Climbing fibers control purkinje cell representations of behavior

A crucial issue in understanding cerebellar function is the interaction between simple spike (SS) and complex spike (CS) discharge, the twofundamentallydifferent activitymodalities of Purkinjecells. Althoughseveral hypotheseshaveprovidedinsightsintotheinteraction, none fully explains or is completely consistent with the spectrum of experimental observations. Here, we show that during a pseudorandom manual tracking task in the monkey (Macaca mulatta), climbing fiber discharge dynamically controls the information present in the SS firing, triggering robust and rapid changes in the SS encoding of motor signals in 67% of Purkinje cells. The changes in encoding, tightly coupled to CS occurrences, consist of either increases or decreases in the SS sensitivity to kinematics or position errors and are not due to differences in SS firing rates or variability. Nor are the changes in sensitivity due to CS rhythmicity. In addition, the CS-coupled changes in encoding are not evoked by changes in kinematics or position errors. Instead, CS discharge most often leads alterations in behavior. Increases in SS encoding of a kinematic parameter are associated with larger changes in that parameter than are decreases in SS encoding. Increases in SS encoding of position error are followed by and scale with decreases in error. The results suggest a novel function of CSs, in which climbing fiber input dynamically controls the state of Purkinje cell SS encoding in advance of changes in behavior.