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Clinical Trial
, 389 (10081), 1821-1830

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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Clinical Trial

Restoration of Reaching and Grasping Movements Through Brain-Controlled Muscle Stimulation in a Person With Tetraplegia: A Proof-Of-Concept Demonstration

A Bolu Ajiboye et al. Lancet.

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.

Conflict of interest statement

Declarations and Conflicts of Interest

No author has any declarations or conflicts of interest to report.

Figures

Figure 1
Figure 1
Overview of the FES+iBCI System. (A) Neural activity is recorded from two microelectrode arrays implanted in the motor cortex. The recorded activity is then decoded into command signals that control the stimulation of biceps, triceps, forearm, and hand muscles, as well as the actuation of a mobile arm support (MAS), to enable cortical control of whole arm movements. Muscle stimulation was performed through percutaneous intramuscular fine-wire electrodes, and instrumented goniometers (Biometrics Ltd.-US, Ladysmith, VA) quantified the resultant wrist, elbow, and hand aperture movements, while an orientation sensor quantified MAS movements. (B) Simulation patterns convert the decoded command signals into the appropriate pulse widths to apply to each individual FES electrode, enabling the participant to coordinate the action of multiple electrodes and muscles using only a single command. Example stimulation patterns for the elbow, wrist, and hand are shown; supplementary Figure 8 illustrates how a stimulation pattern controls the angle of a joint.
Figure 2
Figure 2
Session overview. (A) Timeline of implants and experimental sessions. All days are referenced to the day of cortical implant (December 1, 2014 – 0 Days Post Implant). (B) Example image from the virtual reality game. The virtual arm is opaque while the target arm configuration (wrist flexion in this case) is translucent. (C) During the VR vs. FES comparison sessions, the participant completed three different experimental conditions. Block diagrams of each condition and an example session timeline are shown. (D) Example raster plots showing the timing of threshold crossings (top rows) and the average threshold crossing rates (bottom row) of a single channel tuned to wrist flexion and extension during a single-joint wrist movement task. The dotted line at t=0 indicates the presentation of the target movement. This channel records more threshold crossings when flexion targets are presented and has similar tuning properties during all three experimental conditions.
Figure 3
Figure 3
Single-joint FES and mobile arm support (MAS) movements under real-time brain control. (A) (1st column) Restored arm and hand movements and achievable ranges of motion. Line drawings are made from actual photographs of restored movements, and show complete range of restored motion. (2nd–4th columns) Overlaid time series of joint motions towards each target (columns) during an example block of each movement (rows). Each line illustrates a single movement from the example FES block (blue) or virtual reality block (pink). Gray rectangles illustrate the target and the tolerance allowed for target acquisition. Target distances (from the flexion to extension target) and allowed tolerances (widths) were 43.4°±6.0° (elbow), 24°±3.4° (wrist), 35.8°±5.8° (hand), and 41.3°±5.1° (MAS). The participant was in full control of the joint at all times (the joint position was not reset after a target was acquired). Example blocks with high success rates were chosen for illustration. (B) Success rate and average movement time is summarized for each FES block (circles). Circles are different colors if they occurred on different days. Average virtual reality performance (blue dotted line) and chance performance (red dotted line) are shown for reference. Supplementary Table 4 gives a more detailed quantification with accompanying statistical tests.
Figure 4
Figure 4
The participant using the FES+iBCI system to take a drink of coffee. (A) He reached out to grasp the cup of coffee (left) and bringing it to his mouth to take a drink through a straw (right). Photos taken on trial day 392 (2015.12.28). (B) The length of time it took to complete each phase of the drinking task. Data is shown for 12 trials completed within a single experimental session; only one trial was failed when the cup was dropped. (C) Example time series of elbow and hand motion when the FES+iBCI system was turned on (left) and when the FES system was turned off (right). When the system was on, the decoded neural commands (blue) and the elbow and hand joint angles (orange) changed appropriately as the participant moved through the phases of the task, enabling him to take a drink of coffee. When the system was off, he could only make small, uncontrolled elbow jerks caused by his residual shoulder motion and could not move his hand at all. Data for panels B and C collected on trial day 463 (2016.03.08).

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