Three-dimensional eye position during static roll and pitch in humans

Abstract

We investigated how three-dimensional (3D) eye position is influenced by static head position relative to gravity, a reflex probably mediated by the otolith organs. In monkeys, the torsional component of eye position is modulated by gravity, but little data is available in humans. Subjects were held in different head/body tilts in roll and pitch for 35 s while we measured 3D eye position with scleral coils, and we used methods that reduced torsion artifacts produced by the eyelids pressing on the contact lens and exit wire. 3D eye positions were described by planar fits to the data (Listing's plane), and changes in these planes showed how torsion varied with head position. Similar to findings in monkeys, the eyes counterrolled during roll tilts independent of horizontal and vertical eye position, reaching a maximum torsion of 4.9°. Counterroll was not proportional to the shear force on the macula of the utricles: gain (torsion/sine of the head roll angle) decreased by 50% from near upright to ear down. During pitch forward, torsion increased when subjects looked right, and decreased when they looked left. However, the maximum change of torsion was only −0.06° per degree of horizontal eye position, which is less than reported in monkey. Also in contrast to monkey, we found little change in torsion when subjects were pitched backwards.