Morphology of the middle ear of golden moles (Chrysochloridae)

The middle ear structures of nine species of golden moles (family Chrysochloridae) were examined under the light microscope. Auditory structures of several of these species are described here for the first time in detail, the emphasis being on the ossicular apparatus. Confirming previous observations, some golden moles (e.g. Amblysomus species) have ossicles of a morphology typical of mammals, whereas others ( Chrysospalax , Chrysochloris , Cryptochloris and Eremitalpa species) have enormously hypertrophied mallei. Golden moles differ in the nature and extent of the interbullar connection, the shape of the tympanic membrane and that of the manubrium. The stapes has an unusual orientation, projecting dorsomedially from the incus. It has been proposed that hypertrophied ossicles in golden moles are adapted towards the detection of seismic vibrations. The functional morphology of the middle ear apparatus is reconsidered in this light, and it is proposed that adaptations towards low-frequency airborne hearing might have predisposed golden moles towards the evolution of seismic sensitivity through inertial bone conduction. The morphology of the middle ear apparatus sheds little light on the disputed ordinal position of the Chrysochloridae.     

The middle and inner ears of the Palaeogene golden mole Namachloris: A comparison with extant species

Many living species of golden moles (Chrysochloridae) have greatly enlarged middle ear ossicles, believed to be used in the detection of ground vibrations through inertial bone conduction. Other unusual features of chrysochlorids include internally coupled middle ear cavities and the loss of the tensor tympani muscle. Our understanding of the evolutionary history of these characteristics has been limited by the paucity of fossil evidence. In this article, we describe for the first time the exquisitely preserved middle and inner ears of Namachloris arenatans from the Palaeogene of Namibia, visualised using computed tomography, as well as ossicles attributed to this species. We compare the auditory region of this fossil golden mole, which evidently did not possess a hypertrophied malleus, to those of three extant species with similarly sized ear ossicles, Amblysomus hottentotus, Calcochloris obtusirostris, and Huetia leucorhinus. The auditory region of Namachloris shares many common features with the living species, including a pneumatized, trabeculated basicranium and lateral skull wall, arteries and nerves of the middle ear contained in bony tubes, a highly coiled cochlea, a secondary crus commune, and no identifiable canaliculus cochleae for the perilymphatic duct. However, Namachloris differs from extant golden moles in the apparent absence of a basicranial intercommunication between the right and left ears, the possession of a tensor tympani muscle and aspects of ossicular morphology. One Namachloris skull showed what may be pneumatization of some of the dorsal cranial bones, extending right around the brain. Although the ossicles are small in absolute terms, one of the Huetia leucorhinus specimens had a more prominent malleus head than the other. This potentially represents a previously unrecognised subspecific difference.     

Bone conduction and seismic sensitivity in golden moles (Chrysochloridae)

Some genera of golden moles are known to possess enormously hypertrophied auditory ossicles. These structures have been implicated as potentially mediating a form of inertial bone conduction, used by the golden mole to detect seismic vibrations. A simple model of ossicular inertial bone conduction, based on an existing model of the human middle ear from the literature, was used in an attempt to examine vibrational sensitivity in these animals. Those golden moles with hypertrophied ossicles are predicted to possess a sensitive inertial bone conduction response at frequencies below a few hundred hertz, whereas species lacking these middle ear adaptations are predicted to have a far less sensitive response in this ecologically important frequency range. An alternative mode of inertial bone conduction in golden moles, potentially conferring sensitivity to vertically-polarized seismic vibrations such as Rayleigh waves, is proposed. Certain behaviours of golden moles described in the literature are interpreted as augmenting seismic sensitivity.     

Evolution of the middle ear apparatus in Talpid moles

The middle ear structures of eight species of mole in the family Talpidae (Mammalia: Eulipotyphla) were studied under light and electron microscopy. Neurotrichus, Parascalops, and Condylura have a simple middle ear cavity with a loose ectotympanic bone, ossicles of a "microtype" morphology, and they retain a small tensor tympani muscle. These characteristics are ancestral for talpid moles. Talpa, Scalopus, Scapanus, and Parascaptor species, on the other hand, have a looser articulation between malleus and ectotympanic bone and a reduced or absent orbicular apophysis. These species lack a tensor tympani muscle, possess complete bullae, and extensions of the middle ear cavity pneumatize the surrounding basicranial bones. The two middle ear cavities communicate in Talpa, Scapanus, and Parascaptor species. Parascaptor has a hypertrophied malleus, a feature shared with Scaptochirus but not found in any other talpid genus. Differences in middle ear morphology within members of the Talpidae are correlated with lifestyle. The species with middle ears closer to the ancestral type spend more time above ground, where they will be exposed to high-frequency sound: their middle ears appear suited for transmission of high frequencies. The species with derived middle ear morphologies are more exclusively subterranean. Some of the derived features of their middle ears potentially improve low-frequency hearing, while others may reduce the transmission of bone-conducted noise. By contrast, the unusual middle ear apparatus of Parascaptor, which exhibits striking similarities to that of golden moles, probably augments seismic sensitivity by inertial bone conduction.     

Ossicular differentiation of airborne and seismic stimuli in the Cape golden mole (Chrysochloris asiatica)

Comparison between the middle ear anatomy of the Cape golden mole (Chrysochloris asiatica), which exhibits a club-shaped malleus head, and the Desert golden mole (Eremitalpa granti), with a ball-shaped malleus head, suggests differences in sensitivity to airborne sound. Scanning laser Doppler vibrometric measurements of the ossicular behavior in response to both vibration and airborne sound were made in C. asiatica. Two distinct vibrational modes were observed. In response to low-frequency vibration (70–200 Hz), the malleus oscillates about the ligament of the short process of the incus, whereas in response to high-frequency airborne sound (1–6 kHz) the ossicular chain rotates about the long axis of malleus. It is proposed that the club-shaped malleus head in C. asiatica constitutes an adaptation towards bimodal hearing—sensitivity to substrate vibrations and airborne sound. Possible functional differences between these two middle ear types are discussed.     

Ossicular density in golden moles (Chrysochloridae)

The densities of middle ear ossicles of golden moles (family Chrysochloridae, order Afrosoricida) were measured using the buoyancy method. The internal structure of the malleus was examined by high-resolution computed tomography, and solid-state NMR was used to determine relative phosphorus content. The malleus density of the desert golden mole Eremitalpa granti (2.44 g/cm³) was found to be higher than that reported in the literature for any other terrestrial mammal, whereas the ossicles of other golden mole species are not unusually dense. The increased density in Eremitalpa mallei is apparently related both to a relative paucity of internal vascularization and to a high level of mineralization. This high density is expected to augment inertial bone conduction, used for the detection of seismic vibrations, while limiting the skull modifications needed to accommodate the disproportionately large malleus. The mallei of the two subspecies of E. granti, E. g. granti and E. g. namibensis, were found to differ considerably from one another in both size and shape.     

Functional and systematic implications of the ear in golden moles (Chrysochloridae)

Golden moles (Chrysochloridae) are fossorial mammals known to have unusual mallei. The aim of this study was to describe and quantify aspects of the auditory morphology of golden moles in order to determine their systematic and functional implications. Observations were made on skeletal material as well as histological sections. The results of this study do not support the separation of the genus Calcochloris from Amblysomus . It was found that the morphology shared by all the studied genera is indicative of specialization for hearing low frequency sound. The tympanic membrane to stapes footplate ratios, ossicular lever arm ratios and incudomallear joint morphology suggest low frequency specializations in genera with small mallear heads and high frequency specializations in genera with large mallear heads. However, the size and degree of trabeculation of the tympanic cavity are not consistent with this result. It is proposed that all golden moles are low frequency hearers with differences in their range of sensitivity according to how much time they spend foraging above ground.     

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.     

Middle-ear dynamics before and after ossicular replacement

The mechanism of hearing involves conduction of mechanical vibrations along the ossicular chain to the inner ear. An acoustic wave is collected and transformed as it passes down the ear canal and impacts on the tympanic membrane (ear drum). The drum is connected to the inner-ear by three ossicle bones (malleus, incus, and stapes) in a complex arrangement, which serves to further transform the mechanical vibration before it reaches the cochlea of the inner ear. What is the mechanical function of the ossicular chain, and what are the biomechanical consequences of surgical reconstruction with prostheses? To answer these questions, a three-dimensional finite element model of the outer ear canal and middle ear was generated. The dynamical behaviour was predicted for the normal ear, and an ear reconstructed with partial and total ossicular replacement prostheses. For the normal ear, stapes amplitudes of 1x10(-8) m at low frequencies decrease to 4x10(-10)m at approximately 3kHz with several resonance peeks in between, most significantly at approximately 1kHz. Thereafter a further resonance is predicted at 4kHz associated with the ear canal. The behaviour is changed fundamentally by adding a prosthesis; the partial replacement increases the vibratory coupling of the drum and the stapes compared to the normal ear whereas the total replacement does the opposite, and is predicted to have the disadvantage of bringing several new resonances of the ossicular chain into the hearing range. It is hypothesised that the function of the malleus-incus-stapes arrangement is to link the drum to the oval window with the flexibility required for impedance matching but the rigidity to prevent unconstrainable resonances from occurring in the hearing range. If this is true, then the structural stiffness of ossicular chain is the critical design variable for middle-ear replacement prostheses.     

Burkholderia mallei and Burkholderia pseudomallei. Study of immuno- and pathogenesis of glanders and melioidosis. Heterologous vaccines]

Parameters of the infectious activity of B.mallei and B.pseudomallei for animals of various species were determined. Pathomorphological characteristics of the process of malleus and melioidosis were studied on golden hamsters, mice, guinea pigs, rats and monkeys. Tularemia, plague and salmonellosis vaccines were shown to have protective effects in experimental malleus and melioidosis. An insignificant cross immune response between the malleus and melioidosis pathogens was observed.     

The ear in subterranean insectivora and rodentia in comparison with ground-dwelling representatives. I. Sound conducting system of the middle ear.

Compared to acoustically unspecialized mammals (soricids and murids), the middle ear of subterranean insectivores and rodents (twelve species of six families examined) was clearly distinguished and characterized by many common features: rather round and relatively larger eardrum without a pars flaccida; reduced gonial; loose or no connection between the malleus and the tympanic bone; reduced and straightened transversal part of the malleus; enlarged incus; increased and rather flat incudo-mallear joint; rather parallel position of the mallear manubrium and incudal crus longum in some species (and their fusion in bathyergids); reduced or even missing middle ear muscles. Convergent occurrence of these structural features in taxa of different origin and their generally derived character suggest that they cannot be categorized as degenerative. The form of the stapes can be considered as a non-adaptive trait; it was taxon specific yet remarkably polymorphous in some species and exhibited no convergent features among subterranean mammals. Structural retrogression resulting in a columella-like stapes was observed in some species lacking the stapedial artery. The stapedial base was relatively larger than in unspecialized mammals. The subterranean mammals did not exhibit conspicuously enlarged eardrums as would be required for sensitive tuning to low frequencies. It is, however, argued that while selective pressures in the subterranean ecotope promoted hearing of low frequencies, hearing sensitivity did not have to be enhanced.     

Functional morphology of the ear in fossorial rodents, Microtus arvalis and Arvicola terrestris

Functionally relevant features and parameters of the outer, middle, and inner ear were studied morphologically and morphometrically in two species of voles, smaller Microtus arvalis and larger Arvicola terrestris. The findings in these fossorial (i.e., burrowing) rodents with components of surface activity were compared with respective findings reported for taxonomically related muroid rodents representing the same size classes but different eco-morphotypes: obligate subterranean rodents (Ellobius talpinus and Spalax ehrenbergi superspecies) and generalized rodents (Mus domesticus and Rattus norvegicus). The ear in voles was characterized by traits reported for subterranean rodents. The eardrum was round, without a distinct pars flaccida, and had an area of 5.4 mm2 in M. arvalis and 9 mm2 in A. terrestris. The middle ear exhibited reduced goniale, enlarged incus nearly parallel to the manubrium of the malleus. The malleus-incus lever ratio amounted to 2.1 (M. arvalis) and 2.0 (A. terrestris). The malleus-incus complex weighed about 0.8 mg in both vole species. The stapedial footplate had an area of 0.3 mm2 in M. arvalis and 0.4 mm2 in A. terrestris. The cochlea had 2.3 coils in both vole species; the basilar membrane was 8.5 mm and 10.5 mm long in M. arvalis and A. terrestris, respectively. There were on average 1,030 (M. arvalis) and 1,220 (A. terrestris) inner hair cells, and 3,760 (M. arvalis) and 4,250 (A. terrestris) outer hair cells in the organ of Corti. In quantitative terms, all these (as well as some further) traits and parameters were intermediate (related to body size) between those reported for generalized rodents on the one hand and subterranean ones on the other. The sound transmission system of the ear seems to be best tuned to frequencies of about 8-16 kHz with a high-frequency cut-off at about 50-60 kHz. The ear of A. terrestris seems to be tuned to somewhat lower frequencies than that in M. arvalis. In this aspect as well as regarding hearing sensitivity (as judged from the mechanical transmission parameters), voles can be considered intermediate not only in their lifestyle but also in their hearing abilities between the subterranean rodents (mole-vole and blind mole-rat) and the surface dwellers (house mouse and Norway rat).     

The anatomy, physiology, functional significance and evolution of specialized hearing organs of gerbilline rodents

Middle and inner ear anatomy correlates with neurophysiological responses to a wide range of sound frequencies for species of the Gerbillinae representing generalized, intermediate, and specialized anatomical conditions. Neurophysiological data were recorded from 81 specimens of 13 species representing six genera. Anatomical parameters involved in the process of hearing were correlated with the neurophysiological data to assess the effects of different degrees of anatomical specialization on hearing. The 13 species tested in this manner have graphic curves of auditory sensitivity of remarkably similar disposition over the frequencies tested and to those published for Kangaroo Rats. Ears with anatomical specializations show greater auditory sensitivity. The natural history of the Gerbillinae, particularly the kinds of predators, degree of predation, and habitat is reviewed and utilized to interpret the significance of the degree of auditory specialization in the forms studied and to evaluate the prevailing hypothesis that these specializations enhance the ability of these rodents to survive in open desert situations by detecting and evading predators. The middle ear anatomy of five additional genera and species was also studied. Thus, data on the entire spectrum of gerbilline middle ear morphology provide an evolutionary sequence. Certain anatomical parameters of the organ of Corti show a degree of specialization parallel to that of features of the middle ear. The morphological changes and possible functional roles of these features are considered. A very high correlation exists for degree of specialization and aridity of habitat, thus specialization increases with increasing aridity. This increased specialization may result from more effective predation in open xeric environments. Auditory acuity for a wide range of low frequency sounds augmented by auditory specialization is hence more advantageous here. There does not appear to be selection for hearing at particular frequencies in this range. The peaks of greatest auditory sensitivity appear to correspond to the resonant frequencies of the different components of the middle ear transformer and cavity.     

Rotation of middle ear ossicles during cetacean development

Cetacean middle ears are unique among mammals in that they have an elongated tympanic membrane, a greatly reduced manubrium mallei, and an incudal crus longum that is shorter than the crus breve. Elongation of the tympanic membrane and reduction of the manubrium is thought to be related to an evolutionary rotation of the incus and malleus out of the plane of the tympanic membrane. We examined if rotation also occurs during ontogeny by comparing the middle ears of two species of dolphins (Delphinus delphis, Stenella attenuata) at different stages of development. We observed that: the incus has the body and crural proportions as in terrestrial mammals early in development; the incudomallear complex rotates approximately 90 degrees following ossification; the tympanic membrane is not elongated until relatively late in development. Therefore, some of the unique characteristics of the cetacean middle ear develop as modifications of an initially terrestrial-like morphology.     

Assembling a functional tympanic membrane: signals from the external acoustic meatus coordinate development of the malleal manubrium

In terrestrial mammals, hearing starts with the perception of acoustic pressure by the tympanic membrane. Vibrations in this membrane are then transduced into the inner ear by the ossicle chain of the middle ear, composed of the malleus, incus and stapes. The proper connection of the ossicle chain with the tympanic membrane, provided by the insertion of the manubrium of the malleus into the eardrum, is essential for the functionality of the hearing apparatus. We describe here the mechanisms regulating the development of the manubrium and its integration into the tympanic membrane. We show that the external acoustic meatus (EAM), which eventually forms the outer epithelium of the tympanic membrane, plays an essential role in this developmental process. Histological and expression analyses indicate that the manubrium develops close to the EAM with a similar temporal sequence. In addition, when the middle ear ossicles are allowed to develop in vitro under conditions that do not support further EAM development, the manubrium develops only up to the stage of its induction at the time of explantation. Moreover, genetically or teratogenically derived alterations in the EAM also have an effect on manubrial development. Finally, we show that the EAM is the source of two quite opposite activities, one that induces chondrogenesis and another that represses it. The combination of these two activities results in the proper positioning of the manubrium.     

Better than fish on land? Hearing across metamorphosis in salamanders

Early tetrapods faced an auditory challenge from the impedance mismatch between air and tissue in the transition from aquatic to terrestrial lifestyles during the Early Carboniferous (350 Ma). Consequently, tetrapods may have been deaf to airborne sounds for up to 100 Myr until tympanic middle ears evolved during the Triassic. The middle ear morphology of recent urodeles is similar to that of early ‘lepospondyl’ microsaur tetrapods, and experimental studies on their hearing capabilities are therefore useful to understand the evolutionary and functional drivers behind the shift from aquatic to aerial hearing in early tetrapods. Here, we combine imaging techniques with neurophysiological measurements to resolve how the change from aquatic larvae to terrestrial adult affects the ear morphology and sensory capabilities of salamanders. We show that air-induced pressure detection enhances underwater hearing sensitivity of salamanders at frequencies above 120 Hz, and that both terrestrial adults and fully aquatic juvenile salamanders can detect airborne sound. Collectively, these findings suggest that early atympanic tetrapods may have been pre-equipped to aerial hearing and are able to hear airborne sound better than fish on land. When selected for, this rudimentary hearing could have led to the evolution of tympanic middle ears.     

Study of age-related changes in Middle ear transfer function

Abstract

Osteoporosis (OP) is common with advancing age. Several studies have shown a strong correlation between OP and otosclerosis. However, no studies have investigated OP of the malleus, incus or stapes in the human middle ear, its effect on middle ear transfer function. Here, we investigate whether these three ossicles develop OP, and how this affects middle ear transfer function. The effect of OP on middle ear transfer function was investigated in simulations based on a finite element (FE) method. First, the FE model used in our previous study was refined, and optimized by introducing viscoelastic properties to selected soft tissues of the middle ear. Then, the FE model was used to simulate OP of the three ossicles and assess its influence on middle ear transfer function. Other possible age-related changes, such as stiffness of the joints or ligaments in the middle ear, were also investigated. The results indicated that OP of the ossicles could increase the high frequency displacement of both the umbo and stapes footplate (FP). However, the stiffness of the middle ear soft tissue can lead to the decrease of middle ear gain at lower frequencies. Furthermore, loosening of these joints or ligaments could increase displacement of the umbo and stapes FP. In conclusion, although age-related hearing loss is most commonly conceived of as sensorineural hearing loss (SNHL), we found that age-related changes may also include OP and changes in joint stiffness, but these will have little effect on middle ear transfer function in elderly people.     

Auditory rehabilitation

Auditory rehabilitation depends of the cause and the severity of the hearing loss (or deafness). Hearing losses dues to middle ear pathologies can beneficiate of medical or surgical treatments, by ossicular prostheses, if it is necessary to restore the function of the ossicles chain. In the sensorineural hearing losses, with inner ear pathology, the use of auditory aid is immediately considered. In the cases for which they are insufficient because of severity of the hearing loss or not suitable because of local non-tolerance, it is possible to use middle ear implant or cochlear implant. The indications of the auditory brainstern implants remain at this day limited to the total bilateral hearing losses due to a complete destruction of cochleae and auditory nerves. These therapeutic orientations are selected after a multidisciplinary evaluation of the deaf person, evaluation that allows the characterization of the hearing loss and its repercussion. In all the cases, the restoration of a bilateral hearing has to be done if possible, making an improvement of the speech comprehension, mainly in the noisy situations, as well as the localization of the sound sources.     

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.     

Lung-based hearing in an “earless” anuran amphibian

The mechanisms of hearing in the fire-bellied toad Bombina orientalis, an “earless” species of amphibian that lacks a standard tympanic middle ear, were studied using laser Doppler vibrometric and neurophysiological techniques. Laser vibrometry demonstrated that the anterolateral body wall overlying the lung is much more responsive to sound than the lateral head surface overlying the inner ear. Covering the lateral body wall with silicone grease dramatically decreased auditory midbrain sensitivity at all frequencies examined, elevating thresholds by 20–25 dB. Filling the lungs with oxygenated saline produced similar decrements in hearing sensitivity, and both manipulations strongly suggest that the lung is the primary route of sound reception in this species. The precise route of transfer of sound energy from the body wall and lungs to the inner ear remains unclear. The lung-based hearing system of “earless” fire-bellied toads may represent the retention of the first auditory mechanism used by early tetrapod vertebrates for detection of airborne sound. Accepted: 10 December 1998