Primary Sensorimotor Cortex Drives the Common Cortical Network for Gamma Synchronization in Voluntary Hand Movements

Background: Gamma synchronization (GS) may promote the processing between functionally related cortico-subcortical neural populations. Our aim was to identify the sources of GS and to analyze the direction of information flow in cerebral networks at the beginning of phasic movements, and during medi...

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Main Authors: Gertrúd Tamás, Venkata C. Chirumamilla, Abdul R. Anwar, Jan Raethjen, Günther Deuschl, Sergiu Groppa, Muthuraman Muthuraman
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-04-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fnhum.2018.00130/full
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spelling doaj-2cc04e2aea7847b985f301ac16d9c6832020-11-25T03:00:56ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612018-04-011210.3389/fnhum.2018.00130341959Primary Sensorimotor Cortex Drives the Common Cortical Network for Gamma Synchronization in Voluntary Hand MovementsGertrúd Tamás0Venkata C. Chirumamilla1Abdul R. Anwar2Abdul R. Anwar3Jan Raethjen4Günther Deuschl5Sergiu Groppa6Muthuraman Muthuraman7Department of Neurology, Semmelweis University, Budapest, HungarySection of Movement Disorders and Neurostimulation, Biomedical Statistics and Multimodal Signal Processing Unit, Department of Neurology, Focus Program Translational Neuroscience (FTN), University Medical Center of the Johannes Gutenberg University Mainz, Mainz, GermanyDepartment of Neurology, Christian-Albrechts-University, Kiel, GermanyBiomedical Engineering Centre, University of Engineering and Technology, Lahore, PakistanDepartment of Neurology, Christian-Albrechts-University, Kiel, GermanyDepartment of Neurology, Christian-Albrechts-University, Kiel, GermanySection of Movement Disorders and Neurostimulation, Biomedical Statistics and Multimodal Signal Processing Unit, Department of Neurology, Focus Program Translational Neuroscience (FTN), University Medical Center of the Johannes Gutenberg University Mainz, Mainz, GermanySection of Movement Disorders and Neurostimulation, Biomedical Statistics and Multimodal Signal Processing Unit, Department of Neurology, Focus Program Translational Neuroscience (FTN), University Medical Center of the Johannes Gutenberg University Mainz, Mainz, GermanyBackground: Gamma synchronization (GS) may promote the processing between functionally related cortico-subcortical neural populations. Our aim was to identify the sources of GS and to analyze the direction of information flow in cerebral networks at the beginning of phasic movements, and during medium-strength isometric contraction of the hand.Methods: We measured 64-channel electroencephalography in 11 healthy volunteers (age: 25 ± 8 years; four females); surface electromyography detected the movements of the dominant hand. In Task 1, subjects kept a constant medium-strength contraction of the first dorsal interosseus muscle, and performed a superimposed repetitive voluntary self-paced brisk squeeze of an object. In Task 2, brisk, and in Task 3, constant contractions were performed. Time-frequency analysis of the EEG signal was performed with the multitaper method. GS sources were identified in five frequency bands (30–49, 51–75, 76–99, 101–125, and 126–149 Hz) with beamformer inverse solution dynamic imaging of coherent sources. The direction of information flow was estimated by renormalized partial directed coherence for each frequency band. The data-driven surrogate test, and the time reversal technique were performed to identify significant connections.Results: In all tasks, we depicted the first three common sources for the studied frequency bands that were as follows: contralateral primary sensorimotor cortex (S1M1), dorsolateral prefrontal cortex (dPFC) and supplementary motor cortex (SMA). GS was detected in narrower low- (∼30–60 Hz) and high-frequency bands (>51–60 Hz) in the contralateral thalamus and ipsilateral cerebellum in all three tasks. The contralateral posterior parietal cortex was activated only in Task 1. In every task, S1M1 had efferent information flow to the SMA and the dPFC while dPFC had no detected afferent connections to the network in the gamma range. Cortical-subcortical information flow captured by the GS was dynamically variable in the narrower frequency bands for the studied movements.Conclusion: A distinct cortical network was identified for GS in voluntary hand movement tasks. Our study revealed that S1M1 modulated the activity of interconnected cortical areas through GS, while subcortical structures modulated the motor network dynamically, and specifically for the studied movement program.http://journal.frontiersin.org/article/10.3389/fnhum.2018.00130/fullgamma synchronizationnetworkconnectivitydirectionalityhand movements
collection DOAJ
language English
format Article
sources DOAJ
author Gertrúd Tamás
Venkata C. Chirumamilla
Abdul R. Anwar
Abdul R. Anwar
Jan Raethjen
Günther Deuschl
Sergiu Groppa
Muthuraman Muthuraman
spellingShingle Gertrúd Tamás
Venkata C. Chirumamilla
Abdul R. Anwar
Abdul R. Anwar
Jan Raethjen
Günther Deuschl
Sergiu Groppa
Muthuraman Muthuraman
Primary Sensorimotor Cortex Drives the Common Cortical Network for Gamma Synchronization in Voluntary Hand Movements
Frontiers in Human Neuroscience
gamma synchronization
network
connectivity
directionality
hand movements
author_facet Gertrúd Tamás
Venkata C. Chirumamilla
Abdul R. Anwar
Abdul R. Anwar
Jan Raethjen
Günther Deuschl
Sergiu Groppa
Muthuraman Muthuraman
author_sort Gertrúd Tamás
title Primary Sensorimotor Cortex Drives the Common Cortical Network for Gamma Synchronization in Voluntary Hand Movements
title_short Primary Sensorimotor Cortex Drives the Common Cortical Network for Gamma Synchronization in Voluntary Hand Movements
title_full Primary Sensorimotor Cortex Drives the Common Cortical Network for Gamma Synchronization in Voluntary Hand Movements
title_fullStr Primary Sensorimotor Cortex Drives the Common Cortical Network for Gamma Synchronization in Voluntary Hand Movements
title_full_unstemmed Primary Sensorimotor Cortex Drives the Common Cortical Network for Gamma Synchronization in Voluntary Hand Movements
title_sort primary sensorimotor cortex drives the common cortical network for gamma synchronization in voluntary hand movements
publisher Frontiers Media S.A.
series Frontiers in Human Neuroscience
issn 1662-5161
publishDate 2018-04-01
description Background: Gamma synchronization (GS) may promote the processing between functionally related cortico-subcortical neural populations. Our aim was to identify the sources of GS and to analyze the direction of information flow in cerebral networks at the beginning of phasic movements, and during medium-strength isometric contraction of the hand.Methods: We measured 64-channel electroencephalography in 11 healthy volunteers (age: 25 ± 8 years; four females); surface electromyography detected the movements of the dominant hand. In Task 1, subjects kept a constant medium-strength contraction of the first dorsal interosseus muscle, and performed a superimposed repetitive voluntary self-paced brisk squeeze of an object. In Task 2, brisk, and in Task 3, constant contractions were performed. Time-frequency analysis of the EEG signal was performed with the multitaper method. GS sources were identified in five frequency bands (30–49, 51–75, 76–99, 101–125, and 126–149 Hz) with beamformer inverse solution dynamic imaging of coherent sources. The direction of information flow was estimated by renormalized partial directed coherence for each frequency band. The data-driven surrogate test, and the time reversal technique were performed to identify significant connections.Results: In all tasks, we depicted the first three common sources for the studied frequency bands that were as follows: contralateral primary sensorimotor cortex (S1M1), dorsolateral prefrontal cortex (dPFC) and supplementary motor cortex (SMA). GS was detected in narrower low- (∼30–60 Hz) and high-frequency bands (>51–60 Hz) in the contralateral thalamus and ipsilateral cerebellum in all three tasks. The contralateral posterior parietal cortex was activated only in Task 1. In every task, S1M1 had efferent information flow to the SMA and the dPFC while dPFC had no detected afferent connections to the network in the gamma range. Cortical-subcortical information flow captured by the GS was dynamically variable in the narrower frequency bands for the studied movements.Conclusion: A distinct cortical network was identified for GS in voluntary hand movement tasks. Our study revealed that S1M1 modulated the activity of interconnected cortical areas through GS, while subcortical structures modulated the motor network dynamically, and specifically for the studied movement program.
topic gamma synchronization
network
connectivity
directionality
hand movements
url http://journal.frontiersin.org/article/10.3389/fnhum.2018.00130/full
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