Vestibular dysfunction in patients with auditory neuropathy detected by vestibular evoked myogenic potentials

Highlights

• Some auditory neuropathy (AN) patients showed oVEMP and cVEMP abnormalities, indicating vestibular involvement.

• Different VEMP abnormalities in AN patients indicate different stages of vestibular involvement.

• AN patients with vestibular disturbance are better described as having “auditory-vestibular neuropathy”.

Abstract

Objectives

This study aimed to determine vestibular involvement in patients with auditory neuropathy (AN) using ocular vestibular evoked myogenic potential (oVEMP), cervical vestibular evoked myogenic potential (cVEMP), caloric tests, video Head Impulse Tests (vHIT), and Suppression Head Impulse Paradigm (SHIMP) tests.

Methods

Twenty-two patients with AN (study group) and 50 age-and-gender-matched healthy subjects (control group) were enrolled. All patients underwent air-conducted sound oVEMP and cVEMP tests. In the study group, 20 patients underwent a caloric test, 10 patients underwent a video Head Impulse Test (vHIT), and nine patients underwent the Suppression Head Impulse Paradigm (SHIMP) test.

Results

Significant differences in VEMP abnormalities were found between the two groups. Most AN patients showed no VEMP response, while only a few patients showed VEMP responses with normal parameters. Some AN patients presented abnormal VEMP parameters, including thresholds, latencies, and amplitudes. The abnormal rate (including no response and abnormal parameters) was 91% in the cVEMP test and 86% in the oVEMP test. No significant difference was found between oVEMP and cVEMP abnormalities. AN patients exhibited a 70% abnormal rate in the caloric test. Most AN patients showed normal VOR gains. Most patients showed no overt corrective saccades in vHIT, and exhibited normal anticompensatory saccades in the SHIMP test.

Conclusion

Many AN patients experience vestibular dysfunction, which may be detected by using a vestibular functional test battery.

Significance

VEMP abnormalities might reflect the status and degree of vestibular involvement in AN.

Introduction

Auditory neuropathy (AN) was first coined in 1996, and was characterized by an unharmed central nervous system and absent or extremely distorted auditory brainstem responses (ABR), but normal otoacoustic emissions (OAE) and/or cochlear microphonics (CM) (Kaga et al., 1996, Starr et al., 1996). The abnormal auditory nerve response was regarded as the loss of inner hair cells (IHCs) or IHC synapses, impaired synaptic transmission to spiral ganglion neurons (SGNs), the demyelination and axonal loss of nerve fibers, or a combination of these components (Sininger and Starr, 2001, Ye et al., 2012, Santarelli et al., 2013). Recently, Kaga reported that the pathophysiology in the type of acquired AN in adults (as opposed to congenital AN) could be either pre- or postsynaptic, and involves pathology between the IHCs and the cochlear nerve (Kaga, 2016).

Most studies have investigated how AN impacts the auditory system; however, the potential effects of vestibular lesions have been overlooked. Because the vestibular nerve is one of the branches that form the eighth cranial nerve (vestibulocochlear nerve), its impairment might be another aspect of AN. Previously, clinicians detected impaired vestibular function in AN patients (Starr et al., 1996, Kaga et al., 1996). It was suggested that the lesion of the eighth cranial nerve is involved, including the cochlear nerve and, possibly, the vestibular nerve (Starr et al., 1996, Kaga et al., 1996). Some clinicians perfomed vestibular functional tests (including electronystagmography, rotational chair testing, and the caloric test), demonstrating that vestibular neuropathy occurs in AN subjects (Sheykholeslami et al., 2000, Sinha et al., 2013a). However, information about the lesions and extent of vestibular involvement in AN remains limited.

Based on the anatomy of the vestibulocochlear nerve, confusion might arise with respect to the effects of the superior vestibular nerve, inferior vestibular nerve, or a combination of these two branches of the eighth nerve in AN subjects (Masuda et al., 2011). However, it is difficult to distinguish the functional status of the two branches of the vestibular nerve without knowledge of vestibular evoked myogenic potentials (VEMPs), which allows the function of the vestibular end organ (saccule and utricle) and its input pathways to be evaluated separately (Murofushi, 2016, Curthoys et al., 2018). Cervical VEMP (cVEMP) might be derived from the saccule, and transmitted through the inferior vestibular nerve, reflecting the functional status of the ipsilateral inferior vestibular components of the vestibule (saccule and its afferent pathway) (Papathanasiou et al., 2014). Ocular VEMP (oVEMP) is derived from the utricle manifesting the crossed otolith-ocular pathway response, and is transmitted through the superior vestibular nerve. oVEMP is mainly considered to reflect the contralateral superior vestibular components (utricle and its afferent pathway) (Todd et al., 2007, Curthoys et al., 2011). The battery of cVEMP and oVEMP tests represents an important way of assessing vestibular function (Murofushi, 2016, Young, 2018).

As a conventional VEMP, cVEMP is used to assess vestibular function in patients with AN. Previous studies primarily used the caloric test to evaluate the functions of the lateral semicircular canal and the superior vestibular input pathway. Caloric and/or cVEMP tests of AN patients show that the vestibular components of the eighth cranial nerve and/or ear are involved (Sheykholeslami et al., 2005, Akdogan et al., 2008, Sujeet et al., 2014). However, as a newly discovered VEMP, oVEMP is beginning to be used to detect vestibular function in AN patients (Sinha et al., 2013b). Knowledge remains limited on how the utricle and superior vestibular nerves contribute to the detection of AN by oVEMP.

The video Head Impulse Test (vHIT) records eye rotation that is elicited by abrupt, passive, and unpredictable head rotations (head impulse). This test represents an objective measurement for separately evaluating the function of each semicircular canal (McGarvie et al., 2015). By observing the corrective saccades and calculating the gain of vestibulo-ocular reflex (VOR), it is possible to reveal unilateral or bilateral dysfunctions of the semicircular canal. In 2016, Curthoy’s group reported the Suppression Head Impulse Paradigm (SHIMP) (Shen et al., 2016). During the test process, patients were asked to gaze at a head-fixed laser target that moved simultaneously with the head impulse, instead of the earth-fixed target in vHIT tests. In this protocol, VOR started to be suppressed around the end of head rotation. Specifically, large anti-compensatory saccades were present in healthy subjects, while small saccades or no saccades were found in patients with vestibular loss (Macdougall et al., 2016, Halmagyi et al., 2017). To date, SHIMP has been used to measure how the horizontal canal functions in one or both ears. Combined with otolith functional tests (oVEMP and cVEMP), vHIT and SHIMP are used to evaluate the function of all vestibular end-organs.

This study aimed to demonstrate the involvement and extent of vestibular neuropathy in AN. In addition to hearing tests, a vestibular test battery was performed, including oVEMP, cVEMP, caloric tests, vHIT, and SHIMP in patients with AN. This study is expected to advance our understanding on the physiology of AN.