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Disruption of Boundary Encoding During Sensorimotor Sequence Learning: An MEG Study

Music performance relies on the ability to learn and execute actions and their associated sounds. The process of learning these auditory-motor contingencies depends on the proper encoding of the serial order of the actions and sounds. Among the different serial positions of a behavioral sequence, th...

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Autores principales: Michail, Georgios, Nikulin, Vadim V., Curio, Gabriel, Maess, Burkhard, Herrojo Ruiz, María
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6005865/
https://www.ncbi.nlm.nih.gov/pubmed/29946246
http://dx.doi.org/10.3389/fnhum.2018.00240
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author Michail, Georgios
Nikulin, Vadim V.
Curio, Gabriel
Maess, Burkhard
Herrojo Ruiz, María
author_facet Michail, Georgios
Nikulin, Vadim V.
Curio, Gabriel
Maess, Burkhard
Herrojo Ruiz, María
author_sort Michail, Georgios
collection PubMed
description Music performance relies on the ability to learn and execute actions and their associated sounds. The process of learning these auditory-motor contingencies depends on the proper encoding of the serial order of the actions and sounds. Among the different serial positions of a behavioral sequence, the first and last (boundary) elements are particularly relevant. Animal and patient studies have demonstrated a specific neural representation for boundary elements in prefrontal cortical regions and in the basal ganglia, highlighting the relevance of their proper encoding. The neural mechanisms underlying the encoding of sequence boundaries in the general human population remain, however, largely unknown. In this study, we examined how alterations of auditory feedback, introduced at different ordinal positions (boundary or within-sequence element), affect the neural and behavioral responses during sensorimotor sequence learning. Analysing the neuromagnetic signals from 20 participants while they performed short piano sequences under the occasional effect of altered feedback (AF), we found that at around 150–200 ms post-keystroke, the neural activities in the dorsolateral prefrontal cortex (DLPFC) and supplementary motor area (SMA) were dissociated for boundary and within-sequence elements. Furthermore, the behavioral data demonstrated that feedback alterations on boundaries led to greater performance costs, such as more errors in the subsequent keystrokes. These findings jointly support the idea that the proper encoding of boundaries is critical in acquiring sensorimotor sequences. They also provide evidence for the involvement of a distinct neural circuitry in humans including prefrontal and higher-order motor areas during the encoding of the different classes of serial order.
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spelling pubmed-60058652018-06-26 Disruption of Boundary Encoding During Sensorimotor Sequence Learning: An MEG Study Michail, Georgios Nikulin, Vadim V. Curio, Gabriel Maess, Burkhard Herrojo Ruiz, María Front Hum Neurosci Neuroscience Music performance relies on the ability to learn and execute actions and their associated sounds. The process of learning these auditory-motor contingencies depends on the proper encoding of the serial order of the actions and sounds. Among the different serial positions of a behavioral sequence, the first and last (boundary) elements are particularly relevant. Animal and patient studies have demonstrated a specific neural representation for boundary elements in prefrontal cortical regions and in the basal ganglia, highlighting the relevance of their proper encoding. The neural mechanisms underlying the encoding of sequence boundaries in the general human population remain, however, largely unknown. In this study, we examined how alterations of auditory feedback, introduced at different ordinal positions (boundary or within-sequence element), affect the neural and behavioral responses during sensorimotor sequence learning. Analysing the neuromagnetic signals from 20 participants while they performed short piano sequences under the occasional effect of altered feedback (AF), we found that at around 150–200 ms post-keystroke, the neural activities in the dorsolateral prefrontal cortex (DLPFC) and supplementary motor area (SMA) were dissociated for boundary and within-sequence elements. Furthermore, the behavioral data demonstrated that feedback alterations on boundaries led to greater performance costs, such as more errors in the subsequent keystrokes. These findings jointly support the idea that the proper encoding of boundaries is critical in acquiring sensorimotor sequences. They also provide evidence for the involvement of a distinct neural circuitry in humans including prefrontal and higher-order motor areas during the encoding of the different classes of serial order. Frontiers Media S.A. 2018-06-12 /pmc/articles/PMC6005865/ /pubmed/29946246 http://dx.doi.org/10.3389/fnhum.2018.00240 Text en Copyright © 2018 Michail, Nikulin, Curio, Maess and Herrojo Ruiz. 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 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 Neuroscience
Michail, Georgios
Nikulin, Vadim V.
Curio, Gabriel
Maess, Burkhard
Herrojo Ruiz, María
Disruption of Boundary Encoding During Sensorimotor Sequence Learning: An MEG Study
title Disruption of Boundary Encoding During Sensorimotor Sequence Learning: An MEG Study
title_full Disruption of Boundary Encoding During Sensorimotor Sequence Learning: An MEG Study
title_fullStr Disruption of Boundary Encoding During Sensorimotor Sequence Learning: An MEG Study
title_full_unstemmed Disruption of Boundary Encoding During Sensorimotor Sequence Learning: An MEG Study
title_short Disruption of Boundary Encoding During Sensorimotor Sequence Learning: An MEG Study
title_sort disruption of boundary encoding during sensorimotor sequence learning: an meg study
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6005865/
https://www.ncbi.nlm.nih.gov/pubmed/29946246
http://dx.doi.org/10.3389/fnhum.2018.00240
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