NEURONAL SPECIFICATION OF DIRECTION AND DISTANCE DURING REACHING MOVEMENTS IN THE SUPERIOR PRECENTRAL PREMOTOR AREA AND PRIMARY MOTOR CORTEX OF MONKEYS

1. Single-unit neuronal activity was recorded in the primary motor and superior precentral premotor areas of two rhesus monkeys during an ar m reaching task. The task involved moving a cursor displayed on a vide o terminal using a draftsman's armtype manipulandum. From a centrally located start box the animal was required to move to 1 of 48 target bo xes at eight different directions (0-360-degrees in 45-degree interval s) and six distances (1.4-5.4 cm in 0.8-cm increments). Both direction and distance for the upcoming movement were unpredictable. 2. The act ivity of 197 arm movement-related cells was recorded and evaluated for each of the 48 targets. Histological examination showed the cells to be primarily in the primary motor cortex or in the premotor area aroun d the superior precentral sulcus. Each cell's discharge was aligned on movement onset and averaged over five trials for each target. Movemen t kinematics including hand path velocity were also determined. The ta sk time was divided into three epochs, a premovement period (PT), a mo vement period (MT), and total time (TT = PT + MT). For each epoch the average firing was correlated with the direction and distance of the m ovement using various regression procedures. 3. An analysis of varianc e (ANOVA) showed that the majority of neurons were modulated significa ntly by movement direction in each of the three time periods, PT (73.7 %), MT (68.3%), and TT (78.5%). The relationship of the firing to dire ction was fit to a cosine tuning function for each significantly modul ated cell. In 86.3% of the cells the firing was correlated significant ly with a cosine function of movement direction in TT. A cell's prefer red direction varied little for different movement distances. The mean difference in preferred direction for the smallest possible change in distance (0.8 cm) was 12.8 +/- 11.4-degrees (SD) and 17.1 +/- 14.7-de grees for the largest change in distance (4.0 cm). 4. Correlation anal ysis revealed that the activity of the majority of cells was modulated significantly by distance along at least one direction in each of the three time periods, PT (46.8%), MT (68.8%), and TT (67.&%). subsequen tly, a univariate linear regression model was used to quantify a cell' s discharge as a function of distance. For the regressions of firing w ith distance with a statistically significant correlation (r>0.8), the mean slope was 3.59 +/-0.17 spikes.s-1.cm-1 for the total time. The e xistence of a significant distance modulation was not invariably corre lated with a cell's preferred movement direction. There was only a sli ght increase in the likelihood of a significant correlation with dista nce for movements close to a cell's preferred movement direction. Also , the average slope for distance was not greater for movements close t o a cell's preferred direction. 5. A two-way ANOVA was used to test fo r firing modulation with respect to direction and distance and to exam ine whether interactions between these tow parameters exist. Significa nt modulation with either direction, distance, or ''interaction'' betw een these two parameters occurred in 130 of 153 cells evaluated. The i nteraction terms in the model are equivalent to target position. Next, a multivariate regression model was developed to relate the cell's di scharge with direction and distance. A proportional reduction in error (PRE) approach was used to define the terms in the model. The six req uired parameters included distance, a sine and cosine function of dire ction, and target position. The model yielded a significant fit (P<0.0 5) for 119 of the 130 analyzed cells with a mean R2 of 0.61 +/- 0.18. 6. Cell's responses were analyzed on the basis of the partial R2 obtai ned for direction, distance, and target position. In 37 cells only the direction term contributed significantly to the fit and in four cells only distance was significant. In 78 cells either the partial R2 for both distance and direction was significant or the partial R2 for targ et position (interaction terms) was significant. In addition, a tempor al component to the correlation was observed; the discharge during the premovement period was more likely to be significantly correlated wit h direction, whereas the discharge during the movement was correlated with both direction and distance. 7. A similar multivariate analysis o f variance was carried out on a subset (n = 34) of randomly selected c ells. The regression results obtained from single movements were compa red with the results obtained for the average movements. Although the analysis based on single trials lowered the R2, the results were simil ar. 8. On the basis of these results, we propose that both movement di stance (or a tightly coupled parameter) and movement direction are enc oded in the discharge of primary motor and superior precentral premoto r area neurons. Furthermore, for many cells firing was also correlated with target position. The distance-related modulation needs to be con sidered within the wider context that several movement parameters can covary with movement amplitude, including velocity, acceleration, forc e, and muscle activity. Distance information is not preferentially cou pled to a cell's preferred direction. In addition, evidence for a temp oral elaboration of this kinematic information was found. During the p removement period the firing is correlated preferentially with directi on. Correlation with distance was greatest during the movement. These results suggest that some degree of independent processing of distance and direction occurs.