Motor systems are under a continuous adaptive process to maintain behavior throughout developmental changes and disease, a process called motor learning. Simple behaviors with easily measurable inputs and outputs are best suited to understand the neuronal signals that contribute to the required motor learning. Considering simple behaviors, the vestibulo-ocular reflex (VOR) allows quantification of its input and motor output and its neural circuitry is among the best documented. The main candidates for plastic change are the cerebellum and its target neurons in the brainstem. This review focuses on recent data regarding the involvement of the cerebellum in VOR motor learning. Learning can be divided into that acutely acquired over a period of hours and that chronically acquired over longer periods. Both acute and chronic learning have three phases named acquisition, consolidation, and retention. The cerebellar role in retention is disputed, but there is a consensus on the need of an intact cerebellum for acquisition. Data from neuronal recording, lesion studies and transgenic mouse experiments is complex but suggests that the signal representation in the cerebellum contains aspects of both motor output and sensory input. The cerebellum apparently uses different mechanisms for acute and chronic learning as well as for increases and decreases in VOR gain. Recent studies also suggest that the signal content in the cerebellum changes following learning and that the mechanisms used for chronic adaptation involve not only changes in a head velocity component but also in the efference copy of an eye movement command signal reaching Purkinje cells. This data leads to a new conceptual framework having implications for developing theories on the role of the cerebellum in motor learning and in the search for plastic elements within the VOR circuitry. For chronic learning we hypothesize that changes in the head velocity information traveling through the circuitry occur in parallel with changes in the integrator pathway and the efference copy pathway. We further propose that these changes are necessary to maintain the broadband characteristics of the learned behavior.