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Selective Suppression of Local Interneuron Circuits in Human Motor Cortex Contributes to Movement Preparation

Changes in neural activity occur in the motor cortex before movement, but the nature and purpose of this preparatory activity is unclear. To investigate this in the human (male and female) brain noninvasively, we used transcranial magnetic stimulation (TMS) to probe the excitability of distinct sets...

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Autores principales: Hannah, Ricci, Cavanagh, Sean E., Tremblay, Sara, Simeoni, Sara, Rothwell, John C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5792480/
https://www.ncbi.nlm.nih.gov/pubmed/29263237
http://dx.doi.org/10.1523/JNEUROSCI.2869-17.2017
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author Hannah, Ricci
Cavanagh, Sean E.
Tremblay, Sara
Simeoni, Sara
Rothwell, John C.
author_facet Hannah, Ricci
Cavanagh, Sean E.
Tremblay, Sara
Simeoni, Sara
Rothwell, John C.
author_sort Hannah, Ricci
collection PubMed
description Changes in neural activity occur in the motor cortex before movement, but the nature and purpose of this preparatory activity is unclear. To investigate this in the human (male and female) brain noninvasively, we used transcranial magnetic stimulation (TMS) to probe the excitability of distinct sets of excitatory inputs to corticospinal neurons during the warning period of various reaction time tasks. Using two separate methods (H-reflex conditioning and directional effects of TMS), we show that a specific set of excitatory inputs to corticospinal neurons are suppressed during motor preparation, while another set of inputs remain unaffected. To probe the behavioral relevance of this suppression, we examined whether the strength of the selective preparatory inhibition in each trial was related to reaction time. Surprisingly, the greater the amount of selective preparatory inhibition, the faster the reaction time was. This suggests that the inhibition of inputs to corticospinal neurons is not involved in preventing the release of movement but may in fact facilitate rapid reactions. Thus, selective suppression of a specific set of motor cortical neurons may be a key aspect of successful movement preparation. SIGNIFICANCE STATEMENT Movement preparation evokes substantial activity in the motor cortex despite no apparent movement. One explanation for the lack of movement is that motor cortical output in this period is gated by an inhibitory mechanism. This notion was supported by previous noninvasive TMS studies of human motor cortex indicating a reduction of corticospinal excitability. On the contrary, our data support the idea that there is a coordinated balance of activity upstream of the corticospinal output neurons. This includes a suppression of specific local circuits that supports, rather than inhibits, the rapid generation of prepared movements. Thus, the selective suppression of local circuits appears to be an essential part of successful movement preparation instead of an external control mechanism.
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spelling pubmed-57924802018-02-15 Selective Suppression of Local Interneuron Circuits in Human Motor Cortex Contributes to Movement Preparation Hannah, Ricci Cavanagh, Sean E. Tremblay, Sara Simeoni, Sara Rothwell, John C. J Neurosci Research Articles Changes in neural activity occur in the motor cortex before movement, but the nature and purpose of this preparatory activity is unclear. To investigate this in the human (male and female) brain noninvasively, we used transcranial magnetic stimulation (TMS) to probe the excitability of distinct sets of excitatory inputs to corticospinal neurons during the warning period of various reaction time tasks. Using two separate methods (H-reflex conditioning and directional effects of TMS), we show that a specific set of excitatory inputs to corticospinal neurons are suppressed during motor preparation, while another set of inputs remain unaffected. To probe the behavioral relevance of this suppression, we examined whether the strength of the selective preparatory inhibition in each trial was related to reaction time. Surprisingly, the greater the amount of selective preparatory inhibition, the faster the reaction time was. This suggests that the inhibition of inputs to corticospinal neurons is not involved in preventing the release of movement but may in fact facilitate rapid reactions. Thus, selective suppression of a specific set of motor cortical neurons may be a key aspect of successful movement preparation. SIGNIFICANCE STATEMENT Movement preparation evokes substantial activity in the motor cortex despite no apparent movement. One explanation for the lack of movement is that motor cortical output in this period is gated by an inhibitory mechanism. This notion was supported by previous noninvasive TMS studies of human motor cortex indicating a reduction of corticospinal excitability. On the contrary, our data support the idea that there is a coordinated balance of activity upstream of the corticospinal output neurons. This includes a suppression of specific local circuits that supports, rather than inhibits, the rapid generation of prepared movements. Thus, the selective suppression of local circuits appears to be an essential part of successful movement preparation instead of an external control mechanism. Society for Neuroscience 2018-01-31 /pmc/articles/PMC5792480/ /pubmed/29263237 http://dx.doi.org/10.1523/JNEUROSCI.2869-17.2017 Text en Copyright © 2018 Hannah et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Hannah, Ricci
Cavanagh, Sean E.
Tremblay, Sara
Simeoni, Sara
Rothwell, John C.
Selective Suppression of Local Interneuron Circuits in Human Motor Cortex Contributes to Movement Preparation
title Selective Suppression of Local Interneuron Circuits in Human Motor Cortex Contributes to Movement Preparation
title_full Selective Suppression of Local Interneuron Circuits in Human Motor Cortex Contributes to Movement Preparation
title_fullStr Selective Suppression of Local Interneuron Circuits in Human Motor Cortex Contributes to Movement Preparation
title_full_unstemmed Selective Suppression of Local Interneuron Circuits in Human Motor Cortex Contributes to Movement Preparation
title_short Selective Suppression of Local Interneuron Circuits in Human Motor Cortex Contributes to Movement Preparation
title_sort selective suppression of local interneuron circuits in human motor cortex contributes to movement preparation
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5792480/
https://www.ncbi.nlm.nih.gov/pubmed/29263237
http://dx.doi.org/10.1523/JNEUROSCI.2869-17.2017
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