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When Corticospinal Inhibition Favors an Efficient Motor Response

SIMPLE SUMMARY: Scientific evidence has demonstrated that in social contexts the motor system integrates predictions about the actions of others and plans the most appropriate responses. However, it is not yet known how these processes are reflected in the modulation of excitatory and inhibitory cor...

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Autores principales: Betti, Sonia, Zani, Giovanni, Guerra, Silvia, Granziol, Umberto, Castiello, Umberto, Begliomini, Chiara, Sartori, Luisa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9953307/
https://www.ncbi.nlm.nih.gov/pubmed/36829607
http://dx.doi.org/10.3390/biology12020332
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author Betti, Sonia
Zani, Giovanni
Guerra, Silvia
Granziol, Umberto
Castiello, Umberto
Begliomini, Chiara
Sartori, Luisa
author_facet Betti, Sonia
Zani, Giovanni
Guerra, Silvia
Granziol, Umberto
Castiello, Umberto
Begliomini, Chiara
Sartori, Luisa
author_sort Betti, Sonia
collection PubMed
description SIMPLE SUMMARY: Scientific evidence has demonstrated that in social contexts the motor system integrates predictions about the actions of others and plans the most appropriate responses. However, it is not yet known how these processes are reflected in the modulation of excitatory and inhibitory corticospinal mechanisms. Our goal was to reveal the behavioral and neurophysiological signatures characterizing different stages of these motor responses. Greater corticospinal inhibition was found when participants prepared their motor response after observing an interactive request compared with a non-interactive gesture, and this in turn favored a faster and more efficient execution of the action. With this neural finding, we shed light on the critical intermediate phase of motor processing between the observation of the action and the action integration phase aimed at achieving a joint goal. Taken together, these results will contribute to the understanding of motor processes that occur in social situations such as those we routinely encounter in our daily lives. ABSTRACT: Many daily activities involve responding to the actions of other people. However, the functional relationship between the motor preparation and execution phases still needs to be clarified. With the combination of different and complementary experimental techniques (i.e., motor excitability measures, reaction times, electromyography, and dyadic 3-D kinematics), we investigated the behavioral and neurophysiological signatures characterizing different stages of a motor response in contexts calling for an interactive action. Participants were requested to perform an action (i.e., stirring coffee or lifting a coffee cup) following a co-experimenter’s request gesture. Another condition, in which a non-interactive gesture was used, was also included. Greater corticospinal inhibition was found when participants prepared their motor response after observing an interactive request, compared to a non-interactive gesture. This, in turn, was associated with faster and more efficient action execution in kinematic terms (i.e., a social motor priming effect). Our results provide new insights on the inhibitory and facilitatory drives guiding social motor response generation. Altogether, the integration of behavioral and neurophysiological indexes allowed us to demonstrate that a more efficient action execution followed a greater corticospinal inhibition. These indexes provide a full picture of motor activity at both planning and execution stages.
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spelling pubmed-99533072023-02-25 When Corticospinal Inhibition Favors an Efficient Motor Response Betti, Sonia Zani, Giovanni Guerra, Silvia Granziol, Umberto Castiello, Umberto Begliomini, Chiara Sartori, Luisa Biology (Basel) Article SIMPLE SUMMARY: Scientific evidence has demonstrated that in social contexts the motor system integrates predictions about the actions of others and plans the most appropriate responses. However, it is not yet known how these processes are reflected in the modulation of excitatory and inhibitory corticospinal mechanisms. Our goal was to reveal the behavioral and neurophysiological signatures characterizing different stages of these motor responses. Greater corticospinal inhibition was found when participants prepared their motor response after observing an interactive request compared with a non-interactive gesture, and this in turn favored a faster and more efficient execution of the action. With this neural finding, we shed light on the critical intermediate phase of motor processing between the observation of the action and the action integration phase aimed at achieving a joint goal. Taken together, these results will contribute to the understanding of motor processes that occur in social situations such as those we routinely encounter in our daily lives. ABSTRACT: Many daily activities involve responding to the actions of other people. However, the functional relationship between the motor preparation and execution phases still needs to be clarified. With the combination of different and complementary experimental techniques (i.e., motor excitability measures, reaction times, electromyography, and dyadic 3-D kinematics), we investigated the behavioral and neurophysiological signatures characterizing different stages of a motor response in contexts calling for an interactive action. Participants were requested to perform an action (i.e., stirring coffee or lifting a coffee cup) following a co-experimenter’s request gesture. Another condition, in which a non-interactive gesture was used, was also included. Greater corticospinal inhibition was found when participants prepared their motor response after observing an interactive request, compared to a non-interactive gesture. This, in turn, was associated with faster and more efficient action execution in kinematic terms (i.e., a social motor priming effect). Our results provide new insights on the inhibitory and facilitatory drives guiding social motor response generation. Altogether, the integration of behavioral and neurophysiological indexes allowed us to demonstrate that a more efficient action execution followed a greater corticospinal inhibition. These indexes provide a full picture of motor activity at both planning and execution stages. MDPI 2023-02-20 /pmc/articles/PMC9953307/ /pubmed/36829607 http://dx.doi.org/10.3390/biology12020332 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Betti, Sonia
Zani, Giovanni
Guerra, Silvia
Granziol, Umberto
Castiello, Umberto
Begliomini, Chiara
Sartori, Luisa
When Corticospinal Inhibition Favors an Efficient Motor Response
title When Corticospinal Inhibition Favors an Efficient Motor Response
title_full When Corticospinal Inhibition Favors an Efficient Motor Response
title_fullStr When Corticospinal Inhibition Favors an Efficient Motor Response
title_full_unstemmed When Corticospinal Inhibition Favors an Efficient Motor Response
title_short When Corticospinal Inhibition Favors an Efficient Motor Response
title_sort when corticospinal inhibition favors an efficient motor response
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9953307/
https://www.ncbi.nlm.nih.gov/pubmed/36829607
http://dx.doi.org/10.3390/biology12020332
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