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The Journal of Neurophysiology Vol. 81 No. 5 May 1999, pp. 2538-2557
Copyright ©1999 by the American Physiological Society
Department of Neurobiology, Pharmacology and Physiology, University of Chicago, Chicago, Illinois 60637
Chen-Huang, Chiju and
Robert A. McCrea.
Effects of Viewing Distance on the Responses of Vestibular
Neurons to Combined Angular and Linear Vestibular Stimulation. J. Neurophysiol. 81: 2538-2557, 1999.
Effects of viewing distance on the responses of vestibular neurons to
combined angular and linear vestibular stimulation. The firing
behavior of 59 horizontal canal-related secondary vestibular neurons
was studied in alert squirrel monkeys during the combined angular and
linear vestibuloocular reflex (CVOR). The CVOR was evoked by
positioning the animal's head 20 cm in front of, or behind, the axis
of rotation during whole body rotation (0.7, 1.9, and 4.0 Hz). The
effect of viewing distance was studied by having the monkeys fixate
small targets that were either near (10 cm) or far (1.3-1.7 m) from
the eyes. Most units (50/59) were sensitive to eye movements and were
monosynaptically activated after electrical stimulation of the
vestibular nerve (51/56 tested). The responses of eye movement-related
units were significantly affected by viewing distance. The viewing
distance-related change in response gain of many eye-head-velocity and
burst-position units was comparable with the change in eye movement
gain. On the other hand, position-vestibular-pause units were
approximately half as sensitive to changes in viewing distance as were
eye movements. The sensitivity of units to the linear vestibuloocular
reflex (LVOR) was estimated by subtraction of angular vestibuloocular reflex (AVOR)-related responses recorded with the head in the center
of the axis of rotation from CVOR responses. During far target viewing,
unit sensitivity to linear translation was small, but during near
target viewing the firing rate of many units was strongly modulated.
The LVOR responses and viewing distance-related LVOR responses of most
units were nearly in phase with linear head velocity. The signals
generated by secondary vestibular units during voluntary cancellation
of the AVOR and CVOR were comparable. However, unit sensitivity to
linear translation and angular rotation were not well correlated either
during far or near target viewing. Unit LVOR responses were also not
well correlated with their sensitivity to smooth pursuit eye movements
or their sensitivity to viewing distance during the AVOR. On the other
hand there was a significant correlation between static eye position
sensitivity and sensitivity to viewing distance. We conclude that
secondary horizontal canal-related vestibuloocular pathways are an
important part of the premotor neural substrate that produces the LVOR.
The otolith sensory signals that appear on these pathways have been
spatially and temporally transformed to match the angular eye movement
commands required to stabilize images at different distances. We
suggest that this transformation may be performed by the circuits
related to temporal integration of the LVOR.
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