The impact of size on middle-ear sound transmission in elephants, the largest terrestrial mammal.

Elephants have a unique auditory system that is larger than any other terrestrial mammal. To quantify the impact of larger middle ear (ME) structures, we measured 3D ossicular motion and ME sound transmission in cadaveric temporal bones from both African and Asian elephants in response to air-conducted (AC) tonal pressure stimuli presented in the ear canal (PEC). Results were compared to similar measurements in humans. Velocities of the umbo (VU) and stapes (VST) were measured using a 3D laser Doppler vibrometer in the 7-13,000 Hz frequency range, stapes velocity serving as a measure of energy entering the cochlea-a proxy for hearing sensitivity. Below the elephant ME resonance frequency of about 300 Hz, the magnitude of VU/PEC was an order of magnitude greater than in human, and the magnitude of VST/PEC was 5x greater. Phase of VST/PEC above ME resonance indicated that the group delay in elephant was approximately double that of human, which may be related to the unexpectedly high magnitudes at high frequencies. A boost in sound transmission across the incus long process and stapes near 9 kHz was also observed. We discuss factors that contribute to differences in sound transmission between these two large mammals.

The influence of tympanic-membrane orientation on acoustic ear-canal quantities: A finite-element analysis.

Assuming plane waves, ear-canal acoustic quantities, collectively known as wideband acoustic immittance (WAI), are frequently used in research and in the clinic to assess the conductive status of the middle ear. Secondary applications include compensating for the ear-canal acoustics when delivering stimuli to the ear and measuring otoacoustic emissions. However, the ear canal is inherently non-uniform and terminated at an oblique angle by the conical-shaped tympanic membrane (TM), thus potentially confounding the ability of WAI quantities in characterizing the middle-ear status. This paper studies the isolated possible confounding effects of TM orientation and shape on characterizing the middle ear using WAI in human ears. That is, the non-uniform geometry of the ear canal is not considered except for that resulting from the TM orientation and shape. This is achieved using finite-element models of uniform ear canals terminated by both lumped-element and finite-element middle-ear models. In addition, the effects on stimulation and reverse-transmission quantities are investigated, including the physical significance of quantities seeking to approximate the sound pressure at the TM. The results show a relatively small effect of the TM orientation on WAI quantities, except for a distinct delay above 10 kHz, further affecting some stimulation and reverse-transmission quantities.

The impact of size on middle-ear sound transmission in elephants, the largest terrestrial mammal.

Elephants have a unique auditory system that is larger than any other terrestrial mammal. To quantify the impact of larger middle ear (ME) structures, we measured 3D ossicular motion and ME sound transmission in cadaveric temporal bones from both African and Asian elephants in response to air-conducted (AC) tonal pressure stimuli presented in the ear canal (P EC ). Results were compared to similar measurements in humans. Velocities of the umbo (V U ) and stapes (V ST ) were measured using a 3D laser Doppler vibrometer in the 7-13,000 Hz frequency range, stapes velocity serving as a measure of energy entering the cochlea-a proxy for hearing sensitivity. Below the elephant ME resonance frequency of about 300 Hz, the magnitude of V U /P EC was an order of magnitude greater than in human, and the magnitude of V ST /P EC was 5x greater. Phase of V ST /P EC above ME resonance indicated that the group delay in elephant was approximately double that of human, which may be related to the unexpectedly high magnitudes at high frequencies. A boost in sound transmission across the incus long process and stapes near 9 kHz was also observed. We discuss factors that contribute to differences in sound transmission between these two large mammals.

The Rhode non-linearity and its impact on cochlear mechanics.

The Reflections series takes a look back on historical articles from The Journal of the Acoustical Society of America that have had a significant impact on the science and practice of acoustics.

Human middle-ear muscle pulls change tympanic-membrane shape and low-frequency middle-ear transmission magnitudes and delays.

The three-bone flexible ossicular chain in mammals may allow independent alterations of middle-ear (ME) sound transmission via its two attached muscles, for both acoustic and non-acoustic stimuli. The tensor tympani (TT) muscle, which has its insertion on the malleus neck, is thought to increase tension of the tympanic membrane (TM). The stapedius (St) muscle, which has its insertion on the stapes posterior crus, is known to stiffen the stapes annular ligament. We produced ME changes in human cadaveric temporal bones by statically pulling on the TT and St muscles. The 3D static TM shape and sound-induced umbo motions from 20 Hz to 10 kHz were measured with optical coherence tomography (OCT); stapes motion was measured using laser-Doppler vibrometry (LDV). TT pulls made the TM shape more conical and moved the umbo medially, while St pulls moved the umbo laterally. In response to sound below about 1 kHz, stapes-velocity magnitudes generally decreased by about 10 dB due to TT pulls and 5 dB due to St pulls. In the 250 to 500 Hz region, the group delay calculated from stapes-velocity phase showed a decrease in transmission delay of about 150 µs by TT pulls and 60 µs by St pulls. Our interpretation of these results is that ME-muscle activity may provide a way of mechanically changing interaural time- and level-difference cues. These effects could help the brain align head-centered auditory and ocular-centered visual representations of the environment.

Stimulus-frequency otoacoustic emissions and middle-ear pressure gains in a finite-element mouse model.

For evoked otoacoustic emissions (OAEs), the stimulus and emission signals traverse the middle ear (ME) in forward and reverse directions, respectively. In this study, a fully coupled three-dimensional finite-element model of the mouse ear canal (EC), ME, and cochlea was used to calculate ME pressure gains, impedances, and reflectances at the EC-entrance and stapes-footplate-cochlear-fluid interfaces. The cochlear model incorporates a series of interdigitated Y-shaped structures sandwiched between the basilar membrane and reticular lamina, each comprised of a Deiters' cell, its phalangeal-process extension, and an outer hair cell (OHC). By introducing random perturbations to the OHC gains, stimulation-frequency otoacoustic emissions (SFOAEs) were generated. Raising the perturbation magnitude from 10% to 80% increased the SFOAE magnitude by up to 24 dB in the 10-30 kHz frequency range. Increasing or decreasing the stiffness of the stapes annular ligament and eardrum by a factor of 8 changed the SFOAEs by up to 30 dB, but the round-trip ME gain as measured could not account for this. A modified round-trip ME gain, with reflections removed at the EC-entrance and stapes-cochlea boundaries, eliminated a ±10 dB discrepancy and allowed ME changes to be quantitatively associated with changes in measured OAEs.

Cochlear motion across the reticular lamina implies that it is not a stiff plate.

Within the cochlea, the basilar membrane (BM) is coupled to the reticular lamina (RL) through three rows of piezo-like outer hair cells (OHCs) and supporting cells that endow mammals with sensitive hearing. Anatomical differences across OHC rows suggest differences in their motion. Using optical coherence tomography, we measured in vivo and postmortem displacements through the gerbil round-window membrane from approximately the 40-47 kHz best-frequency (BF) regions. Our high spatial resolution allowed measurements across the RL surface at the tops of the three rows of individual OHCs and their bottoms, and across the BM. RL motion varied radially; the third-row gain was more than 3 times greater than that of the first row near BF, whereas the OHC-bottom motions remained similar. This implies that the RL mosaic, comprised of OHC and phalangeal-process tops joined together by adhesion molecules, is much more flexible than the Deiters' cells connected to the OHCs at their bottom surfaces. Postmortem, the measured points moved together approximately in phase. These imply that in vivo, the RL does not move as a stiff plate hinging around the pillar-cell heads near the first row as has been assumed, but that its mosaic-like structure may instead bend and/or stretch.

Cochlear Fluid Spaces and Structures of the Gerbil High-Frequency Region Measured Using Optical Coherence Tomography (OCT).

Since it has been difficult to directly observe the morphology of the living cochlea, our ability to infer the mechanical functioning of the living ear has been limited. Nearly all our knowledge about cochlear morphology comes from postmortem tissue that was fixed and processed using procedures that possibly distort the structures and fluid spaces of the organ of Corti. In this study, optical coherence tomography was employed to obtain volumetric images of the high-frequency hook region of the gerbil cochlea, as viewed through the round window, with far better resolution capability than had been possible before. The anatomical structures and fluid spaces of the organ of Corti were segmented and quantified in vivo and over a 90-min postmortem period. We find that the arcuate-zone and pectinate-zone widths change very little postmortem. The volume of the scala tympani between the round-window membrane and basilar membrane and the volume of the inner spiral sulcus decrease in the first 60-min postmortem. While textbook drawings of the mammalian organ of Corti and cortilymph prominently depict the tunnel of Corti, the outer tunnel is typically missing. This is likely because textbook drawings are typically made from images obtained by histological methods. Here, we show that the outer tunnel is nearly twice as big as the tunnel of Corti or the space of Nuel. This larger outer tunnel fluid space could have a substantial, little-appreciated effect on cochlear micromechanics. We speculate that the outer tunnel forms a resonant structure that may affect reticular-lamina motion.

Comparative study of efficiency and characteristics of FMT and DRT installed in human cadavers for round-window stimulation.

Acoustic hearing aids generate amplified sound in the ear canal, and they are the standard of care for patients with mild to moderate sensorineural hearing loss. However, because of their limited frequency bandwidth, gain, and feedback, there is substantial room for improvement. Active middle ear implants, which directly vibrate the middle ear and cochlea, are an alternative approach to conventional acoustic hearing aids. They provide an opportunity to improve sound quality and speech understanding with amplification rehabilitation. For floating-mass type and direct-rod type (DRT) middle ear transducers, a differential floating-mass transducer (DFMT) and a tri-coil bellows transducer (TCBT), respectively, were fabricated to measure the output characteristics in four human temporal bones. Both were fabricated to have similar output forces per unit input and were placed in four human temporal bones to measure their output performances. The TCBT resulted in higher output than did the DFMT throughout the audible frequency range, and the output was more prominent at lower frequency ranges. In this study, we showed that DRT was a more effective method for round window stimulation. Because of its frequency characteristics and vibration efficiency, this implantation method can be utilized as a driving solution for middle ear implants.

In situ motions of individual inner-hair-cell stereocilia from stapes stimulation in adult mice.

In vertebrate hearing organs, mechanical vibrations are converted to ionic currents through mechanoelectrical-transduction (MET) channels. Concerted stereocilia motion produces an ensemble MET current driving the hair-cell receptor potential. Mammalian cochleae are unique in that the tuning of sensory cells is determined by their mechanical environment and the mode of hair-bundle stimulation that their environment creates. However, little is known about the in situ intra-hair-bundle motions of stereocilia relative to one another, or to their environment. In this study, high-speed imaging allowed the stereocilium and cell-body motions of inner hair cells to be monitored in an ex vivo organ of Corti (OoC) mouse preparation. We have found that the OoC rotates about the base of the inner pillar cell, the hair bundle rotates about its base and lags behind the motion of the apical surface of the cell, and the individual stereocilia move semi-independently within a given hair bundle.

Mouse middle-ear forward and reverse acoustics.

The mouse is an important animal model for hearing science. However, our knowledge of the relationship between mouse middle-ear (ME) anatomy and function is limited. The ME not only transmits sound to the cochlea in the forward direction, it also transmits otoacoustic emissions generated in the cochlea to the ear canal (EC) in the reverse direction. Due to experimental limitations, a complete characterization of the mouse ME has not been possible. A fully coupled finite-element model of the mouse EC, ME, and cochlea was developed and calibrated against experimental measurements. Impedances of the EC, ME, and cochlea were calculated, alongside pressure transfer functions for the forward, reverse, and round-trip directions. The effects on sound transmission of anatomical changes such as removing the ME cavity, pars flaccida, and mallear orbicular apophysis were also calculated. Surprisingly, below 10 kHz, the ME cavity, eardrum, and stapes annular ligament were found to significantly affect the cochlear input impedance, which is a result of acoustic coupling through the round window. The orbicular apophysis increases the delay of the transmission line formed by the flexible malleus, incus, and stapes, and improves the forward sound-transmission characteristics in the frequency region of 7-30 kHz.

A Vibro-Acoustic Hybrid Implantable Microphone for Middle Ear Hearing Aids and Cochlear Implants.

To develop totally implantable middle ear and cochlear implants, a miniature microphone that is surgically easy to implant and has a high sensitivity in a sufficient range of audio frequencies is needed. Of the various implantable acoustic sensors under development, only micro electro-mechanical system-type acoustic sensors, which attach to the umbo of the tympanic membrane, meet these requirements. We describe a new vibro-acoustic hybrid implantable microphone (VAHIM) that combines acceleration and sound pressure sensors. Each sensor can collect the vibration of the umbo and sound pressure of the middle ear cavity. The fabricated sensor was implanted into a human temporal bone and the noise level and sensitivity were measured. From the experimental results, it is shown that the proposed method is able to provide a wider-frequency band than conventional implantable acoustic sensors.

Achieved Gain and Subjective Outcomes for a Wide-Bandwidth Contact Hearing Aid Fitted Using CAM2.

OBJECTIVES: The objective of this study was to test the ability to achieve, maintain, and subjectively benefit from extended high-frequency amplification in a real-world use scenario, with a device that restores audibility for frequencies up to 10 kHz. DESIGN: A total of 78 participants (149 ears) with mild to moderately-severe sensorineural hearing loss completed one of two studies conducted across eight clinical sites. Participants were fitted with a light-driven contact hearing aid (the Earlens system) that directly drives the tympanic membrane, allowing extended high-frequency output and amplification with minimal acoustic feedback. Cambridge Method for Loudness Equalization 2 - High Frequency (CAM2)-prescribed gains for experienced users were used for initial fitting, and adjustments were made when required according to participant preferences for loudness and comfort or when measures of functional gain (FG) indicated that more or less gain was needed. Participants wore the devices for an extended period. Prescribed versus adjusted output and gain, frequency-specific FG, and self-perceived benefit assessed with the Abbreviated Profile of Hearing Aid Benefit, and a custom questionnaire were documented. Self-perceived benefit results were compared with those for unaided listening and to ratings with participants' own acoustic hearing aids. RESULTS: The prescribed low-level insertion gain from 6 to 10 kHz averaged 53 dB across all ears, with a range from 26 to 86 dB. After adjustment, the gain from 6 to 10 kHz decreased to an average of 45 dB with a range from 16 to 86 dB. Measured FG averaged 39 dB from 6 to 10 kHz with a range from 11 to 62 dB. Abbreviated Profile of Hearing Aid Benefit results revealed a significant improvement in communication relative to unaided listening, averaging 28 to 32 percentage points for the background noise, reverberation, and ease of communication subscales. Relative to participants' own hearing aids, the subscales ease of communication and aversiveness showed small but significant improvements for Earlens ranging from 6 to 7 percentage points. For the custom satisfaction questionnaire, most participants rated the Earlens system as better than their own hearing aids in most situations. CONCLUSIONS: Participants used and reported subjective benefit from the Earlens system. Most participants preferred slightly less gain at 6 to 10 kHz than prescribed for experienced users by CAM2, preferring similar gains to those prescribed for inexperienced users, but gains over the extended high frequencies were high relative to those that are currently available with acoustic hearing aids.

Organ of Corti vibration within the intact gerbil cochlea measured by volumetric optical coherence tomography and vibrometry.

There is indirect evidence that the mammalian cochlea in the low-frequency apical and the more commonly studied high-frequency basal regions function in fundamentally different ways. Here, we directly tested this hypothesis by measuring sound-induced vibrations of the organ of Corti (OoC) at three turns of the gerbil cochlea using volumetric optical coherence tomography vibrometry (VOCTV), an approach that permits noninvasive imaging through the bone. In the apical turn, there was little frequency selectivity, and the displacement-vs.-frequency curves had low-pass filter characteristics with a corner frequency of ~0.5-0.9 kHz. The vibratory magnitudes increased compressively with increasing stimulus intensity at all frequencies. In the middle turn, responses were similar except for a slight peak in the response at ~2.5 kHz. The gain was ~50 dB at the peak and 30-40 dB at lower frequencies. In the basal turn, responses were sharply tuned and compressively nonlinear, consistent with observations in the literature. These data demonstrated that there is a transition of the mechanical response of the OoC along the length of the cochlea such that frequency tuning is sharper in the base than in the apex. Because the responses are fundamentally different, it is not appropriate to simply frequency shift vibratory data measured at one cochlear location to predict the cochlear responses at other locations. Furthermore, this means that the number of hair cells stimulated by sound is larger for low-frequency stimuli and smaller for high-frequency stimuli for the same intensity level. Thus the mechanisms of central processing of sounds must vary with frequency. NEW & NOTEWORTHY A volumetric optical coherence tomography and vibrometry system was used to probe cochlear mechanics within the intact gerbil cochlea. We found a gradual transition of the mechanical response of the organ of Corti along the length of the cochlea such that tuning at the base is dramatically sharper than that at the apex. These data help to explain discrepancies in the literature regarding how the cochlea processes low-frequency sounds.

Human ossicular-joint flexibility transforms the peak amplitude and width of impulsive acoustic stimuli.

The role of the ossicular joints in the mammalian middle ear is still debated. This work tests the hypothesis that the two synovial joints filter potentially damaging impulsive stimuli by transforming both the peak amplitude and width of these impulses before they reach the cochlea. The three-dimensional (3D) velocity along the ossicular chain in unaltered cadaveric human temporal bones (N = 9), stimulated with acoustic impulses, is measured in the time domain using a Polytec (Waldbronn, Germany) CLV-3D laser Doppler vibrometer. The measurements are repeated after fusing one or both of the ossicular joints with dental cement. Sound transmission is characterized by measuring the amplitude, width, and delay of the impulsive velocity profile as it travels from the eardrum to the cochlea. On average, fusing both ossicular joints causes the stapes velocity amplitude and width to change by a factor of 1.77 (p = 0.0057) and 0.78 (p = 0.011), respectively. Fusing just the incudomalleolar joint has a larger effect on amplitude (a factor of 2.37), while fusing just the incudostapedial joint decreases the stapes velocity on average. The 3D motion of the ossicles is altered by fusing the joints. Finally, the ability of current computational models to predict this behavior is also evaluated.

Cochlear amplification and tuning depend on the cellular arrangement within the organ of Corti.

The field of cochlear mechanics has been undergoing a revolution due to recent findings made possible by advancements in measurement techniques. While it has long been assumed that basilar-membrane (BM) motion is the most important determinant of sound transduction by the inner hair cells (IHCs), it turns out that other parts of the sensory epithelium closer to the IHCs, such as the reticular lamina (RL), move with significantly greater amplitude for weaker sounds. It has not been established how these findings are related to the complex cytoarchitecture of the organ of Corti between the BM and RL, which is composed of a lattice of asymmetric Y-shaped elements, each consisting of a basally slanted outer hair cell (OHC), an apically slanted phalangeal process (PhP), and a supporting Deiters' cell (DC). Here, a computational model of the mouse cochlea supports the hypothesis that the OHC micromotors require this Y-shaped geometry for their contribution to the exquisite sensitivity and frequency selectivity of the mammalian cochlea. By varying only the OHC gain parameter, the model can reproduce measurements of BM and RL gain and tuning for a variety of input sound levels. Malformations such as reversing the orientations of the OHCs and PhPs or removing the PhPs altogether greatly reduce the effectiveness of the OHC motors. These results imply that the DCs and PhPs must be properly accounted for in emerging OHC regeneration therapies.

Acoustic stimulation on the round window for active middle ear implants.

Many clinical reports have discussed the effectiveness of stimulating the ear's round window (RW) with a tool to mitigate conductive and mixed hearing loss. The RW is one of the two openings from the middle ear into the inner ear. Various methods have been proposed to construct a highly efficient, easily implanted, and reliable RW transducer. Devices, however, such as floating mass transducers, have difficulty establishing proper contact without some degree of bone incision around the RW. Additionally, vibration energy may not be fully transmitted to the cochlea, but instead will be spread through the soft tissue around the transducer. We propose a more direct RW stimulation with very high acoustical impedance using a receiver that is a volume velocity source. We expect this source to overcome large acoustic impedance by maximizing sound pressure in a confined space, the RW niche. To verify the effectiveness of the proposed method, ear canal pressure, RW pressure, and stapes velocity are measured by acoustic RW stimulation of human temporal bones.

The effects of varying tympanic-membrane material properties on human middle-ear sound transmission in a three-dimensional finite-element model.

An anatomically based three-dimensional finite-element human middle-ear (ME) model is used to test the sensitivity of ME sound transmission to tympanic-membrane (TM) material properties. The baseline properties produce responses comparable to published measurements of ear-canal input impedance and power reflectance, stapes velocity normalized by ear-canal pressure (PEC), and middle-ear pressure gain (MEG), i.e., cochlear-vestibule pressure (PV) normalized by PEC. The mass, Young's modulus (ETM), and shear modulus (GTM) of the TM are varied, independently and in combination, over a wide range of values, with soft and bony TM-annulus boundary conditions. MEG is recomputed and plotted for each case, along with summaries of the magnitude and group-delay deviations from the baseline over low (below 0.75 kHz), mid (0.75-5 kHz), and high (above 5 kHz) frequencies. The MEG magnitude varies inversely with increasing TM mass at high frequencies. Increasing ETM boosts high frequencies and attenuates low and mid frequencies, especially with a bony TM annulus and when GTM varies in proportion to ETM, as for an isotropic material. Increasing GTM on its own attenuates low and mid frequencies and boosts high frequencies. The sensitivity of MEG to TM material properties has implications for model development and the interpretation of experimental observations.

Attenuating the ear canal feedback pressure of a laser-driven hearing aid.

Microphone placement behind the pinna, which minimizes feedback but also reduces perception of the high-frequency pinna cues needed for sound localization, is one reason why hearing-aid users often complain of poor sound quality and difficulty understanding speech in noisy situations. In this paper, two strategies are investigated for minimizing the feedback pressure (thereby increasing the maximum stable gain, MSG) of a wide-bandwidth light-activated contact hearing aid (CHA) to facilitate microphone placement in the ear canal (EC): (1) changing the location of the drive force and its direction at the umbo, and (2) placing an acoustic damper within the EC to reduce the feedback pressure at the microphone location. The MSG and equivalent pressure output (EPO) are calculated in a 3D finite element model of a human middle ear based on micro computed tomography (micro-CT) images. The model calculations indicate that changing the umbo-force direction can decrease feedback pressure, but at the expense of decreased EPO. However the model shows improvements in MSG without sacrificing EPO when an acoustic damper is placed in the EC. This was verified through benchtop experimentation and in human cadaver temporal bones. The results pave the path towards a wide-bandwidth hearing aid that incorporates an EC-microphone design.

Unraveling the mystery of hearing in gerbil and other rodents with an arch-beam model of the basilar membrane.

The mammalian basilar membrane (BM) consists of two collagen-fiber layers responsible for the frequency-to-place tonotopic mapping in the cochlea, which together form a flat beam over at least part of the BM width. The mechanics of hearing in rodents such as gerbil pose a challenge to our understanding of the cochlea, however, because for gerbil the two layers separate to form a pronounced arch over the remaining BM width. Moreover, the thickness and total width normally thought to determine the local stiffness, and tonotopic mapping in turn, change little along the cochlear length. A nonlinear analysis of a newly developed model, incorporating flat upper and arched lower fiber layers connected by ground substance, explains the initial plateau and subsequent quadratic increase found in measured stiffness vs. deflection curves under point loading, while for pressure loading the model accurately predicts the tonotopic mapping. The model also has applicability to understanding cochlear development and to interpreting evolutionary changes in mammalian hearing.