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The Journal of Neurophysiology Vol. 88 No. 1 July 2002, pp. 13-28
Copyright ©2002 by the American Physiological Society
Aerospace Medical Research Unit, McGill University, Montreal, Quebec H3G 1Y6, Canada
Huterer, Marko and
Kathleen E. Cullen.
Vestibuloocular Reflex Dynamics During High-Frequency and
High-Acceleration Rotations of the Head on Body in Rhesus Monkey. J. Neurophysiol. 88: 13-28, 2002. For frequencies >10 Hz, the vestibuloocular reflex (VOR) has
been primarily investigated during passive rotations of the head on the
body in humans. These prior studies suggest that eye movements lag head
movements, as predicted by a 7-ms delay in the VOR reflex pathways.
However, Minor and colleagues recently applied whole-body rotations of
frequencies
15 Hz in monkeys and found that eye movements were nearly
in phase with head motion across all frequencies. The goal of the
present study was to determine whether VOR response dynamics actually
differ significantly for whole-body versus head-on-body rotations. To
address this question, we evaluated the gain and phase of the VOR
induced by high-frequency oscillations of the head on the body in
monkeys by directly measuring both head and eye movements using the
magnetic search coil technique. A torque motor was used to rotate the
heads of three Rhesus monkeys over the frequency range 5-25 Hz. Peak
head velocity was held constant, first at ±50°/s and then
±100°/s. The VOR was found to be essentially compensatory across all
frequencies; gains were near unity (1.1 at 5 Hz vs. 1.2 at 25 Hz), and
phase lag increased only slightly with frequency (from 2° at 5 Hz to
11° at 25 Hz, a marked contrast to the 63° lag at 25 Hz predicted
by a 7-ms VOR latency). Furthermore, VOR response dynamics were
comparable in darkness and when viewing a target and did not vary with
peak velocity. Although monkeys offered less resistance to the initial
cycles of applied head motion, the gain and phase of the VOR did not
vary for early versus late cycles, suggesting that an efference copy of
the motor command to the neck musculature did not alter VOR response
dynamics. In addition, VOR dynamics were also probed by applying
transient head perturbations with much greater accelerations (peak
acceleration >15,000°/s2) than have been
previously employed. The VOR latency was between 5 and 6 ms, and mean
gain was close to unity for two of the three animals tested. A simple
linear model well described the VOR responses elicited by sinusoidal
and transient head on body rotations. We conclude that the VOR is
compensatory over a wide frequency range in monkeys and has similar
response dynamics during passive rotation of the head on body as during
passive rotation of the whole body in space.
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