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Differential Effects of a Nap on Motor Sequence Learning-Related Functional Connectivity Between Young and Older Adults

In older adults, motor sequence learning (MSL) is largely intact. However, consolidation of newly learned motor sequences is impaired compared to younger adults, and there is evidence that brain areas supporting enhanced consolidation via sleep degrade with age. It is known that brain activity in hi...

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Autores principales: Fang, Zhuo, Smith, Dylan M., Albouy, Genevieve, King, Bradley R., Vien, Catherine, Benali, Habib, Carrier, Julie, Doyon, Julien, Fogel, Stuart
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8582327/
https://www.ncbi.nlm.nih.gov/pubmed/34776932
http://dx.doi.org/10.3389/fnagi.2021.747358
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author Fang, Zhuo
Smith, Dylan M.
Albouy, Genevieve
King, Bradley R.
Vien, Catherine
Benali, Habib
Carrier, Julie
Doyon, Julien
Fogel, Stuart
author_facet Fang, Zhuo
Smith, Dylan M.
Albouy, Genevieve
King, Bradley R.
Vien, Catherine
Benali, Habib
Carrier, Julie
Doyon, Julien
Fogel, Stuart
author_sort Fang, Zhuo
collection PubMed
description In older adults, motor sequence learning (MSL) is largely intact. However, consolidation of newly learned motor sequences is impaired compared to younger adults, and there is evidence that brain areas supporting enhanced consolidation via sleep degrade with age. It is known that brain activity in hippocampal–cortical–striatal areas is important for sleep-dependent, off-line consolidation of motor-sequences. Yet, the intricacies of how both age and sleep alter communication within this network of brain areas, which facilitate consolidation, are not known. In this study, 37 young (age 20–35) and 49 older individuals (age 55–75) underwent resting state functional magnetic resonance imaging (fMRI) before and after training on a MSL task as well as after either a nap or a period of awake rest. Young participants who napped showed strengthening of functional connectivity (FC) between motor, striatal, and hippocampal areas, compared to older subjects regardless of sleep condition. Follow-up analyses revealed this effect was driven by younger participants who showed an increase in FC between striatum and motor cortices, as well as older participants who showed decreased FC between the hippocampus, striatum, and precuneus. Therefore, different effects of sleep were observed in younger vs. older participants, where young participants primarily showed increased communication in the striatal-motor areas, while older participants showed decreases in key nodes of the default mode network and striatum. Performance gains correlated with FC changes in young adults, and this association was much greater in participants who napped compared to those who stayed awake. Performance gains also correlated with FC changes in older adults, but only in those who napped. This study reveals that, while there is no evidence of time-dependent forgetting/deterioration of performance, older adults exhibit a completely different pattern of FC changes during consolidation compared to younger adults, and lose the benefit that sleep affords to memory consolidation.
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spelling pubmed-85823272021-11-12 Differential Effects of a Nap on Motor Sequence Learning-Related Functional Connectivity Between Young and Older Adults Fang, Zhuo Smith, Dylan M. Albouy, Genevieve King, Bradley R. Vien, Catherine Benali, Habib Carrier, Julie Doyon, Julien Fogel, Stuart Front Aging Neurosci Aging Neuroscience In older adults, motor sequence learning (MSL) is largely intact. However, consolidation of newly learned motor sequences is impaired compared to younger adults, and there is evidence that brain areas supporting enhanced consolidation via sleep degrade with age. It is known that brain activity in hippocampal–cortical–striatal areas is important for sleep-dependent, off-line consolidation of motor-sequences. Yet, the intricacies of how both age and sleep alter communication within this network of brain areas, which facilitate consolidation, are not known. In this study, 37 young (age 20–35) and 49 older individuals (age 55–75) underwent resting state functional magnetic resonance imaging (fMRI) before and after training on a MSL task as well as after either a nap or a period of awake rest. Young participants who napped showed strengthening of functional connectivity (FC) between motor, striatal, and hippocampal areas, compared to older subjects regardless of sleep condition. Follow-up analyses revealed this effect was driven by younger participants who showed an increase in FC between striatum and motor cortices, as well as older participants who showed decreased FC between the hippocampus, striatum, and precuneus. Therefore, different effects of sleep were observed in younger vs. older participants, where young participants primarily showed increased communication in the striatal-motor areas, while older participants showed decreases in key nodes of the default mode network and striatum. Performance gains correlated with FC changes in young adults, and this association was much greater in participants who napped compared to those who stayed awake. Performance gains also correlated with FC changes in older adults, but only in those who napped. This study reveals that, while there is no evidence of time-dependent forgetting/deterioration of performance, older adults exhibit a completely different pattern of FC changes during consolidation compared to younger adults, and lose the benefit that sleep affords to memory consolidation. Frontiers Media S.A. 2021-10-28 /pmc/articles/PMC8582327/ /pubmed/34776932 http://dx.doi.org/10.3389/fnagi.2021.747358 Text en Copyright © 2021 Fang, Smith, Albouy, King, Vien, Benali, Carrier, Doyon and Fogel. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Aging Neuroscience
Fang, Zhuo
Smith, Dylan M.
Albouy, Genevieve
King, Bradley R.
Vien, Catherine
Benali, Habib
Carrier, Julie
Doyon, Julien
Fogel, Stuart
Differential Effects of a Nap on Motor Sequence Learning-Related Functional Connectivity Between Young and Older Adults
title Differential Effects of a Nap on Motor Sequence Learning-Related Functional Connectivity Between Young and Older Adults
title_full Differential Effects of a Nap on Motor Sequence Learning-Related Functional Connectivity Between Young and Older Adults
title_fullStr Differential Effects of a Nap on Motor Sequence Learning-Related Functional Connectivity Between Young and Older Adults
title_full_unstemmed Differential Effects of a Nap on Motor Sequence Learning-Related Functional Connectivity Between Young and Older Adults
title_short Differential Effects of a Nap on Motor Sequence Learning-Related Functional Connectivity Between Young and Older Adults
title_sort differential effects of a nap on motor sequence learning-related functional connectivity between young and older adults
topic Aging Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8582327/
https://www.ncbi.nlm.nih.gov/pubmed/34776932
http://dx.doi.org/10.3389/fnagi.2021.747358
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