Volkmar Bruns

Peripheral auditory tuning for fine frequency analysis by the CF-FM Bat,Rhinolophus ferrutnequinum

Summary1.The morphology of the cochlea of the greater horseshoe bat,Rhinolophus ferrumequinum, has been investigated quantitatively in an effort to correlate morphological specialization with the extraordinary sharpness of tuning of the peripheral auditory system. The parameters measured were: height of the scalae, dimensions of the lamina spiralis secundaria, and the length, width, and height (thickness) of the basilar membrane.2.The average length of the basilar membrane is 16.1 mm, much longer than in other mammals of equivalent size, or even other bats emitting purely frequency modulated (FM) orientation sounds.3.There are two conspicuous discontinuities in structure along the cochlea duct. These probably are important to the specialized function of the cochlea.4.The sharpest discontinuity occurs 4.3 to 4.6 mm from the basal end of the basilar membrane, where the thickness of the membrane decreases from 35 to 10 μm. This decrease is due to the loss of thickness of the membrane (pars pectinata) below the outer hair cells of the organ of Corti. At the lower part of this steep slope (between 4.5 and 4.6 mm) the basilar membrane is of minimum width, there is a thickening of the lamina spiralis secundaria, and there is a minimum distance between the lamina spiralis primaria and the lamina spiralis secundaria.5.A second discontinuity occurs at 7.8 mm of basilar membrane length. At this point the membrane begins to widen again and there is a change in form of the lamina spiralis secundaria.6.The role of specialized structures of the cochlear duct is discussed in the context of mechanical frequency analysis.

Postnatal development of the rat organ of Corti

SummaryThe development of the rat organ of Corti was studied during the first postnatal weeks. The temporal and the spatial patterns of cochlear development were investigated between 4 and 24 days after birth by means of semi-thin sections at approx. ten equidistant positions along the entire cochlear duct. At all examined positions width, thickness and cross sectional area of basilar membrane, cross-sectional area of tectorial membrane, of cells of Hensen, Claudius and Boettcher and of the organ of Corti were quantitatively analyzed. The most conspicuous maturational changes occur between 8 and 12 days after birth. These are the detachment of the tectorial membrane, the first appearance of filaments within the basilar membrane, the formation of the tunnel of Corti and the opening of the inner spiral sulcus. Quantitative analysis revealed that structures of a given position along the cochlear duct do not develop synchronously. Width of the basilar membrane and cross-sectional area of the tectorial membrane are already mature at the onset of hearing (10–12 days after birth). Length, thickness and cross-sectional area of the basilar membrane as well as cross-sectional area of the organ of Corti and of the cells of Hensen, Claudius and Boettcher still develop after the onset of hearing (up to 20–24 days after birth). We suggest that basic cochlear function is established by structures which are mature before the onset of hearing. Cochlear structures which develop after the onset of hearing might be involved in this improvement during this period.

Inner ear structure electrophysiological audiograms of the subterranean mole rat, Spalax ehrenbergi

Subterranean mole rats of the Spalax ehrenbergi superspecies in Israel have a distinctly developed vocal repertoire, presumably compensating together with olfaction for their complete blindness, thus providing an efficient communication system underground. Here we describe the unique organization of the cochlea of Spalax among mammals. The cochlea is subdivided into different subsystems where in the apical subsystem the fluid space and the organ of Corti differ remarkably from that in the basal subsystem, a feature as yet unknown in other mammals. The audiograms based on cochlear microphonics and on evoked potential recordings from the midbrain and brainstem, reveal a hearing range from 0.1 kHz-10 kHz with a best sensitivity between 0.5 and 1 kHz.

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

SummaryThe 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.

The innervation of the organ of Corti in the rat

To date our knowledge of the baso-apical distribution of the afferent and efferent nerve fibers innervating the organ of Corti is only fragmentary. This study makes an effort to lay the basis for a comprehensive analysis of cochlear innervation. Using a quantitative electronmicroscopic method, the fiber density of all cochlear fibers along the entire length of the cochlear duct was investigated in adult rats, Rattus norvegicus. Myelinated and unmyelinated nerve fibers in the primary osseous spiral lamina and afferent and efferent nerve fibers to the outer hair cells (OHCs) in the tunnel of Corti were counted. The rat cochlea is innervated by 19000 nerve fibers which consist of 79% afferent and 21% efferent fibers. The inner hair cells (IHCs) are innervated by 14000 afferent and 2000 efferent fibers. The OHCs are innervated by 1000 afferent and 2000 efferent fibers. The maximum fiber density of IHC afferents, OHC afferents and IHC efferents was found in the middle of the cochlea. This corresponds to the region at the basilar membrane where the frequency range of maximum sensitivity is located [8 kHz-31 kHz; Kelly and Masterton, J. Comp. Physiol. Psychol. 91, 930-936 (1977)]. The efferent nerve fibers to the OHCs consists of two different morphological sub-types: large fibers containing mitochondria and neurotubules (type I) and small fibers containing neurofilaments (type II). The fiber density of type I OHC efferents decreases from base to apex corresponding to the frequency dispersion along the basilar membrane. The fiber density of type II OHC efferents has maxima at the base and at the apex and a minimum in the middle of the cochlea. This minimum corresponds to the region at the basilar membrane where the frequency range of maximum sensitivity is located.

Middle ear and cochlear receptors in the subterranean mole-rat, Spalax ehrenbergi

The eardrum and the auditory ossicles of the middle ear, and the population of cochlear receptors in subterranean mole-rats of Spalax ehrenbergi complex were qualitatively and quantitatively analyzed. The area of the eardrum was 10.2 (S.D. = 0.9) mm2, that of the stapedial footplate 0.6 (S.D. = 0.07) mm2, the malleus: incus lever ratio was 1.25:1. The malleus is simply built, not attached to the tympanic ring. The incus is large; its long process is almost parallel to the manubrium of the malleus. The short process of the incus is provided with a peculiar bony cap, a structure thus far undescribed in mammalian auditory ossicles. Firmness of mutual connection of the ossicles may vary among different forms of Spalax. The size and form of the stapes are characterized by a large variability as well. The length of the basilar membrane was 12.6 (S.D. = 0.7) mm. The mean density of inner hair cells amounted to 93.3 that of outer hair cells to 386.4 cells per mm of the basilar membrane length. In general, the density increased from the base towards the apex. On average there were 415 outer, 100 inner hair cells in the organ of Corti; the ratio being constant along the basal 65% of the length and decreasing in the apical part of the organ of Corti. The radial width of the triad of outer hair cells increased and remained constant along the apical half of the Corti organ. Based on available findings of comparative and functional morphology, most of the studied features may be considered correlates of low-frequency tuning of the hearing organ in mole-rats.

Cochlear place-frequency map in the marsupial Monodelphis domestica

In order to determine the place-frequency map of the cochlea in the marsupial Monodelphis domestica, iontophoretic HRP-injections were made at several locations in the ventral cochlear nucleus. Prior to iontophoresis the auditory neurons at these locations were characterized electrophysiologically. The resulting distribution of retrogradely labeled cochlear spiral ganglion cells was analysed by means of a three dimensional reconstruction of the cochlea. The map was established for frequencies between 2.4 and 44.5 kHz, corresponding to positions between 95 to 14% of basilar membrane length (base = 0%). The maximum slope amounted to 1.8 mm/octave. Over the basal-most 60% of the cochlea the slope of the place-frequency map was larger than 1.5 mm/octave, further apically the slope rapidly decreased to values below 0.8 mm/octave. The shape of the cochlear place-frequency map is similar to that described in placental mammals.

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.

Basilar membrane tuning properties in the specialised cochlea of the CF-bat, Rhinolophus ferrumequinum

The greater horseshoe bat has greatly expanded frequency mapping, and morphological specialisations, in the first half turn of its cochlea and a sudden transition to normal mapping. Amplitude and phase of vibration have been measured on various structures in the expanded and normal regions and have not revealed any sharply tuned responses. Amplitudes are much lower than those found in other species and frequently show a deep notch in the 77-84 kHz region. The high-frequency cut-off frequencies are tonotopically organised but deviate from the Bruns map, so that hair-cell tuning appears to occur at a frequency at which basilar membrane vibration is small. In the basal region, phase differences were frequently found between the inner and outer parts of the basilar membrane. These appear to be due to interaction between two components of motion and are probably not indicative of a further filtering mechanism. There is no evidence for reflection of the travelling wave at the transition.

Basilar membrane and its anchoring system in the cochlea of the greater horseshoe bat.

SummaryThe auditory system of Rhinolophus ferrumequinum is sharply tuned to 83 kHz, the frequency of the constant-frequency segment of the bats echolocation signal. On the basis of morphological observations the cochlea of the horseshoe bat can be divided into three regions.(A)In the apical region (8 to 16 mm from the basal end of the organ of Corti; frequency response below 40 kHz) the structure is comparable to that of other mammals sensitive to high frequencies.(B)The basal region (0 to 4.5 mm) which responds to frequencies around 83 kHz is characterized by the following unusual features. (1) The basilar membrane (BM) is 35 μm thick. This thickening sharply decreases to 10 μm at 4.5 mm. (2) The filaments in the BM thickening mainly run spirally rather than exclusively in a radial direction as in other parts of the cochlea and in other mammals. (3) The outer segment of the BM is connected to the secondary spiral lamina by filaments from the inner margin of the spiral ligament. The specialized thick secondary spiral lamina is connected to the outer bony wall only by a thin curved lamella. (4) The large spiral ligament consists mainly of hyaline tissue and is almost devoid of fibers. The inner margin contains fibers in a spirally oriented bundle. (5) The tunnel of Corti is reduced and the first space of Nuel is enlarged by the inward displacement of the feet of the outer pillar cells.(M)In the middle region (4.5 to 8 mm; frequency response 40 to 80 kHz) the outer anchoring system (secondary spiral lamina and spiral ligament) is specialized as in the basal region; whereas all other elements correspond to those of the apical region. Vibration measurements demonstrated that in the basal region the inner and outer segment of the BM vibrate out of phase. To discuss the functional consequences of the specialized BM and associated structures, different models are considered. On the basis of the fine structure and the vibration behavior in the basal region of the horseshoe bats cochlea, a model is proposed which allows a relatively independent motion between the inner and outer segments of the BM and which would apparently result in a mechanical frequency sharpening for 83 kHz.