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

ABSTRACT: BACKGROUND:People with chronic tetraplegia, due to high-cervical spinal cord injury, 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 unrelated and limited in number, volitional movements (eg, facial muscle activity, head movements, shoulder shrugs). We report the findings of an individual with traumatic high-cervical spinal cord injury who coordinated reaching and grasping movements using his own paralysed arm and hand, reanimated through implanted FES, and commanded using his own cortical signals through an intracortical brain-computer interface (iBCI). METHODS:We recruited a participant into the BrainGate2 clinical trial, an ongoing study that obtains safety information regarding an intracortical neural interface device, and investigates the feasibility of people with tetraplegia controlling assistive devices using their cortical signals. Surgical procedures were performed at University Hospitals Cleveland Medical Center (Cleveland, OH, USA). Study procedures and data analyses were performed at Case Western Reserve University (Cleveland, OH, USA) and the US Department of Veterans Affairs, Louis Stokes Cleveland Veterans Affairs Medical Center (Cleveland, OH, USA). The study participant was a 53-year-old man with a spinal cord injury (cervical level 4, American Spinal Injury Association Impairment Scale category A). He received two intracortical microelectrode arrays in the hand area of his motor cortex, and 4 months and 9 months later received a total of 36 implanted percutaneous electrodes in his right upper and lower arm to electrically stimulate his hand, elbow, and shoulder muscles. The participant used a motorised mobile arm support for gravitational assistance and to provide humeral abduction and adduction under cortical control. We assessed the participant's ability to cortically command his paralysed arm to perform simple single-joint arm and hand movements and functionally meaningful multi-joint movements. We compared iBCI control of his paralysed arm with that of a virtual three-dimensional arm. This study is registered with ClinicalTrials.gov, number NCT00912041. FINDINGS:The intracortical implant occurred on Dec 1, 2014, and we are continuing to study the participant. The last session included in this report was Nov 7, 2016. The point-to-point target acquisition sessions began on Oct 8, 2015 (311 days after implant). 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 paralysed arm, the participant volitionally performed self-paced reaches to drink a mug of coffee (successfully completing 11 of 12 attempts within a single session 463 days after implant) and feed himself (717 days after implant). INTERPRETATION:To our knowledge, this is the first report of a combined implanted FES+iBCI neuroprosthesis for restoring both reaching and grasping movements to people with chronic tetraplegia due to spinal cord injury, and represents a major advance, with a clear translational path, for clinically viable neuroprostheses for restoration of reaching and grasping after paralysis. FUNDING:National Institutes of Health, Department of Veterans Affairs.

SUBMITTER: Ajiboye AB

PROVIDER: S-EPMC5516547 | biostudies-literature | 2017 May

REPOSITORIES: biostudies-literature

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

Ajiboye A Bolu AB Willett Francis R FR Young Daniel R DR Memberg William D WD Murphy Brian A BA Miller Jonathan P JP Walter Benjamin L BL Sweet Jennifer A JA Hoyen Harry A HA Keith Michael W MW Peckham P Hunter PH Simeral John D JD Donoghue John P JP Hochberg Leigh R LR Kirsch Robert F RF

Lancet (London, England) 20170328 10081

<h4>Background</h4>People with chronic tetraplegia, due to high-cervical spinal cord injury, 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 unrelated and limited in number, volitional movements (eg, facial muscle activity, head movements, shoulder shrugs). We report the findings of an individual with traumatic high-cervical spi ...[more]

PMID: 28363483

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Project description:BACKGROUND:We hypothesized that a selective neural electrical stimulation of radial and median nerves enables the activation of functional movements in the paralyzed hand of individuals with tetraplegia. Compared to previous approaches for which up to 12 muscles were targeted through individual muscular stimulations, we focused on minimizing the number of implanted electrodes however providing almost all the needed and useful hand movements for subjects with complete tetraplegia. METHODS:We performed acute experiments during scheduled surgeries of the upper limb with eligible subjects. We scanned a set of multicontact neural stimulation cuff electrode configurations, pre-computed through modeling simulations. We reported the obtained isolated and functional movements that were considered useful for the subject (different grasping movements). RESULTS:In eight subjects, we demonstrated that selective stimulation based on multicontact cuff electrodes and optimized current spreading over the active contacts provided isolated, compound, functional and strong movements; most importantly 3 out of 4 had isolated fingers or thumb flexion, one patient performed a Key Grip, another one the Power and Hook Grips, and the 2 last all the 3 Grips. Several configurations were needed to target different areas within the nerve to obtain all the envisioned movements. We further confirmed that the upper limb nerves have muscle specific fascicles, which makes it possible to activate isolated movements. CONCLUSIONS:The future goal is to provide patients with functional restoration of object grasping and releasing with a minimally invasive solution: only two cuff electrodes above the elbow. Ethics Committee / ANSM clearance prior to the beginning of the study (inclusion period 2016-2018): CPP Sud Méditerranée, #ID-RCB:2014-A01752-45, first acceptance 10th of February 2015, amended 12th of January 2016. TRIAL REGISTRATION:(www.clinicaltrials.gov): #NCT03721861, Retrospectively registered on 26th of October 2018.

Project description:BACKGROUND:Active upper-limb prostheses are used to restore important hand functionalities, such as grasping. In conventional approaches, a pattern recognition system is trained over a number of static grasping gestures. However, training a classifier in a static position results in lower classification accuracy when performing dynamic motions, such as reach-to-grasp. We propose an electromyography-based learning approach that decodes the grasping intention during the reaching motion, leading to a faster and more natural response of the prosthesis. METHODS AND RESULTS:Eight able-bodied subjects and four individuals with transradial amputation gave informed consent and participated in our study. All the subjects performed reach-to-grasp motions for five grasp types, while the elecromyographic (EMG) activity and the extension of the arm were recorded. We separated the reach-to-grasp motion into three phases, with respect to the extension of the arm. A multivariate analysis of variance (MANOVA) on the muscular activity revealed significant differences among the motion phases. Additionally, we examined the classification performance on these phases. We compared the performance of three different pattern recognition methods; Linear Discriminant Analysis (LDA), Support Vector Machines (SVM) with linear and non-linear kernels, and an Echo State Network (ESN) approach. Our off-line analysis shows that it is possible to have high classification performance above 80% before the end of the motion when with three-grasp types. An on-line evaluation with an upper-limb prosthesis shows that the inclusion of the reaching motion in the training of the classifier importantly improves classification accuracy and enables the detection of grasp intention early in the reaching motion. CONCLUSIONS:This method offers a more natural and intuitive control of prosthetic devices, as it will enable controlling grasp closure in synergy with the reaching motion. This work contributes to the decrease of delays between the user's intention and the device response and improves the coordination of the device with the motion of the arm.

Dataset Information

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

Publications

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

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