Task-related coding of stimulus and response in cat red nucleus

Summary In the present study we recorded the activity of single neurons in the forelimb area of red nucleus (RN) during performance of three step-tracking tasks designed to dissociate the coding of stimulus and response variables in the discharge of recorded neurons. In two of these tasks, the standard and stimulus-reversal arm tasks, elbow flexion and extension were elicited by different stimuli enabling us to distinguish activity correlated with the forelimb response from the stimulus eliciting it. The third task (neck task) allowed us to determine whether neuronal modulation was related to an unconditioned orienting response that occurred concurrently with the forelimb response. We have previously reported that these three tasks separate neurons in MCx whose modulation precedes the response (lead cells) into three distinct classes in which task-related activity either is correlated with the direction of the forelimb response, correlated with the stimulus, or not correlated with either (Martin and Ghez 1985). All lead cells, however, remained timed to the stimulus rather than to the response. The present results show that RN lead cells can be subdivided into the same three classes as those in MCx and their discharge was also contingent on the subsequent production of a behavioral response. (1) Force-direction neurons (35%; n = 16) showed changes in activity correlated with the production of forearm force in a particular direction suggesting that they could participate in selecting the appropriate forelimb response. The onset of task-related modulation of activity was better timed to the response, in contrast to force-direction neurons in MCx, which were better timed to the stimulus. (2) Stimulus-direction neurons (18%; n = 8) modulated their activity in relation to a particular stimulus evoking either flexor or extensor responses and during neck task performance. These neurons could be involved in processing stimulus information or in the production of neck torque. The task-related discharge of these lead cells was better timed to the stimulus than to either the forelimb or the neck response. (3) Nondirectional neurons (47%; n = 21) modulated their activity during all tasks examined. Their discharge did not correlate with any specific feature of the stimulus or response, and as a group, was better timed to the stimulus than to the response. Nondirectional neurons may participate in some aspect of motor preparation. To determine the relative contributions of RN and MCx lead cells to response initiation, we compared the amount of response latency variance that could be explained by variation in the latency of the unit modulation to the stimulus for the present data and the data in the earlier MCx study (Martin and Ghez 1985). Between 38% and 53% of response latency variance (for trials examined during performance of the standard arm and stimulus reversal tasks) was accounted for by the latency variations of RN force direction neurons; in contrast, 8% and 11% for MCx force-direction neurons. Variations in timing of stimulus-direction neurons in both RN and MCx account for less than 10% of response latency variance. Our findings suggest that, in the tasks examined, RN force-direction neurons play a more direct role than MCx force-direction neurons in initiating and selecting responses to stimuli. We hypothesized that this subcortical control reflects the high degree of stereotypy of the motor response examined.