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

doi:10.1016/S0140-6736(17)30601-3

The Lancet

Volume 389, Issue 10081, 6–12 May 2017, Pages 1821-1830

https://doi.org/10.1016/S0140-6736(17)30601-3 Get rights and content

Summary

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.

Introduction

High-cervical spinal cord injury resulting in tetraplegia prevents affected individuals from performing reaching and grasping movements required for many activities of daily living. Functional electrical stimulation (FES), in the absence of descending motor commands, applies spatiotemporal patterns of stimulation to peripheral nerves and muscles to reanimate paralysed limbs for restoration of lost functions. FES can be delivered through skin surface, intramuscular, or nerve cuff electrodes,1, 2, 3 and has successfully restored grasping to individuals with mid-level to low-level cervical spinal cord injury, who retained both volitional shoulder and elbow movements to command stimulation.4, 5, 6

Restoration of multi-joint reaching and grasping is more difficult in individuals with high-cervical spinal cord injury because the few available command options (sip-and-puff, eye tracking, retained head and neck movements) are unintuitive, scale poorly for commanding coordinated multi-joint movements, and interfere with intact head and face function. Intracortical brain–computer interfaces (iBCIs) that directly map cortical activity to desired movement eschew the need for retained volitional movement, thereby potentially addressing these shortcomings. Intact non-human primates7, 8, 9 and people with paralysis10, 11, 12, 13 have successfully used iBCIs to command cursor movements and reaching and grasping movements using robotic limbs. Temporarily paralysed non-human primates have used iBCIs to command implanted FES-actuated wrist and grasping movements.14, 15 A study published in 2016 used an iBCI coupled with surface electrical stimulation to provide assistive hand grasping to an individual with a C5/C6 spinal cord injury¹⁶ who retained volitional shoulder and elbow function. However, the 25-year-old Freehand implanted FES system (NeuroControl Corporation, Valley View, OH)4, 5, 6 has already successfully restored hand grasping to individuals who retained volitional arm function, without requiring an iBCI. We report the findings of an individual with chronic tetraplegia who used an implanted FES system to make both reaching and grasping movements, intuitively and effectively commanded by an iBCI, with a translational path for future clinical viability.

Research in context

Evidence before this study

We initially searched PubMed using the search terms (“FES” OR “electrical stimulation”) AND (“BMI” OR “BCI” OR “brain-machine interface”, OR “brain-computer interface”), with no language or date restrictions. The date of our last search was Nov 16, 2016. Our search resulted in a large number of studies in people using predominantly non-invasive brain–computer interfaces (BCIs) to command non-focal surface stimulation to restore state-based, all-or-nothing hand opening and closing. Other noteworthy studies used non-invasive BCIs combined with an implanted Freehand functional electrical stimulation (FES) neuroprosthesis to again restore state-based, all-or-nothing hand opening or closing. One study used an intracortical microelectrode array with a surface FES system to restore hand grasping alone to a person with mid-level cervical spinal cord injury. Two non-human primate studies were of note that showed restoration of continuous (graded) control of implanted FES activation of wrist and hand function. Three studies in individuals who were paralysed showed BCI control of robotic arms. However, we found no studies that were similar to this study, either in individuals with spinal cord injury or non-human primate paralysis models, that restored both continuous reaching and grasping functions via electrical stimulation and also had a clear path to clinical translation.

Added value of this study

Our study is the first to restore both reaching and grasping via FES to a person with chronic spinal cord injury that results in complete loss of arm and hand function. By using both an intracortical BCI and percutaneous FES electrodes for muscle activation, as well as a mobile arm support for gravitational assistance, we have shown a proof-of-concept combined technology that allows users to perform functional tasks that require coordinated reaching and grasping. Although other non-invasive BCI and FES hand-only systems have been proposed, none have been shown to be readily adoptable for day-to-day use, and certainly not for restoring both reaching and grasping. The present work has a clear path to clinical translation because of the fully implantable FES technology that already exists, and the continued efforts to develop fully implanted and wireless BCI systems.

Implications of all the available evidence

Our results show the potential of combining implanted FES and iBCI (with a mobile arm support) for restoring self-initiated reaching and grasping movements to individuals with spinal cord injuries that result in chronic paralysis. This work was a crucial step for demonstrating feasibility. Future developments of fully implanted systems, as well as developments in advanced decoders and stimulators, might lead to enhanced neuroprosthetic functional performance and greater independence for individuals with paralysis.

Section snippets

Participant

We enrolled the participant (ID number T8) into the BrainGate2 clinical trial (ClinicalTrials.gov, number NCT00912041). Inclusion and exclusion criteria are available online. 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,

Results

The study commenced on Dec 1, 2014 (day of intracortical implant) and data are until Nov 7, 2016 (717 days after implant). Over the course of the study, the participant had four minor (and no serious) device-related adverse events, all of which were treated, resolved, and reported to the governing regulatory bodies. No additional adverse events had occurred at the time when the last data were collected for this publication, and the participant remains in the BrainGate2 trial.

Neural activity was

Discussion

FES+iBCI restoration of arm and hand functions, combined with a mobile arm support (standard practice for individuals with C4 spinal cord injury implanted with FES arm systems) under iBCI command, represents a neurotechnology-based circumvention of spinal cord injury. This restoration gives individuals with chronic tetraplegia intuitive control over reaching and grasping movements using their paralysed limbs. The study substantially extends previous iBCI research on individuals with paralysis

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

Summary

Background

Methods

Findings

Interpretation

Funding

Introduction

Section snippets

Participant

Results

Discussion

Arch Phys Med Rehabil

J Hand Surg Am

J Hand Surg Am

Lancet

Electroencephalogr Clin Neurophysiol

Neurosci Lett

Implanted neuroprosthesis for restoring arm and hand function in people with high level tetraplegia

Arch Phys Med Rehabil

The functional impact of the Freehand System on tetraplegic hand function. Clinical results

Spinal Cord

The Freehand System: an implantable neuroprosthesis for functional electrostimulation of the upper extremity

Handchir Mikrochir Plast Chir

Direct cortical control of 3D neuroprosthetic devices

Science

Instant neural control of a movement signal

Nature

Cortical control of a prosthetic arm for self-feeding

Nature

Neuronal ensemble control of prosthetic devices by a human with tetraplegia

Nature

Reach and grasp by people with tetraplegia using a neurally controlled robotic arm

Nature

Decoding motor imagery from the posterior parietal cortex of a tetraplegic human

Sci Mag

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