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Neuroimage. 2018 Apr 1;169:419-430. doi: 10.1016/j.neuroimage.2017.12.066. Epub 2017 Dec 24.

Transient synchronization of hippocampo-striato-thalamo-cortical networks during sleep spindle oscillations induces motor memory consolidation.

Author information

1
Unité de Neuroimagerie Fonctionnelle, C.R.I.U.G.M., Montréal, QC, Canada; Université de Montréal, Montréal, QC, Canada. Electronic address: arnaud.boutin@criugm.qc.ca.
2
Unité de Neuroimagerie Fonctionnelle, C.R.I.U.G.M., Montréal, QC, Canada; Université de Montréal, Montréal, QC, Canada; Sorbonne Universités, UPMC Université Paris 06, CNRS, INSERM, Laboratoire d'Imagerie Biomédicale, Paris, France.
3
Unité de Neuroimagerie Fonctionnelle, C.R.I.U.G.M., Montréal, QC, Canada.
4
Unité de Neuroimagerie Fonctionnelle, C.R.I.U.G.M., Montréal, QC, Canada; Université de Montréal, Montréal, QC, Canada; Center for Advanced Research in Sleep Medicine, Hôpital du Sacré-Coeur de Montréal, Montréal, Canada.
5
School of Psychology, University of Ottawa, Ottawa, Canada.
6
Unité de Neuroimagerie Fonctionnelle, C.R.I.U.G.M., Montréal, QC, Canada; Université de Montréal, Montréal, QC, Canada. Electronic address: julien.doyon@mcgill.ca.

Abstract

Sleep benefits motor memory consolidation. This mnemonic process is thought to be mediated by thalamo-cortical spindle activity during NREM-stage2 sleep episodes as well as changes in striatal and hippocampal activity. However, direct experimental evidence supporting the contribution of such sleep-dependent physiological mechanisms to motor memory consolidation in humans is lacking. In the present study, we combined EEG and fMRI sleep recordings following practice of a motor sequence learning (MSL) task to determine whether spindle oscillations support sleep-dependent motor memory consolidation by transiently synchronizing and coordinating specialized cortical and subcortical networks. To that end, we conducted EEG source reconstruction on spindle epochs in both cortical and subcortical regions using novel deep-source localization techniques. Coherence-based metrics were adopted to estimate functional connectivity between cortical and subcortical structures over specific frequency bands. Our findings not only confirm the critical and functional role of NREM-stage2 sleep spindles in motor skill consolidation, but provide first-time evidence that spindle oscillations [11-17 Hz] may be involved in sleep-dependent motor memory consolidation by locally reactivating and functionally binding specific task-relevant cortical and subcortical regions within networks including the hippocampus, putamen, thalamus and motor-related cortical regions.

KEYWORDS:

EEG; Hippocampus; Memory consolidation; Motor sequence learning; Putamen; Sleep; Spindles; fMRI

[Indexed for MEDLINE]

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