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.

Gain adaptation of eye and head movement components of simian gaze shifts.

Gain adaptation of eye and head movement components of simian gaze shifts. J. Neurophysiol. 78: 2817-2821, 1997. To investigate the site of gaze adaptation in primates, we reduced the gain of large head-restrained gaze shifts made to 50 degrees target steps by jumping the target 40% backwards during a targeting saccade and then tested gain transfer to the eye- and head-movement components of head-unrestrained gaze shifts. After several hundred backstep trials, saccadic gain decreased by at least 10% in 8 of 13 experiments, which were then selected for further study. The minimum saccadic gain decrease in these eight experiments was 12.8% (mean = 18.4%). Head-unrestrained gaze shifts to ordinary 50 degrees target steps experienced a gain reduction of at least 9.3% (mean = 14.9%), a mean gain transfer of 81%. Both the eye and head components of the gaze shift also decreased. However, average head movement gain decreased much more (22.1%) than eye movement gain (9.2%). Also, peak head velocity generally decreased significantly (20%), but peak eye velocity either increased or remained constant (average increase of 5.6%). However, the adapted peak eye and head velocities were appropriate for the adapted, smaller gaze amplitudes. Similar dissociations in eye and head metrics occurred when head-unrestrained gaze shifts were adapted directly (n = 2). These results indicated that head-restrained saccadic gain adaptation did not produce adaptation of eye movement alone. Nor did it produce a proportional gain change in both eye and head movement. Rather, normal eye and head amplitude and velocity relations for a given gaze amplitude were preserved. Such a result could be explained most easily if head-restrained adaptation were realized before the eye and head commands had been individualized. Therefore, gaze adaptation is most likely to occur upstream of the creation of separate eye and head movement commands.

Reconstructing the engram: simultaneous, multisite, many single neuron recordings.

Little is known about the physiological principles that govern large-scale neuronal interactions in the mammalian brain. Here, we describe an electrophysiological paradigm capable of simultaneously recording the extracellular activity of large populations of single neurons, distributed across multiple cortical and subcortical structures in behaving and anesthetized animals. Up to 100 neurons were simultaneously recorded after 48 microwires were implanted in the brain stem, thalamus, and somatosensory cortex of rats. Overall, 86% of the implanted microwires yielded single neurons, and an average of 2.3 neurons were discriminated per microwire. Our population recordings remained stable for weeks, demonstrating that this method can be employed to investigate the dynamic and distributed neuronal ensemble interactions that underlie processes such as sensory perception, motor control, and sensorimotor learning in freely behaving animals.