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Watch, Imagine, Attempt: Motor Cortex Single-Unit Activity Reveals Context-Dependent Movement Encoding in Humans With Tetraplegia

Planning and performing volitional movement engages widespread networks in the human brain, with motor cortex considered critical to the performance of skilled limb actions. Motor cortex is also engaged when actions are observed or imagined, but the manner in which ensembles of neurons represent the...

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Autores principales: Vargas-Irwin, Carlos E., Feldman, Jessica M., King, Brandon, Simeral, John D., Sorice, Brittany L., Oakley, Erin M., Cash, Sydney S., Eskandar, Emad N., Friehs, Gerhard M., Hochberg, Leigh R., Donoghue, John P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6262367/
https://www.ncbi.nlm.nih.gov/pubmed/30524258
http://dx.doi.org/10.3389/fnhum.2018.00450
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author Vargas-Irwin, Carlos E.
Feldman, Jessica M.
King, Brandon
Simeral, John D.
Sorice, Brittany L.
Oakley, Erin M.
Cash, Sydney S.
Eskandar, Emad N.
Friehs, Gerhard M.
Hochberg, Leigh R.
Donoghue, John P.
author_facet Vargas-Irwin, Carlos E.
Feldman, Jessica M.
King, Brandon
Simeral, John D.
Sorice, Brittany L.
Oakley, Erin M.
Cash, Sydney S.
Eskandar, Emad N.
Friehs, Gerhard M.
Hochberg, Leigh R.
Donoghue, John P.
author_sort Vargas-Irwin, Carlos E.
collection PubMed
description Planning and performing volitional movement engages widespread networks in the human brain, with motor cortex considered critical to the performance of skilled limb actions. Motor cortex is also engaged when actions are observed or imagined, but the manner in which ensembles of neurons represent these volitional states (VoSs) is unknown. Here we provide direct demonstration that observing, imagining or attempting action activates shared neural ensembles in human motor cortex. Two individuals with tetraplegia (due to brainstem stroke or amyotrophic lateral sclerosis, ALS) were verbally instructed to watch, imagine, or attempt reaching actions displayed on a computer screen. Neural activity in the precentral gyrus incorporated information about both cognitive state and movement kinematics; the three conditions presented overlapping but unique, statistically distinct activity patterns. These findings demonstrate that individual neurons in human motor cortex reflect information related to sensory inputs and VoS in addition to movement features, and are a key part of a broader network linking perception and cognition to action.
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spelling pubmed-62623672018-12-06 Watch, Imagine, Attempt: Motor Cortex Single-Unit Activity Reveals Context-Dependent Movement Encoding in Humans With Tetraplegia Vargas-Irwin, Carlos E. Feldman, Jessica M. King, Brandon Simeral, John D. Sorice, Brittany L. Oakley, Erin M. Cash, Sydney S. Eskandar, Emad N. Friehs, Gerhard M. Hochberg, Leigh R. Donoghue, John P. Front Hum Neurosci Neuroscience Planning and performing volitional movement engages widespread networks in the human brain, with motor cortex considered critical to the performance of skilled limb actions. Motor cortex is also engaged when actions are observed or imagined, but the manner in which ensembles of neurons represent these volitional states (VoSs) is unknown. Here we provide direct demonstration that observing, imagining or attempting action activates shared neural ensembles in human motor cortex. Two individuals with tetraplegia (due to brainstem stroke or amyotrophic lateral sclerosis, ALS) were verbally instructed to watch, imagine, or attempt reaching actions displayed on a computer screen. Neural activity in the precentral gyrus incorporated information about both cognitive state and movement kinematics; the three conditions presented overlapping but unique, statistically distinct activity patterns. These findings demonstrate that individual neurons in human motor cortex reflect information related to sensory inputs and VoS in addition to movement features, and are a key part of a broader network linking perception and cognition to action. Frontiers Media S.A. 2018-11-15 /pmc/articles/PMC6262367/ /pubmed/30524258 http://dx.doi.org/10.3389/fnhum.2018.00450 Text en Copyright © 2018 Vargas-Irwin, Feldman, King, Simeral, Sorice, Oakley, Cash, Eskandar, Friehs, Hochberg and Donoghue. 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(s) 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
Vargas-Irwin, Carlos E.
Feldman, Jessica M.
King, Brandon
Simeral, John D.
Sorice, Brittany L.
Oakley, Erin M.
Cash, Sydney S.
Eskandar, Emad N.
Friehs, Gerhard M.
Hochberg, Leigh R.
Donoghue, John P.
Watch, Imagine, Attempt: Motor Cortex Single-Unit Activity Reveals Context-Dependent Movement Encoding in Humans With Tetraplegia
title Watch, Imagine, Attempt: Motor Cortex Single-Unit Activity Reveals Context-Dependent Movement Encoding in Humans With Tetraplegia
title_full Watch, Imagine, Attempt: Motor Cortex Single-Unit Activity Reveals Context-Dependent Movement Encoding in Humans With Tetraplegia
title_fullStr Watch, Imagine, Attempt: Motor Cortex Single-Unit Activity Reveals Context-Dependent Movement Encoding in Humans With Tetraplegia
title_full_unstemmed Watch, Imagine, Attempt: Motor Cortex Single-Unit Activity Reveals Context-Dependent Movement Encoding in Humans With Tetraplegia
title_short Watch, Imagine, Attempt: Motor Cortex Single-Unit Activity Reveals Context-Dependent Movement Encoding in Humans With Tetraplegia
title_sort watch, imagine, attempt: motor cortex single-unit activity reveals context-dependent movement encoding in humans with tetraplegia
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6262367/
https://www.ncbi.nlm.nih.gov/pubmed/30524258
http://dx.doi.org/10.3389/fnhum.2018.00450
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