Variation, signal, and noise in cerebellar sensory-motor processing for smooth-pursuit eye movements

Neural responses are variable, yet motor performance can be quite precise. To ask how neural signal and noise are processed in the brain during sensory - motor behavior, we have evaluated the trial- by- trial variation of Purkinje cell ( PC) activity in the floccular complex of the cerebellum, an intermediate stage in the neural circuit for smooth- pursuit eye movements. We find strong correlations between small trial- by- trial variations in the simple spike activity of individual PCs and the eye movements at the initiation of pursuit. The correlation is lower but still present during steady- state pursuit. Recordings from a few pairs of PCs verified the predictions of a model of the PC population, that there is a transition from highly covariant PC activity during movement initiation to more independent activity later on. Application to the data of a theoretical and computational analysis suggests that variation in pursuit initiation arises mostly from variation in visual motion signals that provide common inputs to the PC population. Variation in eye movement during steady- state pursuit can be attributed primarily to signal- dependent motor noise that arises downstream from PCs.