Neuron activity in monkey vestibular nuclei during vertical vestibular stimulation and eye movements.

To elucidate how information is processed in the vestibuloocular reflex (VOR) pathways subserving vertical eye movements, extracellular single-unit recordings were obtained from the vestibular nuclei of alert monkeys trained to track a visual target with their eyes while undergoing sinusoidal pitch oscillations (0.2-1.0 Hz). Units with activity related to vertical vestibular stimulation and/or eye movements were classified as either vestibular units (n = 53), vestibular plus eye-position units (n = 30), pursuit units (n = 10), or miscellaneous units (n = 5), which had various combinations of head- and eye-movement sensitivities. Vestibular units discharged in relation to head rotation, but not to smooth eye movements. On average, these units fired approximately in phase with head velocity; however, a broad range of phase shifts was observed. The activities of 8% of the vestibular units were related to saccades. Vestibular plus eye-position units fired in relation to head velocity and eye position and, in addition, usually to eye velocity. Their discharge rates increased for eye and head movements in opposite directions. During combined head and eye movements, the modulation in unit activity was not significantly different from the sum of the modulations during each alone. For saccades, the unit firing rate either decreased to zero or was unaffected. Pursuit units discharged in relation to eye position, eye velocity, or both, but not to head movements alone. For saccades, unit activity usually either paused or was unaffected. The eye-movement-related activities of the vestibular plus eye-position and pursuit units were not significantly different. A quantitative comparison of their firing patterns suggests that vestibular, vestibular plus eye-position, and pursuit neurons in the vestibular nucleus could provide mossy fiber inputs to the flocculus. In addition, the vertical vestibular plus eye-position neurons have discharge patterns similar to those of fibers recorded rostrally in the medial longitudinal fasciculus. Therefore, our data support the view that vertical vestibular plus eye-position neurons are interneurons of the VOR.