A two-layer outer hair cell model with orthotropic piezoelectric properties: correlation of cell resonant frequencies with tuning in the cochlea

The frequency response of outer hair cells (OHCs) of different lengths is studied using a mathematical model of a two-layer cylindrical shell with orthotropic properties. Material properties in the model are determined from experimental measurements reported in the literature, and the variation of material properties with the cell length is studied. The cortical lattice's Poisson ratios are found to remain fairly constant with cell length, while its stiffness changes significantly with cell length. The natural frequencies corresponding to several modes of deformation of an OHC with intracellular and extracellular fluids are calculated from this model. Our results suggest that the best frequency in the cochlea at the position where the OHC is located corresponds to different modes of deformation of the OHC, depending on the OHC length. For short OHCs, the best frequency is close to the natural frequency of the axisymmetric mode; for long OHCs, it is close to the natural frequencies of the beam-like bending and pinched modes. Such a difference in resonant modes for short and long OHCs at the best frequency suggests that different modes of OHC elongation motility may be present in amplifying the basilar membrane motion in the high and low frequency regions of the cochlea.     

Harmonic calls and indifferent females: no preference for human consonance in an anuran

The human music faculty might have evolved from rudimentary components that occur in non-human animals. The evolutionary history of these rudimentary perceptual features is not well understood and rarely extends beyond a consideration of vertebrates that possess a cochlea. One such antecedent is a preferential response to what humans perceive as consonant harmonic sounds, which are common in many animal vocal repertoires. We tested the phonotactic response of female túngara frogs (Physalaemus pustulosus) to variations in the frequency ratios of their harmonically structured mating call to determine whether frequency ratio influences attraction to acoustic stimuli in this vertebrate that lacks a cochlea. We found that the ratio of frequencies present in acoustic stimuli did not influence female response. Instead, the amount of inner ear stimulation predicted female preference behaviour. We conclude that the harmonic relationships that characterize the vocalizations of these frogs did not evolve in response to a preference for frequency intervals with low-integer ratios. Instead, the presence of harmonics in their mating call, and perhaps in the vocalizations of many other animals, is more likely due to the biomechanics of sound production rather than any preference for ‘more musical’ sounds.     

Infrasonic hearing in birds: a review of audiometry and hypothesized structure–function relationships

The perception of airborne infrasound (sounds below 20 Hz, inaudible to humans except at very high levels) has been documented in a handful of mammals and birds. While animals that produce vocalizations with infrasonic components (e.g. elephants) present conspicuous examples of potential use of infrasound in the context of communication, the extent to which airborne infrasound perception exists among terrestrial animals is unclear. Given that most infrasound in the environment arises from geophysical sources, many of which could be ecologically relevant, communication might not be the only use of infrasound by animals. Therefore, infrasound perception could be more common than currently realized. At least three bird species, each of which do not communicate using infrasound, are capable of detecting infrasound, but the associated auditory mechanisms are not well understood. Here we combine an evaluation of hearing measurements with anatomical observations to propose and evaluate hypotheses supporting avian infrasound detection. Environmental infrasound is mixed with non‐acoustic pressure fluctuations that also occur at infrasonic frequencies. The ear can detect such non‐acoustic pressure perturbations and therefore, distinguishing responses to infrasound from responses to non‐acoustic perturbations presents a great challenge. Our review shows that infrasound could stimulate the ear through the middle ear (tympanic) route and by extratympanic routes bypassing the middle ear. While vibration velocities of the middle ear decline towards infrasonic frequencies, whole‐body vibrations – which are normally much lower amplitude than that those of the middle ear in the ‘audible’ range (i.e. >20 Hz) – do not exhibit a similar decline and therefore may reach vibration magnitudes comparable to the middle ear at infrasonic frequencies. Low stiffness in the middle and inner ear is expected to aid infrasound transmission. In the middle ear, this could be achieved by large air cavities in the skull connected to the middle ear and low stiffness of middle ear structures; in the inner ear, the stiffness of round windows and cochlear partitions are key factors. Within the inner ear, the sizes of the helicotrema and cochlear aqueduct are expected to play important roles in shunting low‐frequency vibrations away from low‐frequency hair‐cell sensors in the cochlea. The basilar papilla, the auditory organ in birds, responds to infrasound in some species, and in pigeons, infrasonic‐sensitive neurons were traced back to the apical, abneural end of the basilar papilla. Vestibular organs and the paratympanic organ, a hair cell organ outside of the inner ear, are additional untested candidates for infrasound detection in birds. In summary, this review brings together evidence to create a hypothetical framework for infrasonic hearing mechanisms in birds and other animals.     

Anatomy and physics of the exceptional sensitivity of dolphin hearing (Odontoceti: Cetacea)

During the past 50 years, the high acoustic sensitivity and the echolocation behavior of dolphins and other small odontocetes have been studied thoroughly. However, understanding has been scarce as to how the dolphin cochlea is stimulated by high frequency echoes, and likewise regarding the ear mechanics affecting dolphin audiograms. The characteristic impedance of mammalian soft tissues is similar to that of water, and thus no radical refractions of sound, nor reflections of sound, can be expected at the water/soft tissue interfaces. Consequently, a sound-collecting terrestrial pinna and an outer ear canal serve little purpose in underwater hearing. Additionally, compared to terrestrial mammals whose middle ear performs an impedance match from air to the cochlea, the impedance match performed by the odontocete middle ear needs to be reversed to perform an opposite match from water to the cochlea. In this paper, we discuss anatomical adaptations of dolphins: a lower jaw collecting sound, thus replacing the terrestrial outer ear pinna, and a thin and large tympanic bone plate replacing the tympanic membrane of terrestrial mammals. The paper describes the lower jaw anatomy and hypothetical middle ear mechanisms explaining both the high sensitivity and the converted acoustic impedance match.     

Correlations between auditory structures and hearing sensitivity in non‐human primates

Primates show distinctions in hearing sensitivity and auditory morphology that generally follow phylogenetic patterns. However, few previous studies have attempted to investigate how differences in primate hearing are directly related to differences in ear morphology. This research helps fill this void by exploring the form‐to‐function relationships of the auditory system in a phylogenetically broad sample of non‐human primates. Numerous structures from the outer, middle, and inner ears were measured in taxa with known hearing capabilities. The structures investigated include the overall size and shape of the pinna, the areas of the tympanic membrane and stapedial footplate, the masses and lever arm lengths of the ossicles, the volumes of the middle ear cavities, and the length of the cochlea. The results demonstrate that a variety of auditory structures show significant correlations with certain aspects of hearing (particularly low‐frequency sensitivity). Although the majority of these relationships agree with expectations from auditory theory, some traditional (and possibly outdated) ideas were not supported. For example, the common misconception that higher middle ear transformer ratios (e.g., impedance transformer ratio) result in increased hearing sensitivity was not supported. Although simple correlations between form and function do not necessarily imply causality, the relationships defined in this study not only increase our understanding of auditory patterns in extant taxa but also lay the foundation to begin investigating the hearing in fossil primates. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.     

Scaling of the marsupial middle ear and its functional significance

The marsupial middle ear performs an anatomical impedance matching for acoustic energy travelling in air to reach the cochlea. The size of the middle ear sets constraints for the frequencies transmitted. For generalized placental mammals, it has been shown that the limit for high-frequency hearing can be predicted on the basis of middle ear ossicle mass, provided that the ears fulfil requirements of isometry. We studied the interspecific size variation of the middle ear in 23 marsupial species, with the following measurable parameters: skull mass, condylobasal length, ossicular masses for malleus, incus and stapes, tympanic membrane area, oval window area, and lever arm lengths for malleus and incus. Our results show that the middle ear size grows with negative allometry in relation to body size and that the internal proportions of the marsupial middle ear are largely isometric. This resembles the situation in placental mammals and allows us to use their isometric middle ear model to predict the high-frequency hearing limit for marsupials. We found that the isometry model predicts the high-frequency hearing limit for different marsupials well, indicating that marsupials can be used as auditory models for general therian mammalian hearing. At very high frequencies, other factors, such as the inner ear, seem to constrain mammalian hearing.     

Mechanical responses of the organ of corti to acoustic and electrical stimulation in vitro

The detection of sound by the cochlea involves a complex mechanical interplay among components of the cochlear partition. An in vitro preparation of the second turn of the jird's cochlea provides an opportunity to measure cochlear responses with subcellular resolution under controlled mechanical, ionic, and electrical conditions that simulate those encountered in vivo. Using photodiode micrometry, laser interferometry, and stroboscopic video microscopy, we have assessed the mechanical responses of the cochlear partition to acoustic and electrical stimuli near the preparation's characteristic frequency. Upon acoustic stimulation, the partition responds principally as a rigid plate pivoting around its insertion along the spiral lamina. The radial motion at the reticular lamina greatly surpasses that of the tectorial membrane, giving rise to shear that deflects the mechanosensitive hair bundles. Electrically evoked mechanical responses are qualitatively dissimilar from their acoustically evoked counterparts and suggest the recruitment of both hair-bundle- and soma-based electromechanical transduction processes. Finally, we observe significant changes in the stiffness of the cochlear partition upon tip-link destruction and tectorial-membrane removal, suggesting that these structures contribute considerably to the system's mechanical impedance and that hair-bundle-based forces can drive active motion of the cochlear partition.     

The Inner Ear of Two Late Cretaceous Multituberculate Mammals, and Its Implications for Multituberculate Hearing

The inner ear of the Late Cretaceous multituberculates Nemegtbaatar gobiensis and Chulsan-baatar vulgaris is described from serial sections and enlarged models. The size and proportions of the inner ear as a whole are as expected for extant small mammals. The lengths of the cochlea (Nemegtbaatar gobiensis, 3.0 mm, Chulsanbaatar vulgaris, 2.0 mm) are comparable to those of other multituberculates, when ratios of length of the cochlea to skull length are calculated. The vestibule is not as expanded in the two taxa as in Lambdopsalis, ?Meniscoessus, and ?Catopsalis; the estimated volume for Nemegtbaatar gobiensis is 9 mm³. A slightly laterally curved, anteriomedially directed cochlea, relatively robust ear ossicles, and the estimations of the area of the tympanic membrane and stapedial footplate in Chulsanbaatar suggest high-frequency hearing but a relatively low sensitivity to low-decibel sounds. The semicircular canals of Nemegtbaatar and Chulsanbaatar are fully developed; the size of the anterior, posterior, and lateral canals and their angles and proportions are comparable to those of extant mammals of similar size. The anterior semicircular canal of Nemegtbaatar forms a smooth half-circle and thus is more derived than the angular canal of Ornithorhynchus. The notable differences between the ratio of the width of the lateral semicircular canal to skull length and the size of the vestibule in Nemegtbaatar and the Paleocene multituberculate Lambdopsalis bulla are probably related to different modes of life.     

The relationships between otoacoustic emissions and relative lengths of fingers and toes in humans

Both otoacoustic emissions (OAEs) and the relative length of the index and ring fingers (the 2D:4D ratio) exhibit large sex differences, and both exhibit masculinization effects in female homosexuals and bisexuals. Because these sex differences exist in young children, the implication is that both types of measure are affected by prenatal androgen exposure, but it has been unknown to what degree these two types of measure are related. Accordingly, OAEs and the relative lengths of the fingers and the toes were measured in 59 heterosexual females, 55 heterosexual males, 29 homosexual females, and 33 homosexual males. The correlations between the two types of measure were unexpectedly quite low in both the heterosexual and nonheterosexual groups. For example, the correlation between number of spontaneous OAEs per ear and 2D:4D was less than 0.25, for both sexes and both sexual orientations. One interpretation of these results is that the prenatal hormonal mechanisms producing the sex differences in OAEs differ in quality, degree, or timing from those producing the sex differences in relative finger length. That is, OAEs and 2D:4D may be windows onto slightly different prenatal processes or times during prenatal development. Measures of mental-rotation ability also were obtained on these participants, and those correlations with relative finger length also were small.     

Mechanical filtering of sound in the inner ear.

We have studied the distortion generated by the cochlea to gain insight into the mechanisms responsible for the sharp tuning or 'frequency selectivity' of the inner ear. We used two stimulating tones of moderate intensity which are progressively separated in frequency, and measured the ear canal cubic distortion components which are generated as a consequence of the stimulus interaction in the cochlea. We inferred that the distortion is generated from the frequency region of the higher of the two stimulus tones and that it is then band-pass filtered by a structure which is tuned to a frequency just over half an octave below that of the high-frequency tone. We suggest that the structure responsible for this band-pass filtering is the tectorial membrane, and we conclude that our results support theories of cochlear mechanics in which resonances due to the tectorial membrane interact with those of the basilar membrane to enhance the frequency selectivity of the inner ear.     

Hypothesis on acoustic receptive fields

A hypothesis of acoustic receptive fields is studied, which is based on the fact that the cochlea of the internal ear is a wave guide with traveling waves and the resonance in the critical layer. When a harmonic sound influences the ear, the traveling wave reaches the critical layer for the corresponding frequency and generates there a train of decaying waves about 25 periods in duration, which form a steep slope of the envelope. The funnel-shaped convergence of all neurones innervating the acoustic receptors of the Corti organ along the slope of the envelope gives rise to acoustic receptive fields. The hypothesis is consistent with some other experimental data. Such an acoustic receptive field makes it possible to use the whole train of waves in the critical layer to measure the frequency of the acting sinusoidal sound with the greatest possible accuracy. Similarly, a high accuracy of recognition of short-time sound pulses is provided, which could not be explained earlier.     

Intraspecific variation in laryngeal and ear morphology in male cricket frogs (Acris crepitans)

In a previous report, the authors found significant population variation in the calls of cricket frogs ( Acris crepitans ) that could not be explained by geographic variation in body size alone. Here we extend that work by investigating intraspecific population variation in the morphological characteristics underlying acoustic communication in male cricket frogs from several sites in Texas. We measured the volumes of laryngeal and auditory components responsible for the generation or reception of species-specific vocalizations in male frogs from eight populations. We found significant differences among populations in body size, as well as all the laryngeal and ear components we measured. With the exception of vocal cord and extracolumella volumes, the volumes of these anatomical structures differ among populations independently of body size as determined by a covariate analysis with snout-vent length as the covariate. Call dominant frequency differs among populations in a clinal pattern and head width, arytenoid cartilage, vocal cord and dilator muscle volume show a similar pattern when the residuals of the regression of morphological component on SVL are assessed for this trend. The results show that both larynx and ear structures can change in size independently of body size, yielding significant geographic variation in the behavioral and physiological expressions of the acoustic communication system underlying mate choice.     

In Vivo Impedance of the Gerbil Cochlear Partition at Auditory Frequencies

The specific acoustic impedance of the cochlear partition was measured from 4 to 20 kHz in the basal turn of the gerbil cochlea, where the best frequency is ∼40 kHz. The acoustic impedance was found as the ratio of driving pressure to velocity response. It is the physical attribute that governs cochlear mechanics and has never before been directly measured, to our knowledge. The basilar membrane velocity was measured through the transparent round window membrane. Simultaneously, the intracochlear pressure was measured close to the stapes and quite close to the cochlear partition. The impedance phase was close to −90° and the magnitude decreased with frequency, consistent with stiffness-dominated impedance. The resistive component of the impedance was relatively small. Usually the resistance was negative at frequencies below 8 kHz; this unexpected finding might be due to other vibration modes within the cochlear partition.     

Finite element modelling of human auditory periphery including a feed-forward amplification of the cochlea

A three-dimensional finite element model is developed for the simulation of the sound transmission through the human auditory periphery consisting of the external ear canal, middle ear and cochlea. The cochlea is modelled as a straight duct divided into two fluid-filled scalae by the basilar membrane (BM) having an orthotropic material property with dimensional variation along its length. In particular, an active feed-forward mechanism is added into the passive cochlear model to represent the activity of the outer hair cells (OHCs). An iterative procedure is proposed for calculating the nonlinear response resulting from the active cochlea in the frequency domain. Results on the middle-ear transfer function, BM steady-state frequency response and intracochlear pressure are derived. A good match of the model predictions with experimental data from the literatures demonstrates the validity of the ear model for simulating sound pressure gain of middle ear, frequency to place map, cochlear sensitivity and compressive output for large intensity input. The current model featuring an active cochlea is able to correlate directly the sound stimulus in the ear canal with the vibration of BM and provides a tool to explore the mechanisms by which sound pressure in the ear canal is converted to a stimulus for the OHCs.     

Does the morphology of the ear of the Chinese bamboo rat (Rhizomys sinensis) show “Subterranean” characteristics?

In spite of the growing interest in rodents with subterranean activity in general and the spalacids (Spalacidae) in particular, little is known about the biology of most members of this clade, such as the Chinese bamboo rat (Rhizomys sinensis). Here, we analyzed the ear morphology of R. sinensis with respect to hearing specialization for subterranean or aboveground modes of communication. It is well‐known that ecology and style of life of a particular species can be reflected in morphology of its ear, its hearing and vocalization, so we expect that such information could provide us insight into its style of life and its sensory environment. The ratio between the eardrum and stapedial footplate areas, which influences the efficiency of middle ear sound transmission, suggests low hearing sensitivity, as is typical for subterranean species. The cochlea had 3.25 coils and resembled species with good low frequency hearing typical for subterranean mammals. The length of the basilar membrane was 18.9 ± 0.8 mm and its width slowly increased towards the cochlear apex from 60 to 85 μm. The mean density of outer hair cells was 344 ± 22 and of inner hair cells 114 ± 7.3 per 1 mm length of the organ of Corti, and increased apically. These values (except for relatively low hair cell density) usually characterize ears specialized for low frequency hearing. There was no evidence for an acoustic fovea. Apart of low hair cell density which is common in aboveground animals, this species has also relatively large auricles, suggesting the importance of sound localization during surface activity. The ear of the Chinese bamboo rat thus contains features typical for both aboveground and subterranean mammals and suggests that this spalacid has fossorial habits combined with regular aboveground activity. J. Morphol. 277:575–584, 2016. © 2016 Wiley Periodicals, Inc.     

Theoretical Study on the Dynamic Behavior of a Plate-Like Micro-Cantilever with Multiple Particles Attached

In this study, the dynamic characteristics of a plate-like micro-cantilever beam attached with multiple concentrated masses are studied. The vibration modes of the cantilever plate are represented by combinations of beam functions. Using classical mechanics (the effect of size is not considered) and the corrected Cosserat’s theorem (the effect of size is considered), we employ the Lagrange equations to establish a dynamic model of the plate-like micro-cantilever beam attached with multiple concentrated masses. The accuracy of the model proposed in this paper is verified by comparing with the results of published literature. Then, the natural frequencies of the cantilever plates are calculated with self-compiled algorithms, and the results of the plates with 1–5 masses are displayed. The results are in high accordance with the exact solution, and all errors are within 0.5%. The analysis shows that the proposed model and analysis method converges quickly and is highly efficient. In addition, the effects of characteristic lengths, Poisson''s ratios and plate thickness on the micro-cantilever plate’s resonant frequency for the first five modes are analyzed.     

Auditory systems of Heteromyidae: functional morphology and evolution of the middle ear.

Middle ears (515) from 26 species of the rodent family Heteromyidae - genera Dipodomys, Microdipodops, Perognathus, and Liomys - were studied both grossly and histologically, for qualitative and quantitative comparisons. Middle ear modifications characteristic of each genus are qualitatively described. Quantitative comparisons are made among the 26 species in the study. Some correlations between middle ear size and other measurements are discussed. The middle ear is an acoustical transformer that for best efficiency must match the impedance of the cochlea to the impedance of the air in the external auditory meatus. It accomplishes this by a pressure increase and a velocity decrease through the combined effects of the lever and areal ratios; however, because the important consideration is a matching of two impedances rather than an absolute pressure increase, the pressure transformer ratio is a less informative measure of the middle ear's efficiency than is the impedance transform ratio. The impedance transformer mechanism is explained (from a morphological point of view), and equations are presented. Dipodomys, Microdipodops, and Perognathus have a theoretical transmission (at the resonant frequency) of 94-100% of the incident acoustical energy; Liomys, 78-80%. The areal ratio of stapes footplate to 2/3 tympanic membrane is remarkably constant among the species, varying only from 0.04 to 0.07: in Dipodomys and Microdipodops this small ratio is due to the very large tympanic membrane; in Perognathus and Liomys it is due to the extremely small stapes footplate. The lever ratio of incus to malleus varies from 0.28 to 0.33 in Dipodpmys and Microdipodops, from 0.37 to 0.46 in Perognathus, and from 0.55 to 0.60 in Liomys. In addition, the middle ear volumes and the morphology of tympanic membrane, ossicles, ligaments, and muscles, all combine to minimize both mass and stiffness. All these data suggest middle ear mechanisms which are very efficient over a broad frequency range. The middle ear modifications found in heteromyids are adaptive in predator avoidance, especially in areas of little natural cover; nevertheless, contrary to expectations, there is no firm relationship between habitat and the extent of these modifications in the 26 species. However, environment did apparently plan an important role in the evolution of the family, and this is discussed.     

Contributions of Electric and Acoustic Hearing to Bimodal Speech and Music Perception

Cochlear implant (CI) users have difficulty understanding speech in noisy listening conditions and perceiving music. Aided residual acoustic hearing in the contralateral ear can mitigate these limitations. The present study examined contributions of electric and acoustic hearing to speech understanding in noise and melodic pitch perception. Data was collected with the CI only, the hearing aid (HA) only, and both devices together (CI+HA). Speech reception thresholds (SRTs) were adaptively measured for simple sentences in speech babble. Melodic contour identification (MCI) was measured with and without a masker instrument; the fundamental frequency of the masker was varied to be overlapping or non-overlapping with the target contour. Results showed that the CI contributes primarily to bimodal speech perception and that the HA contributes primarily to bimodal melodic pitch perception. In general, CI+HA performance was slightly improved relative to the better ear alone (CI-only) for SRTs but not for MCI, with some subjects experiencing a decrease in bimodal MCI performance relative to the better ear alone (HA-only). Individual performance was highly variable, and the contribution of either device to bimodal perception was both subject- and task-dependent. The results suggest that individualized mapping of CIs and HAs may further improve bimodal speech and music perception.