Characteristics and stability of sensorimotor activity driven by isolated-muscle group activation in a human with tetraplegia

The topography and temporal stability of movement representations in sensorimotor cortex underlie the quality and durability of neural decoders for brain machine interface (BMI) technology. While single- and multi-unit activity (SUA and MUA) in sensorimotor cortex has been used to characterize the layout of the sensorimotor map, quantifying its stability has not been done outside of injury or targeted interventions. Here we aimed to characterize 1) the bilateral sensorimotor body map associated to isolated muscle group contractions and 2) the stability of multiunit firing responses for a single muscle (the extensor carpi radialis, ECR) over short (minutes) and long (days) time intervals. We concurrently recorded surface electromyograms (EMG) and MUA in a participant with incomplete high-spinal-cord injury as he executed (or attempted to execute) different metronome-paced, isolated muscle group contractions. Furthermore, for 8 recording sessions over 2 months, we characterized the sensorimotor map associated to ECR motions both within and across sessions. For each measurement period, we compared the stability of somatotopy (defined by the number of the channels on which a response was consistently detected) and firing pattern stability for each responsive channel. Stability was calculated for each channel in peri-EMG or peri-cue windows using both mean MUA firing rates and the full time-varying responses (i.e., MUA 99shape99). First, we found that cortical representations of isolated group muscle contractions overlapped, even for muscles from disparate body regions such as facial and distal leg muscles; this was the case for both intact and de-efferented muscles, in both motor and sensory channels. Second, the spatial stability of somatotopy significantly changed over the course of both minutes and days, with the consistency between sessions decreasing across longer bouts of time. Firing pattern stabilities showed distinct profiles; mean MUA firing rates became less stable over time whereas MUA shape remained consistent. Interestingly, sensory channels were overall more consistent than motor channels in terms of spatial stability, mean MUA firing rates, and MUA shape. Our findings suggest that the encoding of muscle-driven specific activity in sensorimotor cortex at the level of MUA is redundant and widespread with complex spatial and temporal characteristics. These findings extend our understanding of how sensorimotor cortex represents movements, which could be leveraged for the design of non-traditional BMI approaches.