Bone-conduction hyperacusis induced by superior canal dehiscence in human: the underlying mechanism.

Our ability to hear through bone conduction (BC) has long been recognized, but the underlying mechanism is poorly understood. Why certain perturbations affect BC hearing is also unclear. An example is BC hyperacusis (hypersensitive BC hearing)-an unnerving symptom experienced by patients with superior canal dehiscence (SCD). We measured BC-evoked sound pressures in scala vestibuli (PSV) and scala tympani (PST) at the basal cochlea in cadaveric human ears, and estimated hearing by the cochlear input drive (PDIFF = PSV - PST) before and after creating an SCD. Consistent with clinical audiograms, SCD increased BC-driven PDIFF below 1 kHz. However, SCD affected the individual scalae pressures in unexpected ways: SCD increased PSV below 1 kHz, but had little effect on PST. These new findings are inconsistent with the inner-ear compression mechanism that some have used to explain BC hyperacusis. We developed a computational BC model based on the inner-ear fluid-inertia mechanism, and the simulated effects of SCD were similar to the experimental findings. This experimental-modeling study suggests that (1) inner-ear fluid inertia is an important mechanism for BC hearing, and (2) SCD facilitates the flow of sound volume velocity through the cochlear partition at low frequencies, resulting in BC hyperacusis.

Superior canal dehiscence with tegmen defect revealed by otoscopy: Video clip demonstration of pulsatile tympanic membrane.

Superior canal dehiscence is a pathologic condition of the otic capsule acting as aberrant window of the inner ear. It results in reduction of inner ear impedance and in abnormal exposure of the labyrinthine neuroepithelium to the action of the surrounding structures. The sum of these phenomena leads to the onset of typical cochleo-vestibular symptoms and signs. Among them, pulsatile tinnitus has been attributed to a direct transmission of intracranial vascular activities to labyrinthine fluids. We present the first video-otoscopic documentation of spontaneous pulse-synchronous movements of the tympanic membrane in two patients with superior canal dehiscence. Pulsating eardrum may represent an additional sign of third-mobile window lesion.

Inner ear contribution to bone conduction hearing in the human.

Bone conduction (BC) hearing relies on sound vibration transmission in the skull bone. Several clinical findings indicate that in the human, the skull vibration of the inner ear dominates the response for BC sound. Two phenomena transform the vibrations of the skull surrounding the inner ear to an excitation of the basilar membrane, (1) inertia of the inner ear fluid and (2) compression and expansion of the inner ear space. The relative importance of these two contributors were investigated using an impedance lumped element model. By dividing the motion of the inner ear boundary in common and differential motion it was found that the common motion dominated at frequencies below 7 kHz but above this frequency differential motion was greatest. When these motions were used to excite the model it was found that for the normal ear, the fluid inertia response was up to 20 dB greater than the compression response. This changed in the pathological ear where, for example, otosclerosis of the stapes depressed the fluid inertia response and improved the compression response so that inner ear compression dominated BC hearing at frequencies above 400 Hz. The model was also able to predict experimental and clinical findings of BC sensitivity in the literature, for example the so called Carhart notch in otosclerosis, increased BC sensitivity in superior semicircular canal dehiscence, and altered BC sensitivity following a vestibular fenestration and RW atresia.

The physics of hearing: fluid mechanics and the active process of the inner ear.

Most sounds of interest consist of complex, time-dependent admixtures of tones of diverse frequencies and variable amplitudes. To detect and process these signals, the ear employs a highly nonlinear, adaptive, real-time spectral analyzer: the cochlea. Sound excites vibration of the eardrum and the three miniscule bones of the middle ear, the last of which acts as a piston to initiate oscillatory pressure changes within the liquid-filled chambers of the cochlea. The basilar membrane, an elastic band spiraling along the cochlea between two of these chambers, responds to these pressures by conducting a largely independent traveling wave for each frequency component of the input. Because the basilar membrane is graded in mass and stiffness along its length, however, each traveling wave grows in magnitude and decreases in wavelength until it peaks at a specific, frequency-dependent position: low frequencies propagate to the cochlear apex, whereas high frequencies culminate at the base. The oscillations of the basilar membrane deflect hair bundles, the mechanically sensitive organelles of the ear's sensory receptors, the hair cells. As mechanically sensitive ion channels open and close, each hair cell responds with an electrical signal that is chemically transmitted to an afferent nerve fiber and thence into the brain. In addition to transducing mechanical inputs, hair cells amplify them by two means. Channel gating endows a hair bundle with negative stiffness, an instability that interacts with the motor protein myosin-1c to produce a mechanical amplifier and oscillator. Acting through the piezoelectric membrane protein prestin, electrical responses also cause outer hair cells to elongate and shorten, thus pumping energy into the basilar membrane's movements. The two forms of motility constitute an active process that amplifies mechanical inputs, sharpens frequency discrimination, and confers a compressive nonlinearity on responsiveness. These features arise because the active process operates near a Hopf bifurcation, the generic properties of which explain several key features of hearing. Moreover, when the gain of the active process rises sufficiently in ultraquiet circumstances, the system traverses the bifurcation and even a normal ear actually emits sound. The remarkable properties of hearing thus stem from the propagation of traveling waves on a nonlinear and excitable medium.

Hydrostatic fluid pressure in the vestibular organ of the guinea pig.

Since inner ear hair cells are mechano-electric transducers the control of hydrostatic pressure in the inner ear is crucial. Most studies analyzing dynamics and regulation of inner ear hydrostatic pressure performed pressure measurements in the cochlea. The present study is the first one reporting about absolute hydrostatic pressure values in the labyrinth. Hydrostatic pressure of the endolymphatic system was recorded in all three semicircular canals. Mean pressure values were 4.06 cmH(2)O ± 0.61 in the posterior, 3.36 cmH(2)O ± 0.94 in the anterior and 3.85 cmH(2)O ± 1.38 in the lateral semicircular canal. Overall hydrostatic pressure in the vestibular organ was 3.76 cmH(2)O ± 0.36. Endolymphatic hydrostatic pressure in all three semicircular canals is the same (p = 0.310). With regard to known endolymphatic pressure values in the cochlea from past studies vestibular pressure values are comparable to cochlear values. Until now it is not known whether the reuniens duct and the Bast's valve which are the narrowest passages in the endolymphatic system are open or closed. Present data show that most likely the endolymphatic system is a functionally open entity.

Fluid coupling in a discrete model of cochlear mechanics.

A discrete model of cochlear mechanics is introduced that includes a full, three-dimensional, description of fluid coupling. This formulation allows the fluid coupling and basilar membrane dynamics to be analyzed separately and then coupled together with a simple piece of linear algebra. The fluid coupling is initially analyzed using a wavenumber formulation and is separated into one component due to one-dimensional fluid coupling and one comprising all the other contributions. Using the theory of acoustic waves in a duct, however, these two components of the pressure can also be associated with a far field, due to the plane wave, and a near field, due to the evanescent, higher order, modes. The near field components are then seen as one of a number of sources of additional longitudinal coupling in the cochlea. The effects of non-uniformity and asymmetry in the fluid chamber areas can also be taken into account, to predict both the pressure difference between the chambers and the mean pressure. This allows the calculation, for example, of the effect of a short cochlear implant on the coupled response of the cochlea.

A two-dimensional cochlear fluid model based on conformal mapping.

Using conformal mapping, fluid motion inside the cochlear duct is derived from fluid motion in an infinite half plane. The cochlear duct is represented by a two-dimensional half-open box. Motion of the cochlear fluid creates a force acting on the cochlear partition, modeled by damped oscillators. The resulting equation is one-dimensional, more realistic, and can be handled more easily than existing ones derived by the method of images, making it useful for fast computations of physically plausible cochlear responses. Solving the equation of motion numerically, its ability to reproduce the essential features of cochlear partition motion is demonstrated. Because fluid coupling can be changed independently of any other physical parameter in this model, it allows the significance of hydrodynamic coupling of the cochlear partition to itself to be quantitatively studied. For the model parameters chosen, as hydrodynamic coupling is increased, the simple resonant frequency response becomes increasingly asymmetric. The stronger the hydrodynamic coupling is, the slower the velocity of the resulting traveling wave at the low frequency side is. The model's simplicity and straightforward mathematics make it useful for evaluating more complicated models and for education in hydrodynamics and biophysics of hearing.

Head rotation evoked tinnitus due to superior semicircular canal dehiscence.

INTRODUCTION: Superior semicircular canal dehiscence affects the auditory and vestibular systems due to a partial defect in the canal's bony wall. In most cases, sound- and pressure-induced vertigo are present, and are sometimes accompanied by pulse-synchronous tinnitus. CASE PRESENTATION: We describe a 50-year-old man with superior semicircular canal dehiscence whose only complaints were head rotation induced tinnitus and autophony. Head rotation in the plane of the right semicircular canal with an angular velocity exceeding 600 degrees/second repeatedly induced a 'cricket' sound in the patient's right ear. High resolution temporal bone computed tomography changes, and an elevated umbo velocity, supported the diagnosis of superior semicircular canal dehiscence. CONCLUSION: In addition to pulse-synchronous or continuous tinnitus, head rotation induced tinnitus can be the only presenting symptom of superior semicircular canal dehiscence without vestibular complaints. We suggest that, in our patient, the bony defect of the superior semicircular canal ('third window') might have enhanced the flow of inner ear fluid, possibly producing tinnitus.

Development of cochlear amplification, frequency tuning, and two-tone suppression in the mouse.

It is generally believed that the micromechanics of active cochlear transduction mature later than passive elements among altricial mammals. One consequence of this developmental order is the loss of transduction linearity, because an active, physiologically vulnerable process is superimposed on the passive elements of transduction. A triad of sensory advantage is gained as a consequence of acquiring active mechanics; sensitivity and frequency selectivity (frequency tuning) are enhanced and dynamic operating range increases. Evidence supporting this view is provided in this study by tracking the development of tuning curves in BALB/c mice. Active transduction, commonly known as cochlear amplification, enhances sensitivity in a narrow frequency band associated with the "tip" of the tuning curve. Passive aspects of transduction were assessed by considering the thresholds of responses elicited from the tuning curve "tail," a frequency region that lies below the active transduction zone. The magnitude of cochlear amplification was considered by computing tuning curve tip-to-tail ratios, a commonly used index of active transduction gain. Tuning curve tip thresholds, frequency selectivity and tip-to-tail ratios, all indices of the functional status of active biomechanics, matured between 2 and 7 days after tail thresholds achieved adultlike values. Additionally, two-tone suppression, another product of active cochlear transduction, was first observed in association with the earliest appearance of tuning curve tips and matured along an equivalent time course. These findings support a traditional view of development in which the maturation of passive transduction precedes the maturation of active mechanics in the most sensitive region of the mouse cochlea.

Transmission of infrasonic pressure waves from cerebrospinal to intralabyrinthine fluids through the human cochlear aqueduct: Non-invasive measurements with otoacoustic emissions.

The cochlear aqueduct connecting intralabyrinthine and cerebrospinal fluids (CSF) acts as a low-pass filter that should be able to transmit infrasonic pressure waves from CSF to cochlea. Recent experiments have shown that otoacoustic emissions generated at 1kHz respond to pressure-related stapes impedance changes with a change in phase relative to the generator tones, and provide a non-invasive means of assessing intracochlear pressure changes. In order to characterize the transmission to the cochlea of CSF pressure waves due to respiration, the distortion-product otoacoustic emissions (DPOAE) of 12 subjects were continuously monitored around 1kHz at a rate of 6.25epochs/s, and their phase relative to the stimulus tones was extracted. The subjects breathed normally, in different postures, while thoracic movements were recorded so as to monitor respiration. A correlate of respiration was found in the time variation of DPOAE phase, with an estimated mean amplitude of 10 degrees , i.e. 60mm water, suggesting little attenuation across the aqueduct. Its phase lag relative to thoracic movements varied between 0 degrees and -270 degrees . When fed into a two-compartment model of CSF and labyrinthine spaces, these results suggest that respiration rate at rest is just above the resonance frequency of the CSF compartment, and just below the corner frequency of the cochlear-aqueduct low-pass filter, in line with previous estimates from temporal bone and intracranial measurements. The fact that infrasonic CSF waves can be monitored through the cochlea opens diagnostic possibilities in neurology.

How does the inner ear generate distortion product otoacoustic emissions?. Results from a realistic model of the human cochlea.

There is general agreement that distortion product (DP) otoacoustic emissions elicited by stimuli up to 80-90 dB SPL originate from the saturating nonlinearity of the cochlear amplifier at the basilar membrane site, S, where the responses to the two primary tones overlap. There are, however, different interpretations of how the inner ear transmits the effects of this process to the stapes. The supporters of transmission line models assert that the phenomenon depends upon two main mechanisms: (1) the generation of forward and backward traveling waves (TWs) by DP oscillations at S; (2) the backward propagation of wave components reflected by 'micromechanical impedance perturbations' at the sites where the DP TWs peak. However, quantitative predictions based on this view are still lacking. In contrast, here we show, using a nonlinear hydrodynamic model, that the emissions are propagated almost instantaneously through the fluid.

Cochlea's graded curvature effect on low frequency waves.

In the ear, sound waves are processed by a membrane of graded mechanical properties that resides in the fluid-filled spiral cochlea. The role of stiffness grading as a Fourier analyzer is well known, but the role of the curvature has remained elusive. Here, we report that increasing curvature redistributes wave energy density towards the cochlea's outer wall, affecting the shape of waves propagating on the membrane, particularly in the region where low frequency sounds are processed.

Mechanism of cochlear excitation at low intensities.

In order to assess the mechanisms of cochlear activation, the cochlear fluids of one cochlea of a guinea-pig (I) were coupled to those of a cochlea of a second guinea-pig (II) by means of a saline-filled narrow bore tube, the ends of which were placed in the fluids around the opened round windows of both cochleae, thus joining the two cochleae from two different animals into a single, larger, unsealed fluid system. In response to air-conducted sound stimulation of cochlea I, auditory nerve-brainstem evoked responses could be recorded in animal II, not only when the coupling tube was filled with saline, but also when it was filled with ultrasound gel (viscosity 100,000 greater than that of water), when there was a very large hole encompassing a relatively large expanse of the cochlear shell of animal I, and even when animal I was no longer alive. The necessary control experiments were performed. Therefore, it is suggested that at low stimulus intensities, the passive, incoming basilar membrane traveling wave may not activate the cochlea. Instead the fluid pressures (condensation/rarefactions) induced in the cochlear fluids by vibrations of the stapes footplate may be adequate to directly activate the outer hair cells, which then generate an active component of basilar membrane displacement.

Determinants of spatial and temporal coding by semicircular canal afferents.

The vestibular semicircular canals are internal sensors that signal the magnitude, direction, and temporal properties of angular head motion. Fluid mechanics within the 3-canal labyrinth code the direction of movement and integrate angular acceleration stimuli over time. Directional coding is accomplished by decomposition of complex angular accelerations into 3 biomechanical components-one component exciting each of the 3 ampullary organs and associated afferent nerve bundles separately. For low-frequency angular motion stimuli, fluid displacement within each canal is proportional to angular acceleration. At higher frequencies, above the lower corner frequency, real-time integration is accomplished by viscous forces arising from the movement of fluid within the slender lumen of each canal. This results in angular velocity sensitive fluid displacements. Reflecting this, a subset of afferent fibers indeed report angular acceleration to the brain for low frequencies of head movement and report angular velocity for higher frequencies. However, a substantial number of afferent fibers also report angular acceleration, or a signal between acceleration and velocity, even at frequencies where the endolymph displacement is known to follow angular head velocity. These non-velocity-sensitive afferent signals cannot be attributed to canal biomechanics alone. The responses of non-velocity-sensitive cells include a mathematical differentiation (first-order or fractional) imparted by hair-cell and/or afferent complexes. This mathematical differentiation from velocity to acceleration cannot be attributed to hair cell ionic currents, but occurs as a result of the dynamics of synaptic transmission between hair cells and their primary afferent fibers. The evidence for this conclusion is reviewed below.

Intralabyrinthine fluid dynamics: Meniere disease.

PURPOSE OF REVIEW: Meniere disease has long been postulated to be a disorder of intralabyrinthine fluid dynamics. RECENT FINDINGS: More recent developments in this field indicate that the control of fluid movement may be at a cellular level and that hormonal influence may be important. SUMMARY: The control of fluid and ion movements through aquaporins and gap junctions in the cell membranes are creating new perspectives in the mechanism of development of endolymphatic hydrops as well as potential methods for treatment. Intralabyrinthine fluid dynamics also play a role in the ability to locally deliver drugs to the inner ear through the middle ear.

The cochlear amplifier as a standing wave: "squirting" waves between rows of outer hair cells?

This paper draws attention to symmetric Lloyd-Redwood (SLR) waves-known in ultrasonics as "squirting" waves-and points out that their distinctive properties make them well-suited for carrying positive feedback between rows of outer hair cells. This could result in standing-wave resonance-in essence a narrow-band cochlear amplifier. Based on known physical properties of the cochlea, such an amplifier can be readily tuned to match the full 10-octave range of human hearing. SLR waves propagate in a thin liquid layer enclosed between two thin compliant plates or a single such plate and a rigid wall, conditions found in the subtectorial space of the cochlea, and rely on the mass of the inter-plate fluid interacting with the stiffness of the plates to provide low phase velocity and high dispersion. The first property means SLR wavelengths can be as short as the distance between rows of outer hair cells, allowing standing wave formation; the second permits wide-range tuning using only an order-of-magnitude variation in cochlear physical properties, most importantly the inter-row spacing. Viscous drag at the two surfaces potentially limits SLR wave propagation at low frequencies, but this can perhaps be overcome by invoking hydrophobic effects.

Prediction of the characteristics of two types of pressure waves in the cochlea: theoretical considerations.

The aim of this study was to predict the characteristics of two types of cochlear pressure waves, so-called fast and slow waves. A two-dimensional finite-element model of the organ of Corti (OC), including fluid-structure interaction with the surrounding lymph fluid, was constructed. The geometry of the OC at the basal turn was determined from morphological measurements of others in the gerbil hemicochlea. As far as mechanical properties of the materials within the OC are concerned, previously determined mechanical properties of portions within the OC were adopted, and unknown mechanical features were determined from the published measurements of static stiffness. Time advance of the fluid-structure scheme was achieved by a staggered approach. Using the model, the magnitude and phase of the fast and slow waves were predicted so as to fit the numerically obtained pressure distribution in the scala tympani with what is known about intracochlear pressure measurement. When the predicted pressure waves were applied to the model, the numerical result of the velocity of the basilar membrane showed good agreement with the experimentally obtained velocity of the basilar membrane documented by others. Thus, the predicted pressure waves appeared to be reliable. Moreover, it was found that the fluid-structure interaction considerably influences the dynamic behavior of the OC at frequencies near the characteristic frequency.

Cochlear aqueduct flow resistance depends on round window membrane position in guinea pigs.

The resistance for fluid flow of the cochlear aqueduct was measured in guinea pigs for different positions of the round window membrane. These different positions were obtained by applying different constant pressures to the middle ear cavity. Fluid flow through the aqueduct was induced by small pressure steps superimposed on these constant pressures. It was found that the resistance for fluid flow through the aqueduct depended on the round window position but not on flow direction. The results can be explained by special fibrous structures that connect the round window with the entrance of the aqueduct. It was also found that the equilibrium inner ear pressure depends on middle ear pressure, indicating that the aqueduct does not connect the inner ear with a cavity with constant pressure.

Do forward- and backward-traveling waves occur within the cochlea? Countering the critique of Nobili et al.

The question of whether or not forward- and backward-traveling waves occur within the cochlea constitutes a long-standing controversy in cochlear mechanics recently brought to the fore by the problem of understanding otoacoustic emissions. Nobili and colleagues articulate the opposition to the traveling-wave viewpoint by arguing that wave-equation formulations of cochlear mechanics fundamentally misrepresent the hydrodynamics of the cochlea [e.g., Nobili et al. (2003) J. Assoc. Res. Otolaryngol. 4:478-494]. To correct the perceived deficiencies of the wave-equation formulation, Nobili et al. advocate an apparently altogether different approach to cochlear modeling--the so-called "hydrodynamic" or "Green's function" approach--in which cochlear responses are represented not as forward- and backward-traveling waves but as weighted sums of the motions of individual basilar membrane oscillators, each interacting with the others via forces communicated instantaneously through the cochlear fluids. In this article, we examine Nobili and colleagues' arguments and conclusions while attempting to clarify the broader issues at stake. We demonstrate that the one-dimensional wave-equation formulation of cochlear hydrodynamics does not misrepresent long-range fluid coupling in the cochlea, as claimed. Indeed, we show that the long-range component of Nobili et al.'s three-dimensional force propagator is identical to the hydrodynamic Green's function representing a one-dimensional tapered transmission line. Furthermore, simulations that Nobili et al. use to discredit wave-equation formulations of cochlear mechanics (i.e., cochlear responses to excitation at a point along the basilar membrane) are readily reproduced and interpreted using a simple superposition of forward- and backward-traveling waves. Nobili and coworkers' critique of wave-equation formulations of cochlear mechanics thus appears to be without compelling foundation. Although the traveling-wave and hydrodynamic formulations impose strikingly disparate conceptual and computational frameworks, the two approaches ultimately describe the same underlying physics.