Stress undermines reward-guided cognitive performance through synaptic depression in the lateral habenula

Autores
Nuno Perez, Alvaro; Trusel, Massimo; Lalive, Arnaud L.; Congiu, Mauro; Gastaldo, Denise; Tchenio, Anna; Lecca, Salvatore; Soiza Reilly, Mariano; Bagni, Claudia; Mameli, Manuel
Año de publicación
2021
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Weighing alternatives during reward pursuit is a vital cognitive computation that, when disrupted by stress, yields aspects of neuropsychiatric disorders. To examine the neural mechanisms underlying these phenomena, we employed a behavioral task in which mice were confronted by a reward and its omission (i.e., error). The experience of error outcomes engaged neuronal dynamics within the lateral habenula (LHb), a subcortical structure that supports appetitive behaviors and is susceptible to stress. A high incidence of errors predicted low strength of habenular excitatory synapses. Accordingly, stressful experiences increased error choices while decreasing glutamatergic neurotransmission onto LHb neurons. This synaptic adaptation required a reduction in postsynaptic AMPA receptors (AMPARs), irrespective of the anatomical source of glutamate. Bidirectional control of habenular AMPAR transmission recapitulated and averted stress-driven cognitive deficits. Thus, a subcortical synaptic mechanism vulnerable to stress underlies behavioral efficiency during cognitive performance.
Fil: Nuno Perez, Alvaro. Universite de Lausanne; Suiza
Fil: Trusel, Massimo. Universite de Lausanne; Suiza
Fil: Lalive, Arnaud L.. Universite de Lausanne; Suiza
Fil: Congiu, Mauro. Universite de Lausanne; Suiza
Fil: Gastaldo, Denise. Universite de Lausanne; Suiza
Fil: Tchenio, Anna. Universite de Lausanne; Suiza
Fil: Lecca, Salvatore. Universite de Lausanne; Suiza
Fil: Soiza Reilly, Mariano. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; Argentina
Fil: Bagni, Claudia. Universite de Lausanne; Suiza
Fil: Mameli, Manuel. Inserm; Francia. Universite de Lausanne; Suiza
Materia
AMPA RECEPTORS
LATERAL HABENULA
REWARD-GUIDED BEHAVIORS
STRESS
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:11336/175287
Acceder
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repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Stress undermines reward-guided cognitive performance through synaptic depression in the lateral habenulaNuno Perez, AlvaroTrusel, MassimoLalive, Arnaud L.Congiu, MauroGastaldo, DeniseTchenio, AnnaLecca, SalvatoreSoiza Reilly, MarianoBagni, ClaudiaMameli, ManuelAMPA RECEPTORSLATERAL HABENULAREWARD-GUIDED BEHAVIORSSTRESShttps://purl.org/becyt/ford/3.1https://purl.org/becyt/ford/3Weighing alternatives during reward pursuit is a vital cognitive computation that, when disrupted by stress, yields aspects of neuropsychiatric disorders. To examine the neural mechanisms underlying these phenomena, we employed a behavioral task in which mice were confronted by a reward and its omission (i.e., error). The experience of error outcomes engaged neuronal dynamics within the lateral habenula (LHb), a subcortical structure that supports appetitive behaviors and is susceptible to stress. A high incidence of errors predicted low strength of habenular excitatory synapses. Accordingly, stressful experiences increased error choices while decreasing glutamatergic neurotransmission onto LHb neurons. This synaptic adaptation required a reduction in postsynaptic AMPA receptors (AMPARs), irrespective of the anatomical source of glutamate. Bidirectional control of habenular AMPAR transmission recapitulated and averted stress-driven cognitive deficits. Thus, a subcortical synaptic mechanism vulnerable to stress underlies behavioral efficiency during cognitive performance.Fil: Nuno Perez, Alvaro. Universite de Lausanne; SuizaFil: Trusel, Massimo. Universite de Lausanne; SuizaFil: Lalive, Arnaud L.. Universite de Lausanne; SuizaFil: Congiu, Mauro. Universite de Lausanne; SuizaFil: Gastaldo, Denise. Universite de Lausanne; SuizaFil: Tchenio, Anna. Universite de Lausanne; SuizaFil: Lecca, Salvatore. Universite de Lausanne; SuizaFil: Soiza Reilly, Mariano. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; ArgentinaFil: Bagni, Claudia. Universite de Lausanne; SuizaFil: Mameli, Manuel. Inserm; Francia. Universite de Lausanne; SuizaCell Press2021-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/175287Nuno Perez, Alvaro; Trusel, Massimo; Lalive, Arnaud L.; Congiu, Mauro; Gastaldo, Denise; et al.; Stress undermines reward-guided cognitive performance through synaptic depression in the lateral habenula; Cell Press; Neuron; 109; 6; 3-2021; 947-9560896-6273CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://linkinghub.elsevier.com/retrieve/pii/S0896627321000088info:eu-repo/semantics/altIdentifier/doi/10.1016/j.neuron.2021.01.008info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:15:31Zoai:ri.conicet.gov.ar:11336/175287instacron: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 10:15:32.064CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Stress undermines reward-guided cognitive performance through synaptic depression in the lateral habenula
title Stress undermines reward-guided cognitive performance through synaptic depression in the lateral habenula
spellingShingle Stress undermines reward-guided cognitive performance through synaptic depression in the lateral habenula
Nuno Perez, Alvaro
AMPA RECEPTORS
LATERAL HABENULA
REWARD-GUIDED BEHAVIORS
STRESS
title_short Stress undermines reward-guided cognitive performance through synaptic depression in the lateral habenula
title_full Stress undermines reward-guided cognitive performance through synaptic depression in the lateral habenula
title_fullStr Stress undermines reward-guided cognitive performance through synaptic depression in the lateral habenula
title_full_unstemmed Stress undermines reward-guided cognitive performance through synaptic depression in the lateral habenula
title_sort Stress undermines reward-guided cognitive performance through synaptic depression in the lateral habenula
dc.creator.none.fl_str_mv Nuno Perez, Alvaro
Trusel, Massimo
Lalive, Arnaud L.
Congiu, Mauro
Gastaldo, Denise
Tchenio, Anna
Lecca, Salvatore
Soiza Reilly, Mariano
Bagni, Claudia
Mameli, Manuel
author Nuno Perez, Alvaro
author_facet Nuno Perez, Alvaro
Trusel, Massimo
Lalive, Arnaud L.
Congiu, Mauro
Gastaldo, Denise
Tchenio, Anna
Lecca, Salvatore
Soiza Reilly, Mariano
Bagni, Claudia
Mameli, Manuel
author_role author
author2 Trusel, Massimo
Lalive, Arnaud L.
Congiu, Mauro
Gastaldo, Denise
Tchenio, Anna
Lecca, Salvatore
Soiza Reilly, Mariano
Bagni, Claudia
Mameli, Manuel
author2_role author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv AMPA RECEPTORS
LATERAL HABENULA
REWARD-GUIDED BEHAVIORS
STRESS
topic AMPA RECEPTORS
LATERAL HABENULA
REWARD-GUIDED BEHAVIORS
STRESS
purl_subject.fl_str_mv https://purl.org/becyt/ford/3.1
https://purl.org/becyt/ford/3
dc.description.none.fl_txt_mv Weighing alternatives during reward pursuit is a vital cognitive computation that, when disrupted by stress, yields aspects of neuropsychiatric disorders. To examine the neural mechanisms underlying these phenomena, we employed a behavioral task in which mice were confronted by a reward and its omission (i.e., error). The experience of error outcomes engaged neuronal dynamics within the lateral habenula (LHb), a subcortical structure that supports appetitive behaviors and is susceptible to stress. A high incidence of errors predicted low strength of habenular excitatory synapses. Accordingly, stressful experiences increased error choices while decreasing glutamatergic neurotransmission onto LHb neurons. This synaptic adaptation required a reduction in postsynaptic AMPA receptors (AMPARs), irrespective of the anatomical source of glutamate. Bidirectional control of habenular AMPAR transmission recapitulated and averted stress-driven cognitive deficits. Thus, a subcortical synaptic mechanism vulnerable to stress underlies behavioral efficiency during cognitive performance.
Fil: Nuno Perez, Alvaro. Universite de Lausanne; Suiza
Fil: Trusel, Massimo. Universite de Lausanne; Suiza
Fil: Lalive, Arnaud L.. Universite de Lausanne; Suiza
Fil: Congiu, Mauro. Universite de Lausanne; Suiza
Fil: Gastaldo, Denise. Universite de Lausanne; Suiza
Fil: Tchenio, Anna. Universite de Lausanne; Suiza
Fil: Lecca, Salvatore. Universite de Lausanne; Suiza
Fil: Soiza Reilly, Mariano. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; Argentina
Fil: Bagni, Claudia. Universite de Lausanne; Suiza
Fil: Mameli, Manuel. Inserm; Francia. Universite de Lausanne; Suiza
description Weighing alternatives during reward pursuit is a vital cognitive computation that, when disrupted by stress, yields aspects of neuropsychiatric disorders. To examine the neural mechanisms underlying these phenomena, we employed a behavioral task in which mice were confronted by a reward and its omission (i.e., error). The experience of error outcomes engaged neuronal dynamics within the lateral habenula (LHb), a subcortical structure that supports appetitive behaviors and is susceptible to stress. A high incidence of errors predicted low strength of habenular excitatory synapses. Accordingly, stressful experiences increased error choices while decreasing glutamatergic neurotransmission onto LHb neurons. This synaptic adaptation required a reduction in postsynaptic AMPA receptors (AMPARs), irrespective of the anatomical source of glutamate. Bidirectional control of habenular AMPAR transmission recapitulated and averted stress-driven cognitive deficits. Thus, a subcortical synaptic mechanism vulnerable to stress underlies behavioral efficiency during cognitive performance.
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/11336/175287
Nuno Perez, Alvaro; Trusel, Massimo; Lalive, Arnaud L.; Congiu, Mauro; Gastaldo, Denise; et al.; Stress undermines reward-guided cognitive performance through synaptic depression in the lateral habenula; Cell Press; Neuron; 109; 6; 3-2021; 947-956
0896-6273
CONICET Digital
CONICET
url http://hdl.handle.net/11336/175287
identifier_str_mv Nuno Perez, Alvaro; Trusel, Massimo; Lalive, Arnaud L.; Congiu, Mauro; Gastaldo, Denise; et al.; Stress undermines reward-guided cognitive performance through synaptic depression in the lateral habenula; Cell Press; Neuron; 109; 6; 3-2021; 947-956
0896-6273
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://linkinghub.elsevier.com/retrieve/pii/S0896627321000088
info:eu-repo/semantics/altIdentifier/doi/10.1016/j.neuron.2021.01.008
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 Cell Press
publisher.none.fl_str_mv Cell 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
_version_ 1844614092171509760
score 13.070432

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