Abstract
Vestibulo-ocular reflexes (VOR) ensure gaze stability during locomotion and passively induced head/body movements. In precocial vertebrates such as amphibians, vestibular reflexes are required very early at the onset of locomotor activity. While the formation of inner ears and the assembly of sensory-motor pathways is largely completed soon after hatching, angular and translational/tilt VOR display differential functional onsets and mature with different time courses. Otolith-derived eye movements appear immediately after hatching, whereas the appearance and progressive amelioration of semicircular canal-evoked eye movements is delayed and dependent on the acquisition of sufficiently large semicircular canal diameters. Moreover, semicircular canal functionality is also required to tune the initially omnidirectional otolith-derived VOR. The tuning is due to a reinforcement of those vestibulo-ocular connections that are co-activated by semicircular canal and otolith inputs during natural head/body motion. This suggests that molecular mechanisms initially guide the basic ontogenetic wiring, whereas semicircular canal-dependent activity is required to establish the spatio-temporal specificity of the reflex. While a robust VOR is activated during passive head/body movements, locomotor efference copies provide the major source for compensatory eye movements during tail- and limb-based swimming of larval and adult frogs. The integration of active/passive motion-related signals for gaze stabilization occurs in central vestibular neurons that are arranged as segmentally iterated functional groups along rhombomere 1–8. However, at variance with the topographic maps of most other sensory systems, the sensory-motor transformation of motion-related signals occurs in segmentally specific neuronal groups defined by the extraocular motor output targets.
Highlights
Accurate perception of the visual world in all vertebrates requires sufficiently long periods of gaze stability given the relatively slow processing of images in the widespread visual circuits (Straka and Dieringer, 2004; Angelaki and Hess, 2005; Angelaki and Cullen, 2008)
Natural head/body movements consist of dynamically altering combinations of angular and linear acceleration components, which are detected and decomposed into individual vector components by semicircular canal and otolith organs
The behavioral onset of the semicircular canal-related angular Vestibulo-ocular reflexes (VOR) in Xenopus laevis tadpoles was determined during passive rotation at different developmental stages (Lambert et al, 2008)
Summary
Accurate perception of the visual world in all vertebrates requires sufficiently long periods of gaze stability given the relatively slow processing of images in the widespread visual circuits (Straka and Dieringer, 2004; Angelaki and Hess, 2005; Angelaki and Cullen, 2008). There is no direct experimental evidence yet for optokinetically driven eye movements in tadpoles smaller than stage 45 (Lambert et al, 2008), spontaneous eye twitches occur at locomotor onset This suggests that at this developmental period all neuronal elements of the vestibulo-ocular reflexes (VOR) circuitry are interconnected and capable to detect body movements and to trigger motor reactions. Following transduction of motion stimuli, alterations of the hair cell membrane potential are synaptically transmitted onto vestibular afferent fibers and encoded as modulated spike discharge (Goldberg, 2000) These signals are relayed to the central vestibular neurons in the hindbrain via parallel signaling pathways with respect to endorgan origin and response dynamics (Straka and Dieringer, 2004; Straka et al, 2009). The relative simplicity of this pathway triggered numerous investigations of the underlying computational processes and made it a uniquely suited system for studying sensory-motor transformation in general (see Robinson, 1985)
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