PHYSIOLOGICAL-PROPERTIES OF VESTIBULAR PRIMARY AFFERENTS THAT MEDIATEMOTOR LEARNING AND NORMAL PERFORMANCE OF THE VESTIBULOOCULAR REFLEX IN MONKEYS

We have used electrical stimulation of the vestibular apparatus to rev eal parallels between the physiological responses of the vestibular af ferents activated at different currents and the properties of the evok ed eye movements before and after magnifying spectacles had been used to cause motor learning in the vestibule-ocular reflex (VOR). Stimulat ion with the lowest currents caused little or no eye motion, but activ ated all the afferents with irregular spontaneous discharge, low sensi tivities to head velocity, and highly phasic responses during rapid he ad turns. Stimulation with moderate currents caused substantial eye mo tion that was weakly affected by motor learning; these currents activa ted 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. Sti mulation at still higher currents caused still larger eye movements th at were strongly altered by motor learning; these currents activated p rimarily afferents that had regular spontaneous discharge, lower sensi tivities to head velocity, and tonic responses during rapid head turns . Stimulation at the highest currents did not cause any further increm ent in the amplitude of the evoked eye movement, but activated the aff erents with the most regular spontaneous discharge and the lowest sens itivities to head velocity. The data imply that the VOR pathways recei ve substantial vestibular inputs from afferents with a middle range of thresholds for electrical stimulation. These afferents have a wide ra nge of physiological properties, including a large group that shows su bstantial phasic responses during rapid head turns. The data also sugg est that only a subset of these afferents, primarily those with more r egular spontaneous discharge, project into the VOR pathways that are m odified in association with motor learning.