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Fast Hand Movements Unveil Multifractal Roots of Adaptation in the Visuomotor Cognitive System

Beyond apparent simplicity, visuomotor dexterity actually requires the coordination of multiple interactions across a complex system that links the brain, the body and the environment. Recent research suggests that a better understanding of how perceptive, cognitive and motor activities cohere to fo...

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Autores principales: Pratviel, Yvan, Deschodt-Arsac, Veronique, Larrue, Florian, Arsac, Laurent M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8330832/
https://www.ncbi.nlm.nih.gov/pubmed/34354603
http://dx.doi.org/10.3389/fphys.2021.713076
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author Pratviel, Yvan
Deschodt-Arsac, Veronique
Larrue, Florian
Arsac, Laurent M.
author_facet Pratviel, Yvan
Deschodt-Arsac, Veronique
Larrue, Florian
Arsac, Laurent M.
author_sort Pratviel, Yvan
collection PubMed
description Beyond apparent simplicity, visuomotor dexterity actually requires the coordination of multiple interactions across a complex system that links the brain, the body and the environment. Recent research suggests that a better understanding of how perceptive, cognitive and motor activities cohere to form executive control could be gained from multifractal formalisms applied to movement behavior. Rather than a central executive “talking” to encapsuled components, the multifractal intuition suggests that eye-hand coordination arises from multiplicative cascade dynamics across temporal scales of activity within the whole system, which is reflected in movement time series. Here we examined hand movements of sport students performing a visuomotor task in virtual reality (VR). The task involved hitting spatially arranged targets that lit up on a virtual board under critical time pressure. Three conditions were compared where the visual search field changed: whole board (Standard), half-board lower view field (LVF) and upper view field (UVF). Densely sampled (90 Hz) time series of hand motions captured by VR controllers were analyzed by a focus-based multifractal detrended fluctuation analysis (DFA). Multiplicative rather than additive interactions across temporal scales were evidenced by testing comparatively phase-randomized surrogates of experimental series, which confirmed nonlinear processes. As main results, it was demonstrated that: (i) the degree of multifractality in hand motion behavior was minimal in LVF, a familiar visual search field where subjects correlatively reached their best visuomotor response times (RTs); (ii) multifractality increased in the less familiar UVF, but interestingly only for the non-dominant hand; and (iii) multifractality increased further in Standard, for both hands indifferently; in Standard, the maximal expansion of the visual search field imposed the highest demand as evidenced by the worst visuomotor RTs. Our observations advocate for visuomotor dexterity best described by multiplicative cascades dynamics and a system-wide distributed control rather than a central executive. More importantly, multifractal metrics obtained from hand movements behavior, beyond the confines of the brain, offer a window on the fine organization of control architecture, with high sensitivity to hand-related control behavior under specific constraints. Appealing applications may be found in movement learning/rehabilitation, e.g., in hemineglect people, stroke patients, maturing children or athletes.
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spelling pubmed-83308322021-08-04 Fast Hand Movements Unveil Multifractal Roots of Adaptation in the Visuomotor Cognitive System Pratviel, Yvan Deschodt-Arsac, Veronique Larrue, Florian Arsac, Laurent M. Front Physiol Physiology Beyond apparent simplicity, visuomotor dexterity actually requires the coordination of multiple interactions across a complex system that links the brain, the body and the environment. Recent research suggests that a better understanding of how perceptive, cognitive and motor activities cohere to form executive control could be gained from multifractal formalisms applied to movement behavior. Rather than a central executive “talking” to encapsuled components, the multifractal intuition suggests that eye-hand coordination arises from multiplicative cascade dynamics across temporal scales of activity within the whole system, which is reflected in movement time series. Here we examined hand movements of sport students performing a visuomotor task in virtual reality (VR). The task involved hitting spatially arranged targets that lit up on a virtual board under critical time pressure. Three conditions were compared where the visual search field changed: whole board (Standard), half-board lower view field (LVF) and upper view field (UVF). Densely sampled (90 Hz) time series of hand motions captured by VR controllers were analyzed by a focus-based multifractal detrended fluctuation analysis (DFA). Multiplicative rather than additive interactions across temporal scales were evidenced by testing comparatively phase-randomized surrogates of experimental series, which confirmed nonlinear processes. As main results, it was demonstrated that: (i) the degree of multifractality in hand motion behavior was minimal in LVF, a familiar visual search field where subjects correlatively reached their best visuomotor response times (RTs); (ii) multifractality increased in the less familiar UVF, but interestingly only for the non-dominant hand; and (iii) multifractality increased further in Standard, for both hands indifferently; in Standard, the maximal expansion of the visual search field imposed the highest demand as evidenced by the worst visuomotor RTs. Our observations advocate for visuomotor dexterity best described by multiplicative cascades dynamics and a system-wide distributed control rather than a central executive. More importantly, multifractal metrics obtained from hand movements behavior, beyond the confines of the brain, offer a window on the fine organization of control architecture, with high sensitivity to hand-related control behavior under specific constraints. Appealing applications may be found in movement learning/rehabilitation, e.g., in hemineglect people, stroke patients, maturing children or athletes. Frontiers Media S.A. 2021-07-20 /pmc/articles/PMC8330832/ /pubmed/34354603 http://dx.doi.org/10.3389/fphys.2021.713076 Text en Copyright © 2021 Pratviel, Deschodt-Arsac, Larrue and Arsac. 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 Physiology
Pratviel, Yvan
Deschodt-Arsac, Veronique
Larrue, Florian
Arsac, Laurent M.
Fast Hand Movements Unveil Multifractal Roots of Adaptation in the Visuomotor Cognitive System
title Fast Hand Movements Unveil Multifractal Roots of Adaptation in the Visuomotor Cognitive System
title_full Fast Hand Movements Unveil Multifractal Roots of Adaptation in the Visuomotor Cognitive System
title_fullStr Fast Hand Movements Unveil Multifractal Roots of Adaptation in the Visuomotor Cognitive System
title_full_unstemmed Fast Hand Movements Unveil Multifractal Roots of Adaptation in the Visuomotor Cognitive System
title_short Fast Hand Movements Unveil Multifractal Roots of Adaptation in the Visuomotor Cognitive System
title_sort fast hand movements unveil multifractal roots of adaptation in the visuomotor cognitive system
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8330832/
https://www.ncbi.nlm.nih.gov/pubmed/34354603
http://dx.doi.org/10.3389/fphys.2021.713076
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