The human vertical translational vestibulo-ocular reflex. Normal and abnormal responses

Abstract

Geometric considerations indicate that the human translational vestibulo-ocular reflex (tVOR) should have substantially different properties than the angular vestibulo-ocular reflex (aVOR). Specifically, tVOR cannot simultaneously stabilize images of distant and near objects on the retina. Most studies make the tacit assumption that tVOR acts to stabilize foveal images even though, in humans, tVOR is reported to compensate for less than 60% of foveal image motion. We have determined that the compensation gain (eye rotational velocity/required eye rotational velocity to maintain foveal target fixation) of tVOR is held steady at approximately 0.6 during viewing of either near or distant targets during vertical (bob) translations in ambient illumination. We postulate that tVOR evolved not to stabilize the image of the target on the fovea, but rather to minimize retinal image motion between objects lying in different depth planes, in order to optimize motion parallax information. Such behavior is optimized when binocular visual cues of both near and distant targets are available in ambient light. Patients with progressive supranuclear palsy or cerebellar ataxia show impaired ability to increase tVOR responses appropriately when they view near targets. In cerebellar patients, impaired ability to adjust tVOR responses to viewing conditions occurs despite intact ability to converge at near. Loss of the ability to adjust tVOR according to viewing conditions appears to represent a distinct disorder of vestibular function.

Figure 1

Representative records from a healthy normal subject (A,B), a patient with PSP (C,D), and a patient with cerebellar ataxia (E,F). At the bottom of each panel, tVOR responsivity (Resp, in degrees*seconds/meter) is stated. Note that, except for vergence (gray lines), individual traces have been offset in position to aid clarity of display. Positive values indicate downward and divergence movement. Note how tVOR (vertical eye rotation) increased during near viewing (17 cm) compared with far viewing (2 m) for the normal subject, but remained less than the eye movement required to keep the fovea (line of sight) pointed at the visual target (dotted lines). The PSP patient showed inability to converge at near, and tVOR did not increase. The patient with cerebellar ataxia was able to converge at near, but could not substantially increase tVOR responsivity. Required eye rotations were computed from measured head movements.

Figure 2

Summary of tVOR responses to bob at 2.0 Hz of 20 normal subjects. (A) Responsivity plotted as a function of vergence angle. Note that during near viewing (diamonds, corresponding to larger vergence angles), responsivity increases substantially compared with far viewing (circles). (B) Box plots, showing percentiles for compensation gain values during far and near viewing; these were similar, despite the large changes of responsivity shown in (A).

Figure 3

Representative records comparing direct versus prism viewing for a single subject. Note how tVOR is larger during viewing the target at 17cm versus 40 cm, but is unaffected by vergence angle. Plotting conventions are similar to Fig. 1.

Figure 4

Representative records of the effects of illumination on tVOR from a single subject. (A) Switching to darkness. Note how vergence angle and tVOR declined when the room lights were turned off (first vertical dashed line), and then increased when lights were turned on again. (B) Strobe illumination (flashes lasting 30 ms at 4 Hz) are indicated by spikes in strobe channel. Note that tVOR and vergence are decreased compared with viewing in ambient light (first part of A). Plotting conventions are similar to Fig. 1.