Semicircular canal-dependent developmental tuning of translational vestibulo-ocular reflexes in Xenopus laevis

Gaze stabilization during head/body movements is achieved to a large extent by vestibular-evoked compensatory eye movements. These reflexes derive from semicircular canal and otolith organs and depend on the transformation of the respective sensory signals into extraocular motor commands. To elicit directionally and dynamically appropriate compensatory eye movements, extraocular motoneurons require spatiotemporally specific inputs from semicircular canals and regions of the utricular epithelium with matching directional sensitivity. The ontogenetic establishment and maturation of the directional tuning of otolith inputs in extraocular motoneurons was studied in Xenopus laevis tadpoles. In young larvae at stage 46-48, superior oblique (SO) extraocular motoneurons receive omnidirectional utricular signals during horizontal translational motion, indicating an absence of spatial tuning. In contrast, in older larvae beyond stage 49 these motoneurons were activated by directionally more restricted otolith inputs with an increasingly enhanced spatial tuning until stage 53. This developmental process limited the origin of otolith signals to a utricular epithelial sector with a hair cell sensitivity that is coaligned with the pulling direction of the SO eye muscle. The maturation of the otolith response vector was abolished by enzymatic prevention of semicircular canal formation in postembryonic tadpoles at stage 44, suggesting that functionally intact semicircular canals are causally responsible for the observed directional tuning of utricular responses. A likely mechanism by which semicircular canals might influence the tuning of the otolith responses includes stabilization of coactivated and centrally converging sensory signals from semicircular canal and spatially aligned epithelial utricular regions during natural head/body motion.