Ensemble recordings of human subcortical neurons as a source of motor control signals for a brain-machine interface

Patients with severe neurological injury, such as quadriplegics, might benefit greatly from a brain-machine interface that uses neuronal activity from motor centers to control a neuroprosthetic device. Here, we report an implementation of this strategy in the human intraoperative setting to assess the feasibility of using neurons in subcortical motor areas to drive a human brain-machine interface.

Acute ensemble recordings from subthalamic nucleus and thalamic motor areas (ventralis oralis posterior [VOP]/ventralis intermediate nucleus [VIM]) were obtained in 11 awake patients during deep brain stimulator surgery by use of a 32-microwire array. During extracellular neuronal recordings, patients simultaneously performed a visual feedback hand-gripping force task. Offline analysis was then used to explore the relationship between neuronal modulation and gripping force.

Individual neurons (n = 28 VOP/VIM, n = 119 subthalamic nucleus) demonstrated a variety of modulation responses both before and after onset of changes in gripping force of the contralateral hand. Overall, 61% of subthalamic nucleus neurons and 81% of VOP/VIM neurons modulated with gripping force. Remarkably, ensembles of 3 to 55 simultaneously recorded neurons were sufficiently information-rich to predict gripping force during 30-second test periods with considerable accuracy (up to R = 0.82, R(2) = 0.68) after short training periods. Longer training periods and larger neuronal ensembles were associated with improved predictive accuracy.

This initial feasibility study bridges the gap between the nonhuman primate laboratory and the human intraoperative setting to suggest that neuronal ensembles from human subcortical motor regions may be able to provide informative control signals to a future brain-machine interface.