Acute consequences of a unilateral VIIIth nerve transection on vestibulo-ocular and optokinetic reflexes in Xenopus laevis tadpoles

Abstract

Loss of peripheral vestibular function provokes severe impairments of gaze and posture stabilization in humans and animals. However, relatively little is known about the extent of the instantaneous deficits. This is mostly due to the fact that in humans a spontaneous loss often goes unnoticed initially and targeted lesions in animals are performed under deep anesthesia, which prevents immediate evaluation of behavioral deficits. Here, we use isolated preparations of Xenopus laevis tadpoles with functionally intact vestibulo-ocular (VOR) and optokinetic reflexes (OKR) to evaluate the acute consequences of unilateral VIIIth nerve sections. Such in vitro preparations allow lesions to be performed in the absence of anesthetics with the advantage to instantly evaluate behavioral deficits. Eye movements, evoked by horizontal sinusoidal head/table rotation in darkness and in light, became reduced by 30% immediately after the lesion and were diminished by 50% at 1.5 h postlesion. In contrast, the sinusoidal horizontal OKR, evoked by large-field visual scene motion, remained unaltered instantaneously but was reduced by more than 50% from 1.5 h postlesion onwards. The further impairment of the VOR beyond the instantaneous effect, along with the delayed decrease of OKR performance, suggests that the immediate impact of the sensory loss is superseded by secondary consequences. These potentially involve homeostatic neuronal plasticity among shared VOR-OKR neuronal elements that are triggered by the ongoing asymmetric activity. Provided that this assumption is correct, a rehabilitative reduction of the vestibular asymmetry might restrict the extent of the secondary detrimental effect evoked by the principal peripheral impairment.

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

“…Particularly surprising was the unexpected inequality in eye motion amplitudes during contraversive versus ipsiversive (with respect to the single ear) rotation, which favored more robust responses during disfacilitation of the singular right ear. Acute lesion of a single stato-acoustic nerve in Xenopus tadpoles showed a physiologically more expected effect where rotation toward the lesion side elicited very poor eye movements, a feature consistent with the sudden loss of a predominant directional sensitivity (Soupiadou et al, 2020), which is likely due to the resulting absence of the driving force supplying relevant extraocular motoneurons (Branoner and Straka, 2018). Here, despite the obvious bidirectional sensitivity of the singular inner ear, such asymmetric motor output highlights individualized differential strengths in computation within brainstem processing regions.…”

Low Gain Values of the Vestibulo-Ocular Reflex Can Optimize Retinal Image Slip

“…Yet another possibility to explain low gain values in Xenopus tadpoles is that semicircular canal-evoked responses saturate much earlier than expected and thus cannot transmit head velocities >30°/s. However, data presented previously show that this explanation is also unlikely [e.g., ( 9 )], and the approximately sinusoidal shape of aVOR responses provides no evidence for a potential saturation of the VOR at the applied stimulus intensities ( 21 ), supported by direct measurements of extraocular motoneuronal spike discharge at increasing stimulus amplitudes ( 22 ). While unusually low in darkness, the aVOR of Xenopus tadpoles in light is supplemented by efficient, visuo-motor reflexes that naturally assist the maintenance of gaze stability ( 21 ).…”

“…However, data presented previously show that this explanation is also unlikely [e.g., ( 9 )], and the approximately sinusoidal shape of aVOR responses provides no evidence for a potential saturation of the VOR at the applied stimulus intensities ( 21 ), supported by direct measurements of extraocular motoneuronal spike discharge at increasing stimulus amplitudes ( 22 ). While unusually low in darkness, the aVOR of Xenopus tadpoles in light is supplemented by efficient, visuo-motor reflexes that naturally assist the maintenance of gaze stability ( 21 ). Even though the overall gain of the aVOR in light is only mildly enhanced, the phase of the aVOR in light matches much better an expected compensatory response ( 21 ).…”

“…An alternative reason for the low VOR gain observed in Xenopus tadpoles could be that the extraocular motor system in these animals might simply be unable to generate faster eye movements. However, this is not the case given the occasional expression of saccadic eye movements with velocities that are considerably higher than required for a perfect VOR ( 21 ). Yet another possibility to explain low gain values in Xenopus tadpoles is that semicircular canal-evoked responses saturate much earlier than expected and thus cannot transmit head velocities >30°/s.…”

“…While unusually low in darkness, the aVOR of Xenopus tadpoles in light is supplemented by efficient, visuo-motor reflexes that naturally assist the maintenance of gaze stability ( 21 ). Even though the overall gain of the aVOR in light is only mildly enhanced, the phase of the aVOR in light matches much better an expected compensatory response ( 21 ). In fact, visuo-motor responses such as the optokinetic reflex are particularly prominent at low-frequencies, although the natural frequency of swimming in tadpoles is even higher than the imposed head motion frequency applied in the current study ( 23 ).…”