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Motor planning brings human primary somatosensory cortex into action-specific preparatory states

Motor planning plays a critical role in producing fast and accurate movement. Yet, the neural processes that occur in human primary motor and somatosensory cortex during planning, and how they relate to those during movement execution, remain poorly understood. Here, we used 7T functional magnetic r...

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Detalles Bibliográficos
Autores principales: Ariani, Giacomo, Pruszynski, J Andrew, Diedrichsen, Jörn
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8786310/
https://www.ncbi.nlm.nih.gov/pubmed/35018886
http://dx.doi.org/10.7554/eLife.69517
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author Ariani, Giacomo
Pruszynski, J Andrew
Diedrichsen, Jörn
author_facet Ariani, Giacomo
Pruszynski, J Andrew
Diedrichsen, Jörn
author_sort Ariani, Giacomo
collection PubMed
description Motor planning plays a critical role in producing fast and accurate movement. Yet, the neural processes that occur in human primary motor and somatosensory cortex during planning, and how they relate to those during movement execution, remain poorly understood. Here, we used 7T functional magnetic resonance imaging and a delayed movement paradigm to study single finger movement planning and execution. The inclusion of no-go trials and variable delays allowed us to separate what are typically overlapping planning and execution brain responses. Although our univariate results show widespread deactivation during finger planning, multivariate pattern analysis revealed finger-specific activity patterns in contralateral primary somatosensory cortex (S1), which predicted the planned finger action. Surprisingly, these activity patterns were as informative as those found in contralateral primary motor cortex (M1). Control analyses ruled out the possibility that the detected information was an artifact of subthreshold movements during the preparatory delay. Furthermore, we observed that finger-specific activity patterns during planning were highly correlated to those during execution. These findings reveal that motor planning activates the specific S1 and M1 circuits that are engaged during the execution of a finger press, while activity in both regions is overall suppressed. We propose that preparatory states in S1 may improve movement control through changes in sensory processing or via direct influence of spinal motor neurons.
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spelling pubmed-87863102022-01-26 Motor planning brings human primary somatosensory cortex into action-specific preparatory states Ariani, Giacomo Pruszynski, J Andrew Diedrichsen, Jörn eLife Neuroscience Motor planning plays a critical role in producing fast and accurate movement. Yet, the neural processes that occur in human primary motor and somatosensory cortex during planning, and how they relate to those during movement execution, remain poorly understood. Here, we used 7T functional magnetic resonance imaging and a delayed movement paradigm to study single finger movement planning and execution. The inclusion of no-go trials and variable delays allowed us to separate what are typically overlapping planning and execution brain responses. Although our univariate results show widespread deactivation during finger planning, multivariate pattern analysis revealed finger-specific activity patterns in contralateral primary somatosensory cortex (S1), which predicted the planned finger action. Surprisingly, these activity patterns were as informative as those found in contralateral primary motor cortex (M1). Control analyses ruled out the possibility that the detected information was an artifact of subthreshold movements during the preparatory delay. Furthermore, we observed that finger-specific activity patterns during planning were highly correlated to those during execution. These findings reveal that motor planning activates the specific S1 and M1 circuits that are engaged during the execution of a finger press, while activity in both regions is overall suppressed. We propose that preparatory states in S1 may improve movement control through changes in sensory processing or via direct influence of spinal motor neurons. eLife Sciences Publications, Ltd 2022-01-12 /pmc/articles/PMC8786310/ /pubmed/35018886 http://dx.doi.org/10.7554/eLife.69517 Text en © 2022, Ariani et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Ariani, Giacomo
Pruszynski, J Andrew
Diedrichsen, Jörn
Motor planning brings human primary somatosensory cortex into action-specific preparatory states
title Motor planning brings human primary somatosensory cortex into action-specific preparatory states
title_full Motor planning brings human primary somatosensory cortex into action-specific preparatory states
title_fullStr Motor planning brings human primary somatosensory cortex into action-specific preparatory states
title_full_unstemmed Motor planning brings human primary somatosensory cortex into action-specific preparatory states
title_short Motor planning brings human primary somatosensory cortex into action-specific preparatory states
title_sort motor planning brings human primary somatosensory cortex into action-specific preparatory states
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8786310/
https://www.ncbi.nlm.nih.gov/pubmed/35018886
http://dx.doi.org/10.7554/eLife.69517
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