Strategies of developmental vestibular plasticity after unilateral embryonic ear removal in Xenopus laevis

Abstract

Appropriate gaze control mechanisms rely on bilateral mirror-symmetric vestibular endorgans, central circuits, and extraocular motor effectors. Embryonic removal of one inner ear prior to the formation of these structures was used to evaluate the extent to which animals can develop appropriate motor outputs in the presence of only a singular inner ear. Near-congenital one-eared tadpoles subjected to separate or combinatorial visuo-vestibular motion stimulation exhibited vestibular-ocular reflexes, though smaller in gain compared to controls, whereas isolated visuo-motor responses remained largely unaltered. Surprisingly, direction-specific responses in one-eared tadpoles revealed a spectrum of vestibulo-ocular reflex performance, where in many cases rather robust responses were observed during head motion towards the missing ear. Rotation toward the remaining ear elicited eye movements which were often severely attenuated. This suggests that embryonically generated one-eared animals develop bidirectional vestibular signal detection and downstream processing capacities that allow activation of robust compensatory eye movements. However, this capability seems to occur at the expense of performance of vestibular reflexes during motion in the canonical activation direction of the singular ear. Consequently, the development of central vestibulo-motor circuits in one-eared animals likely relies on strategies in which the outcome for gaze stabilization is driven by balanced homeostatic levels and individual temporal tuning of abducens motoneuron activity. Despite the lack of bilateral symmetric vestibular afferent input, the developing central nervous system is capable of creating a framework for symmetric sensorimotor transformations.