Contribution of the otoliths to the human torsional vestibulo-ocular reflex

Abstract

The dynamic contribution of the otolith organs to the human ocular torsion response was examined during passive sinusoidal body roll about an earth-horizontal axis (varying otolith inputs) and about an earth-vertical axis (invariant otolith inputs). Torsional eye movements were registered in 5 subjects by means of video-oculography. At a fixed amplitude of 25 degrees, the stimulus frequency was varied from 0.05 to 0.4 Hz. Additionally, at a fixed frequency of 0.2 Hz, the response was also measured at the amplitudes to 12.5 degrees and 50 degrees. The results showed that the gain and phase of the torsional slow component velocity (SCV) did not depend on stimulus amplitude, indicating a linear response. Contribution of the otoliths affected the ocular torsion response in three different ways. First, the gain of the SCV was slightly, but consistently, higher during rotation about an earth-horizontal axis than during rotation about an earth-vertical axis. With invariant otolith inputs the average gain increased from 0.10 at 0.05 Hz to 0.26 at 0.25 Hz. With varying otolith inputs, the average gain increased from 0.14 to 0.37. Second and more substantially, contribution of the otoliths improved the response dynamics by reducing the phase lead at frequencies up to 0.02 Hz. Third, the nystagmus showed considerably less anticompensatory saccades in upright conditions than in supine conditions, even though the SCV gain was lower in the latter. As a consequence, the average excursion of torsional eye position was highest during earth-horizontal rotation. This effect was observed in the entire frequency range. Thus, the otoliths controlled the human torsional VOR not only at low stimulus frequencies by keeping the slow component in phase with head motion, but also in a wider frequency range by modulating the saccadic behavior as to increase the amplitude of ocular torsion. We conclude that the primary concern of the otolith-oculomotor system during head tilt is to stabilize eye position in space, rather than to prevent retinal blur.