Comparison of sheep and human middle-ear ossicles: anatomy and inertial properties.

The sheep middle ear has been used in training to prepare physicians to perform surgeries and to test new ways of surgical access. This study aimed to (1) collect anatomical data and inertial properties of the sheep middle-ear ossicles and (2) explore effects of these features on sound transmission, in comparison to those of the human. Characteristic dimensions and inertial properties of the middle-ear ossicles of White-Alpine sheep (n = 11) were measured from high-resolution micro-CT data, and were assessed in comparison with the corresponding values of the human middle ear. The sheep middle-ear ossicles differed from those of human in several ways: anteroinferior orientation of the malleus handle, relatively small size of the incus with a relatively short distance to the lenticular process, a large area of the articular surfaces at the incudostapedial joint, and a relatively small moment of inertia along the anterior-posterior axis. Analysis in this study suggests that structure and orientation of the middle-ear ossicles in the sheep are conducive to an increase in the hinge-like ossicular-lever-action around the anterior-posterior axis. Considering the substantial anatomical differences, outcomes of middle-ear surgeries would presumably be difficult to assess from experiments using the sheep middle ear.

Ossicular resonance modes of the human middle ear for bone and air conduction.

The mean resonance frequency of the human middle ear under air conduction (AC) excitation is known to be around 0.8-1.2 kHz. However, studies suggest that the mean resonance frequency under bone conduction (BC) excitation is at a higher frequency around 1.5-2 kHz. To identify the cause for this difference, middle-ear responses to both AC and BC excitations were measured at the umbo and lateral process of the malleus using five human cadaver temporal bones. The resonance modes identified from these measurements, along with finite element analysis results, indicate the presence of two ossicular modes below 2 kHz. The dominant mode under AC excitation is the first mode, which typically occurs around 1.2 kHz and is characterized by a "hinging" ossicular motion, whereas the dominant mode under BC excitation is the second mode, which typically occurs around 1.7 kHz and is characterized by a "pivoting" ossicular motion. The results indicate that this second mode is responsible for the translational component in the malleus handle motion. The finding is also consistent with the hypothesis that a middle-ear structural resonance is responsible for the prominent peak seen at 1.5-2 kHz in BC limit data.

Anatomical and functional aspects of ligaments between the malleus and the temporomandibular joint.

The aim of this paper is to investigate the anatomical topography and the relationship between the ligaments, malleus and temporomandibular joint (TMJ) and to determine the role of these ligaments on the movement of the malleus. The malleus, incus, petrotympanic fissure (PTF), chorda tympani, anterior malleolar ligament (AML), discomallear ligament (DML), malleomandibular ligament, sphenomandibular ligament and articular disc were explored in 15 skulls. Traction and tension tests were carried out to clarify their role in malleolar movement. In 12 of the cases, two separate ligaments were connected to the anterior of the malleus, whereas a single ligament from the anterior of the malleus to the PTF was observed in 3 cases. In 12 cases, the DML united the retrodiscal tissues. In the other 3 cases, the medial and the lateral parts of the ligament were connected to the retrodiscal tissue after passing through the PTF. The thickness of the ligaments differed among specimens. When tension was applied to the DML no malleolar movement occurred, but when the AML was overstretched, significant movement was observed in 5 cadavers; little movement in 6 cadavers, and no movement in 4 cadavers. This study suggests that extreme stretching of the condyle in conjunction with the ligaments between the ossicles of the inner ear and the TMJ could be the reason for unexplained otological problems.

Biomechanics of the incudo-malleolar-joint - Experimental investigations for quasi-static loads.

Under large quasi-static loads, the incudo-malleolar joint (IMJ), connecting the malleus and the incus, is highly mobile. It can be classified as a mechanical filter decoupling large quasi-static motions while transferring small dynamic excitations. This is presumed to be due to the complex geometry of the joint inducing a spatial decoupling between the malleus and incus under large quasi-static loads. Spatial Laser Doppler Vibrometer (LDV) displacement measurements on isolated malleus-incus-complexes (MICs) were performed. With the malleus firmly attached to a probe holder, the incus was excited by applying quasi-static forces at different points. For each force application point the resulting displacement was measured subsequently at different points on the incus. The location of the force application point and the LDV measurement points were calculated in a post-processing step combining the position of the LDV points with geometric data of the MIC. The rigid body motion of the incus was then calculated from the multiple displacement measurements for each force application point. The contact regions of the articular surfaces for different load configurations were calculated by applying the reconstructed motion to the geometry model of the MIC and calculate the minimal distance of the articular surfaces. The reconstructed motion has a complex spatial characteristic and varies for different force application points. The motion changed with increasing load caused by the kinematic guidance of the articular surfaces of the joint. The IMJ permits a relative large rotation around the anterior-posterior axis through the joint when a force is applied at the lenticularis in lateral direction before impeding the motion. This is part of the decoupling of the malleus motion from the incus motion in case of large quasi-static loads.

A method to measure sound transmission via the malleus-incus complex.

BACKGROUND: The malleus-incus complex (MIC) plays a crucial role in the hearing process as it transforms and transmits acoustically-induced motion of the tympanic membrane, through the stapes, into the inner-ear. However, the transfer function of the MIC under physiologically-relevant acoustic stimulation is still under debate, especially due to insufficient quantitative data of the vibrational behavior of the MIC. This study focuses on the investigation of the sound transformation through the MIC, based on measurements of three-dimensional motions of the malleus and incus with a full six degrees of freedom (6 DOF). METHODS: The motion of the MIC was measured in two cadaveric human temporal bones with intact middle-ear structures excited via a loudspeaker embedded in an artificial ear canal, in the frequency range of 0.5-5 kHz. Three-dimensional (3D) shapes of the middle-ear ossicles were obtained by sequent micro-CT imaging, and an intrinsic frame based on the middle-ear anatomy was defined. All data were registered into the intrinsic frame, and rigid body motions of the malleus and incus were calculated with full six degrees of freedom. Then, the transfer function of the MIC, defined as velocity of the incus lenticular process relative to velocity of the malleus umbo, was obtained and analyzed. RESULTS: Based on the transfer function of the MIC, the motion of the lenticularis relative to the umbo reduces with frequency, particularly in the 2-5 kHz range. Analysis of the individual motion components of the transfer function indicates a predominant medial-lateral component at frequencies below 1 kHz, with low but considerable anterior-posterior and superior-inferior components that become prominent in the 2-5 kHz range. CONCLUSION: The transfer function of the human MIC, based on motion of the umbo and lenticularis, has been visualized and analyzed. While the magnitude of the transfer function decreases with frequency, its spatio-temporal complexity increases significantly.

Response of the human tympanic membrane to transient acoustic and mechanical stimuli: Preliminary results.

The response of the tympanic membrane (TM) to transient environmental sounds and the contributions of different parts of the TM to middle-ear sound transmission were investigated by measuring the TM response to global transients (acoustic clicks) and to local transients (mechanical impulses) applied to the umbo and various locations on the TM. A lightly-fixed human temporal bone was prepared by removing the ear canal, inner ear, and stapes, leaving the incus, malleus, and TM intact. Motion of nearly the entire TM was measured by a digital holography system with a high speed camera at a rate of 42 000 frames per second, giving a temporal resolution of <24 µs for the duration of the TM response. The entire TM responded nearly instantaneously to acoustic transient stimuli, though the peak displacement and decay time constant varied with location. With local mechanical transients, the TM responded first locally at the site of stimulation, and the response spread approximately symmetrically and circumferentially around the umbo and manubrium. Acoustic and mechanical transients provide distinct and complementary stimuli for the study of TM response. Spatial variations in decay and rate of spread of response imply local variations in TM stiffness, mass, and damping.

On the connection between the tympanic membrane and the malleus.

BACKGROUND: The tympano-mallear connection (TMC) is the soft-tissue connection between the tympanic membrane (TM) and the manubrium of the malleus. Some studies suggest that its mechanical properties may have a substantial influence on the mechanics and transfer function of the middle ear. However, relatively little is known about the dimensions of the TMC and its variability among individuals. METHOD: Thirteen samples were collected from human temporal bones, consisting of only the malleus and the TM. They were imaged using µCT without contrast enhancing agent. From the µCT images, the TMC dimensions were measured in both anterior-posterior direction (TMC width) and medial-lateral direction (TMC thickness). Three selected samples were examined using histological microscopy. RESULTS: Both TMC width and thickness featured a large variability among individuals. The minimal TMC width along the manubrium for different individuals covered a range between 83 and 840 µm. The minimal thickness ranged from 48 to 249 µm and the maximal thickness from 236 to 691 µm. Histological sections showed that the TMC consists of a narrow core of dense regular connective tissue, surrounded by loose connective tissue. In some samples, either of these two components was absent in the TMC at some manubrium locations. The configuration of these components varied among the samples as well. CONCLUSION: Our data confirm that a large inter-individual variability exists in the properties of the TM-malleus connection in humans in terms of its dimensions, tissue composition and configuration. Average data and their variability margins will be useful input for testing the importance of the TMC in finite element models.

Fully implantable hearing aid in the incudostapedial joint gap.

A fully implantable hearing aid is introduced which is a combined sensor-actuator-transducer designed for insertion into the incudostapedial joint gap (ISJ). The active elements each consist of a thin titanium membrane with an applied piezoelectric single crystal. The effectiveness of the operating principle is verified in a temporal bone study. We also take a closer look at the influence of an implantation-induced increase in middle ear stiffness on the transducer's output. An assembly of the transducer with 1 mm thickness is built and inserted into six temporal bones. At this thickness, the stiffness of the annular ligament is considerably increased, which leads to a loss in functional gain for the transducer. It is assumed that a thinner transducer would reduce this effect. In order to examine the performance for a prospective reduced pretension, we increased the gap size at the ISJ by 0.5 mm by removing the capitulum of the stapes in four temporal bones. The TM is stimulated with a broadband multisine sound signal in the audiological frequency range. The movement of the stapes footplate is measured with a laser Doppler vibrometer. The sensor signal is digitally processed and the amplified signal drives the actuator. The resulting feedback is minimized by an active noise control least mean square (LMS) algorithm which is implemented on a field programmable gate array. The dynamic range and the functional gain of the transducer in the temporal bones are determined. The results are compared to measurements from temporal bones without ISJ extension and to the results of Finite Elements Model (FE model) simulations. In the frequency range above 2 kHz a functional gain of 30 dB and more is achieved. This proposes the transducer as a potential treatment for high frequency hearing loss, e.g. for patients with noise-induced hearing loss. The transducer offers sufficient results for a comprehensive application. Adaptations in the transducer design or surgical approach are necessary to cope with ligament stiffening issues. These cause insufficient performance for low frequencies under 1 kHz.

Contribution of the incudo-malleolar joint to middle-ear sound transmission.

The malleus and incus in the human middle ear are linked by the incudo-malleolar joint (IMJ). The mobility of the human IMJ under physiologically relevant acoustic stimulation and its functional role in middle-ear sound transmission are still debated. In this study, spatial stapes motions were measured during acoustic stimulation (0.25-8 kHz) in six fresh human temporal bones for two conditions of the IMJ: (1) normal IMJ and (2) IMJ with experimentally-reduced mobility. Stapes velocity was measured at multiple points on the footplate using a scanning laser Doppler vibrometry (SLDV) system, and the 3D motion components were calculated under both conditions of the IMJ. The artificial reduction of the IMJ mobility was confirmed by measuring the relative motion between the malleus and the incus. The magnitudes of the piston-like motion of the stapes increased with the reduced IMJ mobility above 2 kHz. The increase was frequency dependent and was prominent from 2 to 4 kHz and at 5.5 kHz. The magnitude ratios of the rocking-like motions to the piston-like motion were similar for both IMJ conditions. The frequency-dependent change of the piston-like motion after the reduction of the IMJ mobility suggests that the IMJ is mobile under physiologically relevant levels of acoustic stimulation, especially at frequencies above 2 kHz.

Mouse homolog of KIAA0143 protein: hearing deficit induces specific changes of expression in auditory brainstem neurons.

Hearing deficit induced by mechanical cochlear damage, intense noise or ototoxic drugs produces a variety of structural and functional changes in the inner ear and the auditory brainstem. In the present study, we identified a novel gene that has activity dependent plasticity in the superior olivary complex by using suppression subtractive hybridization. We cloned a gene that encodes mouse homolog of KIAA0143 protein, one derived from a series of unidentified human genes. This gene termed mKIAA0143 shows differential expression of mRNA in the lateral superior olive between mice with hearing deficit and those with normal hearing ability. The mRNA thus obtained encodes a unique membrane-bound protein that consists of 819 amino acids. The gene locus was mapped using genomic DNA databases to the mouse chromosome 15D1. Green fluorescent protein-tagged mKIAA0143 was expressed in COS-1 cells. It was amply seen in the cellular plasma membrane.

Seismic sensitivity in the desert golden mole (Eremitalpa granti): a review.

Behavioral and anatomical studies relating to possible seismic sensitivity in the desert golden mole (Eremitalpa granti) are reviewed. Field studies in the Namib desert have shown that isolated hummocks of dune grass generate low-frequency vibrations, distinct from the background noise at a distance of many meters. The golden mole apparently uses these cues to orient itself toward the hummocks and the prey species within. An analysis of middle ear morphology suggests that the massive malleus of the golden mole is adapted toward a form of inertial bone conduction, suitable for the detection of seismic cues obtained in this manner. The significance of seismic sensitivity in this golden mole is briefly discussed.

The effect of immobilizing the gerbil's pars flaccida on the middle-ear's response to static pressure.

The pars flaccida of the tympanic membrane has a small role in regulating middle-ear static pressure (Acta Physiol. Scand. 118 (1983) 337; Hear. Res. 118 (1998) 35) and can also modify the response of the middle ear to low-frequency sound pressures by shunting ear-canal volume velocity around the pars tensa (Hear. Res. 13 (1984) 83; Hear. Res. 106 (1997) 39; Diversity in Auditory Mechanics (1997) 129; Audiol. Neuro-Otol. 4 (1999) 129). It has been hypothesized that these two functions can interact to reduce the effect of middle-ear static pressure on sound transmission through the middle ear (Hear. Res. 153 (2001) 146). This paper tests this hypothesis by measuring the effect of static pressure on the sensitivity of the p. tensa and the coupled malleus to sound, before and after immobilizing the p. flaccida. The results are consistent with a limited role of the p. flaccida in influencing the effect of static pressure on the p. tensa's acoustic response. However, this effect is only observed at low frequencies and over the +/-1 cm H(2)0 range of middle-ear static pressures. The results also suggest that large negative middle-ear pressures can induce a change in the mode of tympanic membrane motion regardless of the state of the p. flaccida.

Heterodyne interferometer measurements of the frequency response of the manubrium tip in cat.

A heterodyne interferometer proved to be a very accurate tool to measure amplitude and phase of the malleus response during acoustical stimulation. It was shown that to obtain equal accuracy in the acoustical pressure measurements, pressure response must be remeasured at short time intervals. At frequencies above 4 kHz various gross resonances are apparent on the frequency response curves. The resonances are, depending on the animal, more or less pronounced. As a result of the improved accuracy changes of the malleus vibration response with time could clearly be discriminated. These changes can be related to shifts in frequency of the position of these resonances. Comparison of experimental frequency response and lumped parameter model predictions from literature shows that these resonances are not present in the model responses.

Malleus vibration mode changes with frequency.

The mode of vibration of the cat manubrium is investigated by measuring its vibration in response to sound stimulus at four locations between the umbo and the processus lateralis with a heterodyne interferometer. The determination of mode requires high precision in measurement because amplitude differences between the points are small (about 20% at low audio-frequencies). Changes in the frequency response with time have been reported in an earlier paper. The nature and magnitude of this time change is analysed in detail: over a period of 1 h the average change in amplitude is about 5% and in phase 5 degrees. The malleus vibration at some frequencies is purely translational, it is rotational at others and mixed at most frequencies. When the motion is rotational the position of the axis of rotation shifts with frequency, the shifts are so large that the axis can lie near the umbo so that amplitudes at the processus lateralis are larger than at the umbo. The classical concept of the malleus rotating around a fixed axis running from the anterior mallar to the posterior incudal ligament fits our measurements only at low frequencies.

Interferometric measurement of the amplitude and phase of tympanic membrane vibrations in cat.

The amplitude and phase of the tympanic membrane and malleus vibrations were measured over a wide frequency range with a homodyne interferometer. When sound pressure was maintained constant near the tympanic membrane, the malleus frequency response followed the typical pattern up to 10 kHz as measured by previous investigators. At higher frequencies the response changes dramatically. Instead of decreasing with frequency, between 10 and 20 kHz the vibration amplitude oscillates around a value which is only about 20 dB lower than the low frequency plateau level. Measurements of malleus vibration at several points along its length indicate that its mode of vibration changes at high frequencies, and no longer consists of a simple rotational component. All points on the tympanic membrane vibrate in phase with the malleus up to a frequency of 1 kHz. Above 5 kHz discrete resonances are observed, and the response varies strongly with position on the tympanic membrane.

Modelling the malleus vibration as a rigid body motion with one rotational and one translational degree of freedom.

Vibration of a set of points distributed along the manubrium of cat was measured with a heterodyne interferometer in response to sinusoidal acoustic signals. The observed motion did not fit pure rotation of the malleus around a fixed axis coinciding with the anterior mallar and posterior incudal ligament as is classically assumed. As a first approximation a model of motion consisting of a rotational and a translational component was used. At low frequencies the rotation is mostly predominant, but the situation may be entirely reversed at mid and high frequencies. The presence of a translation besides rotation was also found at some frequencies in the motion of the human malleus.

A method for determining three-dimensional vibration in the ear.

In the classical concept of the middle ear function the malleus rotates around a fixed axis which implies that at small amplitudes of vibration its displacement is essentially one dimensional. As a consequence malleus vibrations have been measured previously along a single viewing axis. As a first step in the study of the complete malleus motion we determined the three dimensional components at a single point (umbo) of the manubrium. To define 3-D motion it is in principle necessary to measure the vibrations from widely different observation angles. The viewing angles are limited however in our case by the ear canal geometry to about +/-15 degrees. In order to resolve the 3-D components under these conditions it is necessary to measure the vibration components with high accuracy. Amplitude and phase of the umbo vibrations were measured with a heterodyne interferometer over a wide frequency range (100 Hz to 20 kHz). The system included a two axis goniometer with the axes of rotation positioned at the focal plane of the interferometer objective lens. It was therefore possible to change the viewing angle in small increments around two orthogonal axes while keeping the same point in focus. From a redundant set of measurements the three orthogonal components of vibration were calculated by least squares fitting. The vector sum of the three components gives the three dimensional motion of the observed point. The vibration of the point on the umbo was found not to follow a straight line but an elliptical path instead. The shape of the ellipse and the inclination of the plane of the ellipse with respect to the stationary malleus position changed with frequency. These observations are consistent with our earlier findings that the mode of malleus vibration changes with frequency [Decraemer et al. (1991) Hear. Res. 54, 305-318].

Human tympanic membrane deformation under static pressure.

The effect of static pressures in the range of plus and minus 1.6 kPa on the shape of tympanic membrane is measured using a non-contacting optical technique on a fresh human temporal bone. Full field data of the deformation are presented as well as cross-sections along two major directions. Strong asymmetry between medial and lateral movements is demonstrated. The displacement of the umbo is compared to other work. The rotation angle of the manubrium in function of pressure is calculated and also compared to other work. It is demonstrated that the rotation angels can not account for the measured movement of the umbo, which leads to the conclusion that for static high pressure levels the classical hypothesis of rotation around a fixed axis has to be abandoned. The comparison with data of TM displacement under dynamic stimuli is discussed.

Functional morphology of the middle ear in Chlorotalpa golden moles (Mammalia, Chrysochloridae): predictions from three models.

The ossicular apparatus of golden moles in the genus Chlorotalpa has received comparatively little attention in the literature, although the malleus is known to be intermediate in size between the "unmodified" malleus of Amblysomus and the hypertrophied mallei found in some other golden moles. In the present study, the middle ear structures of three Chlorotalpa species (C. duthieae, C. sclateri, and C. arendsi) are described. Measurements of middle ear structures were applied into three existing models of middle ear function. The predictions from the models suggest that the airborne hearing of Chlorotalpa species is limited to relatively low frequencies, but the impedance transformation by the middle ear apparatus is expected to be reasonably efficient. The sensitivity of the middle ear apparatus to inertial bone conduction is intermediate between that predicted for Amblysomus and that predicted for species with hypertrophied mallei. Hearing in fossorial mammals may be limited by factors other than the middle ear apparatus: the predictions for Chlorotalpa must therefore be treated with caution. However, a consideration of the "intermediate" middle ear morphology of Chlorotalpa species sheds some light on the origin of ossicular hypertrophy in golden moles. The limited enlargement of the malleus seen in Chlorotalpa is expected to have improved seismic sensitivity by bone conduction significantly at low frequencies, while airborne hearing might not have been adversely affected.

Biomechanical properties of sterilized human auditory ossicles.

Bone allograft material is treated with sterilization methods to prevent the transmission of diseases from the donor to the recipient. The effect of some of these treatments on the integrity of the bone is unknown. This study was performed to evaluate the effect of several sterilization methods on the mechanical behaviour of human middle ear bones. Due to the size and composition of the bones (approximately 1.5 mm diameter by 4 mm long), mechanical testing options were limited to the traditional platens compression test. Experiments were first performed with synthetic bone to evaluate the precision of this test applied to small specimens. Following this, fresh frozen human ossicles were thawed and sterilized with (i) 1 N NaOH (n = 12); (ii) 0.9% LpH, a phenolic solution (n = 12); or (iii) steam at 134 degrees C (n = 18). A group of 26 control specimens did not receive any sterilization treatment. Material and structural properties were determined from axial compression testing. Results from the synthetic bone showed that the test was reproducible, with standard deviations less than 20% of the means. Significant differences occurred in stiffness and ultimate force values between NaOH-treated and autoclaved bones when compared to normals (p<0.05), but not for LpH-treated bones. LpH is not approved for medical use, so NaOH is the most appropriate of the treatments studied for the sterilization of ossicle allografts.