Basic organization principles of the VOR: lessons from frogs

Abstract

Locomotion is associated with a number of optical consequences that degrade visual information processing in the absence of appropriate compensatory movements. The resulting retinal image flow is counteracted by coordinated eye-head reflexes that are initiated by optokinetic and vestibular inputs. The contribution of the vestibulo-ocular reflex (VOR) for stabilizing retinal images is relatively small in amplitude in frogs but important in function by compensating for the non-linearities of the neck motor system. The spatial tuning of the VOR networks underlying the angular (AVOR) and linear (LVOR) with respect to canal and extraocular motor coordinates is organized in a common, canal-related reference frame. Thereby, the axes of head and eye rotation are aligned, principle and auxiliary VOR connections transform vestibular into motor signals and parallel AVOR and LVOR circuits mediate vergence and version signals separately. Comparison of these results with data from other vertebrates demonstrates a number of fundamental organization principles common to most vertebrates. However, the fewer degrees of behavioral freedom of frogs are reflected by the absence of, e.g. a functioning velocity storage network or of a fixation suppression of the VOR. In vitro experiments with the isolated brainstem and branches of N.VIII attached were used to study the putative transmitters of vestibular nerve afferent inputs, the postsynaptic receptor subtypes of second-order vestibular neurons and their dynamic response properties. Evidence is presented that suggests that afferent vestibular nerve fibers with different dynamic response properties activate different subtypes of glutamate receptors. The convergence pattern of monosynaptic afferent nerve inputs from different labyrinthine organs onto second-order vestibular neurons is remarkably specific. As a rule, second-order vestibular neurons receive converging afferent nerve inputs from one semicircular canal and from a specific sector of hair cells on one otolith organ. This convergence pattern remains malleable even in adulthood and reorganization is initiated by activity-related changes in vestibular nerve afferent fibers. The output of second-order vestibular neurons is modified by at least three inhibitory control loops. Uncrossed inhibitory vestibular side loops appear to control specifically the dynamic response tuning, whereas coplanar commissural inhibitory inputs improve mainly the spatial tuning and the cerebellar feedback loop controls the response gain. Among the targets of second-order vestibular projection neurons are extraocular motoneurons and internuclear neurons. Extraocular motoneurons differ among each other by the presence of very different response dynamics. These differences may represent a co-adaptation to the response dynamics of twitch and non-twitch extraocular muscle fibers. Different dynamical properties are required for a rapid acceleration of the globe at the one end and for the maintenance of a stable eccentric eye position over long periods of time at the other end of a continuum of variations in dynamic response properties. The maintenance of a given eccentric eye position over long periods of time is especially well developed in frogs and assists visual surveillance during lurking in the absence of saccades.