Roles of primate spinal interneurons in preparation and execution of voluntary hand movement.

To study the contribution of primate cervical interneurons (INs) to preparation and execution of normal voluntary hand movement we investigated their activity and correlational linkages to muscles in monkeys performing tracking tasks. During ramp-and-hold flexion-extension torques about the wrist most task-related spinal INs exhibited some activity during both flexion and extension, in unexpected contrast to the strictly unidirectional activity of corticomotoneuronal (CM) cells and motoneurons. Most INs increased their activity more in one of these two directions; response patterns in their preferred direction were typically tonic or phasic-tonic. Spike-triggered averages of EMG detected significant features in muscle activity for many task-related INs. Premotor INs (PreM-INs) were identified by post-spike facilitation or suppression with appropriate onset latencies after the trigger spike. Muscle fields of PreM-INs were smaller than those of supraspinal PreM cells in cortex and red nucleus, and rarely involved reciprocal effects on antagonist muscles. To investigate the relation of spinal INs to a repertoire of different muscle synergies, activity of INs was recorded from a macaque performing a multidirectional wrist task. The monkey generated isometric torques in flexion/extension, radial/ulnar deviation, pronation/supination, and executed a power grip that co-contracted wrist flexor and extensor muscles. Many INs showing task-modulated activity had preferred directions in this multidirectional space, typically with broadly tuned activation. The role of spinal INs in preparation for voluntary movement was revealed in monkeys performing instructed delay tasks. During the delay between a transient visual cue and a go signal a third of the tested INs showed significant delay modulation (SDM) of firing rate relative to the pre-cue rate. The SDM responses often differed from the INs' responses during the subsequent active torque period. In a monkey instructed by either visual or proprioceptive cues the delay period activity for many INs was similar in visual and perturbation trials, although other INs exhibited different SDM for visually and proprioceptively cued trials. These results suggest that spinal INs are involved, with cortex, in the earliest stages of movement preparation. The sensory input to INs could be identified in transient responses to the torque pulse, which showed two predominant patterns, consistent with inputs from cutaneous or proprioceptive receptors. We also investigated the task-dependent modulation of neural responses to peripheral input in a monkey performing wrist flexion/extension movements in a visually cued instructed delay task. Monosynaptic responses evoked by electrical stimulation of the superficial radial nerve through a cuff electrode were suppressed or abolished during the dynamic movement phase. Since task-related activity of the INs increased at the same time, the suppression was mediated by presynaptic rather than postsynaptic inhibition. These observations indicate that under normal behavioral conditions many spinal INs have response properties comparable to those previously documented for cortical neurons in behaving animals.