Effectiveness of motor and prefrontal cortical areas for brain-controlled functional electrical stimulation neuromodulation

Rizaldi A Fadli; Yuki Yamanouchi; Lazar I Jovanovic; Milos R Popovic; Cesar Marquez-Chin; Taishin Nomura; Matija Milosevic

doi:10.1088/1741-2552/acfa22

Effectiveness of motor and prefrontal cortical areas for brain-controlled functional electrical stimulation neuromodulation

J Neural Eng. 2023 Sep 26;20(5). doi: 10.1088/1741-2552/acfa22.

Authors

Rizaldi A Fadli^{1

2

3}, Yuki Yamanouchi¹, Lazar I Jovanovic^{4

5}, Milos R Popovic^{4

5

6}, Cesar Marquez-Chin^{4

5

6}, Taishin Nomura¹, Matija Milosevic^{1

2

3}

Affiliations

¹ Graduate School of Engineering Science, Department of Mechanical Science and Bioengineering, Osaka University, 1-3 Machikaneyama, Toyonaka 560-8531, Japan.
² Department of Biomedical Engineering, University of Miami College of Engineering, 1251 Memorial Drive, Coral Gables, FL 33146, United States of America.
³ The Miami Project to Cure Paralysis, Department of Neurological Surgery, University of Miami Miller School of Medicine, 1095 NW 14th Terrace, Miami, FL 33136, United States of America.
⁴ Institute of Biomedical Engineering, University of Toronto, 164 College Street, Toronto, Ontario M5S 3G9, Canada.
⁵ KITE Research Institute, Toronto Rehabilitation Institute-University Health Network, 520 Sutherland Drive, Toronto, Ontario M4G 3V9, Canada.
⁶ CRANIA, University Health Network & University of Toronto. 550 University Avenue, Toronto, Ontario M5G 2A2, Canada.

PMID: 37714143
DOI: 10.1088/1741-2552/acfa22

Abstract

Objective. Brain-computer interface (BCI)-controlled functional electrical stimulation (FES) could excite the central nervous system to enhance upper limb motor recovery. Our current study assessed the effectiveness of motor and prefrontal cortical activity-based BCI-FES to help elucidate the underlying neuromodulation mechanisms of this neurorehabilitation approach.Approach. The primary motor cortex (M1) and prefrontal cortex (PFC) BCI-FES interventions were performed for 25 min on separate days with twelve non-disabled participants. During the interventions, a single electrode from the contralateral M1 or PFC was used to detect event-related desynchronization (ERD) in the calibrated frequency range. If the BCI system detected ERD within 15 s of motor imagery, FES activated wrist extensor muscles. Otherwise, if the BCI system did not detect ERD within 15 s, a subsequent trial was initiated without FES. To evaluate neuromodulation effects, corticospinal excitability was assessed using single-pulse transcranial magnetic stimulation, and cortical excitability was assessed by motor imagery ERD and resting-state functional connectivity before, immediately, 30 min, and 60 min after each intervention.Main results. M1 and PFC BCI-FES interventions had similar success rates of approximately 80%, while the M1 intervention was faster in detecting ERD activity. Consequently, only the M1 intervention effectively elicited corticospinal excitability changes for at least 60 min around the targeted cortical area in the M1, suggesting a degree of spatial localization. However, cortical excitability measures did not indicate changes after either M1 or PFC BCI-FES.Significance. Neural mechanisms underlying the effectiveness of BCI-FES neuromodulation may be attributed to the M1 direct corticospinal projections and/or the closer timing between ERD detection and FES, which likely enhanced Hebbian-like plasticity by synchronizing cortical activation detected by the BCI system with the sensory nerve activation and movement related reafference elicited by FES.

Keywords: brain-computer interface; functional electrical stimulation; motor imagery; neuromodulation; upper limb.

Publication types

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

MeSH terms

Brain*
Central Nervous System
Electric Stimulation
Humans
Prefrontal Cortex*
Stereotaxic Techniques