Sleep consolidation potentiates sensorimotor adaptation

Autores
Solano, Agustín Benjamín Ezequiel; Lerner, Gonzalo Martin; Griffa, Guillermina; Deleglise, Álvaro; Caffaro, Pedro Alejandro; Riquelme, Luis; Pérez Chada, Daniel; Della Maggiore, Valeria Monica
Año de publicación
2024
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Contrary to its well-established role in declarative learning, the impact of sleep on motor memory consolidation remains a subject of debate. Current literature suggests that while motor skill learning benefits from sleep, consolidation of sensorimotor adaptation (SMA) depends solely on the passage of time. This has led to the proposal that SMA may be an exception to other types of memories. Here, we addressed this ongoing controversy in humans through three comprehensive experiments using the visuomotor adaptation paradigm (N = 290, 150 females). In Experiment 1, we investigated the impact of sleep on memory retention when the temporal gap between training and sleep was not controlled. In line with the previous literature, we found that memory consolidates with the passage of time. In Experiment 2, we used an anterograde interference protocol to determine the time window during which SMA memory is most fragile and, thus, potentially most sensitive to sleep intervention. Our results show that memory is most vulnerable during the initial hour post-training. Building on this insight, in Experiment 3, we investigated the impact of sleep when it coincided with the critical first hour of memory consolidation. This manipulation unveiled a benefit of sleep (30% memory enhancement) alongside an increase in spindle density and spindle–SO coupling during NREM sleep, two well-established neural markers of sleep consolidation. Our findings reconcile seemingly conflicting perspectives on the active role of sleep in motor learning and point to common mechanisms at the basis of memory formation.
Fil: Solano, Agustín Benjamín Ezequiel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
Fil: Lerner, Gonzalo Martin. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
Fil: Griffa, Guillermina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
Fil: Deleglise, Álvaro. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
Fil: Caffaro, Pedro Alejandro. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
Fil: Riquelme, Luis. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
Fil: Pérez Chada, Daniel. Universidad Austral. Hospital Universitario Austral; Argentina
Fil: Della Maggiore, Valeria Monica. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
Materia
consolidation
EEG
human
motor learning
sleep
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:11336/267409
Acceder
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spelling Sleep consolidation potentiates sensorimotor adaptationSolano, Agustín Benjamín EzequielLerner, Gonzalo MartinGriffa, GuillerminaDeleglise, ÁlvaroCaffaro, Pedro AlejandroRiquelme, LuisPérez Chada, DanielDella Maggiore, Valeria MonicaconsolidationEEGhumanmotor learningsleephttps://purl.org/becyt/ford/1.7https://purl.org/becyt/ford/1Contrary to its well-established role in declarative learning, the impact of sleep on motor memory consolidation remains a subject of debate. Current literature suggests that while motor skill learning benefits from sleep, consolidation of sensorimotor adaptation (SMA) depends solely on the passage of time. This has led to the proposal that SMA may be an exception to other types of memories. Here, we addressed this ongoing controversy in humans through three comprehensive experiments using the visuomotor adaptation paradigm (N = 290, 150 females). In Experiment 1, we investigated the impact of sleep on memory retention when the temporal gap between training and sleep was not controlled. In line with the previous literature, we found that memory consolidates with the passage of time. In Experiment 2, we used an anterograde interference protocol to determine the time window during which SMA memory is most fragile and, thus, potentially most sensitive to sleep intervention. Our results show that memory is most vulnerable during the initial hour post-training. Building on this insight, in Experiment 3, we investigated the impact of sleep when it coincided with the critical first hour of memory consolidation. This manipulation unveiled a benefit of sleep (30% memory enhancement) alongside an increase in spindle density and spindle–SO coupling during NREM sleep, two well-established neural markers of sleep consolidation. Our findings reconcile seemingly conflicting perspectives on the active role of sleep in motor learning and point to common mechanisms at the basis of memory formation.Fil: Solano, Agustín Benjamín Ezequiel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; ArgentinaFil: Lerner, Gonzalo Martin. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; ArgentinaFil: Griffa, Guillermina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; ArgentinaFil: Deleglise, Álvaro. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; ArgentinaFil: Caffaro, Pedro Alejandro. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; ArgentinaFil: Riquelme, Luis. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; ArgentinaFil: Pérez Chada, Daniel. Universidad Austral. Hospital Universitario Austral; ArgentinaFil: Della Maggiore, Valeria Monica. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; ArgentinaSociety for Neuroscience2024-07info: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/11336/267409Solano, Agustín Benjamín Ezequiel; Lerner, Gonzalo Martin; Griffa, Guillermina; Deleglise, Álvaro; Caffaro, Pedro Alejandro; et al.; Sleep consolidation potentiates sensorimotor adaptation; Society for Neuroscience; Journal of Neuroscience; 44; 36; 7-2024; 1-120270-6474CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1523/JNEUROSCI.0325-24.2024info:eu-repo/semantics/altIdentifier/url/https://www.jneurosci.org/content/44/36/e0325242024info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-15T14:20:56Zoai:ri.conicet.gov.ar:11336/267409instacron: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 14:20:56.813CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Sleep consolidation potentiates sensorimotor adaptation
title Sleep consolidation potentiates sensorimotor adaptation
spellingShingle Sleep consolidation potentiates sensorimotor adaptation
Solano, Agustín Benjamín Ezequiel
consolidation
EEG
human
motor learning
sleep
title_short Sleep consolidation potentiates sensorimotor adaptation
title_full Sleep consolidation potentiates sensorimotor adaptation
title_fullStr Sleep consolidation potentiates sensorimotor adaptation
title_full_unstemmed Sleep consolidation potentiates sensorimotor adaptation
title_sort Sleep consolidation potentiates sensorimotor adaptation
dc.creator.none.fl_str_mv Solano, Agustín Benjamín Ezequiel
Lerner, Gonzalo Martin
Griffa, Guillermina
Deleglise, Álvaro
Caffaro, Pedro Alejandro
Riquelme, Luis
Pérez Chada, Daniel
Della Maggiore, Valeria Monica
author Solano, Agustín Benjamín Ezequiel
author_facet Solano, Agustín Benjamín Ezequiel
Lerner, Gonzalo Martin
Griffa, Guillermina
Deleglise, Álvaro
Caffaro, Pedro Alejandro
Riquelme, Luis
Pérez Chada, Daniel
Della Maggiore, Valeria Monica
author_role author
author2 Lerner, Gonzalo Martin
Griffa, Guillermina
Deleglise, Álvaro
Caffaro, Pedro Alejandro
Riquelme, Luis
Pérez Chada, Daniel
Della Maggiore, Valeria Monica
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv consolidation
EEG
human
motor learning
sleep
topic consolidation
EEG
human
motor learning
sleep
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.7
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Contrary to its well-established role in declarative learning, the impact of sleep on motor memory consolidation remains a subject of debate. Current literature suggests that while motor skill learning benefits from sleep, consolidation of sensorimotor adaptation (SMA) depends solely on the passage of time. This has led to the proposal that SMA may be an exception to other types of memories. Here, we addressed this ongoing controversy in humans through three comprehensive experiments using the visuomotor adaptation paradigm (N = 290, 150 females). In Experiment 1, we investigated the impact of sleep on memory retention when the temporal gap between training and sleep was not controlled. In line with the previous literature, we found that memory consolidates with the passage of time. In Experiment 2, we used an anterograde interference protocol to determine the time window during which SMA memory is most fragile and, thus, potentially most sensitive to sleep intervention. Our results show that memory is most vulnerable during the initial hour post-training. Building on this insight, in Experiment 3, we investigated the impact of sleep when it coincided with the critical first hour of memory consolidation. This manipulation unveiled a benefit of sleep (30% memory enhancement) alongside an increase in spindle density and spindle–SO coupling during NREM sleep, two well-established neural markers of sleep consolidation. Our findings reconcile seemingly conflicting perspectives on the active role of sleep in motor learning and point to common mechanisms at the basis of memory formation.
Fil: Solano, Agustín Benjamín Ezequiel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
Fil: Lerner, Gonzalo Martin. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
Fil: Griffa, Guillermina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
Fil: Deleglise, Álvaro. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
Fil: Caffaro, Pedro Alejandro. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
Fil: Riquelme, Luis. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
Fil: Pérez Chada, Daniel. Universidad Austral. Hospital Universitario Austral; Argentina
Fil: Della Maggiore, Valeria Monica. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina
description Contrary to its well-established role in declarative learning, the impact of sleep on motor memory consolidation remains a subject of debate. Current literature suggests that while motor skill learning benefits from sleep, consolidation of sensorimotor adaptation (SMA) depends solely on the passage of time. This has led to the proposal that SMA may be an exception to other types of memories. Here, we addressed this ongoing controversy in humans through three comprehensive experiments using the visuomotor adaptation paradigm (N = 290, 150 females). In Experiment 1, we investigated the impact of sleep on memory retention when the temporal gap between training and sleep was not controlled. In line with the previous literature, we found that memory consolidates with the passage of time. In Experiment 2, we used an anterograde interference protocol to determine the time window during which SMA memory is most fragile and, thus, potentially most sensitive to sleep intervention. Our results show that memory is most vulnerable during the initial hour post-training. Building on this insight, in Experiment 3, we investigated the impact of sleep when it coincided with the critical first hour of memory consolidation. This manipulation unveiled a benefit of sleep (30% memory enhancement) alongside an increase in spindle density and spindle–SO coupling during NREM sleep, two well-established neural markers of sleep consolidation. Our findings reconcile seemingly conflicting perspectives on the active role of sleep in motor learning and point to common mechanisms at the basis of memory formation.
publishDate 2024
dc.date.none.fl_str_mv 2024-07
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/11336/267409
Solano, Agustín Benjamín Ezequiel; Lerner, Gonzalo Martin; Griffa, Guillermina; Deleglise, Álvaro; Caffaro, Pedro Alejandro; et al.; Sleep consolidation potentiates sensorimotor adaptation; Society for Neuroscience; Journal of Neuroscience; 44; 36; 7-2024; 1-12
0270-6474
CONICET Digital
CONICET
url http://hdl.handle.net/11336/267409
identifier_str_mv Solano, Agustín Benjamín Ezequiel; Lerner, Gonzalo Martin; Griffa, Guillermina; Deleglise, Álvaro; Caffaro, Pedro Alejandro; et al.; Sleep consolidation potentiates sensorimotor adaptation; Society for Neuroscience; Journal of Neuroscience; 44; 36; 7-2024; 1-12
0270-6474
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1523/JNEUROSCI.0325-24.2024
info:eu-repo/semantics/altIdentifier/url/https://www.jneurosci.org/content/44/36/e0325242024
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
application/pdf
application/pdf
dc.publisher.none.fl_str_mv Society for Neuroscience
publisher.none.fl_str_mv Society for Neuroscience
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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