Interhemispheric and Intrahemispheric Connectivity From the Left Pars Opercularis Within the Language Network Is Modulated by Transcranial Stimulation in Healthy Subjects

Neural activity related to language can be modulated within widespread networks following learning or in response to disruption—including the experimental application of noninvasive brain stimulation. However, the spatiotemporal characteristics of such modulation remain insufficiently explored. The...

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Main Authors: Woo-Kyoung Yoo, Marine Vernet, Jung-Hoon Kim, Anna-Katharine Brem, Shahid Bashir, Fritz Ifert-Miller, Chang-Hwan Im, Mark Eldaief, Alvaro Pascual-Leone
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-03-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnhum.2020.00063/full
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author Woo-Kyoung Yoo
Marine Vernet
Marine Vernet
Jung-Hoon Kim
Jung-Hoon Kim
Anna-Katharine Brem
Anna-Katharine Brem
Anna-Katharine Brem
Shahid Bashir
Shahid Bashir
Fritz Ifert-Miller
Chang-Hwan Im
Mark Eldaief
Alvaro Pascual-Leone
Alvaro Pascual-Leone
Alvaro Pascual-Leone
author_facet Woo-Kyoung Yoo
Marine Vernet
Marine Vernet
Jung-Hoon Kim
Jung-Hoon Kim
Anna-Katharine Brem
Anna-Katharine Brem
Anna-Katharine Brem
Shahid Bashir
Shahid Bashir
Fritz Ifert-Miller
Chang-Hwan Im
Mark Eldaief
Alvaro Pascual-Leone
Alvaro Pascual-Leone
Alvaro Pascual-Leone
author_sort Woo-Kyoung Yoo
collection DOAJ
description Neural activity related to language can be modulated within widespread networks following learning or in response to disruption—including the experimental application of noninvasive brain stimulation. However, the spatiotemporal characteristics of such modulation remain insufficiently explored. The present study combined transcranial magnetic stimulation (TMS) and electroencephalography (EEG) to explore the modulation of activity across the language network following continuous theta-burst stimulation (cTBS) of the left pars opercularis. In 10 healthy subjects (21 ± 2 years old, four females), neuronavigated cTBS was delivered over the left pars opercularis of the frontal operculum (part of the traditional Broca’s area) at 80% of active motor threshold (AMT) stimulation intensity. Real cTBS and sham cTBS were performed in two different visits separated by at least 48 h. Before, immediately, and 10 min after cTBS, 30 single pulses of TMS were delivered to the left pars opercularis at 80% of the resting motor threshold (RMT), whereas EEG was simultaneously recorded. We examined the cTBS-induced modulation of phase locking values (PLVs) between the TMS-evoked potentials (TEPs) recorded over the pars opercularis and those recorded over its right-hemispheric homolog area, the left supramarginal area, and the left superior temporal area in different EEG frequency bands and different time windows following cTBS. cTBS to the left pars opercularis induced within the gamma band: (1) a significant increase in TEP phase synchronization between the left and right pars opercularis at an early time window (250–350 ms) following cTBS; and (2) significantly increased PLV with the left supramarginal area and the left superior temporal area at a later time window (600–700 ms). In the theta and delta band, cTBS to the left pars opercularis induced significantly increased phase synchronization of TEPs between the left pars opercularis and the posterior left hemispheric language areas at a late time window. In sham condition, there was a significant decrease in TEP phase synchronization of the high beta band between left pars opercularis and left superior temporal area at 200–300 ms. These results contribute to characterize the dynamics of the language network and may have implications in the development of noninvasive stimulation protocols to promote the language rehabilitation in aphasia patients.
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spelling doaj.art-64dab8b339dd48d4b9b0df7ae161453d2022-12-22T00:06:05ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612020-03-011410.3389/fnhum.2020.00063495818Interhemispheric and Intrahemispheric Connectivity From the Left Pars Opercularis Within the Language Network Is Modulated by Transcranial Stimulation in Healthy SubjectsWoo-Kyoung Yoo0Marine Vernet1Marine Vernet2Jung-Hoon Kim3Jung-Hoon Kim4Anna-Katharine Brem5Anna-Katharine Brem6Anna-Katharine Brem7Shahid Bashir8Shahid Bashir9Fritz Ifert-Miller10Chang-Hwan Im11Mark Eldaief12Alvaro Pascual-Leone13Alvaro Pascual-Leone14Alvaro Pascual-Leone15Department of Physical Medicine and Rehabilitation, Hallym University Sacred Heart Hospital, Anyang, South KoreaDepartment of Neurology, Harvard Medical School, Boston, MA, United StatesImpAct Team, Lyon Neuroscience Research Center (CRNL), CNRS UMR5292, INSERM, U1028, University Lyon 1, Bron, FranceWeldon School of Biomedical Engineering, Purdue University, West Lafayette, IN, United StatesDepartment of Biomedical Engineering, Hanyang University, Seoul, South KoreaDepartment of Neurology, Harvard Medical School, Boston, MA, United StatesUniversity Hospital of Old Age Psychiatry, University of Bern, Bern, SwitzerlandDepartment of Neuropsychology, Memory Clinic Zentralschweiz, Lucerne Psychiatry, Lucerne, SwitzerlandDepartment of Neurology, Harvard Medical School, Boston, MA, United StatesDepartment of Neurophysiology, Neuroscience Center, King Fahad Specialist Hospital, Dammam, Saudi ArabiaDepartment of Neurology, Harvard Medical School, Boston, MA, United StatesDepartment of Biomedical Engineering, Hanyang University, Seoul, South KoreaDepartment of Neurology, Harvard Medical School, Boston, MA, United StatesDepartment of Neurology, Harvard Medical School, Boston, MA, United StatesHinda and Arthur Institute for Aging Research and Center for Memory Health, Hebrew SeniorLife, Boston, MA, United States0Guttmann Brain Health Institute, Institut Guttmann de Neurorehabilitation, Universitat Autonoma, Barcelona, SpainNeural activity related to language can be modulated within widespread networks following learning or in response to disruption—including the experimental application of noninvasive brain stimulation. However, the spatiotemporal characteristics of such modulation remain insufficiently explored. The present study combined transcranial magnetic stimulation (TMS) and electroencephalography (EEG) to explore the modulation of activity across the language network following continuous theta-burst stimulation (cTBS) of the left pars opercularis. In 10 healthy subjects (21 ± 2 years old, four females), neuronavigated cTBS was delivered over the left pars opercularis of the frontal operculum (part of the traditional Broca’s area) at 80% of active motor threshold (AMT) stimulation intensity. Real cTBS and sham cTBS were performed in two different visits separated by at least 48 h. Before, immediately, and 10 min after cTBS, 30 single pulses of TMS were delivered to the left pars opercularis at 80% of the resting motor threshold (RMT), whereas EEG was simultaneously recorded. We examined the cTBS-induced modulation of phase locking values (PLVs) between the TMS-evoked potentials (TEPs) recorded over the pars opercularis and those recorded over its right-hemispheric homolog area, the left supramarginal area, and the left superior temporal area in different EEG frequency bands and different time windows following cTBS. cTBS to the left pars opercularis induced within the gamma band: (1) a significant increase in TEP phase synchronization between the left and right pars opercularis at an early time window (250–350 ms) following cTBS; and (2) significantly increased PLV with the left supramarginal area and the left superior temporal area at a later time window (600–700 ms). In the theta and delta band, cTBS to the left pars opercularis induced significantly increased phase synchronization of TEPs between the left pars opercularis and the posterior left hemispheric language areas at a late time window. In sham condition, there was a significant decrease in TEP phase synchronization of the high beta band between left pars opercularis and left superior temporal area at 200–300 ms. These results contribute to characterize the dynamics of the language network and may have implications in the development of noninvasive stimulation protocols to promote the language rehabilitation in aphasia patients.https://www.frontiersin.org/article/10.3389/fnhum.2020.00063/fullnoninvasive brain stimulationTMS-evoked potentialsgamma bandphase synchronizationcontinuous theta-burst stimulation
spellingShingle Woo-Kyoung Yoo
Marine Vernet
Marine Vernet
Jung-Hoon Kim
Jung-Hoon Kim
Anna-Katharine Brem
Anna-Katharine Brem
Anna-Katharine Brem
Shahid Bashir
Shahid Bashir
Fritz Ifert-Miller
Chang-Hwan Im
Mark Eldaief
Alvaro Pascual-Leone
Alvaro Pascual-Leone
Alvaro Pascual-Leone
Interhemispheric and Intrahemispheric Connectivity From the Left Pars Opercularis Within the Language Network Is Modulated by Transcranial Stimulation in Healthy Subjects
Frontiers in Human Neuroscience
noninvasive brain stimulation
TMS-evoked potentials
gamma band
phase synchronization
continuous theta-burst stimulation
title Interhemispheric and Intrahemispheric Connectivity From the Left Pars Opercularis Within the Language Network Is Modulated by Transcranial Stimulation in Healthy Subjects
title_full Interhemispheric and Intrahemispheric Connectivity From the Left Pars Opercularis Within the Language Network Is Modulated by Transcranial Stimulation in Healthy Subjects
title_fullStr Interhemispheric and Intrahemispheric Connectivity From the Left Pars Opercularis Within the Language Network Is Modulated by Transcranial Stimulation in Healthy Subjects
title_full_unstemmed Interhemispheric and Intrahemispheric Connectivity From the Left Pars Opercularis Within the Language Network Is Modulated by Transcranial Stimulation in Healthy Subjects
title_short Interhemispheric and Intrahemispheric Connectivity From the Left Pars Opercularis Within the Language Network Is Modulated by Transcranial Stimulation in Healthy Subjects
title_sort interhemispheric and intrahemispheric connectivity from the left pars opercularis within the language network is modulated by transcranial stimulation in healthy subjects
topic noninvasive brain stimulation
TMS-evoked potentials
gamma band
phase synchronization
continuous theta-burst stimulation
url https://www.frontiersin.org/article/10.3389/fnhum.2020.00063/full
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