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Prefrontal theta modulates sensorimotor gamma networks during the reorienting of attention

The ability to execute a motor plan involves spatiotemporally precise oscillatory activity in primary motor (M1) regions, in concert with recruitment of “higher order” attentional mechanisms for orienting toward current task goals. While current evidence implicates gamma oscillatory activity in M1 a...

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Autores principales: Spooner, Rachel K., Wiesman, Alex I., Proskovec, Amy L., Heinrichs‐Graham, Elizabeth, Wilson, Tony W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7268018/
https://www.ncbi.nlm.nih.gov/pubmed/31621977
http://dx.doi.org/10.1002/hbm.24819
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author Spooner, Rachel K.
Wiesman, Alex I.
Proskovec, Amy L.
Heinrichs‐Graham, Elizabeth
Wilson, Tony W.
author_facet Spooner, Rachel K.
Wiesman, Alex I.
Proskovec, Amy L.
Heinrichs‐Graham, Elizabeth
Wilson, Tony W.
author_sort Spooner, Rachel K.
collection PubMed
description The ability to execute a motor plan involves spatiotemporally precise oscillatory activity in primary motor (M1) regions, in concert with recruitment of “higher order” attentional mechanisms for orienting toward current task goals. While current evidence implicates gamma oscillatory activity in M1 as central to the execution of a movement, far less is known about top‐down attentional modulation of this response. Herein, we utilized magnetoencephalography (MEG) during a Posner attention‐reorienting task to investigate top‐down modulation of M1 gamma responses by frontal attention networks in 63 healthy adult participants. MEG data were evaluated in the time–frequency domain and significant oscillatory responses were imaged using a beamformer. Robust increases in theta activity were found in bilateral inferior frontal gyri (IFG), with significantly stronger responses evident in trials that required attentional reorienting relative to those that did not. Additionally, strong gamma oscillations (60–80 Hz) were detected in M1 during movement execution, with similar responses elicited irrespective of attentional reorienting. Whole‐brain voxel‐wise correlations between validity difference scores (i.e., attention reorienting trials—nonreorienting trials) in frontal theta activity and movement‐locked gamma oscillations revealed a robust relationship in the contralateral sensorimotor cortex, supplementary motor area, and right cerebellum, suggesting modulation of these sensorimotor network gamma responses by attentional reorienting. Importantly, the validity difference effect in this distributed motor network was predictive of overall motor function measured outside the scanner and further, based on a mediation analysis this relationship was fully mediated by the reallocation response in the right IFG. These data are the first to characterize the top‐down modulation of movement‐related gamma responses during attentional reorienting and movement execution.
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spelling pubmed-72680182020-06-12 Prefrontal theta modulates sensorimotor gamma networks during the reorienting of attention Spooner, Rachel K. Wiesman, Alex I. Proskovec, Amy L. Heinrichs‐Graham, Elizabeth Wilson, Tony W. Hum Brain Mapp Research Articles The ability to execute a motor plan involves spatiotemporally precise oscillatory activity in primary motor (M1) regions, in concert with recruitment of “higher order” attentional mechanisms for orienting toward current task goals. While current evidence implicates gamma oscillatory activity in M1 as central to the execution of a movement, far less is known about top‐down attentional modulation of this response. Herein, we utilized magnetoencephalography (MEG) during a Posner attention‐reorienting task to investigate top‐down modulation of M1 gamma responses by frontal attention networks in 63 healthy adult participants. MEG data were evaluated in the time–frequency domain and significant oscillatory responses were imaged using a beamformer. Robust increases in theta activity were found in bilateral inferior frontal gyri (IFG), with significantly stronger responses evident in trials that required attentional reorienting relative to those that did not. Additionally, strong gamma oscillations (60–80 Hz) were detected in M1 during movement execution, with similar responses elicited irrespective of attentional reorienting. Whole‐brain voxel‐wise correlations between validity difference scores (i.e., attention reorienting trials—nonreorienting trials) in frontal theta activity and movement‐locked gamma oscillations revealed a robust relationship in the contralateral sensorimotor cortex, supplementary motor area, and right cerebellum, suggesting modulation of these sensorimotor network gamma responses by attentional reorienting. Importantly, the validity difference effect in this distributed motor network was predictive of overall motor function measured outside the scanner and further, based on a mediation analysis this relationship was fully mediated by the reallocation response in the right IFG. These data are the first to characterize the top‐down modulation of movement‐related gamma responses during attentional reorienting and movement execution. John Wiley & Sons, Inc. 2019-10-17 /pmc/articles/PMC7268018/ /pubmed/31621977 http://dx.doi.org/10.1002/hbm.24819 Text en © 2019 The Authors. Human Brain Mapping published by Wiley Periodicals, Inc. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Spooner, Rachel K.
Wiesman, Alex I.
Proskovec, Amy L.
Heinrichs‐Graham, Elizabeth
Wilson, Tony W.
Prefrontal theta modulates sensorimotor gamma networks during the reorienting of attention
title Prefrontal theta modulates sensorimotor gamma networks during the reorienting of attention
title_full Prefrontal theta modulates sensorimotor gamma networks during the reorienting of attention
title_fullStr Prefrontal theta modulates sensorimotor gamma networks during the reorienting of attention
title_full_unstemmed Prefrontal theta modulates sensorimotor gamma networks during the reorienting of attention
title_short Prefrontal theta modulates sensorimotor gamma networks during the reorienting of attention
title_sort prefrontal theta modulates sensorimotor gamma networks during the reorienting of attention
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7268018/
https://www.ncbi.nlm.nih.gov/pubmed/31621977
http://dx.doi.org/10.1002/hbm.24819
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