Sound abnormally stimulates the vestibular system in canal dehiscence syndrome by generating pathological fluid-mechanical waves

Abstract

Individuals suffering from Tullio phenomena experience dizziness, vertigo, and reflexive eye movements (nystagmus) when exposed to seemingly benign acoustic stimuli. The most common cause is a defect in the bone enclosing the vestibular semicircular canals of the inner ear. Surgical repair often corrects the problem, but the precise mechanisms underlying Tullio phenomenon are not known. In the present work we quantified the phenomenon in an animal model of the condition by recording fluid motion in the semicircular canals and neural activity evoked by auditory-frequency stimulation. Results demonstrate short-latency phase-locked afferent neural responses, slowly developing sustained changes in neural discharge rate, and nonlinear fluid pumping in the affected semicircular canal. Experimental data compare favorably to predictions of a nonlinear computational model. Results identify the biophysical origin of Tullio phenomenon in pathological sound-evoked fluid-mechanical waves in the inner ear. Sound energy entering the inner ear at the oval window excites fluid motion at the location of the defect, giving rise to traveling waves that subsequently excite mechano-electrical transduction in the vestibular sensory organs by vibration and nonlinear fluid pumping.

Semicircular canal biomechanics in health and disease

“…We should stress that earlier reports include the hydraulic mass m and simulate responses above 6 Hz (Oman et al 1987; Rabbitt et al 2003), but high-frequency predictions using Eq. 1 are suspect because membranous labyrinth deformation is not included (Grieser et al 2016; Iversen and Rabbitt 2017; Iversen et al 2018).…”

“…Semicircular canal afferent nerve responses to auditory frequency stimuli in animal models of canal dehiscence syndrome have revealed two characteristic types of responses: 1 ) increases or decreases in action potential discharge rate that build up with the time constant of the canal, and 2 ) entrainment of the discharge rate to the auditory frequency stimulus with action potentials occurring at a precise phase relative to the stimulus (Carey et al 2004; Iversen et al 2018). In mammals, neurons of the first type typically have regular interspike intervals at rest, while neurons with of the second type are calyx bearing and have irregular interspike intervals at rest (Curthoys et al 2016).…”

“…Part of the sound energy entering the inner ear at the oval window is diverted toward the dehiscence, thus accounting for the conductive hearing loss (Songer and Rosowski 2010). This diverted sound energy generates a pressure gradient in the vestibular apparatus that can excite traveling waves along the membranous labyrinth (Grieser et al 2016; Iversen et al 2018). Conservation of mass requires the perilymph volume displacement entering the affected canal near the utricular vestibule to be balanced by an equal volume displacement at the fistula.…”

“…This generates a large pressure gradient acting across the membranous labyrinth between endolymph and perilymph at the site of the fistula. As a result, traveling waves are generated at the fistula and propagate toward the utricle (Iversen et al 2018). The direction of propagation is somewhat counterintuitive, because the waves travel toward the sound source rather than toward the fistula.…”

Bone-Conducted oVEMP Latency Delays Assist in the Differential Diagnosis of Large Air-Conducted oVEMP Amplitudes

“…Diagnosis is best made using a combination of symptoms, CT imaging, and audiovestibular test results, which often includes the recording of vestibular evoked myogenic potentials (VEMPs) (1). VEMP amplitudes are typically enlarged and/or thresholds are reduced as the opening in the superior semicircular canal renders vestibular receptors more susceptible to stimulation by sound and vibration (2)(3)(4)(5). Air-conducted (AC) ocular VEMP (oVEMP) amplitudes, cervical VEMP (cVEMP) thresholds, and high frequency (4000 Hz) AC and bone-conducted (BC) oVEMP amplitudes have high sensitivity in discriminating between dehiscent and normal ears (6)(7)(8)(9).…”