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J Neurophysiol 81: 2415-2428, 1999;
0022-3077/99 $5.00
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The Journal of Neurophysiology Vol. 81 No. 5 May 1999, pp. 2415-2428
Copyright ©1999 by the American Physiological Society

Vertical Eye Position-Dependence of the Human Vestibuloocular Reflex During Passive and Active Yaw Head Rotations

Matthew J. Thurtell,1,2 Ross A. Black,1 G. Michael Halmagyi,1 Ian S. Curthoys,3 and Swee T. Aw1

 1Eye and Ear Research Unit, Department of Neurology, Royal Prince Alfred Hospital, Camperdown, Sydney, New South Wales 2050; and  2Department of Physiology and  3Department of Psychology, University of Sydney, Sydney, New South Wales 2006, Australia

Thurtell, Matthew J., Ross A. Black, G. Michael Halmagyi, Ian S. Curthoys, and Swee T. Aw. Vertical Eye Position-Dependence of the Human Vestibuloocular Reflex During Passive and Active Yaw Head Rotations. J. Neurophysiol. 81: 2415-2428, 1999.Vertical eye position-dependence of the human vestibuloocular reflex during passive and active yaw head rotations. The effect of vertical eye-in-head position on the compensatory eye rotation response to passive and active high acceleration yaw head rotations was examined in eight normal human subjects. The stimuli consisted of brief, low amplitude (15-25°), high acceleration (4,000-6,000°/s2) yaw head rotations with respect to the trunk (peak velocity was 150-350°/s). Eye and head rotations were recorded in three-dimensional space using the magnetic search coil technique. The input-output kinematics of the three-dimensional vestibuloocular reflex (VOR) were assessed by finding the difference between the inverted eye velocity vector and the head velocity vector (both referenced to a head-fixed coordinate system) as a time series. During passive head impulses, the head and eye velocity axes aligned well with each other for the first 47 ms after the onset of the stimulus, regardless of vertical eye-in-head position. After the initial 47-ms period, the degree of alignment of the eye and head velocity axes was modulated by vertical eye-in-head position. When fixation was on a target 20° up, the eye and head velocity axes remained well aligned with each other. However, when fixation was on targets at 0 and 20° down, the eye velocity axis tilted forward relative to the head velocity axis. During active head impulses, the axis tilt became apparent within 5 ms of the onset of the stimulus. When fixation was on a target at 0°, the velocity axes remained well aligned with each other. When fixation was on a target 20° up, the eye velocity axis tilted backward, when fixation was on a target 20° down, the eye velocity axis tilted forward. The findings show that the VOR compensates very well for head motion in the early part of the response to unpredictable high acceleration stimuli---the eye position- dependence of the VOR does not become apparent until 47 ms after the onset of the stimulus. In contrast, the response to active high acceleration stimuli shows eye position-dependence from within 5 ms of the onset of the stimulus. A model using a VOR-Listing's law compromise strategy did not accurately predict the patterns observed in the data, raising questions about how the eye position-dependence of the VOR is generated. We suggest, in view of recent findings, that the phenomenon could arise due to the effects of fibromuscular pulleys on the functional pulling directions of the rectus muscles.




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