Ontogenetic Development of Vestibulo-Ocular Reflexes in Amphibians

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.

Semicircular Canal Influences on the Developmental Tuning of the Translational Vestibulo-Ocular Reflex

“…The omni-directional sensitivity for horizontal translation of this otolith organ as an entity, however, makes it difficult to conceive the mechanism by which hair cell epithelial sectors with particular directional specificity are connected during ontogeny to sets of VOR neurons with spatially matching extraocular motor targets. The orthogonal arrangement of semicircular canals [e.g., ( 17 )], however, is well-suited as spatial reference frame for guiding a central convergence of directionally co-aligned angular and linear acceleration signals during embryonic and early post-embryonic development ( 18 ).…”

Conserved and divergent development of brainstem vestibuloacoustic nuclei

“…Vestibular peripheral organs, hindbrain vestibular nuclei and their connectivity patterns are highly conserved across vertebrates and clear evolutionary relationships can be established (Straka and Baker, 2013). The axial developmental origin and location of vestibular neurons projecting to oculomotor, spinal cord, cerebellar and commissural targets are also conserved (Branoner et al, 2016;Chagnaud et al, 2017;Malinvaud et al, 2010;Straka and Baker, 2013;Straka et al, 2014), however, a comparative analysis of the dorsoventral lineage of hindbrain vestibular neurons has been lacking. Here, we show that in chick, cells derived from rhombic lip Atoh1 + progenitors are present in the Superior, Deiters, Medial and Descending vestibular nuclei, while we observed no contribution from this lineage to the avian exclusive Tangential nucleus (Figures 5 and 6).…”

Segmental Analysis of the Vestibular Nerve and the Efferents of the Vestibular Complex

“…The sensory receptors are contacted by peripheral dendrites of vestibular ganglion cells, which relay the signals through the vestibular nerve to the sensory vestibular complex in the hindbrain. There they are distributed in a topographically ordered pattern along the dorsoventral, mediolateral and rostrocaudal dimensions, depending on their specific sensory receptor origins (reviewed in Uchino et al, ; Straka et al, ; Branoner et al, ). Frequently, these ganglionic vestibular primary afferents give ascending and descending branches that innervate diverse segmental subpopulations of the specific vestibular nuclei in the vestibular column (anteroposterior or longitudinal dimension).…”

“…Finally, we will discuss the idea of the vestibular nuclear complex as a plurisegmental functional hodological mosaic. Some of these topics have been previously reviewed (Diaz and Glover, ; Straka et al, ; Branoner et al, ). Moreover, Joel C. Glover has presented newer findings pertinent to several of the topics covered in this review, including the development of afferent connections and the molecular profiling of vestibular projection neurons at several recent conferences (personal communication).…”

“…). The projection areas in the vestibular nuclei of afferent fibers representing input from individual semicircular canals and otolith organs seem to overlap or vary somewhat individually in vertebrates, and the density of the innervation shows regional variations (Gacek, ; Suarez et al, ; Highstein et al, ; McCormick and Braford, ; Dickman and Fang, ; Büttner‐Ennever, ; Birinyi et al, ; Uchino et al, ; Branoner et al, ). Nevertheless, most vestibular neurons receive monosynaptic excitatory inputs from a specific semicircular canal and/or from only one otolith organ in pigeons (Wilson and Felpel, ), cats (Sans et al, ; Kasahara and Uchino, ) and frogs (Straka et al, b, ).…”