This multimodal approach highlights the impact of different neurodegenerative profiles on learning and social feedback. Our findings inform a promising theoretical and clinical agenda in the fields of social learning, socially reinforced learning and neurodegeneration.Fil: Legaz, Agustina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Neurociencia Cognitiva. Fundación Favaloro. Instituto de Neurociencia Cognitiva; Argentina. Universidad Nacional de Córdoba; ArgentinaFil: Abrevaya, Sofia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Neurociencia Cognitiva. Fundación Favaloro. Instituto de Neurociencia Cognitiva; ArgentinaFil: Dottori, Martín. Universidad de San Andrés; ArgentinaFil: Campo, Cecilia González. Universidad de San Andrés; ArgentinaFil: Birba, Agustina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de San Andrés; ArgentinaFil: Martorell Caro, Miguel Angel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Neurociencia Cognitiva. Fundación Favaloro. Instituto de Neurociencia Cognitiva; ArgentinaFil: Aguirre, María Julieta. Universidad Nacional de Córdoba. Instituto de Investigaciones Psicológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Investigaciones Psicológicas; ArgentinaFil: Slachevsky, Andrea. Universidad de Chile.; ChileFil: Aranguiz, Rafael. Instituto Nacional de Geriatría; ChileFil: Serrano, Cecilia Mariela. Unidad Asistencial "Dr. César Milstein"; ArgentinaFil: Gillan, Claire M.. University of California; Estados UnidosFil: Leroi, Iracema. University of California; Estados UnidosFil: García, Adolfo Martín. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de San Andrés; Argentina. University of California; Estados Unidos. Trinity College; Estados Unidos. Universidad Nacional de Cuyo; Argentina. Universidad de Santiago de Chile; ChileFil: Fittipaldi, Sol. Universidad de San Andrés; ArgentinaFil: Ibañez, Agustin Mariano. Universidad de San Andrés; Argentina. University of California; Estados Unidos. Trinity College; Estados Unidos. Universidad Adolfo Ibañez; Chile. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaOxford University Press2021-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/171513Legaz, Agustina; Abrevaya, Sofia; Dottori, Martín; Campo, Cecilia González; Birba, Agustina; et al.; Multimodal mechanisms of human socially reinforced learning across neurodegenerative diseases; Oxford University Press; Brain; 145; 3; 3-2021; 1052-10680006-8950CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/brain/advance-article/doi/10.1093/brain/awab345/6371182info:eu-repo/semantics/altIdentifier/doi/10.1093/brain/awab345info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:35:00Zoai:ri.conicet.gov.ar:11336/171513instacron: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 09:35:00.824CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Multimodal mechanisms of human socially reinforced learning across neurodegenerative diseases
title Multimodal mechanisms of human socially reinforced learning across neurodegenerative diseases
spellingShingle Multimodal mechanisms of human socially reinforced learning across neurodegenerative diseases
Legaz, Agustina
ALZHEIMER'S DISEASE
BEHAVIOURAL VARIANT FRONTOTEMPORAL DEMENTIA
LEARNING
PARKINSON'S DISEASE
SOCIAL REINFORCEMENT
title_short Multimodal mechanisms of human socially reinforced learning across neurodegenerative diseases
title_full Multimodal mechanisms of human socially reinforced learning across neurodegenerative diseases
title_fullStr Multimodal mechanisms of human socially reinforced learning across neurodegenerative diseases
title_full_unstemmed Multimodal mechanisms of human socially reinforced learning across neurodegenerative diseases
title_sort Multimodal mechanisms of human socially reinforced learning across neurodegenerative diseases
dc.creator.none.fl_str_mv Legaz, Agustina
Abrevaya, Sofia
Dottori, Martín
Campo, Cecilia González
Birba, Agustina
Martorell Caro, Miguel Angel
Aguirre, María Julieta
Slachevsky, Andrea
Aranguiz, Rafael
Serrano, Cecilia Mariela
Gillan, Claire M.
Leroi, Iracema
García, Adolfo Martín
Fittipaldi, Sol
Ibañez, Agustin Mariano
author Legaz, Agustina
author_facet Legaz, Agustina
Abrevaya, Sofia
Dottori, Martín
Campo, Cecilia González
Birba, Agustina
Martorell Caro, Miguel Angel
Aguirre, María Julieta
Slachevsky, Andrea
Aranguiz, Rafael
Serrano, Cecilia Mariela
Gillan, Claire M.
Leroi, Iracema
García, Adolfo Martín
Fittipaldi, Sol
Ibañez, Agustin Mariano
author_role author
author2 Abrevaya, Sofia
Dottori, Martín
Campo, Cecilia González
Birba, Agustina
Martorell Caro, Miguel Angel
Aguirre, María Julieta
Slachevsky, Andrea
Aranguiz, Rafael
Serrano, Cecilia Mariela
Gillan, Claire M.
Leroi, Iracema
García, Adolfo Martín
Fittipaldi, Sol
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 ALZHEIMER'S DISEASE
BEHAVIOURAL VARIANT FRONTOTEMPORAL DEMENTIA
LEARNING
PARKINSON'S DISEASE
SOCIAL REINFORCEMENT
topic ALZHEIMER'S DISEASE
BEHAVIOURAL VARIANT FRONTOTEMPORAL DEMENTIA
LEARNING
PARKINSON'S DISEASE
SOCIAL REINFORCEMENT
purl_subject.fl_str_mv https://purl.org/becyt/ford/3.1
https://purl.org/becyt/ford/3
dc.description.none.fl_txt_mv Social feedback can selectively enhance learning in diverse domains. Relevant neurocognitive mechanisms have been studied mainly in healthy persons, yielding correlational findings. Neurodegenerative lesion models, coupled with multimodal brain measures, can complement standard approaches by revealing direct multidimensional correlates of the phenomenon. To this end, we assessed socially reinforced and non-socially reinforced learning in 40 healthy participants as well as persons with behavioural variant frontotemporal dementia (n = 21), Parkinson's disease (n = 31) and Alzheimer's disease (n = 20). These conditions are typified by predominant deficits in social cognition, feedback-based learning and associative learning, respectively, although all three domains may be partly compromised in the other conditions. We combined a validated behavioural task with ongoing EEG signatures of implicit learning (medial frontal negativity) and offline MRI measures (voxel-based morphometry). In healthy participants, learning was facilitated by social feedback relative to non-social feedback. In comparison with controls, this effect was specifically impaired in behavioural variant frontotemporal dementia and Parkinson's disease, while unspecific learning deficits (across social and non-social conditions) were observed in Alzheimer's disease. EEG results showed increased medial frontal negativity in healthy controls during social feedback and learning. Such a modulation was selectively disrupted in behavioural variant frontotemporal dementia. Neuroanatomical results revealed extended temporo-parietal and fronto-limbic correlates of socially reinforced learning, with specific temporo-parietal associations in behavioural variant frontotemporal dementia and predominantly fronto-limbic regions in Alzheimer's disease. In contrast, non-socially reinforced learning was consistently linked to medial temporal/hippocampal regions. No associations with cortical volume were found in Parkinson's disease. Results are consistent with core social deficits in behavioural variant frontotemporal dementia, subtle disruptions in ongoing feedback-mechanisms and social processes in Parkinson's disease and generalized learning alterations in Alzheimer's disease. This multimodal approach highlights the impact of different neurodegenerative profiles on learning and social feedback. Our findings inform a promising theoretical and clinical agenda in the fields of social learning, socially reinforced learning and neurodegeneration.
Fil: Legaz, Agustina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Neurociencia Cognitiva. Fundación Favaloro. Instituto de Neurociencia Cognitiva; Argentina. Universidad Nacional de Córdoba; Argentina
Fil: Abrevaya, Sofia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Neurociencia Cognitiva. Fundación Favaloro. Instituto de Neurociencia Cognitiva; Argentina
Fil: Dottori, Martín. Universidad de San Andrés; Argentina
Fil: Campo, Cecilia González. Universidad de San Andrés; Argentina
Fil: Birba, Agustina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de San Andrés; Argentina
Fil: Martorell Caro, Miguel Angel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Neurociencia Cognitiva. Fundación Favaloro. Instituto de Neurociencia Cognitiva; Argentina
Fil: Aguirre, María Julieta. Universidad Nacional de Córdoba. Instituto de Investigaciones Psicológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Investigaciones Psicológicas; Argentina
Fil: Slachevsky, Andrea. Universidad de Chile.; Chile
Fil: Aranguiz, Rafael. Instituto Nacional de Geriatría; Chile
Fil: Serrano, Cecilia Mariela. Unidad Asistencial "Dr. César Milstein"; Argentina
Fil: Gillan, Claire M.. University of California; Estados Unidos
Fil: Leroi, Iracema. University of California; Estados Unidos
Fil: García, Adolfo Martín. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de San Andrés; Argentina. University of California; Estados Unidos. Trinity College; Estados Unidos. Universidad Nacional de Cuyo; Argentina. Universidad de Santiago de Chile; Chile
Fil: Fittipaldi, Sol. Universidad de San Andrés; Argentina
Fil: Ibañez, Agustin Mariano. Universidad de San Andrés; Argentina. University of California; Estados Unidos. Trinity College; Estados Unidos. Universidad Adolfo Ibañez; Chile. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
description Social feedback can selectively enhance learning in diverse domains. Relevant neurocognitive mechanisms have been studied mainly in healthy persons, yielding correlational findings. Neurodegenerative lesion models, coupled with multimodal brain measures, can complement standard approaches by revealing direct multidimensional correlates of the phenomenon. To this end, we assessed socially reinforced and non-socially reinforced learning in 40 healthy participants as well as persons with behavioural variant frontotemporal dementia (n = 21), Parkinson's disease (n = 31) and Alzheimer's disease (n = 20). These conditions are typified by predominant deficits in social cognition, feedback-based learning and associative learning, respectively, although all three domains may be partly compromised in the other conditions. We combined a validated behavioural task with ongoing EEG signatures of implicit learning (medial frontal negativity) and offline MRI measures (voxel-based morphometry). In healthy participants, learning was facilitated by social feedback relative to non-social feedback. In comparison with controls, this effect was specifically impaired in behavioural variant frontotemporal dementia and Parkinson's disease, while unspecific learning deficits (across social and non-social conditions) were observed in Alzheimer's disease. EEG results showed increased medial frontal negativity in healthy controls during social feedback and learning. Such a modulation was selectively disrupted in behavioural variant frontotemporal dementia. Neuroanatomical results revealed extended temporo-parietal and fronto-limbic correlates of socially reinforced learning, with specific temporo-parietal associations in behavioural variant frontotemporal dementia and predominantly fronto-limbic regions in Alzheimer's disease. In contrast, non-socially reinforced learning was consistently linked to medial temporal/hippocampal regions. No associations with cortical volume were found in Parkinson's disease. Results are consistent with core social deficits in behavioural variant frontotemporal dementia, subtle disruptions in ongoing feedback-mechanisms and social processes in Parkinson's disease and generalized learning alterations in Alzheimer's disease. This multimodal approach highlights the impact of different neurodegenerative profiles on learning and social feedback. Our findings inform a promising theoretical and clinical agenda in the fields of social learning, socially reinforced learning and neurodegeneration.
publishDate 2021
dc.date.none.fl_str_mv 2021-03
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/11336/171513
Legaz, Agustina; Abrevaya, Sofia; Dottori, Martín; Campo, Cecilia González; Birba, Agustina; et al.; Multimodal mechanisms of human socially reinforced learning across neurodegenerative diseases; Oxford University Press; Brain; 145; 3; 3-2021; 1052-1068
0006-8950
CONICET Digital
CONICET
url http://hdl.handle.net/11336/171513
identifier_str_mv Legaz, Agustina; Abrevaya, Sofia; Dottori, Martín; Campo, Cecilia González; Birba, Agustina; et al.; Multimodal mechanisms of human socially reinforced learning across neurodegenerative diseases; Oxford University Press; Brain; 145; 3; 3-2021; 1052-1068
0006-8950
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/brain/advance-article/doi/10.1093/brain/awab345/6371182
info:eu-repo/semantics/altIdentifier/doi/10.1093/brain/awab345
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
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)
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repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
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