Literature DB >> 29277652

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

Arnaud Boutin1, Basile Pinsard2, Arnaud Boré3, Julie Carrier4, Stuart M Fogel5, Julien Doyon6.   

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.
Copyright © 2018 Elsevier Inc. All rights reserved.

Entities:  

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

Mesh:

Year:  2017        PMID: 29277652     DOI: 10.1016/j.neuroimage.2017.12.066

Source DB:  PubMed          Journal:  Neuroimage        ISSN: 1053-8119            Impact factor:   6.556


  20 in total

1.  The hippocampus is necessary for the consolidation of a task that does not require the hippocampus for initial learning.

Authors:  Anna C Schapiro; Allison G Reid; Alexandra Morgan; Dara S Manoach; Mieke Verfaellie; Robert Stickgold
Journal:  Hippocampus       Date:  2019-06-03       Impact factor: 3.899

2.  Beyond spindles: interactions between sleep spindles and boundary frequencies during cued reactivation of motor memory representations.

Authors:  Samuel Laventure; Basile Pinsard; Ovidiu Lungu; Julie Carrier; Stuart Fogel; Habib Benali; Jean-Marc Lina; Arnaud Boutin; Julien Doyon
Journal:  Sleep       Date:  2018-09-01       Impact factor: 5.849

Review 3.  A sleep spindle framework for motor memory consolidation.

Authors:  Arnaud Boutin; Julien Doyon
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2020-04-06       Impact factor: 6.237

4.  Reward does not facilitate visual perceptual learning until sleep occurs.

Authors:  Masako Tamaki; Aaron V Berard; Tyler Barnes-Diana; Jesse Siegel; Takeo Watanabe; Yuka Sasaki
Journal:  Proc Natl Acad Sci U S A       Date:  2019-12-31       Impact factor: 11.205

5.  The Degree of Nesting between Spindles and Slow Oscillations Modulates Neural Synchrony.

Authors:  Daniel B Silversmith; Stefan M Lemke; Daniel Egert; Joshua D Berke; Karunesh Ganguly
Journal:  J Neurosci       Date:  2020-05-05       Impact factor: 6.167

6.  Slow oscillation-spindle coupling strength predicts real-life gross-motor learning in adolescents and adults.

Authors:  Michael A Hahn; Kathrin Bothe; Dominik Heib; Manuel Schabus; Randolph F Helfrich; Kerstin Hoedlmoser
Journal:  Elife       Date:  2022-02-18       Impact factor: 8.140

7.  Hippocampal Egr1-Dependent Neuronal Ensembles Negatively Regulate Motor Learning.

Authors:  Verónica Brito; Enrica Montalban; Anna Sancho-Balsells; Anika Pupak; Francesca Flotta; Mercè Masana; Silvia Ginés; Jordi Alberch; Claire Martin; Jean-Antoine Girault; Albert Giralt
Journal:  J Neurosci       Date:  2022-05-24       Impact factor: 6.709

Review 8.  The Brain-Derived Neurotrophic Factor: Missing Link Between Sleep Deprivation, Insomnia, and Depression.

Authors:  Maryam Rahmani; Farzaneh Rahmani; Nima Rezaei
Journal:  Neurochem Res       Date:  2019-11-28       Impact factor: 3.996

9.  Dynamics of sleep spindles and coupling to slow oscillations following motor learning in adult mice.

Authors:  Korey Kam; Ward D Pettibone; Kaitlyn Shim; Rebecca K Chen; Andrew W Varga
Journal:  Neurobiol Learn Mem       Date:  2019-10-14       Impact factor: 2.877

10.  Memory instability as a gateway to generalization.

Authors:  Edwin M Robertson
Journal:  PLoS Biol       Date:  2018-03-19       Impact factor: 8.029

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