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      Brain-Computer interface control of stepping from invasive electrocorticography upper-limb motor imagery in a patient with quadriplegia

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          Abstract

          Introduction: Most spinal cord injuries (SCI) result in lower extremities paralysis, thus diminishing ambulation. Using brain-computer interfaces (BCI), patients may regain leg control using neural signals that actuate assistive devices. Here, we present a case of a subject with cervical SCI with an implanted electrocorticography (ECoG) device and determined whether the system is capable of motor-imagery-initiated walking in an assistive ambulator.

          Methods: A 24-year-old male subject with cervical SCI (C5 ASIA A) was implanted before the study with an ECoG sensing device over the sensorimotor hand region of the brain. The subject used motor-imagery (MI) to train decoders to classify sensorimotor rhythms. Fifteen sessions of closed-loop trials followed in which the subject ambulated for one hour on a robotic-assisted weight-supported treadmill one to three times per week. We evaluated the stability of the best-performing decoder over time to initiate walking on the treadmill by decoding upper-limb (UL) MI.

          Results: An online bagged trees classifier performed best with an accuracy of 84.15% averaged across 9 weeks. Decoder accuracy remained stable following throughout closed-loop data collection.

          Discussion: These results demonstrate that decoding UL MI is a feasible control signal for use in lower-limb motor control. Invasive BCI systems designed for upper-extremity motor control can be extended for controlling systems beyond upper extremity control alone. Importantly, the decoders used were able to use the invasive signal over several weeks to accurately classify MI from the invasive signal. More work is needed to determine the long-term consequence between UL MI and the resulting lower-limb control.

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            Nearest neighbor pattern classification

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              Restoring cortical control of functional movement in a human with quadriplegia.

              Millions of people worldwide suffer from diseases that lead to paralysis through disruption of signal pathways between the brain and the muscles. Neuroprosthetic devices are designed to restore lost function and could be used to form an electronic 'neural bypass' to circumvent disconnected pathways in the nervous system. It has previously been shown that intracortically recorded signals can be decoded to extract information related to motion, allowing non-human primates and paralysed humans to control computers and robotic arms through imagined movements. In non-human primates, these types of signal have also been used to drive activation of chemically paralysed arm muscles. Here we show that intracortically recorded signals can be linked in real-time to muscle activation to restore movement in a paralysed human. We used a chronically implanted intracortical microelectrode array to record multiunit activity from the motor cortex in a study participant with quadriplegia from cervical spinal cord injury. We applied machine-learning algorithms to decode the neuronal activity and control activation of the participant's forearm muscles through a custom-built high-resolution neuromuscular electrical stimulation system. The system provided isolated finger movements and the participant achieved continuous cortical control of six different wrist and hand motions. Furthermore, he was able to use the system to complete functional tasks relevant to daily living. Clinical assessment showed that, when using the system, his motor impairment improved from the fifth to the sixth cervical (C5-C6) to the seventh cervical to first thoracic (C7-T1) level unilaterally, conferring on him the critical abilities to grasp, manipulate, and release objects. This is the first demonstration to our knowledge of successful control of muscle activation using intracortically recorded signals in a paralysed human. These results have significant implications in advancing neuroprosthetic technology for people worldwide living with the effects of paralysis.
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                Author and article information

                Contributors
                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                09 January 2023
                2022
                : 16
                : 1077416
                Affiliations
                [1] 1Department of Neurological Surgery, University of Pennsylvania , Philadelphia, PA, United States
                [2] 2Department of Biomedical Engineering, University of Miami , Miami, FL, United States
                [3] 3Department of Electrical and Information Engineering, University of Ruhana , Hapugala, Sri Lanka
                [4] 4Department of Neurological Surgery, University of Miami , Miami, FL, United States
                [5] 5Miami Project to Cure Paralysis, University of Miami , Miami, FL, United States
                Author notes

                Edited by: Malik Muhammad Naeem Mannan, Griffith University, Australia

                Reviewed by: Zeshan Shoaib, Pusan National University, South Korea; Amad Zafar, Sejong University, South Korea; Usman Ghafoor, Pusan National University, South Korea

                These authors have contributed equally to this work

                Specialty section: This article was submitted to Brain-Computer Interfaces, a section of the journal Frontiers in Human Neuroscience

                Article
                10.3389/fnhum.2022.1077416
                9912159
                36776220
                4372c077-3ab1-4bcd-a0dd-0c31ac565b08
                Copyright © 2023 Cajigas, Davis, Prins, Gallo, Naeem, Fisher, Ivan, Prasad and Jagid.

                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.

                History
                : 22 October 2022
                : 19 December 2022
                Page count
                Figures: 4, Tables: 0, Equations: 2, References: 49, Pages: 10, Words: 83901
                Funding
                Funded by: National Institute of Neurological Disorders and Stroke, doi 10.13039/100000065;
                Award ID: R25NS108937-02
                Supported by a private institutional grant from the Miami Project to Cure Paralysis. The Implanted device was donated by Medtronic. Medtronic provided all components of the implant including the external antenna/receiver free of charge to the University of Miami but did not provide funds directly to the institution, the researchers, or the patient. IC was supported in part by National Institutes of Health/National Institute of Neurological Disorders and Stroke (R25NS108937-02).
                Categories
                Human Neuroscience
                Brief Research Report

                Neurosciences
                brain-computer interface,electrocorticography,spinal cord injury,gait,lower-extremity

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