BASAL GANGLIA MOTOR CONTROL .2. LATE PALLIDAL TIMING RELATIVE TO MOVEMENT ONSET AND INCONSISTENT PALLIDAL CODING OF MOVEMENT PARAMETERS

1. We have tested the hypothesis that the basal ganglia initiate some one or several modes of movement by recording the change in discharge frequency of pallidal neurons during visually triggered step and visually paced ramp moves in relation to the visual stimulus onset, the change in the electromyograph (EMG), and the movement onset of trained rhesus monkeys. 2. The modal times of change for globus pallidus pars interna (GPi) were significantly later than those for forearm agonist muscle EMG. By contrast, the modal time of change for the cerebellar dentate nucleus preceded that for wrist agonist EMG. 3. The direction of change in discharge frequency of the GPi cells was for 71% an increase and for 29% a decrease. 4. Because of the relatively late change of activity of GPi neurons, we propose that GPi neurons cannot initiate these movements, as others have also suggested. The commands for the initiation of these movements may instead be generated by structures that include the lateral cerebellum and the anterior cerebral cortex. 5. We have also tested the hypothesis that the pallidum of the basal ganglia or the dentate of the lateral cerebellum may control the direction and other parameters of the trajectory by recording from both structures to see whether cell discharge correlated with the parameter and whether the correlation was consistent across tasks. Two rhesus monkeys were trained to perform hold-ramp-hold and hold-step-hold visually guided movements in opposite directions by flexing and extending the wrist with and against uniform oppositely directed torque loads (0.2 Nm). Wrist position, velocity, force, and EMG were recorded simultaneously. Movement amplitudes and directional intent were computed and inferred, respectively. 6. Task related neurons were classified as follows: 1) directional, if the discharge rate was reciprocal for opposite movements or if it increased or decreased during movement in one direction only; 2) bidirectional, if the discharge rate increased or decreased during movement in both directions; and 3) "other," if it was directional under one load and bidirectional under the other. During step tracking, 34 GPi, 47 globus pallidus pars externa (GPe), and 44 cerebellar dentate nuclear neurons were related to the task. Of the GPi cells, 14 (41%) were directional, 6 (18%) bidirectional, and 14 (41%) other. Of the GPe neurons, 13 (28%) were directional, 19 (40%) bidirectional, and 15 (32%) other. Of the dentate cerebellar nuclear cells, 5 (11%) were directional, 31 (70%) bidirectional, and 8 (18%) other. During ramp tracking, 23 GPi, 37 GPe, and 35 cerebellar dentate cells were related to the task. In GPi 7 (30%) neurons were directional, 7 (30%) bidirectional, and 9 (39%) other. In GPe 3 (8%) neurons were classified as directional, 15 (41%) bidirectional, and 19 (51%) other. In dentate, 6 (17%) neurons were directional, 21 (60%) bidirectional, and 8 (23%) other. 7. Although these data suggested that more than one-third of GPi cells and relatively fewer dentate cells may be related to direction of movement, on further examination it became clear that the relation of pallidal cell discharge to directionality of movement was not constant across the load and direction conditions either within a task or across the two tasks. 8. A similar lack of consistency of relationship was seen also for pallidal cell discharge and movement amplitude, velocity, directional set, joint position, and pattern of muscular activity. The lack of consistent correlation suggests that these movement parameters are not per se controlled by pallidal discharge. The occasional correlations in these and other reports are, instead, apparently due to a compounded correlation among the pallidal discharge, whatever the variable is that pallidal discharge does control, and the observed movement parameters. 9. From the present observations of the late pallidal timing and the lack of a consistent relation of pallidal output to movement parameters, plus the inactivation study described in the following paper, we conclude that the pallidum does not and cannot initiate and directly control the parameters of these movements.