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Home Use of a Percutaneous Wireless Intracortical Brain-Computer Interface by Individuals with Tetraplegia

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This article has been accepted for publication in a future issue of this journal, but has not been fully edited. Content may change prior to final publication. Citation information: DOI 10.1109/TBME.2021.3069119, IEEE Transactions on Biomedical Engineering TBME-00114-2020.R1 Home Use of a Percutaneous Wireless Intracortical Brain-Computer Interface by Individuals With Tetraplegia John D. Simeral*, Senior Member, IEEE, Thomas Hosman, Jad Saab, Sharlene N. Flesher, Marco Vilela, Brian Franco, Jessica Kelemen, David M. Brandman, John G. Ciancibello, Paymon G. Rezaii, Emad N. Eskandar, David M. Rosler, Krishna V. Shenoy§, Senior Member, IEEE, Jaimie M. Henderson§, Arto V. Nurmikko, Fellow, IEEE, and Leigh R. Hochberg Abstract—Objective. Individuals with neurological disease or completed on-screen item selection tasks to assess iBCI-enabled injury such as amyotrophic lateral sclerosis, spinal cord injury or cursor control. Results: Communication bitrates were equivalent stroke may become tetraplegic, unable to speak or even locked-in. between cabled and wireless configurations. Participants also used For people with these conditions, current assistive technologies are the wireless iBCI to control a standard commercial tablet often ineffective. Brain-computer interfaces are being developed computer to browse the web and use several mobile applications. to enhance independence and restore communication in the Within-day comparison of cabled and wireless interfaces absence of physical movement. Over the past decade, individuals evaluated bit error rate, packet loss, and the recovery of spike with tetraplegia have achieved rapid on-screen typing and point- rates and spike waveforms from the recorded neural signals. In a and-click control of tablet apps using intracortical brain-computer representative use case, the wireless system recorded intracortical interfaces (iBCIs) that decode intended arm and hand movements signals from two arrays in one participant continuously through a from neural signals recorded by implanted microelectrode arrays. 24-hour period at home. Significance. Wireless multi-electrode However, cables used to convey neural signals from the brain recording of broadband neural signals over extended periods tether participants to amplifiers and decoding computers and introduces a valuable tool for human neuroscience research and is require expert oversight, severely limiting when and where iBCIs an important step toward practical deployment of iBCI technology could be available for use. Here, we demonstrate the first human for independent use by individuals with paralysis. On-demand use of a wireless broadband iBCI. Methods. Based on a prototype access to high-performance iBCI technology in the home promises system previously used in pre-clinical research, we replaced the to enhance independence and restore communication and mobility external cables of a 192-electrode iBCI with wireless transmitters for individuals with severe motor impairment.1 and achieved high-resolution recording and decoding of broadband field potentials and spiking activity from people with Index Terms—Brain-computer interface, clinical trial, motor paralysis. Two participants in an ongoing pilot clinical trial cortex, neural engineering, wireless transmitter 1Manuscript received January 20, 2020; revised November 13, 2020; J. G. Ciancibello was with the School of Engineering, Brown University. He accepted February 19, 2021. is now with the Center for Bioelectronic Medicine at the Feinstein Institute for This work was supported in part by NIH-NINDS UH2NS095548; the Office Medical Research, Manhasset, NY. of Research and Development, Rehab. R&D Service, Department of Veterans P. G. Rezaii was with the Department of Neurosurgery, Stanford University. Affairs (N9228C, N2864C, A2295R, B6453R, P1155R); NIH-NIDCD He is now with the School of Medicine, Tulane University. R01DC009899, R01DC014034; NIH-NIBIB R01EB007401; The Executive E. Eskandar was with the Department of Neurosurgery, Massachusetts Committee on Research (ECOR) of Massachusetts General Hospital; Conquer General Hospital. He is now with the Department of Neurosurgery, Albert Paralysis Now 004698; MGH-Deane Institute; DARPA REPAIR; Wu Tsai Einstein College of Medicine, Montefiore Medical Center, NY. Neurosciences Institute at Stanford; Larry and Pamela Garlick; Samuel and D. M. Rosler is with CfNN and the School of Engineering and the Robert J. Betsy Reeves; The Howard Hughes Medical Institute at Stanford University. & Nancy D. Carney Institute for Brain Science, Brown University, and also *J. D. Simeral is with the Center for Neurorestoration and Neurotechnology, with the Department of Neurology, Massachusetts General Hospital. Rehabilitation R&D Service, Department of Veterans Affairs Medical Center, K. V. Shenoy is with the Departments of Electrical Engineering, Providence, RI 02908 USA (CfNN) and with the School of Engineering and the Bioengineering and Neurobiology, Wu Tsai Neurosciences Institute, and the Robert J. & Nancy D. Carney Institute for Brain Science, Brown University, Bio-X Institute, Stanford, and also with the Howard Hughes Medical Institute, Providence, RI (e-mail: [email protected]). Stanford University. T. Hosman is with CfNN and the School of Engineering, Brown University. J. M. Henderson is with the Department of Neurosurgery and Wu Tsai J. Saab was with CfNN and the School of Engineering, Brown University. Neurosciences Institute and the Bio-X Institute, Stanford University. He is now with Insight Data Science, New York City, NY. A. V. Nurmikko is with the School of Engineering, Department of Physics, S. N. Flesher was with the Department of Electrical Engineering, and the Robert J. & Nancy D. Carney Institute for Brain Science, Brown Department of Neurosurgery, and Howard Hughes Medical Institute, Stanford University. University. She is now with Apple Inc., Cupertino, CA. L. R. Hochberg is with CfNN, and the School of Engineering and the Robert M. Vilela was with the School of Engineering, Brown University. He is now J. & Nancy D. Carney Institute for Brain Science, Brown University, and the with Takeda, Cambridge, MA. Center for Neurotechnology and Neurorecovery, Department of Neurology, B. Franco was with the Department of Neurology, Massachusetts General Massachusetts General Hospital, Harvard Medical School. Hospital, Boston, MA. He is now with NeuroPace Inc., Mountain View, CA. § K. V. Shenoy and J. M. Henderson contributed equally to this work J. Kelemen is with the Department of Neurology, Massachusetts General This paper has supplementary downloadable material available at Hospital, Boston. http://ieeexplore.ieee.org. D. Brandman was with the School of Engineering, Brown University. He is now with the Department of Neurosurgery, Emory University, Atlanta, GA. Copyright (c) 2021 IEEE. Personal use of this material is permitted. However, permission to use this material for any other purposes must be obtained from the IEEE by sending an email to [email protected]. This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License. For more information, see https://creativecommons.org/licenses/by-nc-nd/4.0/ This article has been accepted for publication in a future issue of this journal, but has not been fully edited. Content may change prior to final publication. Citation information: DOI 10.1109/TBME.2021.3069119, IEEE Transactions on Biomedical Engineering TBME-00114-2020.R1 - SIMERAL et al.: HOME USE OF A PERCUTANEOUS WIRELESS iBCI 2 I. INTRODUCTION methods for high-performance iBCI systems. EUROLOGICAL disease or injury such as amyotrophic Here we report translation of a wireless broadband N lateral sclerosis, stroke and cervical spinal cord injury intracortical BCI system to human use and evaluate its (SCI) can result in tetraplegia, loss of speech or locked-in performance during use at home by two participants in the syndrome. Brain-computer interfaces (BCIs) are being BrainGate pilot clinical trial. The external transmitter developed to restore communication and motor function for underwent commercial manufacturing and preclinical safety individuals living with profound motor disability. Motor BCIs testing in preparation for human investigational use. aim to provide access to assistive devices by decoding user Transmission frequency was configurable such that neural commands from a variety of sources including activity from two 96-channel intracortical arrays could be electroencephalography (EEG), electrocorticography (ECoG), recorded simultaneously without interference. Two transmitters or intracortical signals. In ongoing clinical research, high- and associated commercial receiver hardware were integrated performance intracortical BCIs (iBCIs) are being developed to into the iBCI real-time signal processing system. Both infer a user’s movement intentions [1]–[8] or speech [9], [10] participants then used the BrainGate system to complete a series from neural activity recorded from one or more microelectrode of cursor-based point-and-dwell assessment tasks [1], [7], [28] arrays implanted in motor areas of cortex. By imagining natural to quantify iBCI performance in cabled and wireless hand, finger and arm movements, trial participants with configurations. We demonstrate that the wireless signals could paralysis have achieved reach-and grasp with robotic and be decoded with sufficient quality and reliability to support prosthetic limbs [2], [3], [11] and their own reanimated limb spontaneous user-paced
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