The polarity of high-definition transcranial direct current stimulation affects the planning and execution of movement sequences

Noninvasive brain stimulation of the primary motor cortex has been shown to alter therapeutic outcomes in stroke and other neurological conditions, but the precise mechanisms remain poorly understood. Determining the impact of such neurostimulation on the neural processing supporting motor control i...

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Main Authors: Jake J. Son, Tara D. Erker, Thomas W. Ward, Yasra Arif, Peihan J. Huang, Jason A. John, Kellen M. McDonald, Nathan M. Petro, Grant M. Garrison, Hannah J. Okelberry, Kennedy A. Kress, Giorgia Picci, Elizabeth Heinrichs-Graham, Tony W. Wilson
Format: Article
Language:English
Published: Elsevier 2025-02-01
Series:NeuroImage
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Online Access:http://www.sciencedirect.com/science/article/pii/S1053811925000187
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author Jake J. Son
Tara D. Erker
Thomas W. Ward
Yasra Arif
Peihan J. Huang
Jason A. John
Kellen M. McDonald
Nathan M. Petro
Grant M. Garrison
Hannah J. Okelberry
Kennedy A. Kress
Giorgia Picci
Elizabeth Heinrichs-Graham
Tony W. Wilson
author_facet Jake J. Son
Tara D. Erker
Thomas W. Ward
Yasra Arif
Peihan J. Huang
Jason A. John
Kellen M. McDonald
Nathan M. Petro
Grant M. Garrison
Hannah J. Okelberry
Kennedy A. Kress
Giorgia Picci
Elizabeth Heinrichs-Graham
Tony W. Wilson
author_sort Jake J. Son
collection DOAJ
description Noninvasive brain stimulation of the primary motor cortex has been shown to alter therapeutic outcomes in stroke and other neurological conditions, but the precise mechanisms remain poorly understood. Determining the impact of such neurostimulation on the neural processing supporting motor control is a critical step toward further harnessing its therapeutic potential in multiple neurological conditions affecting the motor system. Herein, we leverage the excellent spatio-temporal precision of magnetoencephalographic (MEG) imaging to identify the spectral, spatial, and temporal effects of high-definition transcranial direct current stimulation (HD-tDCS) on the neural responses supporting motor control. Participants (N = 67) completed three HD-tDCS visits (anode, cathode, sham), with each involving 20 min of left primary motor cortex stimulation and performance of a simple/complex motor sequencing task during MEG. Whole-brain statistical analyses of beta oscillatory responses revealed stimulation-by-task interaction effects in the left primary motor cortex, right occipitotemporal, and the right dorsolateral prefrontal cortices. Broadly, anodal stimulation induced significantly stronger beta oscillatory responses in these regions during simple movement sequences, while neural responses to complex sequences were not affected by stimulation. En masse, these data suggest that the beta oscillations serving motor planning (i.e., pre-movement) are particularly sensitive to the polarity of noninvasive stimulation and that the impact varies based on the difficulty of the movement sequence.
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spelling doaj-art-319899c62a9f4e459e7325567eb609b32025-01-23T05:26:24ZengElsevierNeuroImage1095-95722025-02-01306121018The polarity of high-definition transcranial direct current stimulation affects the planning and execution of movement sequencesJake J. Son0Tara D. Erker1Thomas W. Ward2Yasra Arif3Peihan J. Huang4Jason A. John5Kellen M. McDonald6Nathan M. Petro7Grant M. Garrison8Hannah J. Okelberry9Kennedy A. Kress10Giorgia Picci11Elizabeth Heinrichs-Graham12Tony W. Wilson13Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; College of Medicine, University of Nebraska Medical Center, Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Department of Pharmacology & Neuroscience, Creighton University, Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Department of Pharmacology & Neuroscience, Creighton University, Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Department of Pharmacology & Neuroscience, Creighton University, Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Department of Pharmacology & Neuroscience, Creighton University, Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; College of Medicine, University of Nebraska Medical Center, Omaha, NE, USA; Department of Pharmacology & Neuroscience, Creighton University, Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; College of Medicine, University of Nebraska Medical Center, Omaha, NE, USA; Department of Pharmacology & Neuroscience, Creighton University, Omaha, NE, USA; Corresponding author at: Institute for Human Neuroscience, Boys Town National Research Hospital, Omaha, NE 68010, USA.Noninvasive brain stimulation of the primary motor cortex has been shown to alter therapeutic outcomes in stroke and other neurological conditions, but the precise mechanisms remain poorly understood. Determining the impact of such neurostimulation on the neural processing supporting motor control is a critical step toward further harnessing its therapeutic potential in multiple neurological conditions affecting the motor system. Herein, we leverage the excellent spatio-temporal precision of magnetoencephalographic (MEG) imaging to identify the spectral, spatial, and temporal effects of high-definition transcranial direct current stimulation (HD-tDCS) on the neural responses supporting motor control. Participants (N = 67) completed three HD-tDCS visits (anode, cathode, sham), with each involving 20 min of left primary motor cortex stimulation and performance of a simple/complex motor sequencing task during MEG. Whole-brain statistical analyses of beta oscillatory responses revealed stimulation-by-task interaction effects in the left primary motor cortex, right occipitotemporal, and the right dorsolateral prefrontal cortices. Broadly, anodal stimulation induced significantly stronger beta oscillatory responses in these regions during simple movement sequences, while neural responses to complex sequences were not affected by stimulation. En masse, these data suggest that the beta oscillations serving motor planning (i.e., pre-movement) are particularly sensitive to the polarity of noninvasive stimulation and that the impact varies based on the difficulty of the movement sequence.http://www.sciencedirect.com/science/article/pii/S1053811925000187Beta ERDMagnetoencephalographyPrimary motor cortexdlPFCMEGOscillations
spellingShingle Jake J. Son
Tara D. Erker
Thomas W. Ward
Yasra Arif
Peihan J. Huang
Jason A. John
Kellen M. McDonald
Nathan M. Petro
Grant M. Garrison
Hannah J. Okelberry
Kennedy A. Kress
Giorgia Picci
Elizabeth Heinrichs-Graham
Tony W. Wilson
The polarity of high-definition transcranial direct current stimulation affects the planning and execution of movement sequences
NeuroImage
Beta ERD
Magnetoencephalography
Primary motor cortex
dlPFC
MEG
Oscillations
title The polarity of high-definition transcranial direct current stimulation affects the planning and execution of movement sequences
title_full The polarity of high-definition transcranial direct current stimulation affects the planning and execution of movement sequences
title_fullStr The polarity of high-definition transcranial direct current stimulation affects the planning and execution of movement sequences
title_full_unstemmed The polarity of high-definition transcranial direct current stimulation affects the planning and execution of movement sequences
title_short The polarity of high-definition transcranial direct current stimulation affects the planning and execution of movement sequences
title_sort polarity of high definition transcranial direct current stimulation affects the planning and execution of movement sequences
topic Beta ERD
Magnetoencephalography
Primary motor cortex
dlPFC
MEG
Oscillations
url http://www.sciencedirect.com/science/article/pii/S1053811925000187
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