Listing's plane and the 3D-VOR in microgravity – The role of the otolith afferences

Abstract

The study addresses the question as to what extent the otolith-mediated gravity vector maintains the stability of the coordinate frames of the vestibulo-ocular reflex and the oculomotor system, described by Listing's Plane. Under normal 1 G conditions it has been demonstrated in the monkey that Listing's Plane (LP) and the 3D vestibulo-ocular response (3D-VOR) are close to collinear [10]. In the present study the coordinate frames of the oculomotor system and the three-dimensional vestibulo-ocular reflex (3D-VOR) system were measured under one-g gravity conditions and during a period of prolonged microgravity, on-board the International Space Station (ISS). To this end, the coordinate frame of the oculomotor system is described in Listing's coordinates and that of the 3D-VOR system by the minimal gain vector. The findings demonstrate that under Earthbound, one-g conditions the two coordinate frames diverge by approximately 20° in the human. In the absence of the gravity vector the radical loss in the otolith-mediated contribution to the dynamic VOR leads to a reduction of the torsional VOR component and in turn to a forward tilt of the oculomotor coordinate frame, described by the minimal gain vector. In contrast, the torsional component of LP during horizontal and vertical saccades was found to increase, resulting in a backward tilt of LP. Together with the backward tilt of LP a small but consistent change in LP vergence was observed. The thickness of LP did not appear to change in the absence of gravity. The changes in coordinate frame orientation persisted over the six-month periods spent in zero gravity. The postflight measurements demonstrate that re-adaptation to preflight values proceeds over several days to weeks. The findings demonstrate that the gravity vector represents a common reference for vestibular and oculomotor responses. They also support the idea that the gravity vector provides a central reference for the entire sensorimotor complex.