Sustained and Transient Vestibular Systems: A Physiological Basis for Interpreting Vestibular Function.

Pierre-Paul Vidal,Hamish G Macdougall,Catherine De Waele,Ian S Curthoys

doi:10.3389/fneur.2017.00117

Abstract

Otolithic afferents with regular resting discharge respond to gravity or low-frequency linear accelerations, and we term these the static or sustained otolithic system. However, in the otolithic sense organs, there is anatomical differentiation across the maculae and corresponding physiological differentiation. A specialized band of receptors called the striola consists of mainly type I receptors whose hair bundles are weakly tethered to the overlying otolithic membrane. The afferent neurons, which form calyx synapses on type I striolar receptors, have irregular resting discharge and have low thresholds to high frequency (e.g., 500 Hz) bone-conducted vibration and air-conducted sound. High-frequency sound and vibration likely causes fluid displacement which deflects the weakly tethered hair bundles of the very fast type I receptors. Irregular vestibular afferents show phase locking, similar to cochlear afferents, up to stimulus frequencies of kilohertz. We term these irregular afferents the transient system signaling dynamic otolithic stimulation. A 500-Hz vibration preferentially activates the otolith irregular afferents, since regular afferents are not activated at intensities used in clinical testing, whereas irregular afferents have low thresholds. We show how this sustained and transient distinction applies at the vestibular nuclei. The two systems have differential responses to vibration and sound, to ototoxic antibiotics, to galvanic stimulation, and to natural linear acceleration, and such differential sensitivity allows probing of the two systems. A 500-Hz vibration that selectively activates irregular otolithic afferents results in stimulus-locked eye movements in animals and humans. The preparatory myogenic potentials for these eye movements are measured in the new clinical test of otolith function—ocular vestibular-evoked myogenic potentials. We suggest 500-Hz vibration may identify the contribution of the transient system to vestibular controlled responses, such as vestibulo-ocular, vestibulo-spinal, and vestibulo-sympathetic responses. The prospect of particular treatments targeting one or the other of the transient or sustained systems is now being realized in the clinic by the use of intratympanic gentamicin which preferentially attacks type I receptors. We suggest that it is valuable to view vestibular responses by this sustained-transient distinction.

Highlights

The early recordings of the response of cat single vestibular nucleus neurons to angular acceleration established that different neurons had very different response patterns to identical angular acceleration stimuli [1,2,3]
It is now being replaced by evidence showing that
This anatomical diversity is matched by afferent diversity of physiological response

Summary

INTRODUCTION

The early recordings of the response of cat single vestibular nucleus neurons to angular acceleration established that different neurons had very different response patterns to identical angular acceleration stimuli [1,2,3]. Prior to the SCD, these neurons do not respond to ACS or BCV at the levels used in human clinical testing, whereas after the SCD [which acts to increase fluid displacement [50, 51]] these same irregular afferents show strong phase-locked activation to the same stimulus [33] (Figure 4B) Why is it that regular afferents are not responsive to vibration and sound at such high frequencies? Brief bursts of 500-Hz BCV, which physiology has shown to selectively activate otolithic irregular afferents originating from striolar receptors, cause short-latency stimuluslocked eye movements in guinea pigs [87] and in humans (see Figure 6) [88, 89] The pattern of these vibration-induced eye movements is consistent with the pattern of cat eye movements to direct electrical stimulation of the utricular nerve [90]. Zhou et al [132] have shown how a PID model can closely approximate oculomotor performance

A Complementary View

SUMMARY