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effect, along with the delayed decrease of OKR performance, suggests that the immediate impact of the sensory loss is superseded by secondary consequences.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.

Highlights

  • Unilateral loss of peripheral vestibular function causes severe and incapacitating symptoms [1]

  • The optokinetic reflexes (OKR) remained functionally intact and unaltered immediately after the vestibular loss (0 h) but experienced a considerable reduction starting at 1.5 h postlesion

  • The time course and occurrence of detrimental events at later time points suggest that the immediate impact by the loss of vestibular sensory signals is followed by secondary neuronal consequences involving shared VOR-OKR cellular and/or circuit components

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Summary

Introduction

Unilateral loss of peripheral vestibular function causes severe and incapacitating symptoms [1]. S63 on the magnitude, variety, and progression of acute symptoms that appear instantaneously after an induced loss of peripheral vestibular function This is mostly due to the fact that any peripheral vestibular lesion has to be performed in deeply anesthetized and analgesically treated animals that require a post-surgical recovery period until the behavioral impairments can be faithfully evaluated. Compared to typical patients with a vestibular syndrome that are seen by a clinician days and weeks after the incident, a planned tumor surgery of the VIIIth nerve [9] or a comparable experimental manipulation, e.g. in rabbits [10] or mice [11] are currently the closest conditions that allow an evaluation of the acute stage after a vestibular lesion All these studies suffer from the unavoidable temporal lag between the surgical lesion and the fully awake state of an animal, which is required to estimate the full spectrum of immediate behavioral consequences

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