Eye movements induced by off-vertical axis rotation (OVAR) at small angles of tilt

Abstract

Off-vertical rotation (OVAR) in darkness induced continuous horizontal nystagmus in humans at small tilts of the rotation axis (5 to 30 degrees). The horizontal slow eye velocity had two components: a mean velocity in the direction opposite to head rotation and a sinusoidal modulation around the mean. Mean velocity generally did not exceed 10 deg/s, and was less than or equal to the maximum velocity of optokinetic after-nystagmus (OKAN). Both the mean and modulation components of horizontal nystagmus increased with tilt angle and rotational velocity. Vertical slow eye velocity was also modulated sinusoidally, generally around zero. The amplitude of the vertical modulation increased with tilt angle, but not with rotational velocity. In addition to modulations in eye velocity, there were also modulations in horizontal and vertical eye positions. These would partially compensate for head position changes in the yaw and pitch planes during each cycle of OVAR. Modulations in vertical eye position were regular, increased with increases in tilt angle and were separated from eye velocity by 90 deg. These results are compatible with the interpretation that, during OVAR, mean slow velocity of horizontal nystagmus is produced by the velocity storage mechanism in the vestibular system. In addition, they indicate that the otolith organs induce compensatory eye position changes with regard to gravity for tilts in the pitch, yaw and probably also the roll planes. Such compensatory changes could be utilized to study the function of the otolith organs. A functional interpretation of these results is that nystagmus attempts to stabilize the image on the retina of one point of the surrounding world. Mean horizontal velocity would then be opposite to the estimate of head rotational velocity provided by the output of the velocity storage mechanism, as charged by an otolithic input during OVAR. In spite of the lack of actual translation, an estimate of head translational velocity could, in this condition, be constructed from the otolithic signal. The modulation in horizontal eye position would then be compensatory for the perceived head translation. Modulation of vertical eye velocity would compensate for actual changes in head orientation with respect to gravity.

Using sensory weighting to model the influence of canal, otolith and visual cues on spatial orientation and eye movements

“…5), the horizontal VOR exhibits a sinusoidal modulation with the same rate as the rotation, as well as a small usually compensatory bias in humans (Benson and Bodin 1966b;Darlot et al 1988;Wall and Furman 1990). The compensatory bias arises from the utilization of otolith cues by the CNS, since a bias is still present after canal plugging (Cohen et al 1983;Correia and Money 1970).…”

“…Additional processing is essential, especially at the perceptual level. For example, perceptual responses during yaw rotation about a tilted axis (Darlot et al 1987;Denise et al 1988) or earth-horizontal axis (Guedry 1965) may result from additional low-pass and high-pass filtering of the sensory estimates of gravity and linear acceleration, respectively, as suggested by Mittelstaedt et al (1989).…”

Human 3-D aVOR with and without otolith stimulation

“…In humans, otolith-canal interactions have been studied in other paradigms such as long duration off-vertical axis rotations, where compensatory eye velocity remains after canal signals have decayed (Haslwanter et al 2000;Harris and Barnes 1987;Furman et al 1992;Darlot et al 1988). While some studies suggest caution in interpreting results from paradigms with strong cue-conflicts (Bockisch et al 2003), it is interesting that they produce comparable results: during 100 deg/s rotation about an earth-horizontal axis with subjects oriented parallel to the rotation axis, a step in velocity produces horizontal nystagmus that decays to a very small offset value of perhaps 5% of the rotation velocity (Haslwanter et al 2000).…”

“…Evidence for otolith contribution to the aVOR in nonhumans exists [cat: (Rude and Baker 1988;Blanks et al 1978;Tomko et al 1988); rabbit: (Barmack and Pettorossi 1988;Pettorossi et al 1991); monkey: (Angelaki and Hess 1996;Angelaki et al 2002)]. In humans, similar evidence for a contribution of dynamic otolith signals to the aVOR mainly comes from experiments with stimuli that do not occur in everyday life, for example, long-duration offvertical axis rotation (Haslwanter et al 2000;Harris and Barnes 1987;Furman et al 1992;Darlot et al 1988), peror post-rotatory tilt (Bockisch et al 2003;Fetter et al 1996;Zupan et al 2000), or eccentric rotation about the earth-vertical axis (Merfeld et al 2001;Lansberg et al 1965). These stimuli include strong, unusual conflicts between sensory cues.…”

Bilateral Otolith Contribution to Spatial Coding in the Vestibular System

“…During constant velocity OVAR, the gravity vector elicits two patterns of VOR in darkness: (a) eye oscillations that are dependent on head position relative to gravity, and (b) a unidirectional steady-state nystagmus that is compensatory to head rotation [20, 41,42,60,62,63]. This compensatory nystagmus to head velocity arises primarily in the otolith organs [39], suggesting that otolith organs detect not only head orientation relative to gravity but also angular velocity of the head in space [2].…”