Population code for tracking velocity based on cerebellar Purkinje cell simple spike firing in monkeys.

Velocity is an important determinant of the simple spike discharge of cerebellar Purkinje cells. In a previous study, Purkinje cells in the intermediate and lateral cerebellum recorded during manual tracking were found to be tuned to a combination of direction and speed, (i.e. preferred velocity). In this study a population analysis of this simple spike discharge was used to determine whether the velocity of tracking could be predicted. For the majority (30/32) of direction-speed combinations, the population response accurately specified the target velocity. A temporal analysis showed how the population response gradually converged to the required velocity 200 ms prior to the onset of tracking. Therefore, the simple spike discharge of a Purkinje cell ensemble contains sufficient information to reconstruct target velocity, providing support for the hypothesis that the cerebellum controls or signals movement velocity.

Encoding of target direction and speed during visual instruction and arm tracking in dorsal premotor and primary motor cortical neurons.

The encoding of direction and speed in the discharge of dorsal premotor (PMd) and primary motor (MI) neurons was studied during two-dimensional visually-instructed pursuit arm movements in which eight directions and four constant speeds were independently manipulated. Each trial consisted of equal durations of visual observation of target movement without hand movement (cue) and visual pursuit-tracking of the target with the hand (track). A total of 240 neurons was recorded from PMd and MI in two Macaca mulatta monkeys. Two classes of regression analyses were used to relate neuronal firing during the cue and track periods to direction and speed. First, the average firing from each period was fitted to target direction or speed. Period-averaged firing significantly correlated with direction more frequently in the track than in the cue period. Conversely, correlations with speed (with or without direction) were more common in the cue than in the track period. Secondly, a binwise regression evaluated the temporal evolution of firing correlations with direction and speed. Supporting the period-based results, significant binwise correlations of the discharge with speed occurred preferentially during the cue period when there was no hand movement. Prior to movement, correlations of the firing with direction became significant and continued through the movement. Both analyses demonstrated a distinct tendency for neurons to be modulated by speed information early and by direction information later. This temporal parcellation reflects both the sequential demands of the task and constraints placed on the neural computations. The early representation of target speed is hypothesized to reflect the need to calculate a 'go signal' for the initiation of movement.

Visuomotor processing as reflected in the directional discharge of premotor and primary motor cortex neurons.

Premotor and primary motor cortical neuronal firing was studied in two monkeys during an instructed delay, pursuit tracking task. The task included a premovement "cue period," during which the target was presented at the periphery of the workspace and moved to the center of the workspace along one of eight directions at one of four constant speeds. The "track period" consisted of a visually guided, error-constrained arm movement during which the animal tracked the target as it moved from the central start box along a line to the opposite periphery of the workspace. Behaviorally, the animals tracked the required directions and speeds with highly constrained trajectories. The eye movements consisted of saccades to the target at the onset of the cue period, followed by smooth pursuit intermingled with saccades throughout the cue and track periods. Initially, an analysis of variance (ANOVA) was used to test for direction and period effects in the firing. Subsequently, a linear regression analysis was used to fit the average firing from the cue and track periods to a cosine model. Directional tuning as determined by a significant fit to the cosine model was a prominent feature of the discharge during both the cue and track periods. However, the directional tuning of the firing of a single cell was not always constant across the cue and track periods. Approximately one-half of the neurons had differences in their preferred directions (PDs) of >45 degrees between cue and track periods. The PD in the cue or track period was not dependent on the target speed. A second linear regression analysis based on calculation of the preferred direction in 20-ms bins (i.e., the PD trajectory) was used to examine on a finer time scale the temporal evolution of this change in directional tuning. The PD trajectories in the cue period were not straight but instead rotated over the workspace to align with the track period PD. Both clockwise and counterclockwise rotations occurred. The PD trajectories were relatively straight during most of the track period. The rotation and eventual convergence of the PD trajectories in the cue period to the preferred direction of the track period may reflect the transformation of visual information into motor commands. The widely dispersed PD trajectories in the cue period would allow targets to be detected over a wide spatial aperture. The convergence of the PD trajectories occurring at the cue-track transition may serve as a "Go" signal to move that was not explicitly supplied by the paradigm. Furthermore, the rotation and convergence of the PD trajectories may provide a mechanism for nonstandard mapping. Standard mapping refers to a sensorimotor transformation in which the stimulus is the object of the reach. Nonstandard mapping is the mapping of an arbitrary stimulus into an arbitrary movement. The shifts in the PD may allow relevant visual information from any direction to be transformed into an appropriate movement direction, providing a neural substrate for nonstandard stimulus-response mappings.

Cerebellar Purkinje cell simple spike discharge encodes movement velocity in primates during visuomotor arm tracking.

Pathophysiological, lesion, and electrophysiological studies suggest that the cerebellar cortex is important for controlling the direction and speed of movement. The relationship of cerebellar Purkinje cell discharge to the control of arm movement parameters, however, remains unclear. The goal of this study was to examine how movement direction and speed and their interaction-velocity-modulate Purkinje cell simple spike discharge in an arm movement task in which direction and speed were independently controlled. The simple spike discharge of 154 Purkinje cells was recorded in two monkeys during the performance of two visuomotor tasks that required the animals to track targets that moved in one of eight directions and at one of four speeds. Single-parameter regression analyses revealed that a large proportion of cells had discharge modulation related to movement direction and speed. Most cells with significant directional tuning, however, were modulated at one speed, and most cells with speed-related discharge were modulated along one direction; this suggested that the patterns of simple spike discharge were not adequately described by single-parameter models. Therefore, a regression surface was fitted to the data, which showed that the discharge could be tuned to specific direction-speed combinations (preferred velocities). The overall variability in simple spike discharge was well described by the surface model, and the velocities corresponding to maximal and minimal discharge rates were distributed uniformly throughout the workspace. Simple spike discharge therefore appears to integrate information about both the direction and speed of arm movements, thereby encoding movement velocity.

Relationship of cerebellar Purkinje cell simple spike discharge to movement kinematics in the monkey.

The simple spike discharge of 231 cerebellar Purkinje cells in ipsilateral lobules V and VI was recorded in three monkeys trained to perform a visually guided reaching task requiring movements of different directions and distances. The discharge of 179 cells was significantly modulated during movement to one or more targets. Mean simple spike rate was fitted to a cosine function for direction tuning, a simple linear function for distance modulation, and a multiple linear regression model that included terms for direction, distance, and target position. On the basis of the fit to the direction and distance models, there were more distance-related than direction-related Purkinje cells. The simple spike discharge of most direction-related cells modulated at only one target distance. The preferred directions for the simple spike tuning were not uniformly distributed across the workspace. The discharge of most distance-related cells modulated along only one movement direction. On the basis of the multiple linear regression model, simple spike discharge was also correlated with target position, in addition to direction and distance. Approximately half of the Purkinje cells had simple spike activity associated with only a single parameter, and only a small fraction of the cells with all three. The multiple regression model was extended to evaluate the correlations as a function of time. Considerable overlap occurred in the timing of the simple spike correlations with the parameters. The latency for correlation with movement direction occurred mainly in a 500-ms interval centered on movement onset. The correlations with target position also occurred around movement onset, in the range of -200-500 ms. Distance correlations were more variable, with onset latencies from -500 to 1,000 ms. These results demonstrate that the simple spike discharge of cerebellar Purkinje cells is correlated with movement direction, distance, and target position. Comparing these results to motor cortical discharge shows that the correlations with these parameters were weaker in Purkinje cell simple spike discharge, and that, for the majority of Purkinje cells, the simple spike discharge was significantly related to only a single movement parameter. Other differences between simple spike responses and those of motor cortical cells include the nonuniform distribution of preferred directions and the extensive overlap in the timing of the correlations. These differences suggest that Purkinje cells process, encode, and use kinematic information differently than motor cortical neurons.

Movement kinematics encoded in complex spike discharge of primate cerebellar Purkinje cells.

Monkeys performed a multijoint arm-reaching task that systematically varied movement direction and distance. Purkinje cell activity was recorded from 231 task-related cells, and the complex spike discharge was analyzed in relation to distance and direction. The complex spike activity of 123 Purkinje cells changed significantly relative to the background rate. Of these 123, the activity of 85 cells was related to distance and/or direction. The complex spike activity of 54 of these 85 cells fitted a cosine tuning curve for direction, generally at one distance. Using a simple linear regression model, the complex spike activity of 56 cells was significantly correlated with movement distance, usually in one direction. We conclude that the complex spike discharge of Purkinje cells is spatially tuned and strongly related to movement kinematics.

Effects of levodopa and viscosity on the velocity and accuracy of visually guided tracking in Parkinson's disease.

Deficits in velocity generation and movement accuracy occur in Parkinson's disease and are postulated to contribute to the characteristic bradykinesia. In the present study, we attempted to clarify the relationship between the deficits in velocity generation and movement accuracy. Patients with Parkinson's disease and normal controls tracked visually displayed sinusoidal and step targets with the wrist. Performance was evaluated using measurements of velocity and error. Movement velocity was manipulated by two methods: (i) administration of levodopa; (ii) viscous loading. Dependencies of velocity and error on disease state, medication state and viscosity were examined. Visually guided pursuit tracking was characterized by intermittent and frequent velocity excursions in both the patients and controls. For sinusoidal tracking, levodopa significantly increased velocity in the severely affected parkinsonian patients. Prior to the administration of levodopa, step tracking velocity was significantly lower in all patients than in controls. The "on' state produced an increase in velocity to control levels. Error was significantly greater in the parkinsonian subjects than in controls, but was unchanged by levodopa for both tracking tasks. Manipulations of viscosity produced greater changes in velocity than did levodopa, yet a similar independence with respect to accuracy remained. Velocity significantly changed by 40-60% in the two tracking tasks from the viscous to antiviscous loads. Error did not change significantly in 12 out of 14 comparisons of subgroups based on disease and medication state. This contradicts the hypothesis that patients with Parkinson's disease primarily reduce velocity during tracking to maintain acceptable accuracy in the presence of a defective error correction system. Although parkinsonian subjects tracked with reduced accuracy, both normal and parkinsonian subjects were able to compensate for significant changes in velocity due to external loading. Thus a propulsion deficit exists in parkinsonism that may be alleviated with either antiviscosity or levodopa. An error correction deficit is also present in parkinsonism, but is not modified by antiviscosity or levodopa.

Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons.

1. Several neurophysiological studies of the primary motor and premotor cortices have shown that the movement parameters direction, distance, and target position are correlated with the discharge of single neurons. Here we investigate whether the correlations with these parameters occur simultaneously (i.e., parallel processing), or sequentially (i.e., serial processing). 2. The single-unit data used for the analyses presented in this paper are the same as those used in our earlier study of neuronal specification of movement parameters. We recorded the activity of single neurons in the primary motor and premotor cortices of two rhesus monkeys (Macaca mulatta) while the animals performed reaching movements made in a horizontal plane. Specifically, the animals moved from a centrally located start position to 1 of 48 targets (1 cm2) placed at eight different directions (0-360 degrees in 45 degrees intervals) and six distances (1.4-5.4 cm in 0.8-cm increments) from the start position. 3. We analyzed 130 task-related cells; of these, 127 (99 in primary motor cortex, 28 near the superior precentral sulcus) had average discharges that were significantly modulated with the movement and were related to movement direction, distance, or target position. To determine the temporal profile of the correlation of each cell's discharge with the three parameters, we performed a regression analysis of the neural discharge. We calculated partial R2s for each parameter and the total R2 for the model as a function of time. 4. The discharge of the majority of units (73.2%) was significantly correlated for some time with all three parameters. Other units were found that correlated with different combinations of pairs of parameters (21.3%), and a small number of units appeared to code for only one parameter (5.5%). There was no obvious difference in the presence of correlations between cells recorded in the primary motor versus premotor cortices. 5. On average we found a clear temporal segregation and ordering in the onset of the parameter-related partial R2 values: direction-related discharge occurred first (115 ms before movement onset), followed sequentially by target position (57 ms after movement onset) and movement distance (248 ms after movement onset). Some overlap in the timing of the correlation of these parameters was evident. We found a similar sequential ordering for the latency of the peak of the R2 curves (48, 254, and 515 ms after movement onset, respectively, for direction, target position, and distance).(ABSTRACT TRUNCATED AT 400 WORDS)