Predictive pursuit behavior and activity of cerebellar Purkinje cells during eye tracking of simple and complex two-dimensional trajectories in rhesus monkeys

Smooth pursuit behavior and its neuronal correlates in the cerebellum were studied in rhesus monkeys while they tracked target spots that moved along two-dimensional (2-D) trajectories. Circular and more complex sum-of-two-sines target trajectories were created by simultaneously applying two component sinusoids along orthogonal axes. Monkeys were trained to track each trajectory repeatedly.;The first goal was to determine how precisely monkeys can track the more complex target trajectories in comparison to the sinusoidal components. Predictive pursuit was observed not only during tracking of simple sinusoids and circles, but also during tracking of more complex target motions. The averaged delay for complex pursuit was 19 ms. Predictive control was further confirmed by direct comparisons with visual feedback delays measured from eye movement responses to right-angle perturbations from circular pursuit. On average, pursuit responses were delayed for about 90 ms. Together, these results suggest that complex 2-D smooth pursuit eye movements in primates are controlled by a combination of predictive and feedback mechanisms. We also observed component interactions that suggest the system is slightly non-linear.;The second goal was to investigate the role of the cerebellum during some of the 2-D tracking tasks developed in the behavioral studies. Neural activity was recorded in the cerebellar flocculus and paraflocculus while monkeys tracked directional sinusoids, circles and complex sum-of-two-sines target trajectories. In most cases, Purkinje cell simple spike activities during pursuit were closely related to the eye movement behavior. Preferred directions of those cells that discharged during pursuit were found in all directions with a higher preference for horizontal and vertical axes. However a number of cells showed oblique preferences. Most of the cells demonstrated linear behavior such that their discharge patterns during 2-D pursuit could be approximately predicted from the summations of their responses during pursuit of component waveforms. Interestingly, nonlinear responses were also observed and were most prominent when comparing cell responses during clockwise- and counterclockwise-circular pursuit. The presence of nonlinear cells suggested possible directional specificity and saturation effects.