We followed simple- and complex-spike firing of Purkinje cells (PCs) in the floccular complex of the cerebellum through learned modifications of the pursuit eye movements of two monkeys. Learning was induced by double steps of target speed in which initially stationary targets move at a "learning" speed for 100 ms and then change to either a higher or lower speed in the same direction. In randomly interleaved control trials, targets moved at the learning speed in the opposite direction. When the learning direction was the ON direction for simple-spike responses, learning was associated with statistically significant changes in simple-spike firing for 10 of 32 PCs. Of the 10 PCs that showed significant expressions of learning, 8 showed changes in simple-spike output in the expected direction: increased or decreased firing when eye acceleration increased or decreased through learning. There were no statistically significant changes in simple-spike responses or eye acceleration during pursuit in the control direction. When the learning direction was in the OFF direction for simple-spike responses, none of 15 PCs showed significant correlates of learning. Although changes in simple-spike firing were recorded in only a subset of PCs, analysis of the population response showed that the same relationship between population firing and eye acceleration obtained before and after learning. Thus learning is associated with changes that render the modified population response appropriate to drive the changed behavior. To analyze complex-spike firing during learning we correlated complex-spike firing in the second, third, and fourth 100 ms after the onset of target motion with the retinal image motion in the previous 100 ms. Data were largely consistent with previous evidence that image motion drives complex spikes with a direction selectivity opposite that for simple spikes. Comparison of complex-spike responses at different times after the onset of control and learning target motions in the learning direction implied that complex spikes could guide learning during decreases but not increases in eye acceleration. Learning caused increases or decreases in the sensitivity of complex spikes to image motion in parallel with changes in eye acceleration. Complex-spike responses were similar in all PCs, including many in which learning did not modify simple-spike responses. Our data do not disprove current theories of cerebellar learning but suggest that these theories would have to be modified to account for simple- and complex-spike firing of floccular Purkinje cells reported here.

Learning was induced in smooth pursuit eye movements by repeated presentation of targets that moved at one speed for 100 msec and then changed to a second, higher or lower, speed. The learned changes, measured as eye acceleration for the first 100 msec of pursuit, were largest in a "late" interval from 50 to 80 msec after the onset of pursuit and were smaller and less consistent in the earliest 30 msec of pursuit. In each experiment, target motion in one direction consisted of learning trials, whereas target motion in the opposite (control) direction consisted of trials in which targets moved at a constant speed for the entire duration of the trial. Under these conditions, the learning did not generalize to the control direction. For target motion in the learning direction, the changes in pursuit generalized to responses evoked by targets moving at speeds ranging from 15 to 45 degrees/sec as well as to targets of different colors and sizes. Although learning was induced at the initiation of pursuit, it generalized to the response to image motion in the learning direction when it was presented during pursuit in the learning direction. However, learning did not generalize to the response to image motion in the learning direction when it was presented during pursuit in the control direction. The results suggest that the learning does not occur in purely sensory or motor coordinates but in an intermediate reference frame at least partly defined by the direction of eye movement. The selectivity of learning provides new evidence for a previously hypothesized neural "switch" that gates visual information on the basis of movement direction. This selectivity also suggests that the locus of pursuit learning is in pathways related to the operation of the switch.