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Dynamics of Compensatory Eye Movement Control: an Optimal Estimation Analysis of the Vestibulo-Ocular Reflex

Head movements in vertebrates give rise to involuntary eye movements that stabilize visual images on the retina. Previous models of the vestibulo-ocular reflex (VOR), one of the neural mechanisms responsible for stabilizing the eyes during head movements, have assumed that the VOR transfer function should have unity gain and 180° phase shift. Experimental measurements of VOR gain and phase, however, exhibit frequency dependencies that are not easily interpreted within the framework of existing models. We reanalyze the problem of VOR control using stochastic optimal estimation theory and show that VOR dynamics, in general, should differ from the "ideal" unity-gain, 180° phase shift transfer function. We illustrate this approach by computing the optimal VOR transfer function for a simple, second-order dynamical model of a head–neck system. Despite its simplicity, this model is able to give some insight into the dynamical properties of the VOR. In particular, it qualitatively reproduces an experimentally observed gain peak in monkey VOR at high frequencies. The model also predicts that the gain and phase characteristics of the optimal VOR transfer function should depend on the spectrum of natural head movements, possibly giving rise to species-dependent and gait-dependent differences in the VOR transfer function. We suggest that the applicability of optimal estimation extends beyond the control of compensatory eye movements and that it is probably a universal component of movement control in the nervous system.