Dissociated hysteresis of static ocular counterroll in humans

Abstract

In stationary head roll positions, the eyes are cyclodivergent. We asked whether this phenomenon can be explained by a static hysteresis that differs between the eyes contra- (CE) and ipsilateral (IE) to head roll. Using a motorized turntable, healthy human subjects (n = 8) were continuously rotated about the earth-horizontal naso-occipital axis. Starting from the upright position, a total of three full rotations at a constant velocity (2 degrees/s) were completed (acceleration = 0.05 degrees/s2, velocity plateau reached after 40 s). Subjects directed their gaze on a flashing laser dot straight ahead (switched on 20 ms every 2 s). Binocular three-dimensional eye movements were recorded with dual search coils that were modified (wires exiting inferiorly) to minimize torsional artifacts by the eyelids. A sinusoidal function with a first and second harmonic was fitted to torsional eye position as a function of torsional whole body position at constant turntable velocity. The amplitude and phase of the first harmonic differed significantly between the two eyes (paired t-test: P < 0.05): on average, counterroll amplitude of IE was larger [CE: 6.6 +/- 1.6 degrees (SD); IE: 8.1 +/- 1.7 degrees), whereas CE showed more position lag relative to the turntable (CE: 12.5 +/- 10.7 degrees; IE: 5.1 +/- 8.7 degrees). We conclude that cyclodivergence observed during static ocular counterroll is mainly a result of hysteresis that depends on whether eyes are contra- or ipsilateral to head roll. Static hysteresis also explains the phenomenon of residual torsion, i.e., an incomplete torsional return of the eyes when the first 360 degrees whole body rotation was completed and subjects were back in upright position (extorsion of CE: 2.0 +/- 0.10 degrees; intorsion of IE: 1.4 +/- 0.10 degrees). A computer model that includes asymmetric backlash for each eye can explain dissociated torsional hysteresis during quasi-static binocular counterroll. We hypothesize that ocular torsional hysteresis is introduced at the level of the otolith pathways because the direction-dependent torsional position lag of the eyes is related to the head roll position and not the eye position.