Network-wide reorganization of procedural memory during NREM sleep revealed by fMRI

Sleep is necessary for the optimal consolidation of newly acquired procedural memories. However, the mechanisms by which motor memory traces develop during sleep remain controversial in humans, as this process has been mainly investigated indirectly by comparing pre- and post-sleep conditions. Here,...

Full description

Bibliographic Details
Main Authors: Shahabeddin Vahdat, Stuart Fogel, Habib Benali, Julien Doyon
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-09-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/24987
id doaj-2f080dceec1d4a48ba91ff8f483c1eb1
record_format Article
spelling doaj-2f080dceec1d4a48ba91ff8f483c1eb12021-05-05T13:47:24ZengeLife Sciences Publications LtdeLife2050-084X2017-09-01610.7554/eLife.24987Network-wide reorganization of procedural memory during NREM sleep revealed by fMRIShahabeddin Vahdat0https://orcid.org/0000-0002-0494-6974Stuart Fogel1https://orcid.org/0000-0002-3227-5370Habib Benali2Julien Doyon3https://orcid.org/0000-0002-3788-4271Functional Neuroimaging Unit, Cenre de recherche, Institut universitaire de gériatrie de Montréal, Université de Montreal, Québec, CanadaSchool of Psychology, University of Ottawa, Ontario, CanadaPERFORM Centre, University of Concordia, Montreal, Quebec, Canada; INSERM/UPMC, Pitié-Salpêtrière Hospital, Paris, FranceFunctional Neuroimaging Unit, Cenre de recherche, Institut universitaire de gériatrie de Montréal, Université de Montreal, Québec, CanadaSleep is necessary for the optimal consolidation of newly acquired procedural memories. However, the mechanisms by which motor memory traces develop during sleep remain controversial in humans, as this process has been mainly investigated indirectly by comparing pre- and post-sleep conditions. Here, we used functional magnetic resonance imaging and electroencephalography during sleep following motor sequence learning to investigate how newly-formed memory traces evolve dynamically over time. We provide direct evidence for transient reactivation followed by downscaling of functional connectivity in a cortically-dominant pattern formed during learning, as well as gradual reorganization of this representation toward a subcortically-dominant consolidated trace during non-rapid eye movement (NREM) sleep. Importantly, the putamen functional connectivity within the consolidated network during NREM sleep was related to overnight behavioral gains. Our results demonstrate that NREM sleep is necessary for two complementary processes: the restoration and reorganization of newly-learned information during sleep, which underlie human motor memory consolidation.https://elifesciences.org/articles/24987motor learningsleepconsolidationfMRIstriatumneuroplasticity
collection DOAJ
language English
format Article
sources DOAJ
author Shahabeddin Vahdat
Stuart Fogel
Habib Benali
Julien Doyon
spellingShingle Shahabeddin Vahdat
Stuart Fogel
Habib Benali
Julien Doyon
Network-wide reorganization of procedural memory during NREM sleep revealed by fMRI
eLife
motor learning
sleep
consolidation
fMRI
striatum
neuroplasticity
author_facet Shahabeddin Vahdat
Stuart Fogel
Habib Benali
Julien Doyon
author_sort Shahabeddin Vahdat
title Network-wide reorganization of procedural memory during NREM sleep revealed by fMRI
title_short Network-wide reorganization of procedural memory during NREM sleep revealed by fMRI
title_full Network-wide reorganization of procedural memory during NREM sleep revealed by fMRI
title_fullStr Network-wide reorganization of procedural memory during NREM sleep revealed by fMRI
title_full_unstemmed Network-wide reorganization of procedural memory during NREM sleep revealed by fMRI
title_sort network-wide reorganization of procedural memory during nrem sleep revealed by fmri
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2017-09-01
description Sleep is necessary for the optimal consolidation of newly acquired procedural memories. However, the mechanisms by which motor memory traces develop during sleep remain controversial in humans, as this process has been mainly investigated indirectly by comparing pre- and post-sleep conditions. Here, we used functional magnetic resonance imaging and electroencephalography during sleep following motor sequence learning to investigate how newly-formed memory traces evolve dynamically over time. We provide direct evidence for transient reactivation followed by downscaling of functional connectivity in a cortically-dominant pattern formed during learning, as well as gradual reorganization of this representation toward a subcortically-dominant consolidated trace during non-rapid eye movement (NREM) sleep. Importantly, the putamen functional connectivity within the consolidated network during NREM sleep was related to overnight behavioral gains. Our results demonstrate that NREM sleep is necessary for two complementary processes: the restoration and reorganization of newly-learned information during sleep, which underlie human motor memory consolidation.
topic motor learning
sleep
consolidation
fMRI
striatum
neuroplasticity
url https://elifesciences.org/articles/24987
work_keys_str_mv AT shahabeddinvahdat networkwidereorganizationofproceduralmemoryduringnremsleeprevealedbyfmri
AT stuartfogel networkwidereorganizationofproceduralmemoryduringnremsleeprevealedbyfmri
AT habibbenali networkwidereorganizationofproceduralmemoryduringnremsleeprevealedbyfmri
AT juliendoyon networkwidereorganizationofproceduralmemoryduringnremsleeprevealedbyfmri
_version_ 1721461279038636032