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

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.

Acute findings in an acquired neurosensory dysfunction

“…Because sound activation of saccule and utricle produce cervical and ocular VEMPs, respectively, it is not inconceivable that resonant energy in that range could affect vestibular function. In fact, the occupational health literature indicates that intense ultrasonic radiation can produce “a syndrome involving manifestations of nausea, headache, tinnitus, pain, dizziness, and fatigue …”

“…In fact, the occupational health literature indicates that intense ultrasonic radiation can produce "a syndrome involving manifestations of nausea, headache, tinnitus, pain, dizziness, and fatigue. 13,14 The potential mechanisms for injury by incident energy include cavitation bubble formation in body fluids. Cavitation bubbles can be produced in aqueous solutions by directed energy sources.…”

Cytochrome P450 26b1-mediated specification of vestibular striola and central zones is required for transient responses in linear acceleration

“…8c, d). Power spectra of head movements revealed higher power for Cyp26b1 cKO mutants than controls at high frequency (5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20) Hz) for all six dimensions (Fig. 8e, f).…”

“…Next, we tested whether the VOR was also affected in the Cyp26b1 cKO mutants based on the hypothesis that the striolar/central zone is important for vestibular-reflex function 13,20 . The VOR plays an important role in ensuring gaze stabilization during everyday activities by producing compensatory eye movements in the opposite direction of the head movement 39 .…”

“…We evaluated the importance of the striola to the VsEP evoked by linear jerk stimulation, a method that allows in vivo assessment of macular function independently of other sensory and motor contributions [16][17][18] . Several lines of indirect evidence implicate irregular afferents, which innervate the striola, in generating the VsEP 2,16,19,20 .…”