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      Restoration of reaching and grasping in a person with tetraplegia through brain-controlled muscle stimulation: a proof-of-concept demonstration

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          SUMMARY

          Background

          People with chronic tetraplegia due to high cervical spinal cord injury (SCI) can regain limb movements through coordinated electrical stimulation of peripheral muscles and nerves, known as Functional Electrical Stimulation (FES). Users typically command FES systems through other preserved, but limited and unrelated, volitional movements (e.g. facial muscle activity, head movements). We demonstrate an individual with traumatic high cervical SCI performing coordinated reaching and grasping movements using his own paralyzed arm and hand, reanimated through FES, and commanded using his own cortical signals through an intracortical brain-computer-interface (iBCI).

          Methods

          The study participant (53 years old, C4, ASIA A) received two intracortical microelectrode arrays in the hand area of motor cortex, and 36 percutaneous electrodes for electrically stimulating hand, elbow, and shoulder muscles. The participant used a motorized mobile arm support for gravitational assistance and to provide humeral ab/adduction under cortical control. We assessed the participant’s ability to cortically command his paralyzed arm to perform simple single-joint arm/hand movements and functionally meaningful multi-joint movements. We compared iBCI control of his paralyzed arm to that of a virtual 3D arm. This study is registered with ClinicalTrials.gov, NCT00912041.

          Findings

          The participant successfully cortically commanded single-joint and coordinated multi-joint arm movements for point-to-point target acquisitions (80% – 100% accuracy) using first a virtual arm, and second his own arm animated by FES. Using his paralyzed arm, the participant volitionally performed self-paced reaches to drink a mug of coffee (successfully completing 11 of 12 attempts within a single session) and feed himself.

          Interpretation

          This is the first demonstration of a combined FES+iBCI neuroprosthesis for both reaching and grasping for people with SCI resulting in chronic tetraplegia, and represents a major advance, with a clear translational path, for clinically viable neuroprostheses for restoring reaching and grasping post-paralysis.

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          Most cited references25

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          High-performance neuroprosthetic control by an individual with tetraplegia.

          Paralysis or amputation of an arm results in the loss of the ability to orient the hand and grasp, manipulate, and carry objects, functions that are essential for activities of daily living. Brain-machine interfaces could provide a solution to restoring many of these lost functions. We therefore tested whether an individual with tetraplegia could rapidly achieve neurological control of a high-performance prosthetic limb using this type of an interface. We implanted two 96-channel intracortical microelectrodes in the motor cortex of a 52-year-old individual with tetraplegia. Brain-machine-interface training was done for 13 weeks with the goal of controlling an anthropomorphic prosthetic limb with seven degrees of freedom (three-dimensional translation, three-dimensional orientation, one-dimensional grasping). The participant's ability to control the prosthetic limb was assessed with clinical measures of upper limb function. This study is registered with ClinicalTrials.gov, NCT01364480. The participant was able to move the prosthetic limb freely in the three-dimensional workspace on the second day of training. After 13 weeks, robust seven-dimensional movements were performed routinely. Mean success rate on target-based reaching tasks was 91·6% (SD 4·4) versus median chance level 6·2% (95% CI 2·0-15·3). Improvements were seen in completion time (decreased from a mean of 148 s [SD 60] to 112 s [6]) and path efficiency (increased from 0·30 [0·04] to 0·38 [0·02]). The participant was also able to use the prosthetic limb to do skilful and coordinated reach and grasp movements that resulted in clinically significant gains in tests of upper limb function. No adverse events were reported. With continued development of neuroprosthetic limbs, individuals with long-term paralysis could recover the natural and intuitive command signals for hand placement, orientation, and reaching, allowing them to perform activities of daily living. Defense Advanced Research Projects Agency, National Institutes of Health, Department of Veterans Affairs, and UPMC Rehabilitation Institute. Copyright © 2013 Elsevier Ltd. All rights reserved.
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            Direct cortical control of 3D neuroprosthetic devices.

            Three-dimensional (3D) movement of neuroprosthetic devices can be controlled by the activity of cortical neurons when appropriate algorithms are used to decode intended movement in real time. Previous studies assumed that neurons maintain fixed tuning properties, and the studies used subjects who were unaware of the movements predicted by their recorded units. In this study, subjects had real-time visual feedback of their brain-controlled trajectories. Cell tuning properties changed when used for brain-controlled movements. By using control algorithms that track these changes, subjects made long sequences of 3D movements using far fewer cortical units than expected. Daily practice improved movement accuracy and the directional tuning of these units.
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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

                Journal
                2985213R
                5470
                Lancet
                Lancet
                Lancet (London, England)
                0140-6736
                1474-547X
                18 May 2017
                28 March 2017
                06 May 2017
                06 May 2018
                : 389
                : 10081
                : 1821-1830
                Affiliations
                [1 ]Department of Biomedical Engineering, Case Western Reserve University, 10900 Euclid Ave, Cleveland, Ohio, 44106, USA
                [2 ]Louis Stokes Cleveland Department of Veterans Affairs Medical Center, FES Center of Excellence, Rehab. R&D Service, 10701 East Blvd, Cleveland, Ohio, 44106, USA
                [3 ]Department of Neurology, University Hospitals Case Medical Center, 11100 Euclid Ave, Cleveland, Ohio, 44106, USA
                [4 ]Department of Neurological Surgery, University Hospitals Case Medical Center, 11100 Euclid Ave, Cleveland, Ohio, 44106, USA
                [5 ]Department of Orthopaedics, MetroHealth Medical Center, 2500 MetroHealth Drive, Cleveland, Ohio, 44109, USA
                [6 ]School of Medicine, Case Western Reserve University, 10900 Euclid Ave, Cleveland, Ohio, 44106, USA
                [7 ]School of Engineering, Brown University, 2 Stimson Avenue, Providence, Rhode Island, 02912, USA
                [8 ]Center for Neurorestoration and Neurotechnology, Rehabilitation R&D Service, Department of Veterans Affairs Medical Center, 830 Chalkstone Ave, Providence, Rhode Island, 02908, USA
                [9 ]Brown Institute for Brain Science, Brown University, 2 Stimson Avenue, Providence, Rhode Island, 02912, USA
                [10 ]Department of Neurology, Massachusetts General Hospital, 55 Fruit Street, Boston, Massachusetts, 02114, USA
                [11 ]Department of Neurology, Harvard Medical School, 25 Shattuck Street, Boston, Massachusetts, 02115, USA
                [12 ]Department of Neuroscience, Brown University, 2 Stimson Avenue, Providence, Rhode Island, 02912, USA
                Author notes
                []Corresponding Author: A. Bolu Ajiboye, PhD, Department of Biomedical Engineering, Case Western Reserve University, 10900 Euclid Ave, Cleveland, Ohio, 44106, USA., Telephone: +1.216.368.6814, aba20@ 123456case.edu
                [*]

                Contributed equally.

                [§]

                Full Professor.

                Article
                NIHMS865513
                10.1016/S0140-6736(17)30601-3
                5516547
                28363483
                8ce81eea-1ba7-42f9-99a7-ca26fec1ba10

                This manuscript version is made available under the CC BY-NC-ND 4.0 license.

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                Medicine
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