To understand how the brain learns, we need to identify the full neural circuit for a behavior, characterize how neural responses in the circuit change during behavioral learning, and understand the nature, location, and control of the cellular changes that are responsible for learning. This goal seems attainable for the vestibulo-ocular reflex (VOR), where the neural circuit basis for learning is already partially understood. The current hypothesis for VOR learning postulated cellular changes in the cerebellar cortex and the vestibular nucleus. It suggest that the brainstem contains two parallel pathways that have been modeled on the basis of extensive biological data as unmodified and modified VOR pathways with frequency-dependent internal gains and different time delays. We now show a correspondence between the responses of different groups of neurons in the vestibular nucleus and the signals emanating from the two pathways in the model. Floccular target neurons (FTNs) and position-vestibular-pause neurons (PVPs) were identified by their discharge during eye movements and by the presence or absence of inhibition by floccular stimulation. FTNs had response gains and phases that coincided with predictions for pathways that are modified in association with learning, while PVPs had responses in agreement with predictions for the unmodified pathways. The quantitative agreement of prior model predictions and new data supports the identity of FTNs and PVPs as brainstem interneurons in the modified and unmodified VOR pathways. Other aspects of the data make predictions about how vestibular inputs are transformed as they pass through the two pathways.