The Sharpening of cochlear frequency selectivity in the normal and abnormal cochlea

In the normal (anaesthetized) animal cochlea, the frequency threshold curves for single primary fibres are up to an order of magnitude sharper than the analogous functions derived from various reported measurements of the basilar membrane amplitude of vibration. This enhanced neural frequency selectivity is found in the same species and under conditions similar to those in which the mechanical measurements are taken. The sharpening process (at least near threshold) appears to be linear and is not dependent upon lateral inhibitory mechanisms. The variability of the neural frequency selectivity and its vulnerability to metabolic, chemical and pathological influences suggests the hypothesis that the sharpening is due to some form of ‘second filter’ subsequent to the relatively broadly tuned basilar membrane.

All fibres recorded from in the cochlear nerve in the normal cochlea show this enhanced frequency selectivity; in contrast, in pathological cochleas, all fibres, or a substantial proportion, have high-threshold, broadly tuned characteristics, approximating to those of the basilar membrane.

The frequency selectivity of normal cochlear fibres is adequate to account for the analogous psychophysical measures of hearing. It is proposed that loss of this normal frequency selectivity occurs in deafness of cochlear origin, accounting for widening of the critical band. A new hypothesis for recruitment is proposed on this basis.

Finally, invetigations of the cochlear nerve fibre frequency responses under conditions of hypoxia give grounds for the speculation that more than one mechanism is involved in the excitation of a single fibre, related to the separate functioning of the inner and outer hair cells.     

A possibility of sharp tuning in a linear transversally inhomogeneous cochlear model

Considerable sharpening of basilar membrane frequency selectivity and simultaneous decreasing of phase lag can be obtained in a linear ('passive') hydromechanical three-dimensional cochlear model, if the transverse geometry of the cochlea is taken into account. Both the tuning qualities, Q10, and the phase angles at CF of some transversally inhomogeneous linear models can be set into the range of experimental data [Sellick et al. (1983) Hear. Res. 10, 93-108; Robles et al. (1986) J. Acoust. Soc. Am. 80, 1364-1379.] The calculations are developed on the base of WKB-approximation. The integral coefficients of eiconal equation are the transversally averaged means of basilar membrane surface mass density and stiffness: (formula; see text) where eta(y) is the major eigenfunction of basilar membrane cross-sectional vibrations. The classical Ritz's method is used for calculation of the cross-sectional eigenfunctions. The size and the form of cochlear cross-section are found also to alter the tuning. The rapid increase of the model response towards the peak is due to that damping remains negligible up to the peak position, where the imaginery part of the wave-number begins to increase sharply.     

Narrow-band action potentials of the guinea-pig cochlea as compared with the ordinary electrocochleograms under normal and pathological conditions

The narrow-band action potentials (NAP) and the ordinary electrocochleograms were recorded from the guinea-pig cochlea under normal and pathological conditions in order to study whether the NAP could be a useful measure to detect cochlear dysfunctions. The cochlea damaged either by the administration of kanamycin or by a mechanical lesion of the round window served as pathological materials. Recordings showed that the threshold and amplitude measured for the N1 potential of NAPs ran in parallel with those of the cochlear microphonic potentials (CM), under both normal and pathological conditions of the cochlea. This implies that the CM could be replaced by the NAP when difficulties were present in recording CMs. It may be inferred that the NAP reflects responses of the inner hair-cells and cochlear nerves, while the CM would mainly be derived from responses of the outer hair-cells to the frequency-specific movements of the basilar membrane. If so, the NAP should offer a good means for the objective audiometry. Recording NAPs is also superior to the ordinary electrocochleography in that the method makes it possible to obtain responses generated near the apex of the cochlea, i.e., responses to low-pitch sound stimuli.     

Measurement of basilar membrane vibrations and evaluation of the cochlear condition

The experimental procedure for measuring basilar membrane responses to acoustic signals is described. The surgical procedure developed for opening the cochlea with minimal trauma is presented. Each experiment included sound pressure level measurements to define the input signal, cochlear microphonic (CM) measurements to monitor the cochlear condition, interferometric measurements and histological evaluation of the cochleas. The characteristic frequency (CF) and the sensitivity at CF for the basilar membrane response is correlated with the change of CM response observed in six animals. It is demonstrated that both tuning characteristics are extremely sensitive to cochlear trauma as evidenced by changes of CM.     

Functional role of the olivo-cochlear bundle: a motor unit control system in the mammalian cochlea

A fiber optic lever is applied to the measurement of the motion of the basilar membrane motion in guinea pigs. In response to intense tones from either ear, the motion includes a substantial summating shift in the mean position in addition to a travelling wave originally described by von Békésy. His stroboscopic technique and most techniques used since have been concentrated upon measuring vibrations of the basilar membrane synchronous with the stimulus and have been insensitive to variations in the baseline position such as a summating component of motion analogous to the extracellular summating potential. In addition to the role of the outer hair cells in providing normal hearing sensitivity, they evidently play a role in regulating the mean position of the basilar membrane. For a fixed frequency, the polarity of the mean position varies systematically with sound level and place and summates with time since onset. Since these cells are the target cells for the olivocochlear bundle, homeostasis in the cochlea would appear to be linked efferent function and involve cochlear mechanics. The negative damping hypothesis asserts that hair cell activity is necessary for low thresholds. The results presented here demonstrate that OHC activity exists independent of neural thresholds. The discussion develops the concept that threshold losses are due to a mismatch of opposing tonic forces which normally maintain the mean position of the basilar membrane. Structure is examined in relation to function and the group of outer hair cells innervated by a single medial efferent neuron is identified as a motor unit. Implications of central control of individual motor units include peripheral involvement in selective attention tasks.     

Recent developments in cochlear physiology

Recent findings in cochlear physiology have caused many of our long held ideas about how sound is analyzed by the ear to be reevaluated. This article describes changes which have occurred in three classical ideas of cochlear transduction: (1) There is a gradient of frequency representation along the cochlea with high frequencies being represented at the base and lower frequencies represented progressively toward the apex. It is now known that the specific frequency which is represented at a given location along the cochlea is not invariant but changes systematically during the normal development of hearing. (2) The place code and frequency tuning along the cochlea are due to the conventional traveling wave of von Békésy and basilar membrane mechanics. Experiments in nonmammalian vertebrates which lack a traveling wave have shown that other mechanisms, including the mechanical resonance of hair cell stereocilia, may contribute to tonotopic organization and frequency tuning. It is possible that hair cell stereocilia also contribute to frequency representation and tuning in the mammalian cochlea. (3) The vibration of the basilar membrane to sound is determined by its passive mechanical properties. It is now known that the response of the basilar membrane, and that of the cochlear partition as a whole, is influenced by physiological processes which utilize metabolic energy. The active processes are likely expressed through the motile activity of outer hair cells.     

Reverse correlation study of cochlear filtering in normal and pathological guinea pig ears

The filtering properties of single cochlear fibres have been determined in normal and kanamycin-treated guinea pigs using the reverse correlation technique. This method allows investigation of filtering over a wide dynamic range.For normal guinea pig fibres, the near threshold filter functions obtained with this, method correspond to the tone derived frequency threshold curves (FTCs). The 10 dB bandwidth of the filter functions increased monotonically with increasing noise levels above threshold. Thus with noise levels at approximately 50 dB above threshold, the 10 dB bandwidth had increased by a factor of 1.3–3. The changes in 3 dB bandwidth with increasing levels were, for some fibres, different from those of the 10 dB bandwidths.For the pathological fibres, the derived filter functions corresponded to their tone determined FTCs, and were therefore comparatively broadly tuned. Their tuning (O_10dB) approximated to those of normal fibres when the latter were measured 60 dB or more above threshold (i.e., at similar levels of stimulus), and did not increase further with increase in level.The findings in the normal guinea pig are consistent with those obtained by others in rodents, but are not consistent with those from the cat, where normal filtering is more robust to high levels of stimulus noise.     

Implications from cochlear implant insertion for cochlear mechanics

It is usually thought that the displacements of the two inner ear windows induced by sound stimuli lead to pressure differences across the basilar membrane and to a passive mechanical traveling wave progressing along the membrane. However, opening a hole in the sealed inner ear wall in experimental animals is surprisingly not accompanied by auditory threshold elevations. It has also been shown that even in patients undergoing cochlear implantation, elevation of threshold to low-frequency acoustic stimulation is often not seen accompanying the making of a hole in the wall of the cochlea for insertion of the implant. Such threshold elevations would be expected to result from opening the cochlea, reducing cochlear impedance, altering hydrodynamics. These considerations can be taken as additional evidence that it may not be the passive basilar membrane traveling wave which elicits hearing at low sound intensities, but rather factors connected with cochlear fluid pressures and fluid mechanics.     

Some current concepts of cochlear mechanics

The development of the current concepts is reviewed in historical perspective. Helmholtz's hypothesis of basilar-membrane resonance was partially confirmed and partially defeated by Békésy's experiments on models and postmortem cochlear preparations. He discovered that sound was propagated in the cochlea in the form of traveling waves which reached a flat maximum at a frequency-dependent location. Mathematical theory explained this type of sound propagation as a special case of surface waves. Johnstone and his coworkers discovered that the maximum of cochlear vibration in living animals was much sharper than postmortem, and more recently Khanna and Johnstone independently determined the maximum to be nearly as sharp as the tuning curves of the inner hair cells and the auditory-nerve fibers. These findings, together with the work at the Massachusetts Institute of Technology on alligator lizards, have led to new concepts of cochlear mechanics which include hypothesized micromechanical processes in the organ of Corti. These concepts deal not only with the sharpness of basilar-membrane tuning but also with the details of the basilar-membrane amplitude and phase characteristics, as well as with the hair cell and neural tuning curves and response phases. They suggest that some sharpening of the tuning curves occurs between the basilar membrane and hair-cell responses. Such sharpening has been demonstrated in lizards, but in the mammalian ear, the relation is less clear.     

Modulation of responses of spiral ganglion cells in the guinea pig cochlea by low frequency sound

Period histograms were generated from single unit data obtained from the spiral ganglion of the first turn of the guinea pig cochlea in response to continuous tones between 40 and 500 Hz. With the lowest intensities used, spontaneous activity was suppressed during basilar membrane displacement (inferred from cochlear microphonic phase) towards scala vestibuli and activity was enhanced during displacement towards scala tympani. At higher intensities the response changed to excitation during maximal basilar membrane velocity towards scala vestibuli. These patterns were delayed by about 0.5 ms producing large phase delays at the higher frequencies. We postulate that the displacement response is produced by cochlear microphonic originating from the outer hair cells acting on the inner hair cell membrane. In contrast, the velocity response is produced by the inner hair cell receptor potential. The effect of a 40 Hz tone on activity evoked by tones above, at, and below the characteristic frequency was investigated by generating period histograms synchronous with the 40 Hz tone. We found that activity evoked by tones around the characteristic frequency of the cell was suppressed during displacement of the basilar membrane towards scala tympani and enhanced in the opposite direction at 40 Hz intensities that had no effect on spontaneous activity. Further increase in the 40 Hz intensity produced suppression during scala vestibuli displacement with activity remaining only during the zero crossings. Still further increase produces the 40 Hz tone alone response. Activity evoked by tones in the low frequency ‘tails’ of the frequency threshold curve was not similarly modulated. This phenomenon is thought to be related to basilar membrane nonlinearity for frequencies close to the cut-off. Investigation of the effect of a 40 Hz tone on the threshold of the compound action potential confirmed data obtained from single units.     

Cochlear model with three-dimensional fluid, inner sulcus and feed-forward mechanism

A three-dimensional model of the guinea pig cochlea using the phase-integral method is presented. This model incorporates the viscous fluid effects in the cochlea, dimensional and material property variation along the cochlear duct and the active feed-forward mechanism of the outer hair cells. Two degrees of freedom of the basilar membrane are considered, which results in two traveling waves propagating along the duct for a given frequency. Basilar membrane response with the active feed-forward mechanism compares favorably with published experimental measurements.     

The consequences of neural degeneration regarding optimal cochlear implant position in scala tympani: a model approach

Cochlear implant research endeavors to optimize the spatial selectivity, threshold and dynamic range with the objective of improving the speech perception performance of the implant user. One of the ways to achieve some of these goals is by electrode design. New cochlear implant electrode designs strive to bring the electrode contacts into close proximity to the nerve fibers in the modiolus: this is done by placing the contacts on the medial side of the array and positioning the implant against the medial wall of scala tympani. The question remains whether this is the optimal position for a cochlea with intact neural fibers and, if so, whether it is also true for a cochlea with degenerated neural fibers. In this study a computational model of the implanted human cochlea is used to investigate the optimal position of the array with respect to threshold, dynamic range and spatial selectivity for a cochlea with intact nerve fibers and for degenerated nerve fibers. In addition, the model is used to evaluate the predictive value of eCAP measurements for obtaining peri-operative information on the neural status. The model predicts improved threshold, dynamic range and spatial selectivity for the peri-modiolar position at the basal end of the cochlea, with minimal influence of neural degeneration. At the apical end of the array (1.5 cochlear turns), the dynamic range and the spatial selectivity are limited due to the occurrence of cross-turn stimulation, with the exception of the condition without neural degeneration and with the electrode array along the lateral wall of scala tympani. The eCAP simulations indicate that a large P(0) peak occurs before the N(1)P(1) complex when the fibers are not degenerated. The absence of this peak might be used as an indicator for neural degeneration.     

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.     

Effect of modulation of basilar membrane position on the cochlear microphonic

Certain characteristics of the extracellular cochlear microphonic (CM) recorded by intracochlear electrodes change in a bimodal manner as a function of prior acoustic exposure, intensity of stimulation, or stimulus frequency. In the present study, it as shown that blasing the basilar membrane position toward scala tympani serves to enhance the CM amplitude when the cochlea is unfatigued, when low-intensity stimuli are used, or when frequencies below the best frequency of a differential electrode pair are used. Conversely, after acoustic fatigue, or during high-intensity or high-frequency stimulation, the microphonic potential is enhanced by a movement of the basilar membrane toward the scala vestibuli. The two populations of hair cells, whose responses are enhanced and diminished on opposing positions of the basilar membrane, are probably outer and inner hair cells.     

A simple model of cochlear micromechanics in the mammal and lizard

A model is presented which is a simple representation of cochlear micromechanics in the lizard and mammal. The model is a linear, time-invariant mechanical system, consisting of two coupled mechanical filters. It is capable of a sharply tuned first and second filter, consistent with the sharply tuned basilar membrane and auditory nerve fibers in the mammal. When parameters are adjusted for the alligator lizard (Gerrhonotus multicarinatus), the model generates a sharply tuned second filter without a sharply tuned first filter. In the alligator lizard, the auditory nerve fibers are sharply tuned but the basilar membrane is not. The model supports the hypothesis that cochlear transduction is not fundamentally different in the mammal and the alligator lizard.     

A Simple Model of Cochlear Micromechanics in the Mammal and Lizard

A model is presented which is a simple representation of cochlear micromechanics in the lizard and mammal. The model is a linear, time-invariant mechanical system, consisting of two coupled mechanical filters. It is capable of a sharply tuned first and second filter, consistent with the sharply tuned basilar membrane and auditory nerve fibers in the mammal. When parameters are adjusted for the alligator lizard (Gerrhonotus multicarinatus), the model generates a sharply tuned second filter without a sharply tuned first filter. In the alligator lizard, the auditory nerve fibers are sharply tuned but the basilar membrane is not. The model supports the hypothesis that cochlear transduction is not fundamentally different in the mammal and the alligator lizard.     

Some Current Concepts of Cochlear Mechanics

The development of the current concepts is reviewed in historical perspective. Helmholtz's hypothesis of basilar-membrane resonance was partially confirmed and partially defeated by Békésy's experiments on models and postmortem cochlear preparations. He discovered that sound was propagated in the cochlea in the form of traveling waves which reached a flat maximum at a frequency-dependent location. Mathematical theory explained this type of sound propagation as a special case of surface waves. Johnstone and his coworkers discovered that the maximum of cochlear vibration in living animals was much sharper than postmortem, and more recently Khanna and Johnstone independently determined the maximum to be nearly as sharp as the tuning curves of the inner hair cells and the auditory-nerve fibers. These findings, together with the work at the Massachusetts Institute of Technology on alligator lizards, have led to new concepts of cochlear mechanics which include hypothesized micromechanical processes in the organ of Corti. These concepts deal not only with the sharpness of basilar-membrane tuning but also with the details of the basilar-membrane amplitude and phase characteristics, as well as with the hair cell and neural tuning curves and response phases. They suggest that some sharpening of the tuning curves occurs between the basilar membrane and hair-cell responses. Such sharpening has been demonstrated in lizards, but in the mammalian ear, the relation is less clear.     

Cochlear compression: perceptual measures and implications for normal and impaired hearing

This article provides a review of recent developments in our understanding of how cochlear nonlinearity affects sound perception and how a loss of the nonlinearity associated with cochlear hearing impairment changes the way sounds are perceived. The response of the healthy mammalian basilar membrane (BM) to sound is sharply tuned, highly nonlinear, and compressive. Damage to the outer hair cells (OHCs) results in changes to all three attributes: in the case of total OHC loss, the response of the BM becomes broadly tuned and linear. Many of the differences in auditory perception and performance between normal-hearing and hearing-impaired listeners can be explained in terms of these changes in BM response. Effects that can be accounted for in this way include poorer audiometric thresholds, loudness recruitment, reduced frequency selectivity, and changes in apparent temporal processing. All these effects can influence the ability of hearing-impaired listeners to perceive speech, especially in complex acoustic backgrounds. A number of behavioral methods have been proposed to estimate cochlear nonlinearity in individual listeners. By separating the effects of cochlear nonlinearity from other aspects of hearing impairment, such methods may contribute towards identifying the different physiological mechanisms responsible for hearing loss in individual patients. This in turn may lead to more accurate diagnoses and more effective hearing-aid fitting for individual patients. A remaining challenge is to devise a behavioral measure that is sufficiently accurate and efficient to be used in a clinical setting.     

Spatial Tuning Curves Along the Chick Basilar Papilla in Normal and Sound-Exposed Ears

Intense sound exposure destroys chick short hair cells and damages the tectorial membrane. Within a few days postexposure, signs of repair appear resulting in nearly complete structural recovery of the inner ear. Tectorial membrane repair, however, is incomplete, leaving a permanent defect on the sensory surface. The consequences of this defect on cochlear function, and particularly frequency analysis, are unclear. The present study organizes the sound-induced discharge activity of cochlear nerve units to describe the distribution of neural activity along the tonotopic axis of the basilar papilla. The distribution of this activity is compared in 12-day postexposed and age-matched control groups. Spontaneous activity, tuning curves, and rate–intensity functions were measured in each unit. Discharge activity at 60 frequency and intensity combinations was identified in the tuning curves of hundreds of units. Activity at each of these criterion frequency/intensity combinations was plotted against the units characteristic frequency to construct spatial tuning curves (STCs). The STCs depict tone-driven cochlear nerve activity along the length of the papilla. Tuning sharpness, low- and high- frequency slopes, and the maximum response were quantified for each STC. The sharpness of tuning increased with increasing criterion frequency. However, within a frequency, increasing sound intensity yielded more broadly tuned STCs. Also, the high-frequency slope was consistently steeper than the low-frequency slope. The STCs of exposed ears exhibited slightly less frequency selectivity than control ears across all frequencies and larger maximum responses for STCs with criterion frequencies spanning the tectorial membrane defect. When rate–intensity types were segregated, differences were observed in the STCs between saturating and sloping-up units. We propose that STC shape may be determined by global mechanical events, as well as localized tuning and nonlinear processes associated with individual hair cells. The results indicated that 12 days after intense sound exposure, global and local contributions to spatially distributed neural activity are restored.