Cell Directional Spread Determines Accuracy, Precision, and Length of the Neuronal Population Vector

The neuronal population vector (NPV) for movement direction is the sum of weighted neuronal directional contributions. Based on theoretical considerations, we proposed recently that the sharpness of tuning will impact the directional precision, accuracy, and length of the NPV, such that sharper tuning will yield NPV with higher precision, higher accuracy, and shorter length (Mahan and Georgopoulos in Front Neural Circuits 7:92, 2013). Furthermore, we proposed that controlling the inhibitory drive in a local network could be the mechanism by which the sharpness of directional tuning would be varied, resulting in a continuous specification and control of movement's directional precision, accuracy, and speed (Mahan and Georgopoulos in Front Neural Circuits 7:92, 2013, Fig. 5). As a first step in testing this idea, here we analyzed data from 899 cells recorded in the motor cortex during performance of a center → out task. There were two major findings. First, directional selectivity varied with cell activity, such that it was higher in cells with lower mean discharge rates. And second, NPVs calculated from subsets of cells with higher directional selectivity (and, correspondingly, lower mean discharge rates) were more accurate (i.e., closer to the movement), precise (i.e., less variable), and shorter (i.e., slower; Schwartz in Science 265:540-542, 1994). These findings confirm our predictions above made from modeling (Mahan and Georgopoulos in Front Neural Circuits 7:92, 2013) and provide a simple mechanism by which desired attributes of the directional motor command can be implemented. We hypothesize that the inhibitory drive in a local network is controlled directly and independently of recurrent collaterals or common excitatory inputs to other cells. This could be achieved by a private excitation/inhibition of key inhibitory interneurons in a way similar to that in operation for Renshaw cells in the spinal cord. The presence of such a private line of inhibitory control remains to be investigated.