3D finite element analyses of insertion of the Nucleus standard straight and the Contour electrode arrays into the human cochlea

Previous experimental studies of insertion of the Nucleus standard straight and the Contour arrays into the scala tympani have reported that the electrode arrays cause damage to various cochlear structures. However, the level of insertion-induced damage by these electrode arrays to cochlear structures (the spiral ligament, the basilar membrane and the osseous spiral lamina) has not been quantified. Although it has been suggested that rotation can overcome this resistance and prevent the basilar membrane from being pierced by the tip of the Nucleus standard straight array, there has not been any attempt to study the relationship between the rotation and the reduction of damage to the basilar membrane. In this study, 3D finite element analyses of insertions of the Nucleus standard straight array and the Contour array into the scala tympani have been undertaken. The perforation of the basilar membrane by the tip of the Nucleus standard straight array at the region of 11-14 mm from the round window appears to be compounded by the geometry of the spiral passage of the scala tympani. Anti-clockwise rotations between 25 degrees and 90 degrees applied at the basal end of the electrode array (for the right cochlea) were shown to significantly reduce the contact stresses exerted by the tip on the basilar membrane which support the practice of applying small rotation partway through insertion of electrode array to minimize damage to the basilar membrane. Although the Contour array (with its stylet intact) is stiffer than the Nucleus standard straight array, a slight withdrawal of the stylet from the Contour array before insertion was found to significantly reduce damage by the electrode array to the spiral ligament and the basilar membrane.     

Structure and function of the cochlea in the African mole rat (Cryptomys hottentotus): evidence for a low frequency acoustic fovea

Summary The cochlea of the mole rat Cryptomys hottentotus was investigated with physiological and anatomical methods. In order to reveal the place-frequency map of the cochlea, iontophoretic HRP-applications were made in the cochlear nucleus at physiologically characterized locations. Subsequent HRP-transport in auditory nerve fibres and labeling patterns of spiral ganglion cells within the cochlea were evaluated.A cochlear place-frequency map was constructed from 17 HRP-applications in the cochlear nucleus at positions where neurons had characteristic frequencies between 0.1 and 12.6 kHz. As in other mammals, high frequencies were found to be represented at the cochlear base, low frequencies at the cochlear apex. The placefrequency map had three distinct parts which were characterized by their different slopes. A clear overrepresentation of the frequencies between 0.6 and 1 kHz was revealed, in this frequency range the slope of the place-frequency map amounted to 5.3 mm/octave. As calculated from the regression analysis, below 0.6 kHz the slope of the cochlear place-frequency map amounted to 0.24 mm/octave, above 1 kHz to 0.9 mm/octave.As in other mammals width of the basilar membrane (BM) increased from the cochlear base towards the cochlear apex. Also in concordance with the findings in other mammals, BM-thickness decreased from the cochlear base to the apex. However, it was remarkable to find that there was no or little change in BM-width and thickness between 40 and 85% BM-length. It was also revealed that scala tympani was only 1/10th the size found in the rat or other mammals of similar body size.On the basis of the cochlear place-frequency map and the morphological findings we speculate that in Cryptomys hottentotus an acoustic fovea is present in the frequency range between 0.6 and 1 kHz. In analogy to echolocating bats, about half of the cochlea is devoted to the analysis of a narrow frequency band within the hearing range.Abbreviations BM basilar membrane - CF characteristic frequency - CN cochlear nucleus     

Auditory systems of heteromyidae: Cochlear diversity

Cochleae (125) from 26 species of the rodent family Heteromyidae (genera Dipodomys. Microdipodops, Perognathus, and Liomys) were compared. In Perognathus and Liomys the scala tympani in the apical portion is extremely narrow with a correspondingly minute helicotrema. In Liomys there is no bone separating scala tympani from spiral ganglion in the upper second and entire third turn. In all species studied the zona pectinata of the basilar membrane is enlarged, with a hyaline mass between upper and lower basilar membrane fibers. This zona pectinata hypertrophy is least at the base of the cochlea and greatest in the upper second turn, decreasing again toward the apex. Basilar membrane width increases rapidly in the first turn and then changes only slightly. Except for Liomys, all the heteromyids studied have hypertrophied Hensen's cells with long apical processes supporting and forming an elevated reticular lamina. These Hensen's cells reach their maximum size in the upper second and lower third turns; throughout they rest on inner Claudius' cells rather than the basilar membrane. Relative to naso-occipital length the cochlear specializations are greatest in Microdipodops and least in Liomys just as is the case for middle ear modifications. The morphological data are consistent with the concept that standing wave phenomena may be important in heteromyid cochlear biomechanics. Single unit data of other workers are also consistent with this interpretation. Like middle ear morphology, inner ear morphology appears adapted to low-frequency sensitivity–especially in Dipodomys and Microdipodops.     

The cochlear frequency map of the mustache bat,Pteronotus parnellii

The frequency-place map of the cochlea of mustache bats was constructed by the analysis of HRP-transport patterns in spiral ganglion cells following iontophoretic tracer injections into cochlear nucleus regions responsive to different frequencies. The cochlea consists of 5 half turns (total length 14.3 mm) and the representation of certain frequency bands can be assigned to specific cochlear regions: The broad high frequency range between 70 and 111 kHz is represented in the most basal half turn within only 3.2 mm. This region is terminated apically by a distinct narrowing of the scala vestibuli that coincides with a pronounced increase in basilar membrane (BM) thickness. The narrow intermediate frequency range between 54 and 70 kHz is expanded onto 50% of cochlear length between 4.0 and 11.1 mm distance from apex. The frequency range around 60 kHz, where the tuning characteristics of the auditory system are exceptionally sharp, is located in the center of this expanded BM-region in the second half turn within a maximum of innervation density. These data can account for the vast overrepresentation of neurons sharply tuned to about 60 kHz at central stations of the auditory pathway. In the cochlear region just basal to the innervation maximum, where label from injections at 66 and 70 kHz was found, a number of morphological specializations coincide: the BM is maximally thickened, innervation density is low, the spiral ligament is locally enlarged, and the 'thick lining', a dense covering of the scala tympani throughout the basal halfturn, suddenly disappears. Low frequencies up to 54 kHz are represented within the apical half turns over a 4 mm span of the basilar membrane. The data are compared to the cochlea of horseshoe bats and the possible functional role of the morphological discontinuities for sharp tuning and the generation of otoacoustic emissions is discussed.     

Quantitative X-ray tomography of the mouse cochlea

Imaging with hard X-rays allows visualizing cochlear structures while maintaining intrinsic qualities of the tissue, including structure and size. With coherent X-rays, soft tissues, including membranes, can be imaged as well as cells making use of the so-called in-line phase contrast. In the present experiments, partially coherent synchrotron radiation has been used for micro-tomography. Three-dimensional reconstructions of the mouse cochlea have been created using the EM3D software and the volume has been segmented in the Amira Software Suite. The structures that have been reconstructed include scala tympani, scala media, scala vestibuli, Reissner's membrane, basilar membrane, tectorial membrane, organ of Corti, spiral limbus, spiral ganglion and cochlear nerve. Cross-sectional areas of the scalae were measured. The results provide a realistic and quantitative reconstruction of the cochlea.     

Osseous inner ear structures and hearing in early marsupials and placentals

Based on the internal anatomy of petrosal bones as shown in radiographs and scanning electron microscopy, the inner ear structures of Late Cretaceous marsupials and placentals (about 65 Myr ago) from the Bug Creek Anthills locality of Montana, USA, are described. The inner ears of Late Cretaceous marsupials and placentals are similar to each other in having the following tribosphenic therian synapomorphies: a fully coiled cochlea, primary and secondary osseous spiral laminae, the perilymphatic recess merging with the scala tympani of the cochlea, an aqueductus cochleae, a true fenestra cochleae, a radial pattern of the cochlear nerve and an elongate basilar membrane extending to the region between the fenestra vestibuli and fenestra cochleae. The inner ear structures of living therians differ from those of their Late Cretaceous relatives mainly in having a greater number of spiral turns of the cochlea and a longer basilar membrane. Functionally, a coiled cochlea not only permits the development of an elongate basilar membrane within a restricted space in the skull but also allows a centralized nerve system to innervate the elongate basilar membrane. Qualitative and quantitative analyses show that, with a typical therian inner ear, Late Cretaceous marsupials and placentals were probably capable of high-frequency hearing.     

Modulation of activity in starling cochlear ganglion units by middle-ear muscle contractions,perilymph movements and lagena stimuli

In the present study three groups of cochlear ganglion neurons were detected which differed in respect to their tone-evoked and spontaneous activity: auditory units which showed an irregular spontaneous discharge, non-auditory neurones with regular activity and such with an irregular spontaneous discharge pattern. Electrically-elicited contractions of the middle-ear muscle influenced the tone-evoked and/or the spontaneous activity of the auditory and the non-auditory neurones with irregular spontaneous discharge but not, however, the regularly firing units. Similar results were obtained with imposed perilymph movements in the cochlea (evoked via the vestibular system. Fractions of all three groups of cochlear ganglion neurones were responsive to direct deformations of the membraneous lagena. Several (auditory and non-auditory) units with irregular discharge were excited during a basilar membrane displacement towards scala vestibuli whereas a basilar membrane motion towards scala tympani resulted in a decrease of the discharge rate. A few units showed a different reaction. The results provide evidence that the neurones with periodic spontaneous discharge innervate the lagena and that this sense organ has no auditory significance in birds. The peripheral origin of the 'non-auditory' neurones with irregular spontaneous activity remains undecided and might be the macula lagenae or the apical portion of the basilar papilla.     

Morphometry of the chinchilla organ of Corti and stria vascularis

This research describes a procedure for a morphometric analysis of the organ of Corti and stria vascularis in the chinchilla. In nine normal cochleae the length of the basilar membrane and the stria vascularis measured 18.47 and 25.22 mm, respectively. An average of 1910 inner and 7501 outer hair cells were present while an average of 15 inner and 90 outer hair cells were absent. In all cochleae examined there were always some missing hair cells in varying numbers even though the animals had no known ototoxic exposure. Stria area, width and thickness increased from the cochlear apex toward the base. Consistency of changes in stria dimensions among animals was enhanced by expressing position in terms of percentage stria length rather than distance as such. Total stria volume was estimated at 0.15 microliter.     

Cochlea in old world mice and rats (Muridae)

Morphometric analysis of the cochlea was performed in wild and laboratory murids: Mus musculus, Apodemus sylvaticus, Rattus rattus, R. norvegicus, NMRI mouse, and Wistar rat. Results are based on light microscopic examination of surface specimens and serial sections and on three-dimensional computer reconstruction. The cochleae have 1.75-2.2 coils. The length of the basilar membrane varies from 6.0 to 12.1 mm. Mean density of outer hair cells ranges between 363 and 411, inner hair cells 98 and 121, neurons 1,230 and 1,760 per 1 mm. Following parameters change from base to apex: basilar membrane width 66.0 (+/- 8.2) to 175.0 (+/- 24.7) microns, basilar membrane thickness 17.0 (+/- 2.6) to 1.9 (+/- 0.1) microns, width of triad of outer hair cells 13.2 (+/- 0.7) to 28.8 (+/- 4.4) microns. The given numbers are mean "murid" values (with respective standard deviations). Maximum of dimensions of scalae is located at 10-15%, that of density of outer hair cells at 65%, density of inner hair cells at 2.8 mm, maximum of innervation density at 40-60% from the base. The following parameters are correlated with pinna size: length and maximum width of basilar membrane, dimensions of scalae, total number of receptors, and probably resolution capabilities. The following parameters are correlated with body size: maximum width of triad of outer hair cells, density and total number of neurons, ratio of neurons to receptors, apicobasal difference in basilar membrane stiffness and width of triad of outer hair cells; inversely proportional is receptor density and ratio of outer to inner hair cells and probably low-frequency cut-off. Thickness, and minimum width of basilar membrane and triad of outer hair cells and probably high-frequency cutoff are species-specific and independent of pinna or body size. The parameters mentioned indicate that the examined murids are acoustically unspecialized mammals and their cochleae approximate the generalized plan for a mammalian cochlea. Differences between domesticated and wild murids are stated.     

The Biophysical Origin of Traveling-Wave Dispersion in the Cochlea

Sound processing begins at the peripheral auditory system, where it undergoes a highly complex transformation and spatial separation of the frequency components inside the cochlea. This sensory signal processing constitutes a neurophysiological basis for psychoacoustics. Wave propagation in the cochlea, as shown by measurements of basilar membrane velocity and auditory nerve responses to sound, has demonstrated significant frequency modulation (dispersion), in addition to tonotopic gain and active amplification. The physiological and physical basis for this dispersion remains elusive. In this article, a simple analytical model is presented, along with experimental validation using physiological measurements from guinea pigs, to identify the origin of traveling-wave dispersion in the cochlea. We show that dispersion throughout the cochlea is fundamentally due to the coupled fluid-structure interaction between the basilar membrane and the scala fluids. It is further influenced by the variation in physical and geometrical properties of the basilar membrane, the sensitivity or gain of the hearing organ, and the relative dominance of the compression mode at about one-third octave beyond the best frequency.     

Quantitative characteristics of the basilar membrane in the mammalian cochlea

The variations in width and height of the basilar membrane along the cochlea in four species of laboratory animals: white rat, guinea pig, chinchilla and cat have been investigated. The results obtained have been used to calculate the height/width ratio along the cochlea, suggested by Bruns as an estimate of basilar membrane stiffness. The given characteristic is practically identical in all species studied despite the differences in the frequency ranges of auditory reception and, therefore, cannot be used either for characterizing the basilar membrane stiffness or for frequency mapping the cochlea of mammals.     

Model of cochlear microphonic explores the tuning and magnitude of hair cell transduction current

The mammalian cochlea relies on the active forcing of sensory outer hair cells (OHCs) to amplify traveling wave responses along the basilar membrane. These forces are the result of electromotility, wherein current through the OHCs leads to conformational changes in the cells that provide stresses on surrounding structures. OHC transducer current can be detected via the voltage in the scala tympani (the cochlear microphonic, CM), and the CM can be used as an indicator of healthy cochlear operation. The CM represents a summation of OHC currents (the inner hair cell contribution is known to be small) and to use CM to probe the properties of OHC transduction requires a model that simulates that summation. We developed a finite element model for that purpose. The pattern of current generators (the model input) was initially based on basilar membrane displacement, with the current size based on in vitro data. The model was able to reproduce the amplitude of experimental CM results reasonably well when the input tuning was enhanced slightly (peak increased by ∼6 dB), which can be regarded as additional hair bundle tuning, and with a current/input value of 200–260 pA/nm, which is ∼4 times greater than the largest in vitro measures.     

Fine structure of the intracochlear potential field. I. The silent current.

Field potentials were recorded along radial tracks in scala tympani and scala vestibuli of the guinea-pig cochlea. A current density analysis revealed standing current density profiles that were qualitatively similar between animals and between the second and third cochlear turns. Radial standing current densities were greatest at or near the spiral ligament. All the scala vestibuli current density profiles were scaled versions of one another while the scala tympani current density profiles showed more variability. Acoustic stimuli modulated the standing current and there was a cochlear microphonic current density peak in scala tympani near the organ of Corti. The results are summarized with a current-density field line model, the key element of which is a constant current pumped into scale media by the stria vascularis. The standing potential gradients drive current from each perilymphatic chamber into the spiral ligament en route to the lateral surface of the stria vascularis. The strial current is divided between the receptor cell pathway and leakage pathways. The standing current through the leakage pathways is indirectly modulated by acoustic stimulation through the modulation of the endocochlear potential. The reciprocal modulation of current between hair cell and leakage pathways suggests that the stria vascularis maintains a constant current during acoustic stimulation. The cochlear standing current is similar to the retinal dark current in its importance for sensory transduction but the fact that the silent current is generated by the stria vascularis and not the receptor cells provides significant benefits for the detection of mechanical stimuli.     

The ultrastructure of the cochlear basilar membrane of the guinea pig

The ultrastructure of the basilar membrane of the guinea pig cochlea is analysed. Measurements were made of the thickness of fibrillar and homogeneous layers along the cochlea of the width of bundles and spaces between them, and the distribution density of fibrils in the bundles. The analysis of the obtained characteristics has demonstrated that the homogeneous ground substance significantly contributes to the buildup of longitudinal stiffness of the basilar membrane.     

Localization of the cochlear amplifier in living sensitive ears

Background

To detect soft sounds, the mammalian cochlea increases its sensitivity by amplifying incoming sounds up to one thousand times. Although the cochlear amplifier is thought to be a local cellular process at an area basal to the response peak on the spiral basilar membrane, its location has not been demonstrated experimentally.

Methodology and Principal Findings

Using a sensitive laser interferometer to measure sub-nanometer vibrations at two locations along the basilar membrane in sensitive gerbil cochleae, here we show that the cochlea can boost soft sound-induced vibrations as much as 50 dB/mm at an area proximal to the response peak on the basilar membrane. The observed amplification works maximally at low sound levels and at frequencies immediately below the peak-response frequency of the measured apical location. The amplification decreases more than 65 dB/mm as sound levels increases.

Conclusions and Significance

We conclude that the cochlea amplifier resides at a small longitudinal region basal to the response peak in the sensitive cochlea. These data provides critical information for advancing our knowledge on cochlear mechanisms responsible for the remarkable hearing sensitivity, frequency selectivity and dynamic range.     

The Importance of the Hook Region of the Cochlea for Bone-Conduction Hearing

For the most part, the coiled shape of the cochlea has been shown to have only minor importance for air-conducted hearing. It is hypothesized, however, that this coiled shape may play a more significant role for the bone-conducted (BC) route of hearing, through inertial forces exerted by the middle ear and cochlear fluid, and that this can be tested by comparing the results of applying BC stimuli in a variety of different directions. A three-dimensional finite element model of a human middle ear coupled to the inner ear was formulated. BC excitations were simulated by applying rigid-body vibrations normal to the surface of the basilar membrane (BM) at 0.8 (d¹), 5.8 (d²), 15.6 (d³), and 33.1 (d⁴) mm from the base of the cochlea, such that relative motions of the fluid within the cochlea produced excitations of the BM. The vibrational direction normal to the BM surface at the base of the cochlea (d¹) produced the highest BM velocity response across all tested frequencies—higher than an excitation direction normal to the BM surface at the nonbasal locations (d²–d⁴), even when the stimulus frequency matched the best frequency for each location. The basal part of the human cochlea features a well-developed hook region, colocated with the cochlear vestibule, that features the largest difference in fluid volume between the scala vestibuli (SV) and scala tympani (ST) found in the cochlea. The proximity of the hook region to the oval and round windows, combined with it having the biggest fluid-volume difference between the SV and ST, is thought to result in a maximization of the pressure difference between the SV and ST for BC stimuli normal to the BM in this region, and consequently a maximization of the resulting BM velocity.     

Interplay between traveling wave propagation and amplification at the apex of the mouse cochlea

Sounds entering the mammalian ear produce waves that travel from the base to the apex of the cochlea. An electromechanical active process amplifies traveling wave motions and enables sound processing over a broad range of frequencies and intensities. The cochlear amplifier requires combining the global traveling wave with the local cellular processes that change along the length of the cochlea given the gradual changes in hair cell and supporting cell anatomy and physiology. Thus, we measured basilar membrane (BM) traveling waves in vivo along the apical turn of the mouse cochlea using volumetric optical coherence tomography and vibrometry. We found that there was a gradual reduction in key features of the active process toward the apex. For example, the gain decreased from 23 to 19 dB and tuning sharpness decreased from 2.5 to 1.4. Furthermore, we measured the frequency and intensity dependence of traveling wave properties. The phase velocity was larger than the group velocity, and both quantities gradually decrease from the base to the apex denoting a strong dispersion characteristic near the helicotrema. Moreover, we found that the spatial wavelength along the BM was highly level dependent in vivo, such that increasing the sound intensity from 30 to 90 dB sound pressure level increased the wavelength from 504 to 874 μm, a factor of 1.73. We hypothesize that this wavelength variation with sound intensity gives rise to an increase of the fluid-loaded mass on the BM and tunes its local resonance frequency. Together, these data demonstrate a strong interplay between the traveling wave propagation and amplification along the length of the cochlea.     

Ear morphology of the frog-eating bat (Trachops cirrhosus,family: Phyllostomidae): Apparent specializations for low-freqency hearing

The frog-eating bat (Trachops cirrhosus) is unusual among bats studied because of its reliance on low-frequency (<5 kHz) sounds emitted by frogs for prey localization. We investigated the ear of this bat in order to identify anatomical features that might serve as adaptations for low-frequency hearing. Trachops cirrhosus has a variety of anatomical features that might enhance low-frequency hearing, either by increasing sensitivity to low-frequency sounds or expanding the total frequency range to include lower frequencies. These bats have long pinnae, and a long and wide basilar membrane. The basal portion of the basilar membrane is much stiffer than the apical portion, and the basal portion of the tectorial membrane is more massive than the apical portion. There is also a concentration of mass in the apical portion of the cochlea. T. cirrhosus possesses the largest number of cochlear neurons reported for any mammal, the second highest density of cochlear neurons innervation known among mammals, and three peaks of cochlear neuron density. Other bats have two peaks of cochlear neuron density, lacking the apical concentration, while other mammals usually have only one. T. cirrhosus differs from most other small mammals and bats in characteristics of the apical portion of the cochlea, i.e., that area where the place theory of hearing predicts that low frequencies are detected.     

Responses of cat auditory cortical neurons to tones of different frequencies and electrical stimulation of corresponding regions of the cochlea

Characteristic frequencies of neurons in the cat auditory cortex (area AI) whose receptive fields are located in different parts of the basilar membrane of the cochlea were determined in cats anesthetized with pentobarbital. The higher the characteristic frequency of a neuron in area AI, the nearer its receptive field lies to the base of the cochlea. Receptive fields of neurons with a characteristic frequency higher than 4 kHz lie on the first 10 mm of the basilar membrane. Receptive fields of neurons with a characteristic frequency below 4 kHz lie on the remaining 11–12 mm of the membrane. The effect of electrical stimulation of the center of the receptive field of a neuron corresponds to its response to a tone of characteristic frequency. The more the frequency of the acting tone differs from the characteristic frequency, or the further the point of stimulation from the center of the receptive field of the neuron, the less likely is the neuron to respond with an action potential. Neurons with a low characteristic frequency have wider receptive fields than neurons with a high characteristic frequency. Receptive fields of neurons with close characteristic frequencies on the basilar membrane overlap considerably. It was shown by the method of paired stimulation that excitation evoked in neurons in area AI by the action of a tone of a particular frequency is followed by long-lasting inhibition. This inhibition lasts longest and is most effective if a tone of the characteristic frequency is used.