Differential Contribution of Sensorimotor Cortex and Subthalamic Nucleus to Unimanual and Bimanual Hand Movements

Abstract

AbstractWhy does unilateral subthalamic nucleus deep brain stimulation improve motor function bilaterally? To address this clinical observation, we collected parallel neural recordings from sensorimotor cortex and the subthalamic nucleus during repetitive ipsilateral, contralateral, and bilateral hand movements in patients with Parkinson’s disease undergoing subthalamic nucleus deep brain stimulation. We used a cross-validated electrode-wise encoding model to map EMG data to the neural signals. Electrodes in the subthalamic nucleus encoded movement in a comparable manner for both hands during unimanual and bimanual movements, whereas sensorimotor cortex electrodes displayed a strong contralateral bias. To examine representational overlap in encoding across the two hands, we trained the model with data from one condition (contralateral hand) and used the trained weights to predict neural activity for movements produced with the other hand (ipsilateral hand). Overall, between-hand generalization was poor and this limitation was evident in both SMC and STN. A similar method was used to probe representational overlap across different task contexts (unimanual vs. bimanual). Task context was more important for the STN compared to the SMC indicating that neural activity in the STN showed greater divergence between the unimanual and bimanual conditions. These results indicate that whereas SMC activity is strongly lateralized and relatively context-free, STN integrates contextual information with the ongoing behavior.Significance StatementUnilateral subthalamic nucleus deep brain stimulation (DBS) improves both contralateral and ipsilateral motor symptoms of Parkinson’s disease. To explore mechanisms for bilateral improvement, parallel neural recordings from the sensorimotor cortex (SMC) and subthalamic nucleus (STN) were recorded in patients with Parkinson’s disease undergoing DBS. Neural activity and muscle activity from the hands were collected while patients performed unimanual and bimanual repetitive hand movements. Activity in SMC primarily encoded contralateral movements and was relatively context-free. In contrast, STN encoded movements in a comparable manner for both hands and was sensitive to the behavioral context.