The effect of craniokinesis on the middle ear of domestic chickens (Gallus gallus domesticus).

The avian middle ear differs from that of mammalians and contains a tympanic membrane, one ossicle (bony columella and cartilaginous extra-columella), some ligaments and one muscle. The rim of the eardrum (closing the middle ear cavity) is connected to the neurocranium and, by means of a broad ligament, to the otic process of the quadrate. Due to the limited number of components in the avian middle ear, the possibilities of attenuating the conduction of sound seem to be limited to activity of the stapedius muscle. We investigate to what extent craniokinesis may impact the components of the middle ear because of the connection of the eardrum to the movable quadrate. The quadrate is a part of the beak suspension and plays an important role in craniokinesis. Micro-computed tomography was used to visualize morphology and the effect of craniokinesis on the middle ear in the domestic chicken (Gallus gallus domesticus). Both hens and roosters are considered because of their difference in vocalization capacity. It is hypothesized that effects, if present, of craniokinesis on the middle ear will be greater in roosters because of their louder vocalization. Maximal lower jaw depression was comparable for hens and roosters (respectively 34.1 ± 2.6° and 32.7 ± 2.5°). There is no overlap in ranges of maximal upper jaw elevation between the sexes (respectively 12.7 ± 2.5° and 18.5 ± 3.8°). Frontal rotation about the transversal quadrato-squamosal, and inward rotation about the squamosal-mandibular axes of the quadrate were both considered to be greater in roosters (respectively 15.4 ± 2.8° and 11.1 ± 2.5°). These quadrate rotations did not affect the columellar position or orientation. In hens, an influence of the quadrate movements on the shape of the eardrum could not be detected either; however, craniokinesis caused slight stretching of the eardrum towards the caudal rim of the otic process of the quadrate. In roosters, an inward displacement of the conical tip of the tympanic membrane of 0.378 ± 0.21 mm, as a result of craniokinesis, was observed. This is linked to a flattening and slackening of the eardrum. These changes most likely go along with a deformation of the extra-columella. Generally, in birds, larger beak opening is related to the intensity of vocalization. The coupling between larger maximal upper jaw lifting in roosters and the slackening of the eardrum suggest the presence of a passive sound attenuation mechanism during self-vocalization.

How does prestrain in the tympanic membrane affect middle-ear function? A finite-element model study in rabbit.

Experiments have shown that prestrain exists in the rabbit tympanic membrane (TM), also in the absence of external loads. To date, it is unclear how prestrain influences the vibration response of the middle ear (ME). In this study, a detailed 3D finite-element model of the rabbit ME was constructed based on experimentally validated material properties. The model incorporates different degrees of prestrain in the TM and simulates the ME vibration response to sound as a linear harmonic perturbation around the prestressed reference state. To account for finite deformations associated with large prestrains, a framework was developed that iteratively updates the initial unstrained geometry until the prestrained geometry is in agreement with the given reference geometry. After validating the model using quasi-static and acoustic measurement data, it was shown that small levels of prestrain already have a substantial impact on the normal umbo and footplate response due to a phenomenon known as prestress stiffening. Although the approach is not preferable, it was possible to replicate the effect of prestrain in the normal ME by appropriately scaling the elastic moduli and damping factors in the base model. To evaluate the effect of possible changes in TM prestrain when the normal state of the ear is altered due to pathological modifications in the ME structure, we created a model with a perforation in the TM. It was shown that the change in vibration response after perforation is affected at low frequencies by a release of TM prestrain. In future studies, it may be necessary to incorporate prestrain in ME models to better understand the function of the diseased or reconstructed ME, which may be relevant for the development of reconstructive tissue grafts in the middle ear.

Structural stiffening in the human middle ear due to static pressure: Finite-element analysis of combined static and dynamic middle-ear behavior.

The vibration response of the middle ear (ME) to sound changes when static pressure gradients are applied across the tympanic membrane (TM). To date, it has not been well understood which mechanisms lead to these changes in ME vibration response. In this study, a 3D finite-element model of the human ME was developed that simulates the sound-induced ME vibration response when positive and negative static pressures of up to 4 kPa are applied to the TM. Hyperelasticity of the soft-tissue components was considered to simulate large deformations under static pressure. Some ME components were treated as viscoelastic materials to capture the difference between their static and dynamic stiffness, which was needed to replicate both static and dynamic ME behavior. The change in dynamic stiffness with static preload was simulated by linearization of the hyperelastic constitutive model around the predeformed state. For the preloaded harmonic response, we found that the statically deformed ME geometry introduced asymmetry in the vibration loss between positive and negative pressure, which was due to the TM cone shape. As opposed to previous assumptions, the prestress in the ME due to static pressure had a substantial impact on the vibration response. We also found that material nonlinearity led to a higher stiffening at the umbo but a less pronounced stiffening at the footplate compared to the linear elastic condition. The results suggest that flexibility of the incudomalleolar joint (IMJ) enhances the decoupling of static umbo and footplate displacements, and that viscosity and viscoelasticity of the IMJ could play a role in the transfer of sound-induced vibrations from the umbo to the footplate. The components of the incudostapedial joint had minimal effect on ME mechanical behavior.

Prestrain in the rabbit eardrum measured by digital image correlation and micro-incisions.

Prestrain in the absence of external loads can have an important effect on the vibrational behavior of mechanical systems such as the middle ear. Studies that measure tympanic membrane (TM) prestrain are scarce, however, and provide no conclusive answer on the existence and nature of the prestrain. In this study, prestrain is measured in the TM of cadaveric rabbit ears by stereo digital image correlation. To release the prestrain, straight incisions of 0.33 mm are made on different locations in the TM with a direction parallel to either the radial or circular fibers in the membrane. The effect of sample dehydration during different stages in the experimental procedure is assessed and eliminated by rehydrating the samples directly before each measurement. The measurements demonstrate average prestrain values around the incisions between 3.52±2.34% and 13.62±7.92% for the different locations, with a noise floor of 0.07%. No clear differences were found between the prestrain values obtained for radial and circular incisions. Observed local variations in TM prestrain could not be clearly related to specific locations on the TM. The results suggest that TM prestrain may need to be considered in future studies of middle-ear function if the findings can be confirmed in human ears.

How flexibility and eardrum cone shape affect sound conduction in single-ossicle ears: a dynamic model study of the chicken middle ear.

It is believed that non-mammals have poor hearing at high frequencies because the sound-conduction performance of their single-ossicle middle ears declines above a certain frequency. To better understand this behavior, a dynamic three-dimensional finite-element model of the chicken middle ear was constructed. The effect of changing the flexibility of the cartilaginous extracolumella on middle-ear sound conduction was simulated from 0.125 to 8 kHz, and the influence of the outward-bulging cone shape of the eardrum was studied by altering the depth and orientation of the eardrum cone in the model. It was found that extracolumella flexibility increases the middle-ear pressure gain at low frequencies due to an enhancement of eardrum motion, but it decreases the pressure gain at high frequencies as the bony columella becomes more resistant to extracolumella movement. Similar to the inward-pointing cone shape of the mammalian eardrum, it was shown that the outward-pointing cone shape of the chicken eardrum enhances the middle-ear pressure gain compared to a flat eardrum shape. When the outward-pointing eardrum was replaced by an inward-pointing eardrum, the pressure gain decreased slightly over the entire frequency range. This decrease was assigned to an increase in bending behavior of the extracolumella and a reduction in piston-like columella motion in the model with an inward-pointing eardrum. Possibly, the single-ossicle middle ear of birds favors an outward-pointing eardrum over an inward-pointing one as it preserves a straight angle between the columella and extrastapedius and a right angle between the columella and suprastapedius, which provides the optimal transmission.

De novo topology optimization of total ossicular replacement prostheses.

Conductive hearing loss, due to middle ear pathologies or traumas, affects more than 5% of the population worldwide. Passive prostheses to replace the ossicular chain mainly rely on piston-like titanium and/or hydroxyapatite devices, which in the long term suffer from extrusion. Although the basic shape of such devices always consists of a base for contact with the eardrum and a stem to have mechanical connection with the residual bony structures, a plethora of topologies have been proposed, mainly to help surgical positioning. In this work, we optimize the topology of a total ossicular replacement prosthesis, by maximizing the global stiffness and under the smallest possible volume constraint that ensures material continuity. This investigation optimizes the prosthesis topology in response to static displacement loads with amplitudes that normally occur during sound stimulation in a frequency range between 100 Hz and 10 kHz. Following earlier studies, we discuss how the presence and arrangement of holes on the surface of the prosthesis plate in contact with the umbo affect the overall geometry. Finally, we validate the designs through a finite-element model, in which we assess the prosthesis performance upon dynamic sound pressure loads by considering four different constitutive materials: titanium, cortical bone, silk, and collagen/hydroxyapatite. The results show that the selected prostheses present, almost independently of their constitutive material, a vibroacustic behavior close to that of the native ossicular chain, with a slight almost constant positive shift that reaches a maximum of ≈5 dB close to 1 kHz. This work represents a reference for the development of a new generation of middle ear prostheses with non-conventional topologies for fabrication via additive manufacturing technologies or ultraprecision machining in order to create patient-specific devices to recover from conductive hearing loss.

Evaluation of Artificial Fixation of the Incus and Malleus With Minimally Invasive Intraoperative Laser Vibrometry (MIVIB) in a Temporal Bone Model.

BACKGROUND: A significant number of adults suffer from conductive hearing loss due to chronic otitis media, otosclerosis, or other pathologies. An objective measurement of ossicular mobility is needed to avoid unnecessarily invasive middle ear surgery and to improve hearing outcomes. METHODS: Minimally invasive intraoperative laser vibrometry provides a method that is compatible with middle ear surgery, where the tympanic membrane is elevated. The ossicles were driven by a floating mass transducer and their mobility was measured using a laser Doppler vibrometer. Utilising this method, we assessed both the absolute velocities of the umbo and incus long process as well as the incus-to-umbo velocity ratio during artificial fixation of the incus alone or incus and malleus together. RESULTS: The reduction of absolute velocities was 8 dB greater at the umbo and 17 dB at the incus long process for incus-malleus fixations when compared with incus fixation alone. Incus fixation alone resulted in no change to the incus-to-umbo velocity ratio where incus-malleus fixations reduced this ratio (-11 dB). The change in incus velocity was shown to be the most suitable parameter to distinguish between incus fixation and incus-malleus fixation. When the whole frequency range was analyzed, one could also differentiate these two fixations from previously published stapes fixation, where the higher frequencies were less affected. CONCLUSION: Minimally invasive intraoperative laser vibrometry provides a promising objective analysis of ossicular mobility that would be useful intraoperatively.

The effect of single-ossicle ear flexibility and eardrum cone orientation on quasi-static behavior of the chicken middle ear.

In the single-ossicle ear of chickens, the quasi-static displacement of the umbo shows great asymmetry; umbo displacements are much larger for negative than for positive pressure in the middle ear, which is opposite to the typical asymmetry observed in mammal ears. To better understand this behavior, a finite-element model was created of the static response of the chicken middle ear. The role of flexibility of the extracolumella in the model was investigated, and the potential effect of the outward orientation of the tympanic-membrane cone was studied by building two adapted models with a flat membrane and an inverted conical membrane. It is found that the extracolumella must be made of flexible material to explain the large inward displacements of the umbo, and that displacements of the footplate are much smaller due to bending of the flexible extracolumella. However, increasing extracolumellar stiffness mostly reduces umbo displacement rather than increasing footplate displacement. The results suggest that the inverted orientation of the membrane cone is responsible for the change in asymmetry of the umbo displacement curve. The asymmetry of the footplate displacement curve in the normal model is smaller, but increases towards positive middle-ear pressure in the case of a flat or inverted membrane geometry.

Sound localization in the lizard using internally coupled ears: A finite-element approach.

A number of interesting differences become apparent when comparing the hearing systems of terrestrial vertebrates, especially between mammals and non-mammals. Almost all non-mammals possess only a single ossicle, enabling impedance matching and hearing below 10 kHz. The middle ear (ME) evolved as a chain of three ossicles in mammals, enabling sound transmission up to higher frequencies than in similar-sized non-mammals. The relatively low-frequency hearing in non-mammals is associated with audible wavelengths that are significantly larger than the head. Therefore, it is unlikely that localization of the sound source can be obtained by using external cues between the ears (intensity and time difference between both sides), especially when compared to similarly sized mammals. The heads of many non-mammals contain large air-filled cavities, which acoustically couple both MEs. This article studies acoustic responses and sound-source localization capabilities of the coupled MEs of the brown anole (Anolis sagrei), using finite-element modeling. Based on high-resolution µCT data, 3D finite-element models of the ME and interaural cavity were constructed. The parameter values in the ME model were determined such that the response of the isolated ME matches experimental data of literature and the velocity ratio between the tympanic membrane (apex) and footplate reflects the anatomical arrangement of the columellar lever in the anole. It was found from simulation of the coupled ME model that the interaural connection amplifies intensity differences between both sides and thus enhances the capability of sound-source localization. In addition, the interaural canal doubles the phase differences of the incident external sound waves between the eardrums. In isolated ears, generating such phase differences would require head sizes twice as large. Effects of the inner-ear loading on the sound-source localization of the coupled MEs were investigated as well. The inner-ear load lowered the peak velocity ratios between the ears, but created broader plateaus of useful directionality, indicating that inner-ear loading not only influences sound perception but also sound localization in internally connected ears.

Quasi-static and dynamic motions of the columellar footplate in ostrich (Struthio camelus) measured ex vivo.

The nature of the movement of the columellar footplate (CFP) in birds is still a matter of ongoing debate. Some sources claim that rocking motion is dominant, while others propose a largely piston-like motion. In this study, motions of the CFP are experimentally investigated in the ostrich using a post-mortem approach. For quasi-static loads, micro-CT scans of ostrich heads were made under positive and negative middle-ear pressures of 1 kPa. For dynamic loads, laser Doppler vibrometry was used to measure the velocity on multiple locations of the CFP as a function of excitation frequency from 0.125 to 4 kHz, and digital stroboscopic holography was used to assess the 1D full-field out-of-plane displacement of the CFP at different excitation frequencies. To expose the CFP in the experiments, measurements were made from the medial side of the CFP after opening and draining the inner ear. To determine the influence of the inner-ear load on CFP motions, a finite element model was created of the intact ostrich middle ear with inner-ear load included. For quasi-static loads, the CFP performed largely piston-like motions under positive ME pressure, while under negative ME pressure the difference between piston and rocking motion was smaller. For dynamic loads, the CFP motion was almost completely piston-like for frequencies below 1 kHz. For higher frequencies, the motions became more complicated with an increase of the rocking components, although they never exceeded the piston component. When including the inner-ear load to the model, the rocking components started to increase relative to the piston component when compared to the result of the model with unloaded CFP, but only at high frequencies above 1 kHz. In this frequency range, the motion could no longer be identified as purely piston-like or rocking. As a conclusion, the current results suggest that CFP motion is predominantly piston-like below 1 kHz, while at higher frequencies the motion becomes too complicated to be described as purely piston-like or rocking.

Do high sound pressure levels of crowing in roosters necessitate passive mechanisms for protection against self-vocalization?

High sound pressure levels (>120dB) cause damage or death of the hair cells of the inner ear, hence causing hearing loss. Vocalization differences are present between hens and roosters. Crowing in roosters is reported to produce sound pressure levels of 100dB measured at a distance of 1m. In this study we measured the sound pressure levels that exist at the entrance of the outer ear canal. We hypothesize that roosters may benefit from a passive protective mechanism while hens do not require such a mechanism. Audio recordings at the level of the entrance of the outer ear canal of crowing roosters, made in this study, indeed show that a protective mechanism is needed as sound pressure levels can reach amplitudes of 142.3dB. Audio recordings made at varying distances from the crowing rooster show that at a distance of 0.5m sound pressure levels already drop to 102dB. Micro-CT scans of a rooster and chicken head show that in roosters the auditory canal closes when the beak is opened. In hens the diameter of the auditory canal only narrows but does not close completely. A morphological difference between the sexes in shape of a bursa-like slit which occurs in the outer ear canal causes the outer ear canal to close in roosters but not in hens.

Deformation of avian middle ear structures under static pressure loads, and potential regulation mechanisms.

Static pressure changes can alter the configuration and mechanical behavior of the chain of ossicles, which may affect the acoustic transfer function. In mammals, the Eustachian tube plays an important role in restoring ambient middle ear pressure, hence restoring the acoustic transfer function and excluding barotrauma of the middle and inner ear. Ambient pressure fluctuations can be potentially extreme in birds and due to the simple structure of the avian middle ear (one ossicle, one muscle), regulation of the middle ear pressure via reflexive opening of the pharyngotympanic tube appears all the more important. In this study the deformations of the chicken (Gallus gallus domesticus) middle ear structures, as a result of middle ear pressure alterations, are quantified, using micro-CT scanning. It was experimentally tested whether reflexive opening of the pharyngotympanic tube to restore ambient middle ear pressure is present in chicken and mallard (Anas platyrhynchos) and whether this mechanism depends on sensing middle ear pressure indirectly via deformations of the middle ear components or sensing the middle ear pressure directly. A translation of the columella footplate was observed when middle ear pressure was kept at 1kPa and -1kPa relative to ambient pressure. Deformation of the tympanic membrane was larger than the columella footplate translation. Bending and deformation of the extracolumella was observed. Opening of the pharyngotympanic tube occurred at random pressure for both chicken and mallard when middle ear pressure was raised and lowered by 1.5kPa relative to ambient pressure. We also did not find a difference in middle ear venting rate when middle ear pressure was held constant at 0.5, 1, 1.5, -0.5, -1 and -1.5kPa for chickens and at 1, 2, 4, -1, -2 and -4kPa for mallards. As a result, no statement can be made about pressure within the avian middle ear being measured directly or indirectly. Our experiments do not support the presence of a short-loop reflexive control of pressure equilibration via the pharyngotympanic tube. However, it is still possible that triggering this loop requires additional sensorial input (e.g. visual, vestibular) or that it occurs voluntarily (being controlled at a higher brain level).

Eardrum and columella displacement in single ossicle ears under quasi-static pressure variations.

Although most birds encounter large pressure variations during flight, motion of the middle ear components as a result of changing ambient pressure are not well known or described. In the present study, motion of the columella footplate and tympanic membrane (extrastapedius) in domestic chickens (Gallus gallus domesticus) under quasi-static pressure conditions are provided. Micro-CT scans were made of cadaveric heads of chickens under positive (0.25 kPa, 0.5 kPa, 1 kPa, and 1.5 kPa) and negative (-0.25 kPa, -0.5 kPa, -1 kPa, and -1.5 kPa) middle ear pressure. Both extrastapedius and columella footplate displacements show a non-linear S-shaped curve as a function of pressure indicating non-linear response characteristics of the middle ear components. The S-curve is also seen in mammals, but unlike in mammals, the lateral piston-like displacement of both the columella footplate and extrastapedius, which is caused by an increased middle ear pressure are smaller than the medial piston-like displacements, caused by a decreased middle ear pressure of the same magnitude. Columella footplate piston displacements are always smaller than the extrastapedius piston displacements, indicating the flexibility of the extracolumella. The cone-shape of the avian tympanic membrane with inverted apex in comparison to the mammalian tympanic membrane can cause the inverted shape of the pressure response curve.

Tympanic membrane pressure buffering function at quasi-static and low-frequency pressure variations.

Deformation of the tympanic membrane is known to contribute to the pressure regulation processes in the middle ear cleft. In this paper we investigated pressure variations in the rabbit middle ear in response to sinusoidal varying pressures applied to the ear canal, with frequencies ranging from 0.5 Hz to 50 Hz and pressure amplitudes ranging between 0.25 kPa and 1 kPa. The transtympanic pressure difference was found to be smallest in the quasi-static range, and quickly increased as a function of frequency. The response curves showed asymmetry, with larger transtympanic pressures when positive pressures were applied in the ear canal. Normalized transtympanic pressure amplitudes remained fairly constant as a function of input pressure, with values in the range of 60%-70% relative to the applied pressure. The total harmonic distortion of the middle ear pressure signal was calculated and was found to be very small (≤2%) for low-pressure amplitudes and low frequencies. For pressure amplitudes in the order of 0.25 kPa-0.5 kPa, it increased to about 10% at 50 Hz. When a 1 kPa pressure amplitude was applied, variation between animals became large and distortion values up to 30% at 50 Hz were observed. The results showed that pressure buffering due to tympanic membrane displacement was most effective for compensating small transtympanic pressure loads at low frequencies.

Sound attenuation in the ear of domestic chickens (Gallus gallus domesticus) as a result of beak opening.

Because the quadrate and the eardrum are connected, the hypothesis was tested that birds attenuate the transmission of sound through their ears by opening the bill, which potentially serves as an additional protective mechanism for self-generated vocalizations. In domestic chickens, it was examined if a difference exists between hens and roosters, given the difference in vocalization capacity between the sexes. To test the hypothesis, vibrations of the columellar footplate were measured ex vivo with laser Doppler vibrometry (LDV) for closed and maximally opened beak conditions, with sounds introduced at the ear canal. The average attenuation was 3.5 dB in roosters and only 0.5 dB in hens. To demonstrate the importance of a putative protective mechanism, audio recordings were performed of a crowing rooster. Sound pressures levels of 133.5 dB were recorded near the ears. The frequency content of the vocalizations was in accordance with the range of highest hearing sensitivity in chickens. The results indicate a small but significant difference in sound attenuation between hens and roosters. However, the amount of attenuation as measured in the experiments on both hens and roosters is small and will provide little effective protection in addition to other mechanisms such as stapedius muscle activity.

Acoustic input impedance of the avian inner ear measured in ostrich (Struthio camelus).

In both mammals and birds, the mechanical behavior of the middle ear structures is affected by the mechanical impedance of the inner ear. In this study, the aim was to quantify the acoustic impedance of the avian inner ear in the ostrich, which allows us to determine the effect on columellar vibrations and middle ear power flow in future studies. To determine the inner ear impedance, vibrations of the columella were measured for both the quasi-static and acoustic stimulus frequencies. In the frequency range of 0.3-4 kHz, we used electromagnetic stimulation of the ossicle and a laser Doppler vibrometer to measure the vibration response. At low frequencies, harmonic displacements were imposed on the columella using piezo stimulation and the resulting force response was measured with a force sensor. From these measurement data, the acoustic impedance of the inner ear could be determined. A simple RLC model in series of the impedance measurements resulted in a stiffness reactance of KIE = 0.20·10(12) Pa/m³, an inertial impedance of MIE = 0.652·10(6) Pa s(2)/m³, and a resistance of RIE = 1.57·10(9) Pa s/m. We found that values of the inner ear impedance in the ostrich are one to two orders in magnitude smaller than what is found in mammal ears.

A single-ossicle ear: Acoustic response and mechanical properties measured in duck.

To date, the single-ossicle avian middle ear (ME) is poorly understood, despite its striking resemblance to the design of many currently used ossicular replacement prostheses. This study aims to improve comprehension of this system. The acoustic response and the mechanical properties of the mallard middle ear were studied by means of optical interferometry experiments and finite element (FE) simulations. A finite element model was constructed based on µCT data and validated using the experimental results. Stroboscopic holography was used to measure the full-field displacement of the tympanic membrane (TM) under acoustic stimulation, and the transfer function was obtained with laser Doppler vibrometry. A sensitivity analysis concluded that the most influential parameters for ME mechanics are the elasticity of the TM, the extracolumella (the cartilaginous part of the columella) and the annular ligament of the columellar footplate. Estimates for the Young's modulus of the TM were obtained by iteratively updating the FE model to match experimental data. A considerable inter-individual variability was found for the TM's elasticity. Comparison of the experimental results and the optimized FE model shows that, similar to the human middle ear, damping needs to be present in the TM to describe the specific spatial and frequency dependent vibrations of the TM. In summary, our results indicate which mechanical parameters are essential to the good functioning of the avian ME and provide a first estimation of their values.