Stabilization of Gaze during Early Xenopus Development by Swimming-Related Utricular Signals

Abstract

Locomotor maturation requires concurrent gaze stabilization improvement for maintaining visual acuity [1, 2]. The capacity to stabilize gaze, in particular in small aquatic vertebrates where coordinated locomotor activity appears very early, is determined by assembly and functional maturation of inner ear structures and associated sensory-motor circuitries [3-7]. Whereas utriculo-ocular reflexes become functional immediately after hatching [8, 9], semicircular canal-dependent vestibuloocular reflexes (VOR) appear later [10]. Thus, small semicircular canals are unable to detect swimming-related head oscillations, despite the fact that corresponding acceleration components are well-suited to trigger an angular VOR [11]. This leaves the utricle as sole vestibular origin for swimming-related compensatory eye movements [12, 13]. We report a remarkable ontogenetic plasticity of swimming-related head kinematics and vestibular endorgan recruitment in Xenopus tadpoles with beneficial consequences for gaze-stabilization. Swimming of older larvae generates sinusoidal head undulations with small, similar curvature angles on the left and right side that optimally activate horizontal semicircular canals. Young larvae swimming causes leftright head undulations with narrow curvatures and strong, bilaterally dissimilar centripetal acceleration components well-suited to activate utricular hair cells and to substitute the absent semicircular canal function at this stage. The capacity of utricular signals to supplant semicircular canal function was confirmed by recordings of eye movements and extraocular motoneurons during off-center rotations in control and semicircular canal-deficient tadpoles. Strong alternating curvature angles and thus linear acceleration profiles during swimming in young larvae therefore represents a technically elegant solution to compensate for the incapacity of small semicircular canals to detect angular acceleration components.

Locomotion-induced ocular motor behavior in larval Xenopus is developmentally tuned by visuo-vestibular reflexes

“…Thereafter, animals were allowed to further develop until usage in respective experiments. As demonstrated, such tadpoles anatomically lack all semicircular canals as well as corresponding ocular motor re exes, while the utricle and associated sensory-motor computations remain functionally preserved 15,25 .…”

“…This is particularly critical in small aquatic vertebrates, where coordinated locomotor activity is generally acquired very early after hatching 14,17 . In accordance with this requirement, utriculo-ocular re exes become functional immediately after hatching in zebra sh 18 and anuran larvae 19 followed, though conspicuously later, by semicircular canal-derived vestibulo-ocular re exes (VOR) 15,20 . The different developmental acquisition of individual VOR components, as demonstrated for Xenopus larvae, but likely also of visuo-ocular re exes, might have signi cant interactive in uences on the maturation of locomotor pro ciency with respective reciprocal consequences for efference copy-driven gaze-stabilization 8 .…”

“…Progressive developmental improvements of locomotor performance are tightly linked to the maturation of gaze-and posture-stabilizing re exes 14,15,16 . The structural assembly and functional initiation of inner ear sensation and associated sensory-motor computations are decisive factors for the onset and e ciency of gaze-stabilization as well as locomotion 17 .…”

Locomotion-induced ocular motor behavior in larvalXenopusis developmentally tuned by visuo-vestibular reflexes

“…Thereafter, animals were allowed to further develop until usage in experiments on semi-intact preparations. As demonstrated, such tadpoles anatomically lack all semicircular canals as well as corresponding ocular motor reflexes, while the utricle and associated sensory-motor computations remain functionally preserved 15,25 .…”

“…This sequence complies with the onset of otolith organ-dependent reflexive eye movements. Hence, from stage 42 onward, the maturation of otolith organs allows detection of gravitoinertial head movements 15,20 . In contrast, vestibular projections to the spinal cord are fully established at stage 42-43 37 .…”