TMS with fast and accurate electronic control: measuring the orientation sensitivity of corticomotor pathways

Victor Hugo Souza; Jaakko O. Nieminen; Sergei Tugin; Lari M. Koponen; Oswaldo Baffa; Risto J. Ilmoniemi

doi:10.1016/j.brs.2022.01.009

TMS with fast and accurate electronic control: measuring the orientation sensitivity of corticomotor pathways

Victor Hugo Souza^*, Jaakko O. Nieminen, Sergei Tugin, Lari M. Koponen, Oswaldo Baffa, Risto J. Ilmoniemi

^*Corresponding author for this work

Psychology

Research output: Contribution to journal › Article › peer-review

4 Citations (Scopus)

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Abstract

Background: Transcranial magnetic stimulation (TMS) coils allow only a slow, mechanical adjustment of the stimulating electric field (E-field) orientation in the cerebral tissue. Fast E-field control is needed to synchronize the stimulation with the ongoing brain activity. Also, empirical models that fully describe the relationship between evoked responses and the stimulus orientation and intensity are still missing.

Objective: We aimed to (1) develop a TMS transducer for manipulating the E-field orientation electronically with high accuracy at the neuronally meaningful millisecond-level time scale and (2) devise and validate a physiologically based model describing the orientation selectivity of neuronal excitability.

Methods: We designed and manufactured a two-coil TMS transducer. The coil windings were computed with a minimum-energy optimization procedure, and the transducer was controlled with our custom-made electronics. The electronic E-field control was verified with a TMS characterizer. The motor evoked potential amplitude and latency of a hand muscle were mapped in 3° steps of the stimulus orientation in 16 healthy subjects for three stimulation intensities. We fitted a logistic model to the motor response amplitude.

Results: The two-coil TMS transducer allows one to manipulate the pulse orientation accurately without manual coil movement. The motor response amplitude followed a logistic function of the stimulus orientation; this dependency was strongly affected by the stimulus intensity.

Conclusion: The developed electronic control of the E-field orientation allows exploring new stimulation paradigms and probing neuronal mechanisms. The presented model helps to disentangle the neuronal mechanisms of brain function and guide future non-invasive stimulation protocols.

Original language	English
Pages (from-to)	306-315
Number of pages	10
Journal	Brain stimulation
Volume	15
Issue number	2
Early online date	14 Jan 2022
DOIs	https://doi.org/10.1016/j.brs.2022.01.009
Publication status	Published - Mar 2022

Bibliographical note

Funding Information:
This research has received funding from the Academy of Finland (Decisions No. 255347 , 265680 , 294625 , and 306845 ), the Finnish Cultural Foundation , Jane and Aatos Erkko Foundation , Erasmus Mundus SMART2 (No. 552042-EM-1-2014-1-FR-ERA MUNDUSEMA2 ), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; grant number 140787/2014-3 ), the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme (grant agreement No 810377 ), and the Research, Innovation and Dissemination Center for Neuromathematics (FAPESP; grant number 2013/07699-0 ).

Publisher Copyright:
© 2022 The Authors

Keywords

Automated brain stimulation
Electric field
Motor evoked potential
Multi-coil TMS
Multi-locus TMS
Orientation sensitivity
Transcranial magnetic stimulation

ASJC Scopus subject areas

General Neuroscience
Biophysics
Clinical Neurology

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Cite this

@article{d0d93a27e28646ad847214dd12234258,

title = "TMS with fast and accurate electronic control: measuring the orientation sensitivity of corticomotor pathways",

abstract = "Background: Transcranial magnetic stimulation (TMS) coils allow only a slow, mechanical adjustment of the stimulating electric field (E-field) orientation in the cerebral tissue. Fast E-field control is needed to synchronize the stimulation with the ongoing brain activity. Also, empirical models that fully describe the relationship between evoked responses and the stimulus orientation and intensity are still missing. Objective: We aimed to (1) develop a TMS transducer for manipulating the E-field orientation electronically with high accuracy at the neuronally meaningful millisecond-level time scale and (2) devise and validate a physiologically based model describing the orientation selectivity of neuronal excitability. Methods: We designed and manufactured a two-coil TMS transducer. The coil windings were computed with a minimum-energy optimization procedure, and the transducer was controlled with our custom-made electronics. The electronic E-field control was verified with a TMS characterizer. The motor evoked potential amplitude and latency of a hand muscle were mapped in 3° steps of the stimulus orientation in 16 healthy subjects for three stimulation intensities. We fitted a logistic model to the motor response amplitude. Results: The two-coil TMS transducer allows one to manipulate the pulse orientation accurately without manual coil movement. The motor response amplitude followed a logistic function of the stimulus orientation; this dependency was strongly affected by the stimulus intensity. Conclusion: The developed electronic control of the E-field orientation allows exploring new stimulation paradigms and probing neuronal mechanisms. The presented model helps to disentangle the neuronal mechanisms of brain function and guide future non-invasive stimulation protocols.",

keywords = "Automated brain stimulation, Electric field, Motor evoked potential, Multi-coil TMS, Multi-locus TMS, Orientation sensitivity, Transcranial magnetic stimulation",

author = "Souza, {Victor Hugo} and Nieminen, {Jaakko O.} and Sergei Tugin and Koponen, {Lari M.} and Oswaldo Baffa and Ilmoniemi, {Risto J.}",

note = "Funding Information: This research has received funding from the Academy of Finland (Decisions No. 255347 , 265680 , 294625 , and 306845 ), the Finnish Cultural Foundation , Jane and Aatos Erkko Foundation , Erasmus Mundus SMART2 (No. 552042-EM-1-2014-1-FR-ERA MUNDUSEMA2 ), the Conselho Nacional de Desenvolvimento Cient{\'i}fico e Tecnol{\'o}gico (CNPq; grant number 140787/2014-3 ), the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme (grant agreement No 810377 ), and the Research, Innovation and Dissemination Center for Neuromathematics (FAPESP; grant number 2013/07699-0 ). Publisher Copyright: {\textcopyright} 2022 The Authors",

year = "2022",

month = mar,

doi = "10.1016/j.brs.2022.01.009",

language = "English",

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pages = "306--315",

journal = "Brain stimulation",

issn = "1935-861X",

publisher = "Elsevier",

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T1 - TMS with fast and accurate electronic control

T2 - measuring the orientation sensitivity of corticomotor pathways

AU - Souza, Victor Hugo

AU - Nieminen, Jaakko O.

AU - Tugin, Sergei

AU - Koponen, Lari M.

AU - Baffa, Oswaldo

AU - Ilmoniemi, Risto J.

N1 - Funding Information: This research has received funding from the Academy of Finland (Decisions No. 255347 , 265680 , 294625 , and 306845 ), the Finnish Cultural Foundation , Jane and Aatos Erkko Foundation , Erasmus Mundus SMART2 (No. 552042-EM-1-2014-1-FR-ERA MUNDUSEMA2 ), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; grant number 140787/2014-3 ), the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme (grant agreement No 810377 ), and the Research, Innovation and Dissemination Center for Neuromathematics (FAPESP; grant number 2013/07699-0 ). Publisher Copyright: © 2022 The Authors

PY - 2022/3

Y1 - 2022/3

N2 - Background: Transcranial magnetic stimulation (TMS) coils allow only a slow, mechanical adjustment of the stimulating electric field (E-field) orientation in the cerebral tissue. Fast E-field control is needed to synchronize the stimulation with the ongoing brain activity. Also, empirical models that fully describe the relationship between evoked responses and the stimulus orientation and intensity are still missing. Objective: We aimed to (1) develop a TMS transducer for manipulating the E-field orientation electronically with high accuracy at the neuronally meaningful millisecond-level time scale and (2) devise and validate a physiologically based model describing the orientation selectivity of neuronal excitability. Methods: We designed and manufactured a two-coil TMS transducer. The coil windings were computed with a minimum-energy optimization procedure, and the transducer was controlled with our custom-made electronics. The electronic E-field control was verified with a TMS characterizer. The motor evoked potential amplitude and latency of a hand muscle were mapped in 3° steps of the stimulus orientation in 16 healthy subjects for three stimulation intensities. We fitted a logistic model to the motor response amplitude. Results: The two-coil TMS transducer allows one to manipulate the pulse orientation accurately without manual coil movement. The motor response amplitude followed a logistic function of the stimulus orientation; this dependency was strongly affected by the stimulus intensity. Conclusion: The developed electronic control of the E-field orientation allows exploring new stimulation paradigms and probing neuronal mechanisms. The presented model helps to disentangle the neuronal mechanisms of brain function and guide future non-invasive stimulation protocols.

AB - Background: Transcranial magnetic stimulation (TMS) coils allow only a slow, mechanical adjustment of the stimulating electric field (E-field) orientation in the cerebral tissue. Fast E-field control is needed to synchronize the stimulation with the ongoing brain activity. Also, empirical models that fully describe the relationship between evoked responses and the stimulus orientation and intensity are still missing. Objective: We aimed to (1) develop a TMS transducer for manipulating the E-field orientation electronically with high accuracy at the neuronally meaningful millisecond-level time scale and (2) devise and validate a physiologically based model describing the orientation selectivity of neuronal excitability. Methods: We designed and manufactured a two-coil TMS transducer. The coil windings were computed with a minimum-energy optimization procedure, and the transducer was controlled with our custom-made electronics. The electronic E-field control was verified with a TMS characterizer. The motor evoked potential amplitude and latency of a hand muscle were mapped in 3° steps of the stimulus orientation in 16 healthy subjects for three stimulation intensities. We fitted a logistic model to the motor response amplitude. Results: The two-coil TMS transducer allows one to manipulate the pulse orientation accurately without manual coil movement. The motor response amplitude followed a logistic function of the stimulus orientation; this dependency was strongly affected by the stimulus intensity. Conclusion: The developed electronic control of the E-field orientation allows exploring new stimulation paradigms and probing neuronal mechanisms. The presented model helps to disentangle the neuronal mechanisms of brain function and guide future non-invasive stimulation protocols.

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TMS with fast and accurate electronic control: measuring the orientation sensitivity of corticomotor pathways

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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