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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Bibliographic Details
Published in:PloS one 2017-04, Vol.12 (4), p.e0174755-e0174755
Main Authors: Fogel, Stuart, Albouy, Genevieve, King, Bradley R, Lungu, Ovidiu, Vien, Catherine, Bore, Arnaud, Pinsard, Basile, Benali, Habib, Carrier, Julie, Doyon, Julien
Format: Article
Language:English
Subjects:
Activation
Activity patterns
Adult
Biology and Life Sciences
Brain
Brain research
Cerebellum - anatomy & histology
Cerebellum - physiology
Cerebral Cortex - anatomy & histology
Cerebral Cortex - physiology
Consolidation
Corpus Striatum - anatomy & histology
Corpus Striatum - physiology
Efferent Pathways - anatomy & histology
Efferent Pathways - physiology
Electroencephalography
Female
Human health and pathology
Humans
Learning
Learning - physiology
Life Sciences
Magnetic resonance
Magnetic Resonance Imaging
Male
Medical imaging
Medicine and Health Sciences
Memory
Memory Consolidation - physiology
Motor ability
Physiology
Polysomnography
Psychomotor Performance - physiology
Research and Analysis Methods
Rodents
Skills
Sleep
Sleep - physiology
Social Sciences
Spindles
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Summary: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.
ISSN:1932-6203
1932-6203
DOI:10.1371/journal.pone.0174755