Cochlear Tuning Research Articles

Further studies on the mechanics of the cochlear partition in the mustached bat. I. Ultrastructural observations on the tectorial membrane and its attachments

From semithin and ultrathin sections of the mustached bat cochlea, baso-apical gradients in ultrastructural composition, shape and attachment site of the tectorial membrane (TM) were determined in relation to gradients in hair cell size and stereocilia size. These provide a data base for estimates of the mechanical properties of the organ of Corti as they relate to specialized aspects of the cochlear frequency map (Kössl and Vater, 1996). As in other mammals, the TM is composed of type A and type B protofibrils. Measurements of the packing density of type A protofibrils reveal gradients in both the radial and longitudinal direction. Distinct variations in packing density of type A protofibrils across the radial extent of the TM allow the definition of more subregions than in other mammals. Throughout the cochlea, packing density is highest in the ‘stripe’ region located close to the spiral limbus. The centrally located ‘core’ region of the middle zone contains distinctly fewer type A protofibrils than the laterally located ‘mantle’ region of the middle zone. The TM in the specialized basal turn (first and second half-turns) features a higher packing density of type A protofibrils in the ‘mantle’ than the TM in the apical cochlea (upper third to fifth half-turns), and an incorporation of longitudinally directed type A protofibrils in the marginal zone. Among cochlear turns, there are pronounced changes in cross-sectional area of the TM and the extent of its limbal attachment site. Within the densely innervated second half-turn that contains an expanded representation of the 60 kHz constant frequency (CF) component of the echolocation signal, both the cross-sectional area (see also Henson and Henson, 1991) and the attachment site of the TM are enlarged. An extended limbal attachment site is also observed in the densely innervated region of the lower first half-turn that represents the upper harmonics of the call. Within the sparsely innervated region of the upper first half-turn, the limbal attachment site of the TM is significantly diminished. Size of outer hair cells WHO ranges between 12 and 13 μm throughout the basal 80% of cochlear length and reaches maximal values of 20 μm in the apex. Size of OHC stereocilia ranges between 0.7 and 0.8 μm throughout the basal 60% of cochlear length and reaches a maximal size of 2.2 μm in the apex. These data corroborate and extend previous notions that morphological specializations of the TM in concert with specializations of the basilar membrane and perilymphatic spaces play an integral role in creating specialized cochlear tuning in the mustached bat.

Acoustic distortion products from the cochlea of the blind African mole rat, Cryptomys spec.

The measurement of distortion-product otoacoustic emissions is a noninvasive method that can be used for assessing the sensitivity and the frequency tuning of nonlinear cochlear mechanics. During stimulation with two pure tones f1 and f2, the acoustic 2f1-f2 distortion was recorded in the ear canal of Cryptomys spec. to study specializations in cochlear mechanics that could be associated with the presence of a frequency expanded cochlear region between 0.8-1 kHz. In addition, a distortion threshold curve was obtained which describes relative threshold of nonlinear cochlear mechanics. Sensitive distortion thresholds could be measured for stimulus frequencies between 0.4 to 18 kHz with a broad minimum between 0.75 to 2.5 kHz. The distortion threshold curve extends to higher frequencies than previous neuronal data indicated. As a measure of mechanical tuning sharpness in the cochlea, suppression tuning curves of 2f1-f2 were recorded. The tuning curves reflected the typical mammalian pattern with shallow low frequency and steep high frequency slopes. Their tuning sharpness was poor with Q10dB values between 0.3 and 1.88. In the range of the frequency expanded region, the Q10dB values were below 0.5. This finding emphasizes that the presence of frequency expansion does not necessarily lead to enhanced mechanical tuning in the cochlea and one has to consider if in certain bat species with cochlear frequency expansion and particularly sharp cochlear tuning, the two phenomena may not be interlinked.

Hot topics in physiological acoustics

For those in the Society whose main interest lies in other acoustic fields, the presentation will review current topics in physiology of audition. Much basic physiological research has been focused on the micromechanics of the cochlea, the end organ of hearing. For many years the cochlear tuning process was through to be passive and mechanical; however, recent studies indicate that active motion of one group of cochlear hair cells adds to and sharpens the tuning. The results and implications of studies of outer hair cell motion will be discussed. Also discussed will be the cochlear implant, a device that addresses injury or loss of cochlear hair cells, the cause of most incurable forms of deafness. With this device, the electric fields of electrodes surgically implanted in the cochlea stimulate the nerve supply in the absence of normal hair cells. Also presented will be recent advances in molecular biology that attempt to induce growth or regrowth of hair cells in cochleae that have none.

Orthotropic piezoelectric properties of the cochlear outer hair cell wall.

The mammalian outer hair cell has been shown to possess significant coupling between mechanical and electrical properties. This electromotile property may play a key role in cochlear tuning. In order to characterize quantitatively the electrical and mechanical behavior, the cell wall is modeled as a thin linear elastic piezoelectric material. Experimental findings from several investigators are used to determine the mechanical and electrical generalized stiffness coefficients described by the model. The model analysis indicates that orthotropic mechanical properties in the plane of the cell wall are required to match experimental behavior. The calculated orthotropic coefficients predict that the outer hair cell deforms due to cilia deflection with a force gain of 0.5 for perfectly constrained end conditions and a displacement gain of 3.6 for free end conditions. These values reflect the potential role of the OHC as a feedback mechanism to the basilar membrane. Results are for small deformation and quasi-static conditions with viscosity and inertial effects neglected. It is further assumed that cell permeability is negligible at the time scale of the fast deformation considered here.

Labile cochlear tuning in the mustached bat. II. Concomitant shifts in neural tuning.

Acoustic stimuli near 60 kHz elicit pronounced resonance in the cochlea of the mustached bat (Pteronotus parnellii parnellii). The cochlear resonance frequency (CRF) is near the second harmonic, constant frequency (CF2) component of the bat's biosonar signals. Within narrow bands where CF2 and third harmonic (CF3) echoes are maintained, the cochlea has sharp tuning characteristics that are conserved throughout the central auditory system. The purpose of this study was to examine the effects of temperature-related shifts in the CRF on the tuning properties of neurons in the cochlear nucleus and inferior colliculus. Eighty-two single and multi-unit recordings were characterized in 6 awake bats with chronically implanted cochlear microphonic electrodes. As the CRF changed with body temperature, the tuning curves of neurons sharply tuned to frequencies near the CF2 and CF3 shifted with the CRF in every case, yielding a change in the unit's best frequency. The results show that cochlear tuning is labile in the mustached bat, and that this lability produces tonotopic shifts in the frequency response of central auditory neurons. Furthermore, results provide evidence of shifts in the frequency-to-place code within the sharply tuned CF2 and CF3 regions of the cochlea. In conjunction with the finding that biosonar emission frequency and the CRF shift concomitantly with temperature and flight, it is concluded that the adjustment of biosonar signals accommodates the shifts in cochlear and neural tuning that occur with active echolocation.

Labile cochlear tuning in the mustached bat. I. Concomitant shifts in biosonar emission frequency.

The cochlea of the mustached bat (Pteronotus parnellii) has sharp tuning characteristics and pronounced resonance within a narrow band near the second harmonic, constant frequency (CF2) component of the animal's biosonar signals. That fine frequency discrimination occurs within this narrow band is evident from Doppler-shift compensation, whereby bats in flight lower the frequency of emitted CF2s to maintain returning echoes within this band. This study examined various factors capable of producing shifts in both the cochlear resonance frequency (CRF) and CF2s emitted by stationary bats and bats actively Doppler-shift compensating on a pendulum. Each of three experimental factors shifted the CRF in a reversible manner. Changes in body temperature produced an average CRF shift of 39 +/- 18 Hz/degrees C. The CRF increased with flight by 150 +/- 100 Hz and returned to baseline values within 10 min after flight. Contralateral sound exposure produced smaller (100 +/- 20 Hz), rapid shifts in the CRF, suggesting that a mechanism different from the temperature- and flight-related shifts was involved. Changes in the CRF induced by temperature and flight were accompanied by shifts in the emitted CF2 of stationary and moving bats. Coupled with a companion study of associated shifts in neural tuning, the concomitant changes in CRF and CF2 provide evidence of cochlear tuning lability in the mustached bat.

High-frequency two-tone distortions from the ear of the mustached bat, Pteronotus parnellii reflect enhanced cochlear tuning.

High-frequency two-tone distortions from the ear of the mustached bat, Pteronotus parnellii reflect enhanced cochlear tuning.

Stretch sensitivity of the lateral wall of the auditory outer hair cell from the guinea pig

The inner and outer hair cells of the mammalian hearing organ are mechano-transducer cells. Here we report evidence that the lateral wall of outer hair cells (OHCs) is a mechano-receptor. This mechano-sensitivity appears to complement that of the stereocilia. Patch clamping studies showed that stretching of the membrane patches by suction at the pipette activated potassium channels with 130 pS unit conductance specifically localized in the lateral wall. Application of an osmotic tension to the entire cell membrane under whole-cell recording produced a 10 mV hyperpolarization. The reversal potential and the magnitude of the macroscopic current under voltage clamp were consistent with the single-channel properties of stretch-activated potassium channels. The elongated cylindrical cell body of the OHC is optimally positioned in the cochlea to sense axial force due to the vibrations of the basilar membrane during sound stimulation. This sensitivity can explain the production of a predominantly hyperpolarizing response to sound stimuli, unique to the OHC. Coupled with voltage-dependent OHC motility, the stretch-activated channels may play an important role in producing a mechanical feedback, an indispensable element in cochlear tuning.

Cochlear and CNS tonotopy: Normal physiological shifts in the mustached bat

The ear of the mustached bat (itPteronotus parnellii) shows marked cochlear resonance near 60 kHz and many sharply tuned neurons throughout the brain have best frequencies (BF) near the cochlear resonance frequency (CRF). Controlled changes in the normal physiological range of body temperature (approx 37–42°C) were used to change the CRF and to study the tuning properties of neurons in the cochlear nucleus (CN) and inferior colliculus (1C). In all cases there were concomitant shifts in the CRF and the BFs. Results were the same for single and multi-units, and for CN and IC units. Although the BF reliably changed with shifts in the CRF, the majority of the units showed no change in minimum threshold or the sharpness ( Q 10 dB) of tuning. The temperature-induced effects on cochlear tuning were similar to those previously described in nonmammalian vertebrates. The physiological data reveal that, within a narrow frequency band, cochlear and CNS tonotopy are labile in the mustached bat. The lability of tuning is further substantiated by adaptations of biosonar emission behavior with shifts in CRF (Henson et al., 1990).

The role of outer hair cell motility in cochlear tuning

The mammalian cochlea's remarkable sensitivity and frequency selectivity are thought to be mediated by the mechanical feedback action of outer hair cells. New tools for measuring the movement of cochlear elements, and recent advances in modeling are increasing our knowledge of cochlear mechanics.

Frequency Dependent Maturation of the Cochlea and Brainstem Evoked Potentials

The anatomical development of the human cochlea starts in the middle basal turn and progresses both toward the base and the apex. Behavioral responses, in contrast, appear to emerge for lower frequencies first. Cochlear tuning may continue to change during early development and so effect electrophysiological and behavioral measures of maturation. The maturation of the cochlear traveling wave delay as well as the ABR I-V interval was investigated using the derived response technique which permits a frequency dependent analysis of this maturation. It was found that the traveling wave delay decreased significantly with age for the most basal part of the cochlea; however, it was not affected by age for more apical locations. The I-V delay difference with the adult values was found significantly shorter in the derived octave band with CF = 2.8 kHz than in all other bands for the preterm, term and infant groups. This suggests that the frequency dependent electrophysiological maturation of the brainstem parallels the anatomical development of the cochlea.

Detuning of cochlear action potential tuning curves at high sound pressure levels: influence of temporal, spectral and intensity variables.

Action potential (AP) tuning curves (TCs), generated by probe stimuli of 60-65 dB SPL with short rise and decay (r&d) times, are less sensitive (have elevated tip thresholds) and are detuned (the frequency is shifted away from that of the probe stimulus, towards a middle frequency of the audiogram). These effects are more pronounced with forward than with simultaneous masking. TCs generated by masking tonal and narrow band noise stimuli are nearly identical, even though the spectrum is much wider for the noise stimulus. Decreasing r&d time has the same effect on TCs generated from both noise and tonal stimuli, even when it only measurably increases the acoustic splatter of the latter. Detuning appears to be related to a temporal-intensity interaction.

Modulation of cochlear tuning by low-frequency sound

An intense, low-frequency tone (about 30 Hz) modulates the sensitivity of the inner ear to high-frequency stimulation. This modulation is correlated with the displacement of the basilar membrane. The findings suggest that the modulation may also affect cochlear tuning. We have investigated modulation of cochlear tuning by low-frequency sound in the guinea pig. Applying indirect methods of measurement (narrow-band analysis of compound action potentials and compound-action-potential tuning curves), the results suggest a shift of the excitation pattern along the basilar membrane towards higher-frequency areas. The shift occurred for both scala tympani and scala vestibuli displacement of the cochlear partition. Tuning curves, obtained from single units in the cochlear nerve, show sensitivity loss and a tip shift towards lower frequencies. This was also found for both scala tympani displacement and scala vestibuli displacement. The shift of the tip of the tuning curve towards lower frequencies corresponds to the inferred high-frequency shift of the excitation pattern. The relationship of these phenomena with the pathophysiology of Ménière's disease and with possible active mechanisms in cochlear transduction is discussed.

Cochlear tuning characteristics infants and adults

Cochlear tuning characteristics were estimated by obtaining suppression tuning curves (STCs) for spontaneous otoacoustic emissions (SOAEs) in infant and adult subjects. STCs were derived using 8 to 12 suppressor frequencies per SOAE. Infants were tested at approximately 3 weeks, 2 months, and 3 months of age. Adults were tested three times over a period of 3 months. Quantitative analyses include Q‐10, Q‐20, slopes of the high‐ and low‐frequency segments of the tuning curve and tip frequency. Results indicate that cochlear tuning properties in infants approximate those found in adults; however, greater variability is observed for repeated measures of infants STCs. The results are discussed with respect to the development of frequency selectivity. [Work supported by NINCDS.]

Group delay measurement from spiral ganglion cells in the basal turn of the guinea pig cochlea.

Measurements of group delay were made extracellularly from spiral ganglion cells in the 3.7 to 5.0-mm region of the guinea pig cochlea, using sinusoidally amplitude modulated tones with constant modulating frequency (100 Hz) and depth of modulation (0.19). Threshold cochlear tuning was accompanied by frequency-dependent group delays. The group delay on the low-frequency tail was independent of carrier frequency; the interunit variation was 0.28-1.28 ms. The difference in group delay between CF and the low-frequency tail decreased as the CF threshold increased (-0.09 +/- 0.02 ms per 10 dB, beginning at 0.62 +/- 0.07 ms at 0 dB SPL). The group delay decreased above CF; at the units' maximum frequency it was less than the low-frequency tail value, and was sometimes negative. Following arterial injections of furosemide the CF threshold increased and the group delay peak decreased; the low-frequency tail was unaffected. The group delay decreased with increasing intensity; the reduction near and above CF was not only larger than that on the low-frequency tail, but also the change at 5-10 dB above threshold was far greater than expected from the Q10dB of the suprathreshold iso-rate tuning curves. A minimum-phase analysis suggested that the group delay response above CF, together with its nonlinear behavior, can be accounted for by a high-frequency, level-independent, amplitude plateau, in combination with the single unit, amplitude nonlinearity which is known to exist above CF.

Electrophysiological measures of cochlear function in guinea pigs with long-term endolymphatic hydrops.

Experimental endolymphatic hydrops was induced in guinea pigs by obliteration of the endolymphatic sac and duct. From 3 to 24 months after this operation, cochlear action potential (AP) audiograms and AP tuning curves were measured. The purpose of this study was to establish parallels, if any, between this supposed animal model of Menière's disease and the auditory symptoms of the disease in man. In some animals, low and middle frequency AP threshold elevations were observed whilst higher frequency regions maintained normal sensitivity. Other animals developed flat or very gradually sloping AP audiograms. These patterns are qualitatively similar to those found clinically in Menière's disease. AP tuning curves measured in frequency regions of threshold elevation indicated a deterioration of cochlear frequency selectivity; psychophysical and electrocochleographic studies demonstrate related changes in Menière's patients. One animal exhibited modifications in AP thresholds and tuning as a result of glycerol administration. These observations improve our confidence in the validity of this animal model for further studies of the pathophysiology of Menière's disease.

A micromechanical contribution to cochlear tuning and tonotopic organization.

The response properties of hair cells and nerve fibers in the alligator lizard cochlea are frequency selective and tonotopically organized with longitudinal position in the organ. The lengths of the hair-cell hair bundles also vary monotonically with longitudinal position. In this study, quantitative measurements were made of the motion of individual hair bundles in an excised preparation of the cochlea stimulated at auditory frequencies. The angular displacement of hair bundles is frequency selective and tonotopically organized, demonstrating the existence of a micromechanical tuning mechanism.

Group delay measurements from spiral ganglion cells in the guinea pig cochlea.

Measurements of group delay were made extracellularly from spiral ganglion cells in the basal turn of the guinea pig cochlea, using sinusoidally amplitude modulated tones, with constant modulating frequency and modulation depth at the microphone input. Threshold cochlear tuning was accompanied by a frequency dependent group delay, with relative peak proportional to Q10. For sensitive units with steep intensity functions, the group delay decreased with increasing sound pressure level above threshold, without a significant change of Q10.

Animal models of tinnitus.

There are few physiological data available on the origin and nature of tinnitus. It is not even known whether tinnitus associated with cochlear pathology is a manifestation of increased or decreased activity in the cochlear nerve. In previous investigations of cochlear pathology, the spontaneous neural activity has generally been found to be depressed. In the present experiments, an animal model has been established by the administration of sodium salicylate in doses producing blood concentrations that evoke tinnitus in humans. Under these conditions, changes occur in cochlear nerve-fibre thresholds and tuning, similar to those obtained in other types of cochlear pathology. However, under salicylate, the distribution of spontaneous discharge shifts significantly to higher rates than normal. These changes are accompanied in some, but not all, fibres by changes in the temporal patterns of discharge suggestive of excitation. In the second animal model studied, a normal guinea-pig that had a naturally occurring continuous tonal emission, analogous to that recently recorded in human "physiological" tinnitus, was investigated in detail. The emitted signal was recorded in the ear-canal acoustic pressure and in the round-window potential. Several lines of evidence point to the signal as being cochlear in origin, including: its resistance to muscular paralysis and section of the stapedius muscle; the effects of changes in middle-ear pressure; its reversible elimination by hypoxia; and its suppression by tones of higher frequency.

Acoustic correlates of tonal tinnitus.

A sensitive microphone has been developed which can pick up tonal signals (spontaneous acoustic emissions) in the sealed ear-canal of certain subjects. Various properties of these frequency components suggest that they arise from an active, frequency-selective self-limiting feedback process within the cochlea and that they rely on internal reflection from the middle ear. An external tone can synchronize, frequency-lock, suppress of frequency-shift the acoustic component. These interactions are frequency-dependent in a way suggestive of cochlear tuning properties. Positive or negative middle-ear pressure can also influence the components by increasing their frequency and in some cases can enhance one component at the expense of a neighbouring one. Some subjects hear these components as tinnitus and can report on the measured changes. Other subjects do not hear the measured signals, which otherwise behave similarly. A third group of subjects have tinnitus but no objective sound can be detected. In this last group there are, nevertheless, sometimes notches or other discontinuities in the audiogram which correspond to their tinnitus pitch-matches. It appears likely that the recordable type of tinnitus is essentially non-pathological and represents hypersensitivity of the system, whereas the non-recordable type might be associated with local pathological changes at the end-organ or more centrally.