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Benchtop and bedside validation of a low-cost programmable cortical stimulator in a testbed for bi-directional brain-computer-interface research

Sohn, Won Joon and Lim, Jeffrey and Wang, Po T. and Pu, Haoran and Malekzadeh-Arasteh, Omid and Shaw, Susan J. and Armacost, Michelle and Gong, Hui and Kellis, Spencer and Andersen, Richard A. and Liu, Charles Y. and Heydari, Payam and Nenadic, Zoran and Do, An H. (2023) Benchtop and bedside validation of a low-cost programmable cortical stimulator in a testbed for bi-directional brain-computer-interface research. Frontiers in Neuroscience, 16 . Art. No. 1075971. ISSN 1662-453X. PMCID PMC9878125. doi:10.3389/fnins.2022.1075971. https://resolver.caltech.edu/CaltechAUTHORS:20230213-466109600.28

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Abstract

Introduction: Bi-directional brain-computer interfaces (BD-BCI) to restore movement and sensation must achieve concurrent operation of recording and decoding of motor commands from the brain and stimulating the brain with somatosensory feedback. Methods: A custom programmable direct cortical stimulator (DCS) capable of eliciting artificial sensorimotor response was integrated into an embedded BCI system to form a safe, independent, wireless, and battery powered testbed to explore BD-BCI concepts at a low cost. The BD-BCI stimulator output was tested in phantom brain tissue by assessing its ability to deliver electrical stimulation equivalent to an FDA-approved commercial electrical cortical stimulator. Subsequently, the stimulator was tested in an epilepsy patient with subcortical electrocorticographic (ECoG) implants covering the sensorimotor cortex to assess its ability to elicit equivalent responses as the FDA-approved counterpart. Additional safety features (impedance monitoring, artifact mitigation, and passive and active charge balancing mechanisms) were also implemeneted and tested in phantom brain tissue. Finally, concurrent operation with interleaved stimulation and BCI decoding was tested in a phantom brain as a proof-of-concept operation of BD-BCI system. Results: The benchtop prototype BD-BCI stimulator's basic output features (current amplitude, pulse frequency, pulse width, train duration) were validated by demonstrating the output-equivalency to an FDA-approved commercial cortical electrical stimulator (R² > 0.99). Charge-neutral stimulation was demonstrated with pulse-width modulation-based correction algorithm preventing steady state voltage deviation. Artifact mitigation achieved a 64.5% peak voltage reduction. Highly accurate impedance monitoring was achieved with R² > 0.99 between measured and actual impedance, which in-turn enabled accurate charge density monitoring. An online BCI decoding accuracy of 93.2% between instructional cues and decoded states was achieved while delivering interleaved stimulation. The brain stimulation mapping via ECoG grids in an epilepsy patient showed that the two stimulators elicit equivalent responses. Significance: This study demonstrates clinical validation of a fully-programmable electrical stimulator, integrated into an embedded BCI system. This low-cost BD-BCI system is safe and readily applicable as a testbed for BD-BCI research. In particular, it provides an all-inclusive hardware platform that approximates the limitations in a near-future implantable BD-BCI. This successful benchtop/human validation of the programmable electrical stimulator in a BD-BCI system is a critical milestone toward fully-implantable BD-BCI systems.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.3389/fnins.2022.1075971DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc9878125/PubMed CentralArticle
ORCID:
AuthorORCID
Sohn, Won Joon0000-0002-0992-4555
Lim, Jeffrey0000-0003-4775-1867
Wang, Po T.0000-0002-6611-3863
Pu, Haoran0000-0002-6787-5907
Malekzadeh-Arasteh, Omid0000-0003-2481-7077
Gong, Hui0000-0001-5519-6248
Kellis, Spencer0000-0002-5158-1058
Andersen, Richard A.0000-0002-7947-0472
Liu, Charles Y.0000-0001-6423-8577
Heydari, Payam0000-0002-1008-1559
Nenadic, Zoran0000-0001-5569-3797
Additional Information:© 2023 Sohn, Lim, Wang, Pu, Malekzadeh-Arasteh, Shaw, Armacost, Gong, Kellis, Andersen, Liu, Heydari, Nenadic and Do. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. This study was supported by the National Science Foundation awards 1646275. We acknowledge the contribution from the participants in this study. Data availability statement. The datasets presented in this article are not readily available because the human data from the participant of this study may not be disclosed to the public. However, the benchtop analysis data may be available upon reasonable request. Requests to access the datasets should be directed to ude.icu@dna. Ethics statement. The studies involving human participants were reviewed and approved by Ethics Committee is UCI and Rancho IRB. The patients/participants provided their written informed consent to participate in this study. Author contributions. WS, PW, CL, RA, HP, ZN, and AD conceived and designed the study. WS, PW, JL, and AD developed the software and hardware of the BD-BCI system. WS, PW, and JL performed the benchtop tests and data analysis. WS, JL, PW, SS, MA, HG, and AD conducted the bedside tests. WS drafted the manuscript. AD critically reviewed the manuscript. All authors reviewed and approved the final manuscript.
Group:Tianqiao and Chrissy Chen Institute for Neuroscience
Funders:
Funding AgencyGrant Number
NSFCNS-1646275
PubMed Central ID:PMC9878125
DOI:10.3389/fnins.2022.1075971
Record Number:CaltechAUTHORS:20230213-466109600.28
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20230213-466109600.28
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:119251
Collection:CaltechAUTHORS
Deposited By: Research Services Depository
Deposited On:23 Mar 2023 23:47
Last Modified:23 Mar 2023 23:47

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