Extensive literatures have shown approaches for decoding upper limb kinematics or muscle activity using multichannel cortical spike recordings toward brain machine interface (BMI) applications. However, similar topics regarding lower limb remain relatively scarce. We previously reported a system for training monkeys to perform visually guided stand and squat tasks. The current study, as a follow-up extension, investigates whether lower limb kinematics and muscle activity characterized by electromyography (EMG) signals during monkey performing stand/squat movements can be accurately decoded from neural spike trains in primary motor cortex (M1).

Two monkeys were used in this study. Subdermal intramuscular EMG electrodes were implanted to 8 right leg/thigh muscles. With ample data collected from neurons from a large brain area, we performed a spike triggered average (SpTA) analysis and got a series of density contours which revealed the spatial distributions of different muscle-innervating neurons corresponding to each given muscle. Based on the guidance of these results, we identified the locations optimal for chronic electrode implantation and subsequently carried on chronic neural data recordings. A recursive Bayesian estimation framework was proposed for decoding EMG signals together with kinematics from M1 spike trains.

Two specific algorithms were implemented: a standard Kalman filter and an unscented Kalman filter. For the latter one, an artificial neural network was incorporated to deal with the nonlinearity in neural tuning. High correlation coefficient and signal to noise ratio between the predicted and the actual data were achieved for both EMG signals and kinematics on both monkeys. Higher decoding accuracy and faster convergence rate could be achieved with the unscented Kalman filter. These results demonstrate that lower limb EMG signals and kinematics during monkey stand/squat can be accurately decoded from a group of M1 neurons with the proposed algorithms. Our findings provide new insights for extending current BMI design concepts and techniques on upper limbs to lower limb circumstances. Brain controlled exoskeleton, prostheses or neuromuscular electrical stimulators for lower limbs are expected to be developed, which enables the subject to manipulate complex biomechatronic devices with mind in more harmonized manner.

Background: Determining neuronal topographical information in the cerebral cortex is of fundamental importance for developing neuroprosthetics. Significant progress has been achieved in decoding hand voluntary movement with cortical neuronal activity in nonhuman primates. However, there are few successful reports in scientific literature for decoding lower limb voluntary movement with the cortical neuronal firing. We once reported an experimental system, which consists of a specially designed chair, a visually guided stand and squat task training paradigm and an acute neuron recording setup. With this system, we can record high quality cortical neuron activity to investigate the correlation between these neuronal signals and stand/squat movement.

Methods/Results: In this research, we train two monkeys to perform the visually guided stand and squat task, and record neuronal activity in the vast areas targeted to M1 hind-limb region, at a distance of 1 mm. We find that 76.9% of recorded neurons (1230 out of 1598 neurons) showing task-firing modulation, including 294 (18.4%) during the pre-response window; 310 (19.4%) for standing up; 104 (6.5%) for the holding stand phase; and 205 (12.8%) during the sitting down. The distributions of different type neurons have a high degree of overlap. They are mainly ranged from +7.0 to 13 mm in the Posterior-Anterior dimension, and from +0.5 to 4.0 mm in Dosal-lateral dimension, very close to the midline, and just anterior of the central sulcus.

Conclusions/Significance: The present study examines the neuronal activity related to lower limb voluntary movements in M1 and find topographical information of various neurons tuned to different stages of the stand and squat task. This work may contribute to understanding the fundamental principles of neural control of lower limb movements. Especially, the topographical information suggests us where to implant the chronic microelectrode arrays to harvest the most quantity and highest quality neurons related to lower limb movements, which may accelerate to develop cortically controlled lower limb neuroprosthetics for spinal cord injury subjects.