The value of corticospinal excitability and intracortical inhibition in predicting motor skill improvement driven by action observation

The observation of other's actions represents an essential element for the acquisition of motor skills. While action observation is known to induce changes in the excitability of the motor cortices, whether such modulations may explain the amount of motor improvement driven by action observatio...

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Main Authors: Arturo Nuara, Maria Chiara Bazzini, Pasquale Cardellicchio, Emilia Scalona, Doriana De Marco, Giacomo Rizzolatti, Maddalena Fabbri-Destro, Pietro Avanzini
Format: Article
Language:English
Published: Elsevier 2023-02-01
Series:NeuroImage
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Online Access:http://www.sciencedirect.com/science/article/pii/S1053811922009466
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author Arturo Nuara
Maria Chiara Bazzini
Pasquale Cardellicchio
Emilia Scalona
Doriana De Marco
Giacomo Rizzolatti
Maddalena Fabbri-Destro
Pietro Avanzini
author_facet Arturo Nuara
Maria Chiara Bazzini
Pasquale Cardellicchio
Emilia Scalona
Doriana De Marco
Giacomo Rizzolatti
Maddalena Fabbri-Destro
Pietro Avanzini
author_sort Arturo Nuara
collection DOAJ
description The observation of other's actions represents an essential element for the acquisition of motor skills. While action observation is known to induce changes in the excitability of the motor cortices, whether such modulations may explain the amount of motor improvement driven by action observation training (AOT) remains to be addressed. Using transcranial magnetic stimulation (TMS), we first assessed in 41 volunteers the effect of action observation on corticospinal excitability, intracortical inhibition, and transcallosal inhibition. Subsequently, half of the participants (AOT-group) were asked to observe and then execute a right-hand dexterity task, while the controls had to observe a no-action video before practicing the same task. AOT participants showed greater performance improvement relative to controls. More importantly, the amount of improvement in the AOT group was predicted by the amplitude of corticospinal modulation during action observation and, even more, by the amount of intracortical inhibition induced by action observation. These relations were specific for the AOT group, while the same patterns were not found in controls. Taken together, our findings demonstrate that the efficacy of AOT in promoting motor learning is rooted in the capacity of action observation to modulate the trainee's motor system excitability, especially its intracortical inhibition. Our study not only enriches the picture of the neurophysiological effects induced by action observation onto the observer's motor excitability, but linking them to the efficacy of AOT, it also paves the way for the development of models predicting the outcome of training procedures based on the observation of other's actions.
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spelling doaj.art-29196576c19c4f158d6d83a5f5d70b6d2023-01-05T04:31:25ZengElsevierNeuroImage1095-95722023-02-01266119825The value of corticospinal excitability and intracortical inhibition in predicting motor skill improvement driven by action observationArturo Nuara0Maria Chiara Bazzini1Pasquale Cardellicchio2Emilia Scalona3Doriana De Marco4Giacomo Rizzolatti5Maddalena Fabbri-Destro6Pietro Avanzini7CNR Neuroscience Institute, via Volturno 39/E, Parma 43125, Italy; Corresponding author.Department of Medicine, University of Parma, ItalyIIT@UniFe Center for Translational Neurophysiology, Istituto Italiano di Tecnologia, Ferrara, ItalyCNR Neuroscience Institute, via Volturno 39/E, Parma 43125, Italy; Specialità Medico-Chirurgiche, Scienze Radiologiche e Sanità Pubblica (DSMC), Università degli studi di Brescia, ItaliaCNR Neuroscience Institute, via Volturno 39/E, Parma 43125, ItalyCNR Neuroscience Institute, via Volturno 39/E, Parma 43125, ItalyCNR Neuroscience Institute, via Volturno 39/E, Parma 43125, ItalyCNR Neuroscience Institute, via Volturno 39/E, Parma 43125, Italy; Istituto Clinico Humanitas, Humanitas Clinical and Research Center, Milan, Rozzano, ItalyThe observation of other's actions represents an essential element for the acquisition of motor skills. While action observation is known to induce changes in the excitability of the motor cortices, whether such modulations may explain the amount of motor improvement driven by action observation training (AOT) remains to be addressed. Using transcranial magnetic stimulation (TMS), we first assessed in 41 volunteers the effect of action observation on corticospinal excitability, intracortical inhibition, and transcallosal inhibition. Subsequently, half of the participants (AOT-group) were asked to observe and then execute a right-hand dexterity task, while the controls had to observe a no-action video before practicing the same task. AOT participants showed greater performance improvement relative to controls. More importantly, the amount of improvement in the AOT group was predicted by the amplitude of corticospinal modulation during action observation and, even more, by the amount of intracortical inhibition induced by action observation. These relations were specific for the AOT group, while the same patterns were not found in controls. Taken together, our findings demonstrate that the efficacy of AOT in promoting motor learning is rooted in the capacity of action observation to modulate the trainee's motor system excitability, especially its intracortical inhibition. Our study not only enriches the picture of the neurophysiological effects induced by action observation onto the observer's motor excitability, but linking them to the efficacy of AOT, it also paves the way for the development of models predicting the outcome of training procedures based on the observation of other's actions.http://www.sciencedirect.com/science/article/pii/S1053811922009466Transcranial magnetic stimulationAction observation treatmentMirror mechanismMirror neuron systemintracortical inhibition
spellingShingle Arturo Nuara
Maria Chiara Bazzini
Pasquale Cardellicchio
Emilia Scalona
Doriana De Marco
Giacomo Rizzolatti
Maddalena Fabbri-Destro
Pietro Avanzini
The value of corticospinal excitability and intracortical inhibition in predicting motor skill improvement driven by action observation
NeuroImage
Transcranial magnetic stimulation
Action observation treatment
Mirror mechanism
Mirror neuron system
intracortical inhibition
title The value of corticospinal excitability and intracortical inhibition in predicting motor skill improvement driven by action observation
title_full The value of corticospinal excitability and intracortical inhibition in predicting motor skill improvement driven by action observation
title_fullStr The value of corticospinal excitability and intracortical inhibition in predicting motor skill improvement driven by action observation
title_full_unstemmed The value of corticospinal excitability and intracortical inhibition in predicting motor skill improvement driven by action observation
title_short The value of corticospinal excitability and intracortical inhibition in predicting motor skill improvement driven by action observation
title_sort value of corticospinal excitability and intracortical inhibition in predicting motor skill improvement driven by action observation
topic Transcranial magnetic stimulation
Action observation treatment
Mirror mechanism
Mirror neuron system
intracortical inhibition
url http://www.sciencedirect.com/science/article/pii/S1053811922009466
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