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Weaker Inter-hemispheric and Local Functional Connectivity of the Somatomotor Cortex During a Motor Skill Acquisition Is Associated With Better Learning

Recently, an increasing interest in investigating interactions between brain regions using functional connectivity (FC) methods has shifted the initial focus of cognitive neuroimaging research from localizing functional circuits based on task activation to mapping brain networks based on intrinsic F...

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Autores principales: Gabitov, Ella, Lungu, Ovidiu, Albouy, Geneviève, Doyon, Julien
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6890719/
https://www.ncbi.nlm.nih.gov/pubmed/31827459
http://dx.doi.org/10.3389/fneur.2019.01242
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author Gabitov, Ella
Lungu, Ovidiu
Albouy, Geneviève
Doyon, Julien
author_facet Gabitov, Ella
Lungu, Ovidiu
Albouy, Geneviève
Doyon, Julien
author_sort Gabitov, Ella
collection PubMed
description Recently, an increasing interest in investigating interactions between brain regions using functional connectivity (FC) methods has shifted the initial focus of cognitive neuroimaging research from localizing functional circuits based on task activation to mapping brain networks based on intrinsic FC dynamics. Leveraging the advantages of the latter approach, it has been shown that despite primarily invariant intrinsic organization of the large-scale functional networks, interactions between and within these networks significantly differ between various behavioral and cognitive states. These differences presumably indicate transient reconfiguration of functional connections—an instantaneous process that flexibly mediates and calibrates human behavior according to momentary demands of the environment. Nevertheless, the specificity of these reconfigured FC patterns to the task at hand and their relevance to adaptive processes during learning remain elusive. To address this knowledge gap, we investigated (1) to what extent FC within the somatomotor network is reconfigured during motor skill practice, and (2) how these changes are related to learning. We applied a seed-driven FC approach to data collected during a continuous task-free condition, so-called resting state, and during a motor sequence learning task using functional magnetic resonance imaging. During the task, participants repeatedly performed a short five-element sequence with their non-dominant (left) hand. As predicted, such unimanual sequence production was associated with lateralized activation of the right somatomotor cortex (SMC). Using this “active” region as a seed, here we show that unimanual performance of the motor sequence relies on functional segregation between the two SMC and selective integration between the “active” SMC and supplementary motor area. Whereas, greater segregation between the two SMC was associated with gains in performance rate, greater segregation within the “active” SMC itself was associated with more consistent performance by the end of training. Nether the resting-state FC patterns within the somatomotor network nor their relative modulation by the task state predicted these behavioral benefits of learning. Our results suggest that task-induced FC changes reflect reconfiguration of the connectivity patterns within the somatomotor network rather than a simple amplification or silencing of its intrinsic dynamics. Such reconfiguration not only supports motor behavior but may also predict learning.
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spelling pubmed-68907192019-12-11 Weaker Inter-hemispheric and Local Functional Connectivity of the Somatomotor Cortex During a Motor Skill Acquisition Is Associated With Better Learning Gabitov, Ella Lungu, Ovidiu Albouy, Geneviève Doyon, Julien Front Neurol Neurology Recently, an increasing interest in investigating interactions between brain regions using functional connectivity (FC) methods has shifted the initial focus of cognitive neuroimaging research from localizing functional circuits based on task activation to mapping brain networks based on intrinsic FC dynamics. Leveraging the advantages of the latter approach, it has been shown that despite primarily invariant intrinsic organization of the large-scale functional networks, interactions between and within these networks significantly differ between various behavioral and cognitive states. These differences presumably indicate transient reconfiguration of functional connections—an instantaneous process that flexibly mediates and calibrates human behavior according to momentary demands of the environment. Nevertheless, the specificity of these reconfigured FC patterns to the task at hand and their relevance to adaptive processes during learning remain elusive. To address this knowledge gap, we investigated (1) to what extent FC within the somatomotor network is reconfigured during motor skill practice, and (2) how these changes are related to learning. We applied a seed-driven FC approach to data collected during a continuous task-free condition, so-called resting state, and during a motor sequence learning task using functional magnetic resonance imaging. During the task, participants repeatedly performed a short five-element sequence with their non-dominant (left) hand. As predicted, such unimanual sequence production was associated with lateralized activation of the right somatomotor cortex (SMC). Using this “active” region as a seed, here we show that unimanual performance of the motor sequence relies on functional segregation between the two SMC and selective integration between the “active” SMC and supplementary motor area. Whereas, greater segregation between the two SMC was associated with gains in performance rate, greater segregation within the “active” SMC itself was associated with more consistent performance by the end of training. Nether the resting-state FC patterns within the somatomotor network nor their relative modulation by the task state predicted these behavioral benefits of learning. Our results suggest that task-induced FC changes reflect reconfiguration of the connectivity patterns within the somatomotor network rather than a simple amplification or silencing of its intrinsic dynamics. Such reconfiguration not only supports motor behavior but may also predict learning. Frontiers Media S.A. 2019-11-27 /pmc/articles/PMC6890719/ /pubmed/31827459 http://dx.doi.org/10.3389/fneur.2019.01242 Text en Copyright © 2019 Gabitov, Lungu, Albouy and Doyon. http://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 Neurology
Gabitov, Ella
Lungu, Ovidiu
Albouy, Geneviève
Doyon, Julien
Weaker Inter-hemispheric and Local Functional Connectivity of the Somatomotor Cortex During a Motor Skill Acquisition Is Associated With Better Learning
title Weaker Inter-hemispheric and Local Functional Connectivity of the Somatomotor Cortex During a Motor Skill Acquisition Is Associated With Better Learning
title_full Weaker Inter-hemispheric and Local Functional Connectivity of the Somatomotor Cortex During a Motor Skill Acquisition Is Associated With Better Learning
title_fullStr Weaker Inter-hemispheric and Local Functional Connectivity of the Somatomotor Cortex During a Motor Skill Acquisition Is Associated With Better Learning
title_full_unstemmed Weaker Inter-hemispheric and Local Functional Connectivity of the Somatomotor Cortex During a Motor Skill Acquisition Is Associated With Better Learning
title_short Weaker Inter-hemispheric and Local Functional Connectivity of the Somatomotor Cortex During a Motor Skill Acquisition Is Associated With Better Learning
title_sort weaker inter-hemispheric and local functional connectivity of the somatomotor cortex during a motor skill acquisition is associated with better learning
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6890719/
https://www.ncbi.nlm.nih.gov/pubmed/31827459
http://dx.doi.org/10.3389/fneur.2019.01242
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