Directional Organization of Eye Movement and Visual Signals in the Floccular Lobe of the Monkey Cerebellum

The floccular lobe of the monkey is critical for the generation of visually-guided smooth eye movements. The present experiments reveal physiological correlates of the directional organization in the primate floccular lobe by examining the selectivity for direction of eye motion and visual stimulation in the firing of individual Purkinje cells (PCs) and mossy fibers. During tracking of sinusoidal target motion along different axes in the frontoparallel plane, PCs fell into two classes based on the axis that caused the largest modulation of simple-spike firing rate. For "horizontal" PCs, the response was maximal during horizontal eye movements, with increases in firing rate during pursuit toward the side of recording (ipsiversive). For "vertical" PCs, the response was maximal during eye movement along an axis just off pure vertical, with increases in firing rate during pursuit directed downward and slightly contraversive. During pursuit of target motion at constant velocity, PCs again fell into horizontal and vertical classes that matched the results from sinusoidal tracking. In addition, the directional tuning of the sustained "eye velocity" and transient "visual" components of the neural responses obtained during constant velocity tracking were very similar. PCs displayed very broad tuning approximating a cosine tuning curve; the mean half-maximum bandwidth of their tuning curves was 170-180 degrees. Other cerebellar elements, related purely to eye movement and presumed to be mossy fibers, exhibited tuning approximately 40 degrees narrower than PCs and had best directions that clustered around the four cardinal directions. Our data indicate that the motion signals encoded by PCs in the monkey floccular lobe are segregated into channels that are consistent with a coordinate system defined by the vestibular apparatus and eye muscles. The differences between the tuning properties exhibited by PCs compared with mossy fibers indicate that a spatial transformation occurs within the floccular lobe.