Three-dimensional organization of otolith-ocular reflexes in rhesus monkeys
II. Inertial detection of angular velocity.
ANGELAKI, DORA E. AND BERNHARD J. M. HESS.
Dept. of Surgery (Otolaryngology), University of Mississippi Medical
Center, Jackson MS, Dept. of Neurology, University Hospital Zurich, CH-8091,
APStracts 2:0008N, 1996.
SUMMARY AND CONCLUSIONS
1. The dynamic contribution of otolith signals to three-dimensional angular
vestibulo-ocular reflex (VOR) was studied during off-vertical axis rotations
in rhesus monkeys. In an attempt to separate response components to head
velocity from those to head position relative to gravity during low frequency
sinusoidal oscillations, large oscillation amplitudes were chosen such that
peak-to-peak head displacements exceeded 360. Since the waveforms of head
position and velocity differed in shape and frequency content, the particular
head position and angular velocity sensitivity of otolith-ocular responses
could be independently assessed. 2. During both constant velocity rotation and
low frequency sinusoidal oscillations, the otolith system generated two
different types of oculomotor responses: (a) Modulation of three-dimensional
eye position and/or eye velocity as a function of head position relative to
gravity, as presented in the preceding paper. (b) Slow phase eye velocity as a
function of head angular velocity. These two types of otolith-ocular responses
have been analyzed separately. In this paper, we focus on the angular velocity
responses of the otolith system. 3. During constant velocity off-vertical axis
rotations, a steady-state nystagmus was elicited that was maintained
throughout rotation. During low frequency sinusoidal off-vertical axis
oscillations, dynamic otolith stimulation resulted primarily in a reduction of
phase leads that characterize low frequency VOR during earth-vertical axis
rotations. Both of these effects are the result of an internally generated
head angular velocity signal of otolithic origin that is coupled through a low
pass filter to the VOR. No change in either VOR gain or phase was observed at
stimulus frequencies larger than 0.1 Hz. 4. The dynamic otolith contribution
to low frequency angular VOR exhibited three-dimensional response
characteristics with some quantitative differences in the different response
components. For horizontal VOR, the amplitude of the steady-state slow phase
velocity during constant velocity rotation and the reduction of phase leads
during sinusoidal oscillation were relatively independent of tilt angle (for
angles larger than approximately 10). For vertical and torsional VOR, the
amplitude of steady-state slow phase eye velocity during constant velocity
rotation increased, and the phase leads during sinusoidal oscillation
decreased with increasing tilt angle. The largest steady-state response
amplitudes and smallest phase leads were observed during vertical/torsional
VOR about an earth-horizontal axis. 5. The dynamic range of otolith-borne head
angular velocity information in the VOR was limited to velocities up to
approximately 110/s. Higher head velocities resulted in saturation and a
decrease in the amplitude of the steady-state response components during
constant velocity rotation and in increased phase leads during sinusoidal
oscillations. 6. The response characteristics of otolith-borne angular VORs
were also studied in animals after selective semicircular canal inactivation.
Otolith angular VORs exhibited clear low-pass filtered properties with a
corner frequency of approximately 0.05-0.1 Hz. Vectorial summation of canal
VOR alone (elicited during earth-vertical axis rotations) and otolith VOR
alone (elicited during off-vertical axis oscillations after semicircular canal
inactivation) could not predict VOR gain and phase during off-vertical axis
rotations in intact animals. This suggests a more complex interaction of
semicircular canal and otolith signals. 7. The results of this study show that
the primate low frequency enhancement of VOR dynamics during off vertical axis
rotation is independent of a simultaneous activation of the vertical and
torsional "tilt" otolith-ocular reflexes that have been characterized in the
preceding paper. The observed low frequency enhancement of VOR dynamics is
rather linked to the generation of a steady-state compensatory nystagmus
during constant velocity off-vertical axis rotations. We propose that such
"static" (i.e., steady-state) and low frequency enhancement of VOR dynamics
results from an inertial vestibular mechanism that utilizes both otolith and
semicircular canal afferent information to detect head motion in space.
Received 4 May 1995; accepted in final form 28 December 1995.
APS Manuscript Number J302-5.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1996 The American Physiological Society.
Published in APStracts on 22 January 96