Cognitive spatial-motor processes - 7. The making of movements at an angle from a stimulus direction: studies of motor cortical activity at the single cell and population levels

Two rhesus monkeys were trained to move a handle on a two-dimensional (2-D) working surface either towards a visual stimulus ("direct" task) or in a direction orthogonal and counterclockwise (CCW) from the stimulus ("transformation" task), depending on whether the stimulus appeared dim or bright, respectively. Thus the direction of the stimulus (S, in polar coordinates) and the direction of the movement (M) were the same in the direct task but differed in the transformation task, such that M = S + 90°CCW. The task (i.e. brightness) condition (k = 2, i.e. direct or transformation) and the direction of the stimulus (m = 8, i.e. 8 equally spaced directions on a circle) resulted in 16 combinations (k × m = 16 "classes") that were varied from trial to trial in a randomized block design. In 8 of these combinations the direction of the stimulus was the same for both tasks, whereas the direction of the movement was the same in the remaining 8 cases. The electrical signs of cell activity (N = 394 cells) in the arm area of the motor cortex (contralateral to the performing arm) were recorded extracellularly. The neural activity was analyzed at the single cell and neuronal population levels, and a modeling of the time course of single activity during the transformation task was carried out. We found the following, (a) Individual cells were active in both tasks; no cells were found that were active exclusively in only one of the two tasks. The patterns of single cell activity in the transformation task frequently differed from those observed in the direct task when the stimulus or the movement were the same. More specifically, cells could not be consistently classified as "movement"-or "stimulus"-related for frequently the activity of a particular cell would seem "movement-related" for a particular stimulus-movement combination, "stimulus-related" for another combination, or unrelated to either movement or stimulus for still another combination. Thus no real insight could be gained from such an analysis of single cell activity. (e) In a different analysis, we explored the idea that a changing directional signal could be detected in the time course of single cell activity during the reaction time. For that purpose we modeled the time course of single activity observed in the transformation task as a linear, weighted combination of influences from the direct task, taking the time patterns of cell activity during the stimulus, intermediate and movement directions in the direct task as estimates of the postulated directional influences. The results were inconclusive, in the sense that the best weighting scheme led to more than 46 % error in prediction in more than 50 % of the comparisons. Moreover, various combinations gave closely similar predictions. (c) An analysis of the activity of the neuronal population using the time evolution of the neuronal population vector (Georgopoulos et al. 1984) revealed an orderly rotation of the neuronal population vector from the direction of the stimulus towards the direction of the movement through the 90°CCW angle. (d) The hypothesis was tested that this apparent rotation of the population vector could be the result of activation of two subsets of cells, one with preferred directions at or near the stimulus direction, and the other with preferred directions at or near the movement directions: if cells of the former type were recruited at the beginning of the reaction time, followed by those of the second type, then the vector sum of the two could provide the rotating population vector. However, such a preferential activation of "stimulus-direction" centered and "movement-direction" centered cells was not observed. (e) On the other hand, a true rotation of the population vector could be reflected in the engagement of cells with intermediate preferred directions during the middle of the reaction time. Indeed, such a transient increase in the recruitment of cells with intermediate (i.e. between the stimulus and movement) preferred directions during the middle of the reaction time was observed. This supports the idea of a true rotation of the population signal.