Place-frequency Map Research Articles

Fluid-structure interaction of the stereocilia bundle in relation to mechanotransduction.

Current hypotheses regarding mechanotransduction rely upon motion of the stereocilia relative to the apical surface of the hair cell. The viscosity of the surrounding endolymphatic fluid will, however, attenuate stereocilia motion at higher frequencies of excitation. To investigate stereocilia motion for physiologically reasonable deflections and frequencies of excitation, the fluid-structure interaction of the stereocilia bundle is considered analytically. Solutions in the frequency domain are determined for stereocilia bundle dimensions at several locations along the cochlear duct of the chinchilla. Results indicate that motion of the stereocilia is analogous to that of a low-pass filter. Comparison of these solutions with Greenwood's frequency-place map demonstrates that motion of the stereocilia bundle exists without substantial attenuation at least up to frequencies appropriate for the location of the corresponding hair cell along the cochlear duct. The variation in stereocilia morphology within the mammalian cochlea thus appears to provide a collection of low-pass mechanoreceptors, arranged in order of increasing corner frequency across the auditory spectrum.

Tuning, spontaneous activity and tonotopic map in chicken cochlear ganglion neurons following sound-induced hair cell loss and regeneration

Adult chickens were exposed for 48 h to a 525 Hz, 120 dB SPL tone that destroyed the hair cells and tectorial membrane in a crescent-shaped patch along the abneural edge of the basilar papilla. Single-unit recordings were obtained from cochlear ganglion neurons 0–1, 5, 14 and 28 days post-exposure to determine what effect the cochlear lesion had on neural discharge patterns and if the discharge patterns fully recovered. Immediately after exposure, the tuning curves were extremely broad and CF thresholds were elevated by 30–40 dB. In addition, the average spontaneous rate and percentage of neurons with interspike interval histograms with preferred intervals were greatly reduced, Tuning curves and spontaneous activity started to recover by 5 days post-exposure; however, some W-shaped tuning curves with two distinct tips and a hypersensitive tail were observed at this time. W-shaped tuning curves disappeared and spontaneous activity recovered to normal levels 14–28 days post-exposure. However, the CF thresholds of the most sensitive neurons were still slightly elevated, tuning curve slopes below CF were shallower than normal, and thresholds in the low-frequency tail of the tuning curves were often hypersensitive. These functional deficits were most closely associated with residual damage to the upper fibrous layer of the tectorial membrane. To determine if the cochlear frequency-place map was altered by the cochlear lesion, four physiologically characterized neurons were labeled with biocytin at 5 days post-exposure. The CFs of the labeled neurons were consistent with the normal frequency-place map (Chen et al. (1994) Hearing Research 81, 130–136) indicating that the tonotopic map was not altered.

The cochlear place-frequency map of the adult and developing mongolian gerbil

Gerbils are frequently used in auditory research; however, only limited information on the exact frequency representation in the cochlea is available. Therefore the place-frequency map of the gerbil cochlea was determined by iontophoretic application of horseradish peroxidase in physiologically characterized single auditory nerve fibers. Locations of the labeled nerve fibers at the inner hair cells were determined from a ‘3-dimensional’ reconstruction of the cochleae. The map was established for frequencies between 0.3 and 31.9 kHz. As in other mammals, a baso-apical frequency gradient from high to low frequencies was found. The slope of the place-frequency map amounted to 1.5 mm/octave for higher frequencies. Below 4 kHz the slope decreased to a value of 1 mm/octave at 0.5 kHz. A shift in the frequency map occurs during cochlear maturation. The place-frequency map in subadult gerbils (18 days after birth) is shifted by a distance corresponding to an octave, at least for frequencies above 6 kHz.

The rosette complex in gerbil Deiters cells contains γ actin

The relationship of selected cytoskeletal elements with the rosette complex of Deiters cells was examined immunocytochemically in the gerbil cochlea. By light microscopy, the staining pattern for actin in the apical portion of Deiters cells corresponded with the location of the rosette complex. At the ultrastructural level, the actin antibodies bound selectively at the periphery of the dense trabeculae in the center of the complex. Comparative staining with a battery of polyclonal and isoform-specific monoclonal antibodies revealed selective presence of the γ muscle actin isoform in this location. The loose meshwork at the periphery of the rosette complex stained selectively with a monoclonal antibody to vimentin. β-tubulin was not associated with the rosette complex but occurred in abundance in the microtubule-rich stalk. Actin and vimentin were not detected in the apical compartment of Deiters cells at the extreme base of the cochlea, thus confirming their association with the rosette complex which is not present in regions of the gerbil cochlea tuned to frequencies to 20 kHz or higher (Spicer and Schulte, 1993, 1994). The cytoarchitecture of the rosette complex and its preferential distribution along the place-frequency map promote speculation that Deiters cells may play a role in regulating ion homeostasis and/or micromechanical response properties of the organ of Corti.

Cytological changes related to maturation of the organ of Corti and opening of Corti's tunnel

Maturation of the organ of Corti in the gerbil was analyzed between 2 and 16 days after birth (DAB) by electron microscopy and immunostaining for β-tubulin. At 2 DAB, the organ of Corti consisted of stratified epithelium bearing immature sensory hair cells (HCs) and supporting cells. Maturation of OHCs and Deiters cells progressed in a medial-to-lateral direction and cytoskeletal development in inner pillar cells preceded that in outer pillar cells at the single location studied along the frequency-place map. Pillar cell differentiation progressed through a unique stage characterized by the appearance and stratification of structural features apparently concerned with opening of Corti's tunnel and subsequently showed other structural changes related to maturity toward the adult form. Development of the microtubule cytoskeleton occurred first in the cell's apex and proceeded basally. Ruffling of a middle region of the cell surface by microvilli appeared to promote separation between inner and outer pillar cells and initiate tunnel opening at 4 DAB. Proliferation of distended cisternae of granular reticulum evidenced proteinaceous secretion by these cells between 4 and 8 DAB. Subsequent tunnel expansion at about 14 DAB coincided with appearance in outer pillar cells of tubulocisternal endoplasmic reticulum and associated Golgi complexes that are thought to mediate fluid and ion secretion. Sixteen days postnatally after disappearance of granular and tubulocisternal reticula and Golgi complexes and at the time of clearing of tunnel fluid, lysosomes interpreted as mediating catabolism of endocytosed protein congregated beneath the apicala nd apicolateral plasmalemmae of inner pillar cells. As with pillar cells, development of the microtubule system in Deiters cells proceeded from the cell's apex to base. Following differentiation of their microtubule system by 8 DAB, Deiters cells showed expansion of Golgi cisternae between 10 and 15 DAB and development of tubulocisternal endoplasmic reticulum at 15 DAB. Hair cells possessed abundant, distinctively large mitochondria from 4 to 10 DAB. The subsurface cisternae matured earlier in medial as opposed to lateral outer hair cells. Vesicles budding from underlying cisternae appeared associated with development of subsurface cisternae and at 16 DAB were still observed in third row but not in more mature first row HCs.

Cochlear frequency-place map in adult chickens: Intracellular biocytin labeling

A cochlear frequency-place map was developed for adult chickens by labeling cochlear ganglion neurons with biocytin and correlating the location of each labeled fiber along the basilar papilla with the characteristic frequency of the unit's tuning curve. Labeled fibers showed little or no branching within the sensory epithelium and most fibers appeared to terminate on a single hair cell along the neural side of the basilar papilla. The CFs of the labeled neurons ranged from 353 Hz to 3145 Hz and the location of the labeled neurons ranged from 30.1% to 74.4% of the total distance from the apex of the papilla. CFs increased in an orderly manner from the apex towards the base of the papilla. The cochlear frequency map for adult chickens was similar to that estimated from previous cochlear lesion studies carried out on 30 day old chicks, although the predicted frequencies in the adults were slightly higher in some regions of the basilar papilla than in 30 day old animals. However, previous maps developed in younger animals (≤21 days) using lesion or labeling data predict significantly lower frequencies for a given location than in adult animals particularly in the basal half of the cochlea.

Differences along the place-frequency map in the structure of supporting cells in the gerbil cochlea

The function of supporting cells was investigated by comparing their morphologic adaptations at six different places in the gerbil cochlea. The volume of Deiters cells and tectal (cover) cells increased whereas that of Boettcher and Claudius cells decreased from base to apex. Deiters cells in the basal region tuned between 40 and 20 kHz lacked the unique rosette complex seen in regions encoding frequencies at or below 10 kHz. Deiters cells in high frequency regions differed from those at lower frequency places in several other ways: they possessed more apical microtubules, a larger basal microtubule stalk, mitochondria in the basal compartment, apical mitochondria that were unassociated with plasmalemma and more symmetric, and a less elaborately folded apicomedial plasmalemma enveloping fewer nerves. The tectal cells covering the outer tunnel appeared unlike Hensen cells in location and structure and differed further in exhibiting more variability with position in the cochlea. These covering cells in regions encoding high frequencies (20 and 40 kHz) extended a thin process medially that formed the roof of the outer tunnel and connected with the phalanx of the third Deiters cell. The tectal cells exclusively in places at 10 kHz or below projected numerous fimbriae into the outer tunnel. Hensen cells lateral to the cover cells also differed with frequency in showing abundant apical microvilli and mitochondria and basal juxtaposition to Boettcher cells only in the 40 to 20 kHz region. The observed structural differences provide evidence for functional variability along the place-frequency map. They attest to greater ion resorption from the outer tunnel by Deiters and tectal cells in low to mid frequency regions, and for greater ion exchange between endolymph and perilymph by Hensen, Boettcher and outer sulcus cells in regions of the cochlea encoding high frequencies. Amplification of the Deiters cells' microtubule system in the base of the cochlea possibly imparts increased stiffness to these cells and enhances transmission of mechanical energy at high frequency.

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.

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

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 place-frequency map had three distinct parts which were characterized by their different slopes. A clear over-representation 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.(ABSTRACT TRUNCATED AT 250 WORDS)

Developmental changes of frequency representation in the rat cochlea

The place-frequency map of the developing rat cochlea was measured by iontophoretic HRP-injections into the ventral cochlear nucleus at electrophysiologically characterized positions. Distribution of retrograde HRP transport in cochlear spiral ganglion cells was analysed by means of a three dimensional reconstruction of the cochlea. Cochlear place-frequency maps were derived in rats of two ages groups: 13 to 22 days, and 36 37 day old animals. These maps were compared with the place-frequency map of adult rats (Müller, 1991). No systematic difference in the place-frequency map between 36 37 day old and adult rats was observed. In animals of the younger age group the place-frequency map (for frequencies above 4 kHz) was shifted towards lower frequencies for a given place along the basilar membrane. The morphological and physiological basis for this frequency shift during development is discussed.

Frequency representation and spiral ganglion cell density in the cochlea of the gerbil Pachyuromys duprasi

The tonotopic map of the cochlea in the gerbil Pachyuromys duprasi was analysed by local iontophoretic HRP-application into physiologically defined regions of the cochlear nucleus and mapping of subsequent HRP transport patterns in cochlear spiral ganglion cells. Furthermore the spiral ganglion cell density along the cochlear duct was determined. The cochlear tonotopic map was established in the frequency range between 0.6 and 17.5 kHz. These frequencies corresponded to locations between 86 and 3% basilar membrane length (0% = cochlear base). It was found that the slope of the place-frequency map varied with frequency, the maximum slope being found between 1 and 4 kHz. This frequency range corresponds to the frequency range of highest auditory sensitivity as determined from cochlear microphonic recordings (Plassmann et al., 1987). The density of spiral ganglion cells also varied along the cochlear duct. A pronounced maximum (1927 cells/mm) was located at around 70% basilar membrane length, compared to values of 800 cells per mm near the cochlear apex and base. This region of high ganglion cell density also corresponds to the frequency range of highest auditory sensitivity.

Frequency representation in the rat cochlea

In order to determine the place-frequency map of the rat cochlea, iontophoretic HRP-injections were made into the cochlear nucleus at electrophysiologically characterized positions. Distribution of retrograde HRP transport in cochlear spiral ganglion cells was analysed by means of a three dimensional reconstruction of the cochlea. The map was established for frequencies between 1.2 and 54 kHz, corresponding to positions between 96.5 to 2% of basilar membrane length ( base = 0%). At apex of the cochlea the slope of the place-frequency map was below 0.25 mm/octave. The slope increased to a value of 2.1 mm/octave at 34% basilar membrane length, and remained almost constant towards the cochlear base. The close relationship between frequency range of highest sensitivity and maximum receptor- and innervation-density in the rat cochlea is discussed.

Accident and emergency services

In case of deafness, cochlear implants bypass dysfunctional or lost hair cells by direct electrical stimulation (eCIs) of the auditory nerve. However, spectral selectivity of eCI sound coding is low as the wide current spread from each electrode activates large sets of neurons that align to a place-frequency (tonotopic) map in the cochlea. As light can be better confined in space, optical cochlear implants (oCIs) promise to overcome this shortcoming of eCIs. This requires fine-grained, fast, and power-efficient real-time sound analysis and control of multiple microscale emitters. Here, we describe the development, characterisation, and application for hearing restoration of a preclinical low-weight and wireless LED-based multichannel oCI system and its companion eCI system. The head-worn oCI system enabled deafened rats to perform a locomotion task in response to acoustic stimulation proving the concept of multichannel opto - genetic hearing restoration in rodents.

Developmental alterations in the frequency map of the mammalian cochlea.

The position of an auditory hair cell along the length of the cochlea determines the sound frequency to which it is most sensitive. Receptors located near the proximal end (base) of the cochlea are maximally stimulated by high-frequency sounds; those occupying successively more distal (apical) positions respond best to progressively lower frequencies. At present, it is unclear how this frequency place map emerges with respect to the development of the cochlea. It has been suggested, on the basis of acoustic trauma experiments with developing chicks and cochlear potential recordings from developing gerbils, that this map may arise through systematic changes in the spatial encoding of frequency along the cochlea. Others have inferred from frequency tuning curves derived from auditory-nerve recordings in developing mammals and chicks, that the cochlear frequency-place map remains stable throughout development. We analysed frequency tuning curves obtained from gerbil spiral ganglion cells at a constant location within the basal cochlea, and report here that these cells undergo significant increases (up to 1.5 octaves) in their best-response frequencies between the second and third weeks of postnatal life. These recordings provide direct evidence for developmental changes in the tonotopic organization of the mammalian cochlea.

Cryoprobe-induced apical lesions in the chinchilla. II. Effects on behavioral auditory thresholds.

Lesions of the hair cells in the cochlear apex were produced by a miniature cryoprobe and changes in behavioral auditory thresholds were measured. Monauralized adult chinchillas were behaviorally trained using operant procedures to produce pure-tone audiograms at frequencies from 63 Hz to 40 kHz. Following collection of baseline thresholds, the apical and middle turns of the experimental ear were visualized through a hole drilled in the bulla and a copper cryoprobe that had been cooled in liquid nitrogen was placed on the apical turn of the cochlea. Post-lesion threshold shifts from two subjects showed a flat loss of approximately 20 dB restricted to frequencies below either 710 Hz or 1 kHz; thresholds were normal at higher frequencies. The cytocochleograms, prepared from the ears following completion of threshold testing, show an almost complete loss of both inner and outer hair cells in the apical-most 20% of the cochlea with an abrupt transition region to areas of normal-looking hair cell populations. The relationship between the frequencies at which hearing was impaired and the location of missing hair cells along the basilar membrane is in agreement with the frequency-place map for the chinchilla of Eldredge et al. [(1981) J. Acoust. Soc. Am. 69, 1091-1095]. The magnitude of the loss, however, is less than might be expected based on comparison with threshold shifts produced by similar pathology in the basal turns.

An HRP-study of the frequency-place map of the horseshoe bat cochlea: morphological correlates of the sharp tuning to a narrow frequency band.

The frequency-place map of the horseshoe bat cochlea was studied with the horseradish peroxidase (HRP) technique involving focal injections into various, physiologically defined regions of cochlear nucleus (CN). The locations of labeled spiral ganglion cells and their termination sites on inner hair cells of the organ of Corti from injections into CN-regions responsive to different frequencies were analyzed in three dimensional reconstructions of the cochlea. Horseshoe bats from different geographical populations were investigated. They emit orientation cells with constant frequency (CF) components around 77 kHz (Rhinolophus rouxi from Ceylon) and 84 kHz (Rhinolophus rouxi from India) and their auditory systems are sharply tuned to the respective CF-components. The HRP-map shows that in both populations: the frequency range around the CF-component of the echolocation signal is processed in the second half-turn of the cochlea, where basilar membrane (BM) is not thickened, secondary spiral lamina (LSS) is still present and innervation density is maximal; frequencies more than 5 kHz above the CF-component are processed in the first half-turn, where the thickened BM is accompanied by LSS and innervation density is low; frequencies below the spectral content of the orientation call are represented in apical turns showing no morphological specializations. The data demonstrate that the cochlea of horseshoe bats is normalized to the frequency of the individual specific CF-component of the echolocation call. The HRP-map can account for the overrepresentation of neurons sharply tuned to the CF-signal found in the central auditory system. A comparison of the HRP-map with a map derived with the 'swollen nuclei technique' following loud sound exposure (Bruns 1976b) reveals that the latter is shifted towards cochlear base by about 4 mm. This discrepancy warrants a new interpretation of the functional role of specialized morphological structures of the cochlea within the mechanisms giving rise to the exceptionally high frequency selectivity of the auditory system.

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.

Physiological and morphological characterization of efferent neurones in the guinea pig cochlea

Efferent neurones within the intraganglionic spiral bundle of the guinea pig cochlea were characterized in terms of their response properties, and their pattern of termination within the receptor organ revealed by intracellular labelling with horseradish peroxidase. All neurones subsequently identified as efferent neurones had clear features of their response properties which distinguished them from primary auditory afferents. They had long latency, low maximum discharge rate and low levels of spontaneous activity under Nembutal/Innovar anaesthesia. The pattern of discharge was extremely regular, revealed by symmetrical interspike interval histograms. 49.4% responded best to ipsilateral, 43.3% to contralateral sound and a third group of 7.3% responded equally well to either ipsilateral or contralateral sound. In cochleae in good physiological condition, these efferents were as sensitive and as sharply tuned as primary afferents with the same characteristic frequencies (CFs). All efferents fully traced in histological processing terminated on the outer hair cells. Several efferents showed extensive branching beneath the inner hair cells which might represent en passant synapses with other neuronal elements. There was clear evidence of tonotopic organization of the efferent projection. The site of termination on the outer hair cells in most instances was very close to the region of the cochlea predicted from the fibres' CF and the known place-frequency map for primary afferent neurones in the guinea pig.

Auditory nerve activity and cochlear morphology after noise exposure.

Four chinchillas were exposed for 5 days to an octave band of noise centered at 4 kHz and having an SPL of 86 dB. After a recovery period of approximately 6 months, behavioral audiograms were obtained and auditory nerve fiber activity was recorded. The animals were killed and the cochleas embedded in plastic to obtain a surface preparation and 1 mu radial sections of the organ of Corti. Behavioral threshold shifts ranged from 5 to 20 dB at frequencies between 4 and 11 kHz. Auditory nerve fiber thresholds were elevated up to 70 dB for units with characteristic frequencies between 4 and 14 kHz. Units with higher and lower characteristic frequencies had normal thresholds. Cochleagrams showed narrow lesions of inner and/or outer hair cells over approximately a 1 mm distance. A comparison of the three realms of data revealed the following: (1) The greatest threshold shifts from the noise exposure were seen in the single nerve fiber thresholds while the smallest shifts were seen in the behavioral thresholds, (2) the greatest behavioral and neural threshold shifts and greatest cochlear damage occurred 1 octave above the center frequency of the noise exposure, and (3) based on the frequency-place map of the chinchilla cochlea, the range of fibers with elevated thresholds exceeded the extent of the OHC lesion. A number of anatomical changes were seen that effectively increased the extent of the damage found in the chochleagram. These changes included: distortions in the surface topography of the organ of Corti affecting the orientation of IHC; missing pillar cells in the presence of normal OHC and/or IHC and protrusion of the IHC cuticular plate into the subtectorial space.