Relations of motor cortex neural discharge to kinematics of passive and active elbow movements in the monkey

1. Bedingham and Tatton recently reported that in cats trained not to resist imposed limb perturbations, some motor cortex (area 4) neurons responded predominantly to acceleration or jerk (the third derivative of position). The questions arose whether motor cortex neurons responding to higher derivatives of limb displacement exist in the primate in a resist-perturbation task and, if so, whether discharge of such neurons responds to the same kinematics in active (voluntary) movements. 2. To answer these questions we studied the discharge patterns of 203 motor cortex neurons that responded to torque pulse perturbations about the elbow and fired during active elbow flexions and extensions in four monkeys. Detailed analysis was performed on 66 neurons that responded reciprocally in both situations. 3. Reciprocal neurons discharged at short latency (20-40 ms) for one direction of arm perturbation. For the opposite direction they were initially silent or inhibited and then discharged at a variety of latencies but in apparent relation to limb kinematics. Based on the timing and overall pattern of their discharge the majority of neurons (68%) were classified as being acceleration-like. 4. Twenty-four (36%) of these reciprocal neurons had only sensory (kinematic)-like properties in active movements, i.e., they discharged after (and not before) movement onset. Discharge of these neurons followed the timing, but not the magnitude, of acceleration (20 neurons) or velocity (4 neurons). The discharge of these neurons also had a static component as the arm was held stationary. 5. Twenty-nine (44%) of reciprocal neurons commenced firing before movement onset for one direction of active movement, while for the opposite direction their discharge occurred after movement onset. Thus their discharge appeared to be muscle-related: both when the muscle was contracting as an agonist and stretched as an antagonist. 6. Although in these tasks discharge of MCNs could be generated either by sensory feedback or by motor responses, the strong response sensitivity of many neurons to acceleration supports the hypothesis that feedback based on higher derivatives of limb displacement could represent a "predictive" control system for accurate regulation of limb motion.