Restoration of grasp following paralysis through brain-controlled stimulation of muscles

Abstract

Patients with spinal cord injury lack the connections between brain and spinal cord circuits that are essential for voluntary movement. Clinical systems that achieve muscle contraction through functional electrical stimulation (FES) have proven to be effective in allowing patients with tetraplegia to regain control of hand movements and to achieve a greater measure of independence in daily activities. In existing clinical systems, the patient uses residual proximal limb movements to trigger pre-programmed stimulation that causes the paralysed muscles to contract, allowing use of one or two basic grasps. Instead, we have developed an FES system in primates that is controlled by recordings made from microelectrodes permanently implanted in the brain. We simulated some of the effects of the paralysis caused by C5 or C6 spinal cord injury by injecting rhesus monkeys with a local anaesthetic to block the median and ulnar nerves at the elbow. Then, using recordings from approximately 100 neurons in the motor cortex, we predicted the intended activity of several of the paralysed muscles, and used these predictions to control the intensity of stimulation of the same muscles. This process essentially bypassed the spinal cord, restoring to the monkeys voluntary control of their paralysed muscles. This achievement is a major advance towards similar restoration of hand function in human patients through brain-controlled FES. We anticipate that in human patients, this neuroprosthesis would allow much more flexible and dexterous use of the hand than is possible with existing FES systems.

Figure 1

Brain-controlled Functional Electrical Stimulation (FES). The monkey’s forearm and digit flexor muscles were temporarily paralyzed by a peripheral nerve block. Recordings from the motor cortex were used to infer the monkey’s attempted patterns of muscle activity and thereby control electrical stimulation that restored the monkey’s ability to perform a functional grasping task. The ball grasp device was equipped with a contact sensor and a task-completion sensor that were activated when the monkey initially touched the ball and dropped it into the tube, respectively.

Figure 2

Grasp-related raw data collected during normal conditions. A) Firing rates of 104 neuronal signals recorded during two grasps. B) Ensemble average of 229 trials aligned to time of ball contact. C) Actual and predicted EMG during the same period as (A), including flexor digitorum superficialis (FDS), flexor digitorum profundus (FDP). flexor carpi radialis (FCR), flexor carpi ulnaris (FCU), extensor carpi radialis (ECR), extensor digitorum communis (EDC), extensor carpi ulnaris (ECU) and flexor policis brevis (FPB). Predicted EMG was computed using multiple input, linear impulse response decoders built from data collected earlier in the session. Vertical dashed lines mark the time of ball contact. R² values indicate prediction accuracy for the 20 minute data file. D) Ensemble averages of EMG activity, aligned to the time of initial contact.

Figure 3

Grasp performance during four consecutive brain-controlled FES trials. A) Neural data B) Predicted EMG signals (red traces) transformed into stimulus commands (black traces). Vertical dashed lines: go tone (“Go”), time of initial ball contact (“Pick up”) and successful task completion (“Reward”). C) Horizontal lines show average success rates for sequential 10-minute blocks during two experimental sessions (light and dark lines), including FES trials (green lines) and catch trials without stimulation (blue lines). The neuroprosthesis dramatically improved the monkey's ability to grasp the ball despite paralysis. D) Average success rates for normal, FES, and catch trials across all sessions (100%, 76% and 10% respectively for Monkey T; 99%, 80% and 1% for Monkey J). Total number of trials (successful and failed) is displayed on the bars for each condition.

Figure 4

FES used to produce controlled palmar grip force during the palmar grasp task. Rectangles indicate the level and time of appearance of force targets. This segment shows three target levels, with the two extremes non-overlapping. The white trace is the force generated by the monkey, resulting from stimulation of FDS and FDP. There were four successful trials with FES (green) and one unsuccessful catch trial (blue). During the catch trial, the monkey made two unsuccessful attempts to squeeze the tube, as seen in the neural activity and EMG predictions