Horizontal Semicircular Canal Orientation and the 3-D Vestibulo-Ocular Reflex

Abstract

Goal. The three-dimensional vestibulo-ocular reflex (3-D VOR) is responsible for the maintenance of stable vision through generating compensatory eye movements in response to head movements. The main functional components of the 3-D VOR are the semicircular canals. The anatomy of the three canals is complicated, requiring the definition of several natural coordinate systems in order to assess the canals' functionality. Most notably, the horizontal canals form a significant angle (25°) with respect to the earth-horizontal (E-H) while the head is upright. The goal of this study was to determine the influence of head pitch orientation on the quality of the VOR, and thus to identify the 3-D VOR dependence on the canal anatomy and orientation. Methods. Eight healthy upright seated subjects underwent whole-body sinusoidal and transient stimulation delivered by a six degree of freedom (6-DOF) motion platform. Small-amplitude sinusoidal oscillation was delivered around the yaw axis and axes in the horizontal plane between roll and pitch at increments of 22.5°. Transients were delivered in yaw, roll and pitch and in the vertical canal planes. This sequence of stimuli was repeated for the subject with his/her head under three different initial positions: upright, pitched nose down 16°and 25°, aligning the horizontal canal prime direction and maximum response direction with the E-H, respectively. 3-D scleral search coils were used for the recording of eye movements. Results. For sinusoidal stimulation around axes in the horizontal plane, a decline in gain and an increase in misalignment were found for increasing downward head pitch, in the light as well as in darkness. All component gains had lower values in darkness than in light. For vertical axis rotation, this decrease in gain and increase in misalignment was also present, except for the torsion component which increased with both upward and downward (from upright) pitch. Transient stimulation yielded overall lower gains than sinusoidal stimulation. No significant differences between the different head pitch orientations were found for vertical axis stimulation. For transients around axes in the horizontal plane however, the horizontal component gain increased with increasing nose-down pitch, while overall the vertical component decreased. Conclusions. The incongruence between the mathematically modelled coordinate systems of the semicircular canals and the obtained results in terms of gain and misalignment, suggests the contribution of other mechanisms to the 3-D VOR. The gravity-induced otolith-mediated VOR is likely to have an additional effect with the head pitched. The inhibitory effect of the otolith-mediated gravity vector on the torsional eye position is a possible explanation for the reduction in gain for sinusoidal rotation around axes in the horizontal plane. The opposite is seen during transient stimulation, which could be attributed to the otolith organs' low-pass behaviour.