The vestibulo-ocular reflex: an outdated concept?

Traditionally, the vestibulo-ocular reflex (VOR) is described as a distinct, phylogenetically old oculomotor subsystem, which serves to stabilize gaze direction. It is supposed to act as a stereotyped reflex with definite input-output relations, which can be measured by rotating a subject passively in darkness, and which are kept at an ideal level by adaptive, parametric adjustments. This paper argues that such a view is not realistic: (1) the VOR in darkness does not have an ideal, or even well defined, gain; (2) a fixed, automatic VOR is not appropriate in most behavioural situations, and would need continuous conditioning by other subsystems. As there is no compelling phylogenetic, physiological or anatomical evidence for an independent VOR subsystem, a more fruitful hypothesis may be that vestibular signals are just one of many inputs to a spatial localization process, which computes the relative position (and motion) between the subject and a target of his choice. The VOR in darkness may represent no more than a default operation, based on incomplete information, of this larger, multiple input gaze control system. Likewise, adaptation phenomena of the VOR in darkness may be merely an epiphenomenon of adaptation of gaze control with vision active.