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.     

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.     

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     

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.     

Auditory brainstem responses to airborne sounds in the aquatic frog Xenopus laevis: correlation with middle ear characteristics

In this study we recorded auditory brainstem responses to airborne sounds to determine the hearing sensitivity of Xenopus laevis frogs and correlated their hearing profiles with middle ear characteristics. In newly metamorphosed frogs (body mass 0.5–0.76 gm, snout-vent length 17–20 mm) best hearing sensitivities were measured in the 2.4–2.8 kHz range, whereas optimal hearing sensitivity of older adults (body mass 18–90 gm; snout-vent length 57–100 mm) ranged from 1.0 to 1.2 kHz. Middle ear volumes reconstructed from serial sections showed approximate volume of 0.002 cc and 0.04–0.07 cc in newly metamorphosed and older frogs, respectively. This inverse frequency–volume relationship is consistent with the properties of an acoustic resonator indicating that differences in best hearing sensitivity are at least in part correlated to variation in middle ear volumes for airborne sounds. These results are consistent with peak frequency vibrational velocity profiles of Xenopus tympanic disk that have been shown to be dependent on underlying middle ear volumes and corroborate the occurrence of peak amplitudes of otoacoustic emissions in the 1.0–1.2 kHz region in adult Xenopus frogs.     

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.     

Biomechanical and neurophysiological studies on audition in eared and earless harlequin frogs (Atelopus)

Tissue displacement of various body surfaces and the auditory midbrain sensitivities to sound were measured in Atelopus species with or without a tympanic middle ear (“eared” and “earless”, respectively). Tissue displacement (vibration) of body regions was measured by laser Doppler vibrometer . The body wall directly overlying the lung is most dramatically displaced by sound pressure in all species tested. The otic (lateral head) region showed low displacement in earless species, but significant displacement to high-frequency sound in eared species. Peak tissue displacement of the body wall occurred within the frequency range of each species' advertisement vocalization. Peak tissue displacement of the otic region of the eared species also occurred within these frequencies. Multi-unit neurophysiological recordings of the auditory midbrain (torus semicircularis) also were obtained. Auditory sensitivity curves showed three distinct regions of sensitivity at low, middle, and high frequencies, the latter located within the frequency range of each species' advertisement vocalization. The correlation between auditory midbrain sensitivity and tissue displacement of the body wall region at advertisement vocalization frequencies, suggests that the body wall/lungs serve as the route of sound transfer to the inner ear in earless species and possibly in the eared species as well. Accepted: 4 April 1998     

Investigation of the human tympanic membrane oscillation ex vivo by Doppler optical coherence tomography

Investigations of the tympanic membrane (TM) can have an important impact on understanding the sound conduction in the ear and can therefore support the diagnosis and treatment of diseases in the middle ear. High‐speed Doppler optical coherence tomography (OCT) has the potential to describe the oscillatory behaviour of the TM surface in a phase‐sensitive manner and additionally allows acquiring a three‐dimensional image of the underlying structure. With repeated sound stimuli from 0.4 kHz to 6.4 kHz, the whole TM can be set in vibration and the spatially resolved frequency response functions (FRFs) of the tympanic membrane can be recorded. Typical points, such as the umbo or the manubrium of malleus, can be studied separately as well as the TM surface with all stationary and wave‐like vibrations. Thus, the OCT methodology can be a promising technique to distinguish between normal and pathological TMs and support the differentiation between ossicular and membrane diseases. (© 2014 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

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.     

Bone‐conduction hearing and seismic sensitivity of the late permian anomodont Kawingasaurus fossilis

An investigation of the internal cranial anatomy of the anomodont Kawingasaurus from the Upper Permian Usili Formation in Tanzania by means of neutron tomography revealed an unusual inner and middle ear anatomy such as extraordinarily inflated vestibules, lateroventrally orientated stapes with large footplates, and a small angle between the planes of the anterior and lateral semicircular canals. The vestibule has a volume, which is about 25 times larger than the human vestibule, although Kawingasaurus has only a skull length of approximately 40 mm. Vestibule inflation and enlarged stapes footplates are thought to be functionally correlated with bone‐conduction hearing; both morphologies have been observed in fossorial vertebrates using seismic signals for communication. The firmly fused triangular head with spatulate snout was probably used for digging and preadapted to seismic signal detection. The quadrate‐quadratojugal complex was able to transmit sound from the articular to the stapes by small vibrations of the quadrate process, which formed a ball and socket joint with the squamosal. Mechanical considerations suggest that the ventrolaterally orientated stapes of Kawingasaurus was mechanically better suited to transmit seismic sound from the ground to the fenestra vestibuli than a horizontal orientated stapes. The low sound pressure level transformer ratio of 2–3 in Kawingasaurus points to a seismic sensitivity of the middle ear and a vestigial or reduced sensitivity to airborne sound. Three hypothetical pathways of bone conduction in Kawingasaurus are discussed: 1) sound transmission via the spatulate snout and skull roof to the otic capsules, 2) relative movements resulting from the inertia of the mandible if sound is percepted with the skull, and 3) bone conduction from the substrate via mandible, jaw articulation, and stapes to the inner ear. J. Morphol. 276:121–143, 2015. © 2014 Wiley Periodicals, Inc.     

Specialization for underwater hearing by the tympanic middle ear of the turtle, Trachemys scripta elegans

Turtles, like other amphibious animals, face a trade-off between terrestrial and aquatic hearing. We used laser vibrometry and auditory brainstem responses to measure their sensitivity to vibration stimuli and to airborne versus underwater sound. Turtles are most sensitive to sound underwater, and their sensitivity depends on the large middle ear, which has a compliant tympanic disc attached to the columella. Behind the disc, the middle ear is a large air-filled cavity with a volume of approximately 0.5 ml and a resonance frequency of approximately 500 Hz underwater. Laser vibrometry measurements underwater showed peak vibrations at 500-600 Hz with a maximum of 300 μm s(-1) Pa(-1), approximately 100 times more than the surrounding water. In air, the auditory brainstem response audiogram showed a best sensitivity to sound of 300-500 Hz. Audiograms before and after removing the skin covering reveal that the cartilaginous tympanic disc shows unchanged sensitivity, indicating that the tympanic disc, and not the overlying skin, is the key sound receiver. If air and water thresholds are compared in terms of sound intensity, thresholds in water are approximately 20-30 dB lower than in air. Therefore, this tympanic ear is specialized for underwater hearing, most probably because sound-induced pulsations of the air in the middle ear cavity drive the tympanic disc.     

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.     

The anterior process of the malleus in extant Lagomorpha (Mammalia)

The anterior anchoring of the malleus of 30 extant species of Lagomorpha (rabbits, hares, pikas) has been studied on the basis of histological serial sections and µCT‐scans. It is shown that former studies of Oryctolagus, Lepus, and Ochotona are incomplete, because the rostral part of the processus anterior of the malleus is always lacking due to damage of this extremely delicate structure. Our study shows that in perinatal stages of Leporidae the praearticulare develops a prominent processus internus that fits into a groove at the ventral side of the tegmen tympani; this “tongue and groove”‐arrangement may act as a hinge. In adult stages, the rostral end of the praearticulare fuses synostotically with the medial process of the ectotympanic. Torsional strain produced by rotation around the axis of the middle ear ossicles at sound transmission must, therefore, be experienced by the extremely thin but highly elastic bony pedicle of the processus internus praearticularis. The free ending processus anterior of a late fetal Ochotona shows a short processus internus praearticularis, which does not articulate with the tegmen tympani. During postnatal development the middle ear of Ochotona becomes considerably remodelled: not only does excessive pneumatization of the tegmen tympani and tympanic cavity wall occur, but the short processus anterior is fused synostotically to a bone trabecula of the tegmen tympani meshwork. The thin and elastic bone bridges are not equivalent in Leporidae and Ochotonidae, that is, they must have evolved convergently. Fleischer's classification with Oryctolagus possessing a “freely mobile type” of middle ear ossicles cannot be supported by our observations. The same holds true for Ochotona, which does not represent a “freely mobile type” either. Thus, we suggest for the lagomorph middle ear ossicles a new category: the “bone elasticity type.”     

Incudomalleal joint formation: the roles of apoptosis,migration and downregulation

Background  

The middle ear of mammals is composed of three endochondrial ossicles, the stapes, incus and malleus. Joints link the malleus to the incus and the incus to the stapes. In the mouse the first arch derived malleus and incus are formed from a single Sox9 and Type II collagen expressing condensation that later subdivides to give rise to two separate ossicles. In contrast the stapes forms from a separate condensation derived from the second branchial arch. Fusion of the malleus and incus is observed in a number of human syndromes and results in conductive hearing loss. Understanding how this joint forms during normal development is thus an important step in furthering our understanding of such defects.     

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.     

The homeobox gene Emx2 underlies middle ear and inner ear defects in the deaf mouse mutant pardon

The semi-dominantly inherited mouse mutation pardon (Pdo) was isolated due to the lack of a Preyer reflex (ear flick) in response to sound from a large-scale N-ethyl-N-nitrosourea (ENU) mutagenesis programme. Dissection of the middle ear revealed malformations in all three ossicles, rendering the ossicular chain incomplete. Hair cell counts in the apical turn of the organ of Corti revealed a significant 22.7% increase in the number of outer hair cells. Raised compound action potential thresholds in Pdo/+ mutants suggested a combined sensorineural/conductive hearing loss. We show that a missense mutation in the homeobox gene Emx2 is responsible for these defects, identifying a new function for this gene in the development of specific structures in the ear.     

Middle ear structure and bone conduction in Spalax,Eospalax, and Tachyoryctes mole‐rats (Rodentia: Spalacidae)

There is evidence that spalacine, tachyoryctine, and myospalacine mole‐rats all communicate with conspecifics through a form of seismic signaling, but the route for the detection of these signals is disputed. It has been proposed that two unusual anatomical adaptations in Spalax allow jaw vibrations to pass to the inner ear via the incus and stapes: a pseudoglenoid (=postglenoid) fossa which accomodates the condylar process of the mandible, and a bony cup, supported by a periotic lamina, through which the incus articulates with the skull. In this study, a combination of dissection and computed tomography was used to examine the ear region in more detail in both Spalax and its subterranean relatives Tachyoryctes and Eospalax, about which much less is known. Tachyoryctes was found to lack a pseudoglenoid fossa, while Eospalax lacks a periotic lamina and bony cup. This shows that these structures need not simultaneously be present for the detection of ground vibrations in mole‐rats. Based on the observed anatomy, three hypothetical modes of bone conduction are argued to represent more likely mechanisms through which mole‐rats can detect ground vibrations: ossicular inertial bone conduction, a pathway involving sound radiation into the external auditory meatus, and a newly‐described fluid pathway between pseudoglenoid fossa and cranial cavity. The caudolateral extension of the tympanic cavity and the presence of a bony cup might represent synapomorphies uniting Spalax and Tachyoryctes, while the loss of the tensor tympani muscle in Spalax and Eospalax may be convergently derived. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.     

Erythrocles microceps, a new emmelichthyid fish from kochi, japan

A new emmelichthyid,Erythrocles microceps, is described from 15 specimens collected in Mimase Fish Market and Tosa Bay, Kochi Prefecture, Japan. It differs from its most similar congener,E. acarina, in having a greater number of lateral line scales (70–72 vs. 62–67 inacarina), more elongate body (body depth 23.8–25.9% SL vs. 27–29% SL), and smaller head (head) length 26.8–28.4% SL vs. 34–36% SL).     

The Origin of the Mammalian Middle Ear

A functional explanation is presented for the shift of the reptilianarticular and quadrate into the mammalian middle ear to becomethe malleus and incus. Modification of the masticatory apparatusof therapsids results in reduction of stresses on the jaw jointand consequently in reduction of posterior elements of the jaw.In the late therapsid, Bienotherium, the quadrate and post-dentaryjaw bones resemble the mammalian malleus and incus which togetherform a lever. The therapsid articular possesses a downturnedretroarticular process (for insertion of M. depressor mandibulae)homologous with the manubrium (force lever arm) of the malleus.About the time of origin of the mammalian (dentarysquamosal)jaw joint and following the origin of the mammalian depressor,the reptilian depressor is lost. This allows the enlarging reptiliantympanum to become attached to the retroarticular process. Thenew lever system thus formed by articular and quadrate increasesthe sensitivity of the ear and the reptilian one-bone systemis replaced. In early mammals the reflected lamina of the angularmigrates posteriorly with the angle of the dentary so that itcontacts and assumes support of the tympanum. Non-homology ofthe monotreme and therian depressors indicates a multiple originof the mammalian middle ear.