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A neural signature for combined action observation and motor imagery? An fNIRS study into prefrontal activation, automatic imitation, and self–other perceptions

INTRODUCTION: Research indicates that both observed and imagined actions can be represented in the brain as two parallel sensorimotor representations. One proposal is that higher order cognitive processes would align these two hypothetical action simulations. METHODS: We investigated this hypothesis...

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Autores principales: Emerson, Jonathan R., Scott, Matthew W., van Schaik, Paul, Butcher, Natalie, Kenny, Ryan P. W., Eaves, Daniel L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8865155/
https://www.ncbi.nlm.nih.gov/pubmed/34994997
http://dx.doi.org/10.1002/brb3.2407
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author Emerson, Jonathan R.
Scott, Matthew W.
van Schaik, Paul
Butcher, Natalie
Kenny, Ryan P. W.
Eaves, Daniel L.
author_facet Emerson, Jonathan R.
Scott, Matthew W.
van Schaik, Paul
Butcher, Natalie
Kenny, Ryan P. W.
Eaves, Daniel L.
author_sort Emerson, Jonathan R.
collection PubMed
description INTRODUCTION: Research indicates that both observed and imagined actions can be represented in the brain as two parallel sensorimotor representations. One proposal is that higher order cognitive processes would align these two hypothetical action simulations. METHODS: We investigated this hypothesis using an automatic imitation paradigm, with functional near‐infrared spectroscopy recordings over the prefrontal cortex during different motor simulation states. On each trial, participants (n = 14) observed a picture of a rhythmical action (instructed action) followed by a distractor movie showing the same or different action. Participants then executed the instructed action. Distractor actions were manipulated to be fast or slow, and instructions were manipulated during distractor presentation: action observation (AO), combined action observation and motor imagery (AO+MI) and observe to imitate (intentional imitation). A pure motor imagery (MI) condition was also included. RESULTS: Kinematic analyses showed that although distractor speed effects were significant under all instructions (shorter mean cycle times in execution for fast compared to slow trials), this imitation bias was significantly stronger for combined AO+MI than both AO and MI, and stronger for intentional imitation than the other three automatic imitation conditions. In the left prefrontal cortex, cerebral oxygenation was significantly greater for combined AO+MI than all other instructions. Participants reported that their representation of the self overlapped with the observed model significantly more during AO+MI than AO. CONCLUSION: Left prefrontal activation may therefore be a neural signature of AO+MI, supporting attentional switching between concurrent representations of self (MI, top‐down) and other (AO, bottom‐up) to increase imitation and perceived closeness.
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spelling pubmed-88651552022-02-27 A neural signature for combined action observation and motor imagery? An fNIRS study into prefrontal activation, automatic imitation, and self–other perceptions Emerson, Jonathan R. Scott, Matthew W. van Schaik, Paul Butcher, Natalie Kenny, Ryan P. W. Eaves, Daniel L. Brain Behav Original Articles INTRODUCTION: Research indicates that both observed and imagined actions can be represented in the brain as two parallel sensorimotor representations. One proposal is that higher order cognitive processes would align these two hypothetical action simulations. METHODS: We investigated this hypothesis using an automatic imitation paradigm, with functional near‐infrared spectroscopy recordings over the prefrontal cortex during different motor simulation states. On each trial, participants (n = 14) observed a picture of a rhythmical action (instructed action) followed by a distractor movie showing the same or different action. Participants then executed the instructed action. Distractor actions were manipulated to be fast or slow, and instructions were manipulated during distractor presentation: action observation (AO), combined action observation and motor imagery (AO+MI) and observe to imitate (intentional imitation). A pure motor imagery (MI) condition was also included. RESULTS: Kinematic analyses showed that although distractor speed effects were significant under all instructions (shorter mean cycle times in execution for fast compared to slow trials), this imitation bias was significantly stronger for combined AO+MI than both AO and MI, and stronger for intentional imitation than the other three automatic imitation conditions. In the left prefrontal cortex, cerebral oxygenation was significantly greater for combined AO+MI than all other instructions. Participants reported that their representation of the self overlapped with the observed model significantly more during AO+MI than AO. CONCLUSION: Left prefrontal activation may therefore be a neural signature of AO+MI, supporting attentional switching between concurrent representations of self (MI, top‐down) and other (AO, bottom‐up) to increase imitation and perceived closeness. John Wiley and Sons Inc. 2022-01-07 /pmc/articles/PMC8865155/ /pubmed/34994997 http://dx.doi.org/10.1002/brb3.2407 Text en © 2021 The Authors. Brain and Behavior published by Wiley Periodicals LLC https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Emerson, Jonathan R.
Scott, Matthew W.
van Schaik, Paul
Butcher, Natalie
Kenny, Ryan P. W.
Eaves, Daniel L.
A neural signature for combined action observation and motor imagery? An fNIRS study into prefrontal activation, automatic imitation, and self–other perceptions
title A neural signature for combined action observation and motor imagery? An fNIRS study into prefrontal activation, automatic imitation, and self–other perceptions
title_full A neural signature for combined action observation and motor imagery? An fNIRS study into prefrontal activation, automatic imitation, and self–other perceptions
title_fullStr A neural signature for combined action observation and motor imagery? An fNIRS study into prefrontal activation, automatic imitation, and self–other perceptions
title_full_unstemmed A neural signature for combined action observation and motor imagery? An fNIRS study into prefrontal activation, automatic imitation, and self–other perceptions
title_short A neural signature for combined action observation and motor imagery? An fNIRS study into prefrontal activation, automatic imitation, and self–other perceptions
title_sort neural signature for combined action observation and motor imagery? an fnirs study into prefrontal activation, automatic imitation, and self–other perceptions
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8865155/
https://www.ncbi.nlm.nih.gov/pubmed/34994997
http://dx.doi.org/10.1002/brb3.2407
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