A review of the scientific basis and practical application of a new test of utricular function--ocular vestibular-evoked myogenic potentials to bone-conducted vibration

Abstract

This is a review of recently published papers showing that bone-conducted vibration of the head causes linear acceleration stimulation of both inner ears and this linear acceleration is an effective way of selectively activating otolithic afferent neurons. This simple stimulus is used in a new test to evaluate clinically the function of the otoliths of the human inner ear. Single neuron studies in animals have shown that semicircular canal neurons are rarely activated by levels of bone-conducted vibration at 500 Hz which generate vigorous firing in otolithic irregular neurons and which result in a variety of vestibulo-spinal and vestibulo-ocular responses, and the latter is the focus of this review. In humans, 500 Hz bone-conducted vibration, delivered at the midline of the forehead, at the hairline (Fz), causes simultaneous and approximately equal amplitude linear acceleration stimulation at both mastoids and results in ocular-evoked myogenic potentials (oVEMPs) beneath both eyes. The first component of this myogenic potential, at a latency to peak of about 10 ms is a negative potential and is called n10 and, in healthy subjects, is equal in amplitude beneath both eyes, but after unilateral vestibular loss, the n10 potential beneath the eye opposite to the lesioned ear is greatly reduced or totally absent. n10 is a myogenic potential due to a crossed otolith-ocular pathway. In patients with total unilateral superior vestibular neuritis, in whom saccular function is largely intact (as shown by the presence of cervical vestibular evoked myogenic potentials (cVEMPs), but utricular function is probably compromised, there is a reduced n10 response beneath the contralesional eye, strongly indicating that n10 is due to utricular otolithic function.

Keywords: Bone conduction; Ocular vestibular-evoked myogenic potentials; Otolith; Vestibular disorder; Vestibular-evoked myogenic potentials.

Fig. 1

Examples of average oVEMPs to Fz BCV stimulation in a healthy subject and a patient with known unilateral vestibular deafferentation (uVL) after vestibular schwannoma surgery. The n10 responses (arrowheads) are the early negative components of the entire ocular vestibular evoked myogenic potential and are approximately equal beneath both eyes in the healthy subject, but in the uVL patient the n10 beneath the contralesional (left) eye is very small or absent, whereas the n10 beneath the ipsilesional eye is of normal amplitude. This asymmetry in n10 simultaneous linear acceleration stimulation of both mastoids is the indicator of otolithic, and, indeed, utricular function.

Fig. 2

A simplified schematic version of some of the known neural vestibulo-ocular projections responsible for the asymmetric oVEMP response to Fz BCV after unilateral vestibular loss. It is based on known anatomical projections and physiological results from Suzuki et al. and Uchino et al. that high frequency electrical stimulation of the utricular nerve results in activation of the contralateral inferior oblique muscle, and the ipsilateral superior oblique muscle via some of the pathways shown schematically here. Afferents from the saccular and utricular macula project to the vestibular nuclei, but the exact termination of these afferents is not yet known so this figure represents the present uncertainty about the exact neural connections of these afferents within the vestibular nuclei as an open box. The otolithic projections to other eye muscles are not shown. Fz stimulation is indicated schematically. The afferents from the saccular macula course predominantly in the inferior vestibular nerve, and synapse on inhibitory neurons in the vestibular nucleus (black hexagon), which, in turn, project to spinal motoneurons controlling the sternocleidomastoid muscle (SCM). So the cVEMP indicates predominantly sacculo-collic function.

Fig. 3

The neural innervation of the vestibular sense organs of the labyrinth (after de Burlet) and clinical tests which evaluate the functional status of the various vestibular sensory regions. The columns labelled Response identify the responses associated with clinical tests of each sense organ.

Fig. 4

The asymmetry ratio of all 13 patients with superior vestibular neuritis (filled diamonds) plotted as a function of age. Also on this graph are the data points from earlier published data from our laboratories 4-6 showing the asymmetry ratios of 67 healthy subjects (open triangles) and 11 patients with complete unilateral vestibular loss (open circles). The mean values and two-tailed 95% confidence intervals for the mean are shown within the square while the boxplots for the medians, quartiles and ranges are shown outside the square. All patients showed an asymmetry ratio greater than any of the normal subjects tested, and the similarity of the AR results for SVN and uVL patients is clear.

Fig. 5

The electrode configuration for optimum recording of oVEMPs. N.B. the subject is looking upwards in the median plane. The point marked X indicates the location of Fz.