Multiple components in direction learning in smooth pursuit eye movements of monkeys

We analyzed behavioral features of smooth pursuit eye movements to characterize the course of acquisition and expression of multiple neural components of motor learning. Monkeys tracked a target that began to move in an initial "pursuit" direction and suddenly, but predictably, changed direction after a fixed interval of 250 ms. As the trial is repeated, monkeys learn to make eye movements that predict the change in target direction. Quantitative analysis of the learned response revealed evidence for multiple, dynamic, parallel processes at work during learning. 1) The overall learning followed at least two trial courses: a fast component grew and saturated rapidly over tens of trials, and a slow component grew steadily over up to 1,000 trials. 2) The temporal specificity of the learned response within each trial was crude during the first 100 trials but then improved gradually over the remaining trials. 3) External influences on the gain of pursuit initiation modulate the expression but probably not the acquisition of learning. The gain of pursuit initiation and the expression of the learned response decreased in parallel, both gradually through a 1,000-trial learning block and immediately between learning trials with different gains in the initiation of pursuit. We conclude that at least two distinct neural mechanisms drive the acquisition of pursuit learning over 100 to 1,000 trials (3 to 30 min). Both mechanisms generate underlying memory traces that are modulated in relation to the gain of pursuit initiation before expression in the final motor output. NEW & NOTEWORTHY We show that cerebellum-dependent direction learning in smooth pursuit eye movements grows in at least two components over 1,100 behavioral learning repetitions. One component grows over tens of trials and the other over hundreds. Within trials, learned temporal specificity gradually improves over hundreds of trials. The expression of each learning component on a given trial can be modified by external factors that do not affect the underlying memory trace.