Otolithic Receptor Mechanisms for Vestibular-Evoked Myogenic Potentials: A Review

Abstract

Air-conducted sound and bone-conduced vibration activate otolithic receptors and afferent neurons in both the utricular and saccular maculae, and trigger small electromyographic (EMG) responses [called vestibular-evoked myogenic potentials (VEMPs)] in various muscle groups throughout the body. The use of these VEMPs for clinical assessment of human otolithic function is built on the following logical steps: (1) that high-frequency sound and vibration at clinically effective stimulus levels activate otolithic receptors and afferents, rather than semicircular canal afferents, (2) that there is differential anatomical projection of otolith afferents to eye muscles and neck muscles, and (3) that isolated stimulation of the utricular macula induces short latency responses in eye muscles, and that isolated stimulation of the saccular macula induces short latency responses in neck motoneurons. Evidence supports these logical steps, and so VEMPs are increasingly being used for clinical assessment of otolith function, even differential evaluation of utricular and saccular function. The proposal, originally put forward by Curthoys in 2010, is now accepted: that the ocular vestibular-evoked myogenic potential reflects predominantly contralateral utricular function and the cervical vestibular-evoked myogenic potential reflects predominantly ipsilateral saccular function. So VEMPs can provide differential tests of utricular and saccular function, not because of stimulus selectivity for either of the two maculae, but by measuring responses which are predominantly determined by the differential neural projection of utricular as opposed to saccular neural information to various muscle groups. The major question which this review addresses is how the otolithic sensory system, with such a high density otoconial layer, can be activated by individual cycles of sound and vibration and show such tight locking of the timing of action potentials of single primary otolithic afferents to a particular phase angle of the stimulus cycle even at frequencies far above 1,000 Hz. The new explanation is that it is due to the otoliths acting as seismometers at high frequencies and accelerometers at low frequencies. VEMPs are an otolith-dominated response, but in a particular clinical condition, semicircular canal dehiscence, semicircular canal receptors are also activated by sound and vibration, and act to enhance the otolith-dominated VEMP responses.

The Evidence for Selective Loss of Otolithic Function

“…17 (3) Neural evidence that these stimuli differentially activate otolithic as opposed to canal receptors. 3,18 (4) Evidence concerning the differential projection of utricular and saccular afferents to different muscle groups. 13,15 (5) Evidence that 500 Hz vibration elicits eye movements in healthy human subjects.…”

“…7,8 Anatomical and physiological evidence shows that n10 is a crossed excitatory potential originating primarily from utricular afferents coursing in the superior division of the contralateral vestibular nerve. 3 In contrast, the first positive component of the cVEMP waveform (called p13 [the initial positive potential of the cVEMP response at a latency of around 13 ms] followed by n23 [the subsequent negative potential of the cVEMP response at a latency of around 23 ms]), is a positive (inhibitory) potential recorded over the partially contracted sternocleidomastoid muscle (SCM; contracted by the subject lifting or turning the head) and it is an uncrossed positive (inhibitory) potential originating primarily from saccular afferents coursing in the ipsilateral inferior vestibular nerve. The combination of vHIT and VEMPs provides a complete picture of peripheral vestibular dynamic function.…”

“…The dynamic function of every semicircular canal in both labyrinths is tested by the video head impulse test (vHIT) reviewed in Halmagyi et al 1 using brief abrupt high acceleration head turns. The dynamic function of every otolithic sense organ (utricle, saccule) is tested by the two types of vestibularevoked myogenic potentials (VEMPs; cervical VEMP [cVEMP], ocular VEMP [oVEMP]), 2,3 whether evoked by airconducted sound (ACS) or bone-conducted vibration (BCV). The oVEMP tests mainly dynamic utricular function and the cVEMP tests mainly dynamic saccular function.…”

“…The oVEMP tests mainly dynamic utricular function and the cVEMP tests mainly dynamic saccular function. 3 The results of these tests have shown instances of complete bilateral loss of all peripheral vestibular function 1 as well as of bilateral loss of just one pair of matched sensory organs such as bilateral horizontal canal loss, 4 and even cases of selective sparing of bilateral anterior canals while other sense organs in both labyrinths are dysfunctional. 5 Other patients have been found to have dysfunction of one individual sense organ within a labyrinth, whereas other sense organs function normally.…”

“…Consider the otolithic system. Physiological evidence shows that 500 Hz sound and vibration selectively activate one class of otolith afferent neurons reviewed in Curthoys et al 3 So the assumption is that reduced otolithic-dependent responses to sound or vibration imply loss of otolith function. That apparently straightforward assumption is subject to caveats-for example, that the reduced or absent response is not due to inadequate stimulation, or central dysfunction, or dysfunction at the neuromuscular junction responsible for the response.…”