Journal of Neuroscience, Vol 14, 1290-1308, Copyright © 1994 by Society for Neuroscience
Physiological properties of vestibular primary afferents that mediate motor learning and normal performance of the vestibulo-ocular reflex in monkeys
HM Bronte-Stewart and SG Lisberger
Department of Physiology, W. M. Keck Foundation Center for Integrative Neuroscience, University of California, San Francisco 94143.
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.