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Reactivation or transformation? Motor memory consolidation associated with cerebral activation time-locked to sleep spindles

Motor memory consolidation is thought to depend on sleep-dependent reactivation of brain areas recruited during learning. However, up to this point, there has been no direct evidence to support this assertion in humans, and the physiological processes supporting such reactivation are unknown. Here,...

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Autores principales: Fogel, Stuart, Albouy, Genevieve, King, Bradley R., Lungu, Ovidiu, Vien, Catherine, Bore, Arnaud, Pinsard, Basile, Benali, Habib, Carrier, Julie, Doyon, Julien
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5396873/
https://www.ncbi.nlm.nih.gov/pubmed/28422976
http://dx.doi.org/10.1371/journal.pone.0174755
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author Fogel, Stuart
Albouy, Genevieve
King, Bradley R.
Lungu, Ovidiu
Vien, Catherine
Bore, Arnaud
Pinsard, Basile
Benali, Habib
Carrier, Julie
Doyon, Julien
author_facet Fogel, Stuart
Albouy, Genevieve
King, Bradley R.
Lungu, Ovidiu
Vien, Catherine
Bore, Arnaud
Pinsard, Basile
Benali, Habib
Carrier, Julie
Doyon, Julien
author_sort Fogel, Stuart
collection PubMed
description Motor memory consolidation is thought to depend on sleep-dependent reactivation of brain areas recruited during learning. However, up to this point, there has been no direct evidence to support this assertion in humans, and the physiological processes supporting such reactivation are unknown. Here, simultaneous electroencephalographic and functional magnetic resonance imaging (EEG-fMRI) recordings were conducted during post-learning sleep to directly investigate the spindle-related reactivation of a memory trace formed during motor sequence learning (MSL), and its relationship to overnight enhancement in performance (reflecting consolidation). We show that brain regions within the striato-cerebello-cortical network recruited during training on the MSL task, and in particular the striatum, were also activated during sleep, time-locked to spindles. Interestingly, the consolidated trace in the striatum was not simply strengthened, but was transformed/reorganized from rostrodorsal (associative) to caudoventral (sensorimotor) subregions. Moreover, the degree of the reactivation was correlated with overnight improvements in performance. Altogether, the present findings demonstrate that striatal reactivation linked to sleep spindles in the post-learning night, is related to motor memory consolidation.
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spelling pubmed-53968732017-05-04 Reactivation or transformation? Motor memory consolidation associated with cerebral activation time-locked to sleep spindles Fogel, Stuart Albouy, Genevieve King, Bradley R. Lungu, Ovidiu Vien, Catherine Bore, Arnaud Pinsard, Basile Benali, Habib Carrier, Julie Doyon, Julien PLoS One Research Article Motor memory consolidation is thought to depend on sleep-dependent reactivation of brain areas recruited during learning. However, up to this point, there has been no direct evidence to support this assertion in humans, and the physiological processes supporting such reactivation are unknown. Here, simultaneous electroencephalographic and functional magnetic resonance imaging (EEG-fMRI) recordings were conducted during post-learning sleep to directly investigate the spindle-related reactivation of a memory trace formed during motor sequence learning (MSL), and its relationship to overnight enhancement in performance (reflecting consolidation). We show that brain regions within the striato-cerebello-cortical network recruited during training on the MSL task, and in particular the striatum, were also activated during sleep, time-locked to spindles. Interestingly, the consolidated trace in the striatum was not simply strengthened, but was transformed/reorganized from rostrodorsal (associative) to caudoventral (sensorimotor) subregions. Moreover, the degree of the reactivation was correlated with overnight improvements in performance. Altogether, the present findings demonstrate that striatal reactivation linked to sleep spindles in the post-learning night, is related to motor memory consolidation. Public Library of Science 2017-04-19 /pmc/articles/PMC5396873/ /pubmed/28422976 http://dx.doi.org/10.1371/journal.pone.0174755 Text en © 2017 Fogel et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Fogel, Stuart
Albouy, Genevieve
King, Bradley R.
Lungu, Ovidiu
Vien, Catherine
Bore, Arnaud
Pinsard, Basile
Benali, Habib
Carrier, Julie
Doyon, Julien
Reactivation or transformation? Motor memory consolidation associated with cerebral activation time-locked to sleep spindles
title Reactivation or transformation? Motor memory consolidation associated with cerebral activation time-locked to sleep spindles
title_full Reactivation or transformation? Motor memory consolidation associated with cerebral activation time-locked to sleep spindles
title_fullStr Reactivation or transformation? Motor memory consolidation associated with cerebral activation time-locked to sleep spindles
title_full_unstemmed Reactivation or transformation? Motor memory consolidation associated with cerebral activation time-locked to sleep spindles
title_short Reactivation or transformation? Motor memory consolidation associated with cerebral activation time-locked to sleep spindles
title_sort reactivation or transformation? motor memory consolidation associated with cerebral activation time-locked to sleep spindles
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5396873/
https://www.ncbi.nlm.nih.gov/pubmed/28422976
http://dx.doi.org/10.1371/journal.pone.0174755
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