Cerebellar flocculus and ventral paraflocculus Purkinje cell activity during predictive and visually driven pursuit...

Purkinje cells in the flocculus and ventral paraflocculus were studied in tasks designed to distinguish predictive versus visually guided mechanisms of smooth pursuit. A sum-of-sines task allowed studies of complex predictive pursuit. A perturbation task examined visually driven pursuit during unpredictable right-angle changes in target direction. A gap task examined pursuit that was maintained when the target was turned off. Neural activity patterns were quantified using multi-linear models with sensitivities to the position, velocity, and acceleration of both motor output (eye motion) and visual input (retinal slip). During the sum-of-sines task, neural responses led eye motion by an average of 12 ms, a value larger than the 9-ms transmission delay between flocculus stimulation and eye motion. This suggests that flocculus/paraflocculus neurons drove pursuit along predictable sum-of-sines trajectories. In contrast, neural responses led eye motion by an average of only 2 ms during the perturbation task and by 6 ms during the gap task. These values suggest a follow-up role during tasks more heavily dependent on visual processing. Activity in all three tasks was explained primarily by sensitivities to eye position and velocity. Eye acceleration played a minor role during ongoing pursuit, although its influence on firing rate increased during the high accelerations following unexpected changes in target motion. Retinal slip had a relatively small influence on responses during pursuit. This was particularly true for the sum-of-sines and gap tasks where predictive control eliminated any consistent retinal-slip signals that might have been used to drive the eye. Surprisingly, the influence of retinal slip did not increase appreciably during unpredictable perturbations in target direction that generated large amounts of retinal slip. Thus although visual control signals are needed in varying amounts during the three pursuit tasks, they have been converted to motor control signals by the time they leave the flocculus/paraflocculus system. Individual neurons showed a remarkable constancy in eye-sensitivity direction across tasks that indicated direct links to oculomotor neurons. However, some neurons showed changes in sensitivity magnitude that suggested changes in control strategy for different tasks. Magnitude differences were largest for the perturbation task. We conclude that the flocculus/paraflocculus system plays a major role in driving predictive pursuit. It also processes visually driven control signals that originate in other brain regions after a slight delay.