Cerebellar Purkinje cells (PCs) generate two responses: the simple spike (SS), with high firing rates (>100 Hz) and the complex spike (CS), characterized by conspicuously low discharge rates (1–2 Hz). Contemporary theories of cerebellar learning suggest that the CS discharge pattern encodes an error signal that drives changes in SS activity ultimately related to changes in motor behavior. This then predicts that CS will discharge in relation to the performance error and at random once the error has been nulled by the new behavior. We tested this hypothesis with saccadic adaptation in macaque monkeys as model of cerebellar-dependent motor learning. During saccadic adaptation, error information unconsciously changes the endpoint of a saccade prompted by a visual target that shifts its final position during the saccade. This form of short-term motor learning requires the integritiy of the posterior cerebellar vermis as shown by lesion studies in monkeys and man (1, 2).

We recorded CS from PCs of the posterior vermis before, during and following saccadic adaptation. In clear contradiction to the "error signal" concept, we found that CS occurred at random before adaptation onset, i.e. when the error was maximal and built up to a specific saccade-related discharge profile during the course of adaptation. This profile became most pronounced at the end of adaptation, i.e. when the error had been nulled (3).

Next we wanted to know if this finding is specific to saccadic learning or can be generalized to other forms of motor learning.