Frequency- and Area-Specific Phase Entrainment of Intrinsic Cortical Oscillations by Repetitive Transcranial Magnetic Stimulation

Synchronous oscillations are ubiquitous throughout the cortex, but the frequency of oscillations differs from area to area. To elucidate the mechanistic architectures underlying various rhythmic activities, we tested whether spontaneous neural oscillations in different local cortical areas and large...

Full description

Bibliographic Details
Main Authors: Yuka O. Okazaki, Yumi Nakagawa, Yuji Mizuno, Takashi Hanakawa, Keiichi Kitajo
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-03-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnhum.2021.608947/full
id doaj-83e31f50d562473491516d578b1e1fef
record_format Article
spelling doaj-83e31f50d562473491516d578b1e1fef2021-03-12T07:17:28ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612021-03-011510.3389/fnhum.2021.608947608947Frequency- and Area-Specific Phase Entrainment of Intrinsic Cortical Oscillations by Repetitive Transcranial Magnetic StimulationYuka O. Okazaki0Yuka O. Okazaki1Yuka O. Okazaki2Yumi Nakagawa3Yuji Mizuno4Yuji Mizuno5Takashi Hanakawa6Takashi Hanakawa7Takashi Hanakawa8Keiichi Kitajo9Keiichi Kitajo10Keiichi Kitajo11RIKEN CBS-TOYOTA Collaboration Center, RIKEN Center for Brain Science, Wako, JapanDivision of Neural Dynamics, Department of System Neuroscience, National Institute for Physiological Sciences, National Institutes of Natural Sciences, Okazaki, JapanDepartment of Physiological Sciences, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI), Okazaki, JapanRIKEN CBS-TOYOTA Collaboration Center, RIKEN Center for Brain Science, Wako, JapanRIKEN CBS-TOYOTA Collaboration Center, RIKEN Center for Brain Science, Wako, JapanIntegrative Brain Imaging Center, National Center of Neurology and Psychiatry, Kodaira, JapanRIKEN CBS-TOYOTA Collaboration Center, RIKEN Center for Brain Science, Wako, JapanIntegrative Brain Imaging Center, National Center of Neurology and Psychiatry, Kodaira, JapanDepartment of Integrated Neuroanatomy and Neuroimaging, Graduate School of Medicine, Kyoto University, Kyoto, JapanRIKEN CBS-TOYOTA Collaboration Center, RIKEN Center for Brain Science, Wako, JapanDivision of Neural Dynamics, Department of System Neuroscience, National Institute for Physiological Sciences, National Institutes of Natural Sciences, Okazaki, JapanDepartment of Physiological Sciences, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI), Okazaki, JapanSynchronous oscillations are ubiquitous throughout the cortex, but the frequency of oscillations differs from area to area. To elucidate the mechanistic architectures underlying various rhythmic activities, we tested whether spontaneous neural oscillations in different local cortical areas and large-scale networks can be phase-entrained by direct perturbation with distinct frequencies of repetitive transcranial magnetic stimulation (rTMS). While recording the electroencephalogram (EEG), we applied single-pulse TMS (sp-TMS) and rTMS at 5, 11, and 23 Hz over the motor or visual cortex. We assessed local and global modulation of phase dynamics using the phase-locking factor (PLF). sp-TMS to the motor and the visual cortex triggered a transient increase in PLF in distinct frequencies that peaked at 21 and 8 Hz, respectively. rTMS at 23 Hz over the motor cortex and 11 Hz over the visual cortex induced a prominent and progressive increase in PLF that lasted for a few cycles after the termination of rTMS. Moreover, the local increase in PLF propagated to other cortical areas. These results suggest that distinct cortical areas have area-specific oscillatory frequencies, and the manipulation of oscillations in local areas impacts other areas through the large-scale oscillatory network with the corresponding frequency specificity. We speculate that rTMS that is close to area-specific frequencies (natural frequencies) enables direct manipulation of brain dynamics and is thus useful for investigating the causal roles of synchronous neural oscillations. Moreover, this technique could be used to treat clinical symptoms associated with impaired oscillations and synchrony.https://www.frontiersin.org/articles/10.3389/fnhum.2021.608947/fullrTMS-EEGphase entrainmentnatural frequencyvisual cortexmotor cortexphase locking
collection DOAJ
language English
format Article
sources DOAJ
author Yuka O. Okazaki
Yuka O. Okazaki
Yuka O. Okazaki
Yumi Nakagawa
Yuji Mizuno
Yuji Mizuno
Takashi Hanakawa
Takashi Hanakawa
Takashi Hanakawa
Keiichi Kitajo
Keiichi Kitajo
Keiichi Kitajo
spellingShingle Yuka O. Okazaki
Yuka O. Okazaki
Yuka O. Okazaki
Yumi Nakagawa
Yuji Mizuno
Yuji Mizuno
Takashi Hanakawa
Takashi Hanakawa
Takashi Hanakawa
Keiichi Kitajo
Keiichi Kitajo
Keiichi Kitajo
Frequency- and Area-Specific Phase Entrainment of Intrinsic Cortical Oscillations by Repetitive Transcranial Magnetic Stimulation
Frontiers in Human Neuroscience
rTMS-EEG
phase entrainment
natural frequency
visual cortex
motor cortex
phase locking
author_facet Yuka O. Okazaki
Yuka O. Okazaki
Yuka O. Okazaki
Yumi Nakagawa
Yuji Mizuno
Yuji Mizuno
Takashi Hanakawa
Takashi Hanakawa
Takashi Hanakawa
Keiichi Kitajo
Keiichi Kitajo
Keiichi Kitajo
author_sort Yuka O. Okazaki
title Frequency- and Area-Specific Phase Entrainment of Intrinsic Cortical Oscillations by Repetitive Transcranial Magnetic Stimulation
title_short Frequency- and Area-Specific Phase Entrainment of Intrinsic Cortical Oscillations by Repetitive Transcranial Magnetic Stimulation
title_full Frequency- and Area-Specific Phase Entrainment of Intrinsic Cortical Oscillations by Repetitive Transcranial Magnetic Stimulation
title_fullStr Frequency- and Area-Specific Phase Entrainment of Intrinsic Cortical Oscillations by Repetitive Transcranial Magnetic Stimulation
title_full_unstemmed Frequency- and Area-Specific Phase Entrainment of Intrinsic Cortical Oscillations by Repetitive Transcranial Magnetic Stimulation
title_sort frequency- and area-specific phase entrainment of intrinsic cortical oscillations by repetitive transcranial magnetic stimulation
publisher Frontiers Media S.A.
series Frontiers in Human Neuroscience
issn 1662-5161
publishDate 2021-03-01
description Synchronous oscillations are ubiquitous throughout the cortex, but the frequency of oscillations differs from area to area. To elucidate the mechanistic architectures underlying various rhythmic activities, we tested whether spontaneous neural oscillations in different local cortical areas and large-scale networks can be phase-entrained by direct perturbation with distinct frequencies of repetitive transcranial magnetic stimulation (rTMS). While recording the electroencephalogram (EEG), we applied single-pulse TMS (sp-TMS) and rTMS at 5, 11, and 23 Hz over the motor or visual cortex. We assessed local and global modulation of phase dynamics using the phase-locking factor (PLF). sp-TMS to the motor and the visual cortex triggered a transient increase in PLF in distinct frequencies that peaked at 21 and 8 Hz, respectively. rTMS at 23 Hz over the motor cortex and 11 Hz over the visual cortex induced a prominent and progressive increase in PLF that lasted for a few cycles after the termination of rTMS. Moreover, the local increase in PLF propagated to other cortical areas. These results suggest that distinct cortical areas have area-specific oscillatory frequencies, and the manipulation of oscillations in local areas impacts other areas through the large-scale oscillatory network with the corresponding frequency specificity. We speculate that rTMS that is close to area-specific frequencies (natural frequencies) enables direct manipulation of brain dynamics and is thus useful for investigating the causal roles of synchronous neural oscillations. Moreover, this technique could be used to treat clinical symptoms associated with impaired oscillations and synchrony.
topic rTMS-EEG
phase entrainment
natural frequency
visual cortex
motor cortex
phase locking
url https://www.frontiersin.org/articles/10.3389/fnhum.2021.608947/full
work_keys_str_mv AT yukaookazaki frequencyandareaspecificphaseentrainmentofintrinsiccorticaloscillationsbyrepetitivetranscranialmagneticstimulation
AT yukaookazaki frequencyandareaspecificphaseentrainmentofintrinsiccorticaloscillationsbyrepetitivetranscranialmagneticstimulation
AT yukaookazaki frequencyandareaspecificphaseentrainmentofintrinsiccorticaloscillationsbyrepetitivetranscranialmagneticstimulation
AT yuminakagawa frequencyandareaspecificphaseentrainmentofintrinsiccorticaloscillationsbyrepetitivetranscranialmagneticstimulation
AT yujimizuno frequencyandareaspecificphaseentrainmentofintrinsiccorticaloscillationsbyrepetitivetranscranialmagneticstimulation
AT yujimizuno frequencyandareaspecificphaseentrainmentofintrinsiccorticaloscillationsbyrepetitivetranscranialmagneticstimulation
AT takashihanakawa frequencyandareaspecificphaseentrainmentofintrinsiccorticaloscillationsbyrepetitivetranscranialmagneticstimulation
AT takashihanakawa frequencyandareaspecificphaseentrainmentofintrinsiccorticaloscillationsbyrepetitivetranscranialmagneticstimulation
AT takashihanakawa frequencyandareaspecificphaseentrainmentofintrinsiccorticaloscillationsbyrepetitivetranscranialmagneticstimulation
AT keiichikitajo frequencyandareaspecificphaseentrainmentofintrinsiccorticaloscillationsbyrepetitivetranscranialmagneticstimulation
AT keiichikitajo frequencyandareaspecificphaseentrainmentofintrinsiccorticaloscillationsbyrepetitivetranscranialmagneticstimulation
AT keiichikitajo frequencyandareaspecificphaseentrainmentofintrinsiccorticaloscillationsbyrepetitivetranscranialmagneticstimulation
_version_ 1724223178771791872