Physiological properties of vestibular primary afferents that mediate motor learning and normal performance of the vestibulo-ocular reflex in monkeys.

We have used electrical stimulation of the vestibular apparatus to reveal parallels between the physiological responses of the vestibular afferents activated at different currents and the properties of the evoked eye movements before and after magnifying spectacles had been used to cause motor learning in the vestibulo-ocular reflex (VOR). Stimulation with the lowest currents caused little or no eye motion, but activated all the afferents with irregular spontaneous discharge, low sensitivities to head velocity, and highly phasic responses during rapid head turns. Stimulation with moderate currents caused substantial eye motion that was weakly affected by motor learning; these currents activated afferents with a wide range of physiological properties, including many that had intermediate discharge regularity, high sensitivity to head velocity, and clear phasic responses during rapid head turns. Stimulation at still higher currents caused still larger eye movements that were strongly altered by motor learning; these currents activated primarily afferents that had regular spontaneous discharge, lower sensitivities to head velocity, and tonic responses during rapid head turns. Stimulation at the highest currents did not cause any further increment in the amplitude of the evoked eye movement, but activated the afferents with the most regular spontaneous discharge and the lowest sensitivities to head velocity. The data imply that the VOR pathways receive substantial vestibular inputs from afferents with a middle range of thresholds for electrical stimulation. These afferents have a wide range of physiological properties, including a large group that shows substantial phasic responses during rapid head turns. The data also suggest that only a subset of these afferents, primarily those with more regular spontaneous discharge, project into the VOR pathways that are modified in association with motor learning.