Gain changes in the vestibuloocular reflex (VOR) during visual-vestibular mismatch stimulation serve as a model system for motor learning. The cerebellar flocculus and its target neurons in the brain stem (FTN) are candidates for the storage of these novel VOR gains. We have recently studied the changes in vertical flocculus Purkinje cells after chronic VOR motor learning. Recently we recorded Y neurons (a vertical type of FTNs) after chronic VOR motor learning and compared these records with vertical floccular Purkinje cells to document any changes in inputs to FTNs and understand how Y neurons and the vertical Purkinje cells fit into a general model for the vertical VOR. Analysis illustrates that the changes observed in Purkinje cells are not transferred to Y neurons, suggesting that the gain of their synaptic interconnection was modified. We quantified changes in both populations and employed simulations to study changes in parallel pathways to FTNs and to extract the role of the flocculus in VOR adaptation. Low-gain adaptation results in more drastic changes than its high-gain counterpart, causing increases in head velocity sensitivity in parallel pathways. Simulations suggest that cerebellar and brain stem plasticity both participate in novel VOR gain storage and that results obtained following floccular lesion are the product of different mechanisms than those operating in the intact animal.