Effective corticospinal excitability neuromodulation elicited by short-duration concurrent and synchronized associative cortical and neuromuscular stimulations

Na Cao; Atsushi Sasaki; Akiko Yuasa; Milos R Popovic; Matija Milosevic; Kimitaka Nakazawa

doi:10.1016/j.neulet.2022.136910

Effective corticospinal excitability neuromodulation elicited by short-duration concurrent and synchronized associative cortical and neuromuscular stimulations

Neurosci Lett. 2022 Nov 1:790:136910. doi: 10.1016/j.neulet.2022.136910. Epub 2022 Oct 10.

Authors

Na Cao¹, Atsushi Sasaki², Akiko Yuasa³, Milos R Popovic⁴, Matija Milosevic⁵, Kimitaka Nakazawa⁶

Affiliations

¹ Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo 153-8902, Japan; Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo 102-0083, Japan.
² Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo 153-8902, Japan; Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo 102-0083, Japan; Department of Mechanical Science and Bioengineering, Graduate School of Engineering Science, Osaka University, 1-3 Machikaneyama, Toyonaka 560-8531, Japan.
³ Department of Rehabilitation Medicine I, Fujita Health University School of Medicine, 1-98 Dengakugakubo, Kutsukake-cho, Toyoake, Aichi 470-1192, Japan.
⁴ Institute of Biomedical Engineering, University of Toronto, 164 College Street, Toronto, Ontario M5S 3G9, Canada; KITE Research Institute, Toronto Rehabilitation Institute - University Health Network, 520 Sutherland Drive, Toronto, Ontario M4G 3V9, Canada; CRANIA, University Health Network & University of Toronto. 550 University Avenue, Toronto, Ontario M5G 2A2, Canada.
⁵ Department of Mechanical Science and Bioengineering, Graduate School of Engineering Science, Osaka University, 1-3 Machikaneyama, Toyonaka 560-8531, Japan. Electronic address: matija@ieee.org.
⁶ Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo 153-8902, Japan.

PMID: 36228774
DOI: 10.1016/j.neulet.2022.136910

Abstract

Optimal parameters of combined repetitive associative transcranial magnetic stimulation (rTMS) and neuromuscular electrical stimulation (NMES) for neuromodulation of central nervous system (CNS) excitability are not well understood. We examined corticospinal excitability after short-duration concurrent and synchronized associative stimulation applied using primary motor cortex rTMS and upper-limb NMES. Intermittent theta burst stimulation (iTBS) was delivered with burst at 50 Hz and repeated at 5 Hz over the course of 192 s as an established cortical facilitation rTMS protocol. NMES was applied to activate the extensor carpi radialis muscle over the same 192 s duration. Four interventions were compared: (1) iTBS with concurrent and synchronized 50 Hz NMES; (2) iTBS with concurrent and synchronized 5 Hz NMES; (3) iTBS with concurrent and asynchronized 41 Hz NMES; (4) iTBS with 5 s delayed and synchronized 50 Hz NMES. Single-pulse motor evoked potential (MEP) responses elicited by transcranial magnetic stimulation of the primary motor cortex and maximum motor responses (M_max) elicited by radial nerve stimulation were compared before and for 30 min after each intervention. Our results showed that corticospinal excitability (MEP/M_max) was only facilitated after the iTBS and concurrent 50 Hz NMES intervention, but the responses returned to baseline within 10 min of completing the intervention. This result demonstrates that short-duration concurrent and synchronized stimulation could be applied to effectively neuromodulate corticospinal excitability. Therefore, repetitive synchronized associative stimulation of the primary motor cortical networks and sensorimotor peripheral circuits may be enhanced using synchronized 50 Hz frequency of activation during concurrent stimulation.

Keywords: Associative; Corticospinal excitability; Neuromodulation; Neuromuscular electrical stimulation; Theta burst stimulation.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Evoked Potentials, Motor / physiology
Motor Cortex* / physiology
Muscle, Skeletal / physiology
Time Factors
Transcranial Magnetic Stimulation / methods