Sound-Evoked Responses in the Vestibulo-Ocular Reflex Pathways of Rats.

Chunming Zhang,Youguo Xu,Hong Zhu,Jun Huang,Matthew C Donald,Tracy Rappai,Yue Yu,Tianwen Chen,Wu Zhou,Michael Zhang,Jerome Allison,William Mustain,Alberto Arteaga,Xuehui Tang

doi:10.3389/fnins.2021.741571

Abstract

Vestibular evoked myogenic potentials (VEMP) have been used to assess otolith function in clinics worldwide. However, there are accumulating evidence suggesting that the clinically used sound stimuli activate not only the otolith afferents, but also the canal afferents, indicating canal contributions to the VEMPs. To better understand the neural mechanisms underlying the VEMPs and develop discriminative VEMP protocols, we further examined sound-evoked responses of the vestibular nucleus neurons and the abducens neurons, which have the interneurons and motoneurons of the vestibulo-ocular reflex (VOR) pathways. Air-conducted clicks (50–80 dB SL re ABR threshold, 0.1 ms duration) or tone bursts (60–80 dB SL, 125–4,000 Hz, 8 ms plateau, 1 ms rise/fall) were delivered to the ears of Sprague-Dawley or Long-Evans rats. Among 425 vestibular nucleus neurons recorded in anesthetized rats and 18 abducens neurons recorded in awake rats, sound activated 35.9% of the vestibular neurons that increased discharge rates for ipsilateral head rotation (Type I neuron), 15.7% of the vestibular neurons that increased discharge rates for contralateral head rotation (Type II neuron), 57.2% of the vestibular neurons that did not change discharge rates during head rotation (non-canal neuron), and 38.9% of the abducens neurons. Sound sensitive vestibular nucleus neurons and abducens neurons exhibited characteristic tuning curves that reflected convergence of canal and otolith inputs in the VOR pathways. Tone bursts also evoked well-defined eye movements that increased with tone intensity and duration and exhibited peak frequency of ∼1,500 Hz. For the left eye, tone bursts evoked upward/rightward eye movements for ipsilateral stimulation, and downward/leftward eye movements for contralateral stimulation. These results demonstrate that sound stimulation results in activation of the canal and otolith VOR pathways that can be measured by eye tracking devices to develop discriminative tests of vestibular function in animal models and in humans.

Highlights

Since the discovery of the vestibular-evoked myogenic potentials (VEMPs) (Colebatch and Halmagyi, 1992), there has been a rapid growth of VEMP research and investigators worldwide have used the VEMPs to characterize a variety of vestibulopathies, including Tullio/superior canal dehiscence syndrome, vestibular neuritis, Ménière’s disease, and vestibular schwannoma (Minor et al, 1998; Rauch, 2006; Rosengren et al, 2010)
Consistent with convergence of canal and otolith inputs on the vestibular nucleus neurons, we showed that the vestibular nucleus neurons exhibited well-defined tone bursts-evoked activation that reflected activation of both the canal and otolith afferents
This convergence of sound activation of the canal and otolith afferents were further observed in the abducens neurons and the tone burst-evoked eye movements

Summary

Introduction

Since the discovery of the vestibular-evoked myogenic potentials (VEMPs) (Colebatch and Halmagyi, 1992), there has been a rapid growth of VEMP research and investigators worldwide have used the VEMPs to characterize a variety of vestibulopathies, including Tullio/superior canal dehiscence syndrome, vestibular neuritis, Ménière’s disease, and vestibular schwannoma (Minor et al, 1998; Rauch, 2006; Rosengren et al, 2010). Because early animal studies showed that loud sound primarily activates the otolith afferents (Murofushi et al, 1995; Murofushi and Curthoys, 1997), the VEMPs are presently used to test otolith function. We further found that the clinical VEMP stimuli activated both the canal and otolith afferents in rats (Zhu et al, 2011b, 2014). Consistent with these single unit recording results, our intraaxonal labeling studies provided anatomical evidence that sound sensitive afferents innervate horizontal and anterior cristae as well as saccular and utricular macule (Zhu et al, 2014)

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