Elimination of the error signal in the superior colliculus impairs saccade motor learning

Significance Theories of cerebellar-dependent motor learning use the error between the desired and actual movement to correct the erroneous movement. To support this idea, several studies have tried to eliminate the error signal to the cerebellum and demonstrate an impairment of learning. However, such former approaches have not been successful because blocking the error signal also affected the movement to be learned. In this study, we selectively block an error signal for saccade adaptation, a type of cerebellar motor learning, by inactivating the source of the error signal in the superior colliculus without affecting the movement to be learned. Saccade adaptation was impaired. Thus, our study provides the first experimental evidence that an error signal is required for cerebellar motor learning. When movements become dysmetric, the resultant motor error induces a plastic change in the cerebellum to correct the movement, i.e., motor adaptation. Current evidence suggests that the error signal to the cerebellum is delivered by complex spikes originating in the inferior olive (IO). To prove a causal link between the IO error signal and motor adaptation, several studies blocked the IO, which, unfortunately, affected not only the adaptation but also the movement itself. We avoided this confound by inactivating the source of an error signal to the IO. Several studies implicate the superior colliculus (SC) as the source of the error signal to the IO for saccade adaptation. When we inactivated the SC, the metrics of the saccade to be adapted were unchanged, but saccade adaptation was impaired. Thus, an intact rostral SC is necessary for saccade adaptation. Our data provide experimental evidence for the cerebellar learning theory that requires an error signal to drive motor adaptation.