Stimulus-frequency-emission group delay: a test of coherent reflection filtering and a window on cochlear tuning

This paper tests and applies a key prediction of the theory of coherent reflection filtering for the generation of reflection-source otoacoustic emissions. The theory predicts that reflection-source-emission group delay is determined by the group delay of the basilar-membrane (BM) transfer function at its peak. This prediction is tested over a seven-octave frequency range in cats and guinea pigs using measurements of stimulus-frequency-emission (SFOAE) group delay. A comparison with group delays calculated from published measurements of BM mechanical transfer functions supports the theory at the basal end of the cochlea. A comparison across the whole frequency range based on variations in the sharpness of neural tuning with characteristic frequency (CF) suggests that the predicted relation holds in the basal-most 60% of the cochlea. At the apical end of the cochlea, however, the measurements disagree with neural and mechanical group delays. This disagreement suggests that there are important differences in cochlear mechanics and/or mechanisms of emission generation between the base and apex of the cochlea. Measurements in humans over a four-octave range indicate that human SFOAE group delays are roughly a factor of 3 longer than their counterparts in cat and guinea pig but manifest similar trends across CF. The measurements thus reveal global deviations from scaling whose form appears quantitatively similar in all three species. Interpreted using the theory of coherent reflection filtering, the group delay measurements indicate that the wavelength at the peak of the traveling wave decreases with increasing CF at a rate of roughly 25% per octave in the base of the cochlea. The measurements and analysis reported here illustrate the rich potential inherent in OAE measurements for obtaining valuable information about basic cochlear properties such as tuning.     

膜迷路积水对豚鼠听觉外周系统振动特性的影响

为探究梅尼埃病引起的膜迷路积水对豚鼠听觉系统振动特性的作用机制,通过药物注射建立了内耳膜迷路积水豚鼠模型模拟梅尼埃病病理,搭建了多普勒激光测振系统对健康和膜迷路积水豚鼠听觉系统的振动特性进行测试研究,得到了健康与膜迷路积水豚鼠的听觉系统振动特性,并通过对比明确了内耳膜迷路积水对豚鼠听觉系统振动特性的影响。实验结果表明,在测试频率范围内,离体豚鼠镫骨及圆窗膜的振动特性与活体豚鼠无明显差异,离体豚鼠听觉系统振动特性与输入声压无关,镫骨及圆窗膜的振动位移与输入声压具有明显的线性关系。膜迷路积水显著降低了豚鼠听觉系统镫骨及圆窗膜的振动幅度,在低频及高频区间尤为明显,在500 Hz处镫骨最高由11.64 nm降低至2.27 nm,圆窗膜由24.97 nm降低至5.05 nm。在10 kHz处,圆窗膜最高由0.45 nm降低至0.03 nm。同时膜迷路积水导致豚鼠耳蜗传递比普遍下降,最高在1 kHz和10 kHz处分别由2.82,2.91下降至1.46,0.28。      

The application of a capacitive probe technique for direct observation of electromechanical processes in the guinea pig cochlea

The demonstration of evoked mechanical responses of the outer hair cells in the mammalian cochlea by indirect measurements introduces a new range of problems into direct mechanical measurements. Direct and indirect measurements indicate that the frequency spectra of evoked electromechanical responses may extend well into the range of audio frequencies, revealing a need to develop terminology and protocols for distinguishing evoked mechanical responses from the traditional traveling wave when both are apparently superimposed on the motion of the basilar membrane in the normally functioning cochlea. Details are presented of a frequency-modulation capacitive probe technique for measurement of vibrating structures of the guinea pig ear. Considerations include the design of the transducer, calibration, sensitivity, linearity, and sources of noise, as well as the influence of the technique upon the animal preparation, and in particular the issues associated with draining scala tympani for the measurement. Relative advantages and disadvantages of the technique are compared with salient features of other techniques currently available. In view of the apparent complexity of cochlear mechanics some preliminary experiments are required to elucidate some of the key questions about reverse-transduction processes in general. A "simple" first experiment is to test existence of any rectifying or motile response.     

Realistic mechanical tuning in a micromechanical cochlear model

Two assumptions were made in the formulation of a recent cochlear model [P.J. Kolston, J. Acoust. Soc. Am. 83, 1481-1487 (1988)]: (1) The basilar membrane has two radial modes of vibration, corresponding to division into its arcuate and pectinate zones; and (2) the impedance of the outer hair cells (OHCs) greatly modifies the mechanics of the arcuate zone. Both of these assumptions are strongly supported by cochlear anatomy. This paper presents a revised version of the outer hair cell, arcuate-pectinate (OHCAP) model, which is an improvement over the original model in two important ways: First, a model for the OHCs is included so that the OHC impedance is no longer prescribed functionally; and, second, the presence of the OHCs enhances the basilar membrane motion, so that the model is now consistent with observed response changes resulting from trauma. The OHCAP model utilizes the unusual spatial arrangement of the OHCs, the Deiters cells, their phalangeal processes, and the pillars of Corti. The OHCs do not add energy to the cochlear partition and hence the OHCAP model is passive. In spite of the absence of active processes, the model exhibits mechanical tuning very similar to those measured by Sellick et al. [Hear. Res. 10, 93-100 (1983)] in the guinea pig cochlea and by Robles et al. [J. Acoust. Soc. Am. 80, 1364-1374 (1986)] in the chinchilla cochlea. Therefore, it appears that mechanical response tuning and response changes resulting from trauma should not be used as justifications for the hypothesis of active processes in the real cochlea.     

Low-frequency characteristics of human and guinea pig cochleae

Previous physiological studies investigating the transfer of low-frequency sound into the cochlea have been invasive. Predictions about the human cochlea are based on anatomical similarities with animal cochleae but no direct comparison has been possible. This paper presents a noninvasive method of observing low frequency cochlear vibration using distortion product otoacoustic emissions (DPOAE) modulated by low-frequency tones. For various frequencies (15-480 Hz), the level was adjusted to maintain an equal DPOAE-modulation depth, interpreted as a constant basilar membrane displacement amplitude. The resulting modulator level curves from four human ears match equal-loudness contours (ISO226:2003) except for an irregularity consisting of a notch and a peak at 45 Hz and 60 Hz, respectively, suggesting a cochlear resonance. This resonator interacts with the middle ear stiffness. The irregularity separates two regions of the middle ear transfer function in humans: A slope of 12 dB/octave below the irregularity suggests mass-controlled impedance resulting from perilymph movement through the helicotrema; a 6-dB/octave slope above the irregularity suggests resistive cochlear impedance and the existence of a traveling wave. The results from four guinea pig ears showed a 6-dB/octave slope on either side of an irregularity around 120 Hz, and agree with published data.     

Vibration responses of the organ of Corti and the tectorial membrane to electrical stimulation

Coupling of somatic electromechanical force from the outer hair cells (OHCs) into the organ of Corti is investigated by measuring transverse vibration patterns of the organ of Cori and tectorial membrane (TM) in response to intracochlear electrical stimulation. Measurement places at the organ of Corti extend from the inner sulcus cells to Hensen's cells and at the lower (and upper) surface of the TM from the inner sulcus to the OHC region. These locations are in the neighborhood of where electromechanical force is coupled into (1) the mechanoelectrical transducers of the stereocilia and (2) fluids of the organ of Corti. Experiments are conducted in the first, second, and third cochlear turns of an in vitro preparation of the adult guinea pig cochlea. Vibration measurements are made at functionally relevant stimulus frequencies (0.48-68 kHz) and response amplitudes (<15 nm). The experiments provide phase relations between the different structures, which, dependent on frequency range and longitudinal cochlear position, include in-phase transverse motions of the TM, counterphasic transverse motions between the inner hair cell and OHCs, as well as traveling-wave motion of Hensen's cells in the radial direction. Mechanics of sound processing in the cochlea are discussed based on these phase relationships.     

A second,low-frequency mode of vibration in the intact mammalian cochlea

The mammalian cochlea is a structure comprising a number of components connected by elastic elements. A mechanical system of this kind is expected to have multiple normal modes of oscillation and associated resonances. The guinea pig cochlear mechanics was probed using distortion components generated in the cochlea close to the place of overlap between two tones presented simultaneously. Otoacoustic emissions at frequencies of the distortion components were recorded in the ear canal. The phase behavior of the emissions reveals the presence of a nonlinear resonance at a frequency about a half octave below that of the high-frequency primary tone. The location of the resonance is level dependent and the resonance shifts to lower frequencies with increasing stimulus intensity. This resonance is thought to be associated with the tectorial membrane. The resonance tends to minimize input to the cochlear receptor cells at frequencies below the high-frequency primary and increases the dynamic load to the stereocilia of the receptor cells at the primary frequency when the tectorial membrane and reticular lamina move in counterphase.     

What type of force does the cochlear amplifier produce?

Recent experimental measurements suggest that the mechanical displacement of the basilar membrane (BM) near threshold in a viable mammalian cochlea is greater than 10(-8) cm, for a stimulus sound-pressure level at the eardrum of 20 microPa. The associated response peak is very sensitive to the physiological condition of the cochlea. In the formulation of all recent cochlear models, it has been explicitly assumed that this peak is produced by the cochlear amplifier injecting a large amount of energy into the cochlea, thereby altering the real component of the BM impedance. In this paper, a new cochlear model is described which produces a realistic response by assuming that the cochlear amplifier force acts at a phase such that the main effect is to reduce the imaginary component of the BM impedance. In this new model, the magnitude of the cochlear amplifier force required to produce a realistic response is much smaller than in the previous models. It is suggested that future experimental investigations should attempt to determine both the magnitude and the phase of the forces associated with the cochlear amplifier.     

The temporal representation of speech in a nonlinear model of the guinea pig cochlea

The temporal representation of speechlike stimuli in the auditory-nerve output of a guinea pig cochlea model is described. The model consists of a bank of dual resonance nonlinear filters that simulate the vibratory response of the basilar membrane followed by a model of the inner hair cell/auditory nerve complex. The model is evaluated by comparing its output with published physiological auditory nerve data in response to single and double vowels. The evaluation includes analyses of individual fibers, as well as ensemble responses over a wide range of best frequencies. In all cases the model response closely follows the patterns in the physiological data, particularly the tendency for the temporal firing pattern of each fiber to represent the frequency of a nearby formant of the speech sound. In the model this behavior is largely a consequence of filter shapes; nonlinear filtering has only a small contribution at low frequencies. The guinea pig cochlear model produces a useful simulation of the measured physiological response to simple speech sounds and is therefore suitable for use in more advanced applications including attempts to generalize these principles to the response of human auditory system, both normal and impaired.     

Inner hair cell response patterns: implications for low-frequency hearing.

Inner hair cell (IHC) responses to tone-burst stimuli were measured from three locations in the apical half of the guinea pig cochlea. In addition to the measurement of ac receptor potentials, average intracellular voltages, reflecting both ac and dc components of the receptor potential, were computed and compared to determine how bandwidth changes with level. Companion phase measures were also obtained and evaluated. Data collected from turn 2, where best frequency (BF) is approximately 4000 Hz, indicate that frequency response functions are asymmetrical with steeper slopes above the best frequency of the cell. However, in turn 4, where BF is around 250 Hz, the opposite behavior is observed and the steepest slopes are measured below BF. The data imply that cochlear filters are generally asymmetrical with steeper slopes above BF. High-pass filtering by the middle ear serves to reduce this asymmetry in turn 3 and to reverse it in turn 4. Apical response patterns are used to assess the degree to which the middle ear transfer function, the IHC's velocity dependence and the shunting effect of the helicotrema influence low-frequency hearing in guinea pigs. Implications for low-frequency hearing in man are also discussed.     

Longitudinal endolymph movements and endocochlear potential changes induced by stimulation at infrasonic frequencies.

The inner ear is continually exposed to pressure fluctuations in the infrasonic frequency range (< 20 Hz) from external and internal body sources. The cochlea is generally regarded to be insensitive to such stimulation. The effects of stimulation at infrasonic frequencies (0.1 to 10 Hz) on endocochlear potential (EP) and endolymph movements in the guinea pig cochlea were studied. Stimuli were applied directly to the perilymph of scala tympani or scala vestibuli of the cochlea via a fluid-filled pipette. Stimuli, especially those near 1 Hz, elicited large EP changes which under some conditions exceeded 20 mV in amplitude and were equivalent to a cochlear microphonic (CM) response. Accompanying the electrical responses was a cyclical, longitudinal displacement of the endolymph. The amplitude and phase of the CM varied according to which perilymphatic scala the stimuli were applied to and whether a perforation was made in the opposing perilymphatic scala. Spontaneously occurring middle ear muscle contractions were also found to induce EP deflections and longitudinal endolymph movements comparable to those generated by perilymphatic injections. These findings suggest that cochlear fluid movements induced by pressure fluctuations at infrasonic frequencies could play a role in fluid homeostasis in the normal state and in fluid disturbances in pathological states.     

Effect of coiling in a cochlear model

Transformation of the three-dimensional equations of fluid motion into cylindrical coordinates allowed analysis of a coiled cochlear model by the WKB technique. The model includes a single transverse mode of basilar membrane deflection and inviscid fluid. The results calculated using realistic parameters for the guinea pig show no significant difference in the basilar membrane amplitude and phase between the straight and coiled models. Some differences exist in the fluid pressure found in the scala. The conclusion is that the macromechanical response is not significantly affected by coiling.     

Acoustic transfer characteristics in human middle ears studied by a SQUID magnetometer method

The middle-ear transfer characteristics for sound in 14 human temporal bones were determined using a SQUID magnetometer method. With this method, the cochlea and middle ear remain intact. Postmortem changes were studied using a guinea pig. The mass-loading effects of the applied magnets were determined and were found to be negligible. The mean umbo displacement was equal to the mean of six other studies. Lever ratios varied between the individual temporal bones and as a function of frequency.     

Cochlear power flux as an indicator of mechanical activity

The question of whether one can conclude just from basilar membrane (BM) vibration data that the cochlea is an active mechanical system is addressed. To this end, a method is developed which computes the power flux through a channel cross section of a short-wave cochlear model from a given BM vibration pattern. The power flux is an important indicator of mechanical activity because a rise in this function corresponds to creation of mechanical energy. The power flux method is applied to BM velocity patterns as measured by Johnstone and Yates [J. Acoust. Soc. Am. 55, 584-587 (1974)] and by Sellick et al. [Hear. Res. 10, 101-108 (1983)] in the guinea pig and by Robles et al. [Peripheral Auditory Mechanisms, edited by J.B. Allen, J.L. Hall, A.E. Hubbard, S.T. Neely, and A. Tubis (Springer, New York, 1986a), pp. 121-128, and J. Acoust. Soc. Am. 80, 1364-1374 (1986b)] in the chinchilla. Before the calculations are performed, the BM data are interpolated and smoothed in order to avoid numerical errors as a result of too few and noisy data points. The choice of the smoothing method influences the computed power flux function considerably. Nevertheless, the calculations appear to make a clear distinction between the "old" data, showing broad BM tuning (Johnstone and Yates, 1974), and the "new" data, in which the response is much more peaked (Sellick et al., 1983; Robles et al., 1986a, b). The former do not give rise to a significant increase of the power flux; the latter do, although less convincingly for the Sellick et al. (1983) data than for the Robles et al. (1986a,b) data. It is thus concluded that the recently obtained, sharply tuned BM responses reflect the presence of mechanical activity in the cochlea.     

In search of basal distortion product generators

The 2f1-f2 distortion product otoacoustic emission (DPOAE) is thought to arise primarily from the complex interaction of components that come from two different cochlear locations. Such distortion has its origin in the nonlinear interaction on the basilar membrane of the excitation patterns resulting from the two stimulus tones, f1 and f2. Here we examine the spatial extent of initial generation of the 2f1-f2 OAE by acoustically traumatizing the base of the cochlea and so eliminating the contribution of the basal region of the cochlea to the generation of 2f1-f2. Explicitly, amplitude-modulated, or continuously varying in level, stimulus tones with f2/f1= 1.2 and f2 =8000-8940 Hz were used to generate the 2f1-f2 DPOAE in guinea pig before and after acoustically traumatizing the basal region of the cochlea (the origin of any basal-to-f2 distortion product generators). It was found, based on correlation analysis, that there does not appear to be a basal-to-f2 distortion product generation mechanism contributing significantly to the guinea pig 2f1-f2 OAE up to L1 = 80 dB sound pressure level (SPL).     

The mechanical waveform of the basilar membrane. IV. Tone and noise stimuli

Analysis of mechanical cochlear responses to wide bands of random noise clarifies many effects of cochlear nonlinearity. The previous paper [de Boer and Nuttall, J. Acoust. Soc. Am. 107, 1497-1507 (2000)] illustrates how closely results of computations in a nonlinear cochlear model agree with responses from physiological experiments. In the present paper results for tone stimuli are reported. It was found that the measured frequency response for pure tones differs little from the frequency response associated with a noise signal. For strong stimuli, well into the nonlinear region, tones have to be presented at a specific level with respect to the noise for this to be true. In this report the nonlinear cochlear model originally developed for noise analysis was modified to accommodate pure tones. For this purpose the efficiency with which outer hair cells modify the basilar-membrane response was made into a function of cochlear location based on local excitation. For each experiment, the modified model is able to account for the experimental findings, within 1 or 2 dB. Therefore, the model explains why the type of filtering that tones undergo in the cochlea is essentially the same as that for noise signals (provided the tones are presented at the appropriate level).     

Auditory physics. Physical principles in hearing theory. II

In the first part of this series of papers [Phys. Reports 62 (1980) 87–174] several physical problems are described that are relevant for the study of the auditory system. The present paper extends this treatment, it describes more facts upon which auditory theory is to be based and it delves considerably deeper into the mechanics of the cochlea (inner ear). The first two chapters treat nonlinear phenomena that are found in physiological and mechanical responses of the cochlea and in psychophysical experiments (listening tests carried out in human subjects). The main part of the paper is devoted to the mechanics of the cochlea. This part is preceded by an overview of the results of mechanical measurements on the cochlea. As it turns out, the newest experimental data present a specific challenge for cochlear mechanics.The central three chapters of the paper describe the development of a linear three-dimensional model of the cochlea. The main intention is to describe this model in a step-by-step fashion (hence the chapter headings borrowed from the field of architecture). Even in this simplified case, the solution for the response of the cochlear model is far from easy. Therefore, a few excursions are made into fields of physics and engineering in which related problems are worked out in analytical form. Just as in Part I of this series of papers, this extended treatment considerably deepens insight into the physical factors involved. Confrontation of the requirements for modelling described in the first few chapters with what has been achieved in the final part reveals how much study in the field of auditory physics remains to be done.     

Using acoustic distortion products to measure the cochlear amplifier gain on the basilar membrane.

Most models of the cochlea developed during the last decade have explained frequency selectivity and sensitivity of the cochlea at threshold by the use of power amplification of the acoustic wave on the basilar membrane. This power amplification has been referred to as the cochlear amplifier (CA). In this paper, a method to measure the cochlear amplifier gain as a function of position along the basilar membrane is derived from a simple model. Next, experimental evidence is presented that strongly restricts the properties of these proposed cochlear amplifier models. Specifically, it is shown that small signals generated by mechanical nonlinearities in the basilar membrane motion are not amplified during basilar membrane propagation, contrary to what would be expected from the cochlear amplifier hypotheses. This paper describes a method of measuring the cochlear power gain as a function of frequency and position, from the stapes to within 2 mm of the place corresponding to the frequency being measured. Experimental results in the cat indicate that the total gain of the cochlear amplifier, over the range of positions measured, must be less than 10 dB. The simplest interpretation of the experimental results is that there is no cochlear amplifier. The results suggest that the cochlea must achieve its frequency selectivity by some other means.     

Laser amplification with a twist: traveling-wave propagation and gain functions from throughout the cochlea

Except at the handful of sites explored by the inverse method, the characteristics-indeed, the very existence-of traveling-wave amplification in the mammalian cochlea remain largely unknown. Uncertainties are especially pronounced in the apex, where mechanical and electrical measurements lack the independent controls necessary for assessing damage to the preparation. At a functional level, the form and amplification of cochlear traveling waves are described by quantities known as propagation and gain functions. A method for deriving propagation and gain functions from basilar-membrane mechanical transfer functions is presented and validated by response reconstruction. Empirical propagation and gain functions from locations throughout the cochlea are obtained in mechanically undamaged preparations by applying the method to published estimates of near-threshold basilar membrane responses derived from Wiener-kernel (chinchilla) and zwuis analysis (cat) of auditory-nerve responses to broadband stimuli. The properties of these functions, and their variation along the length of the cochlea, are described. In both species, and at all locations examined, the gain functions reveal a region of positive power gain basal to the wave peak. The results establish the existence of traveling-wave amplification throughout the cochlea, including the apex. The derived propagation and gain functions resemble those characteristic of an active optical medium but rotated by 90 degrees in the complex plane. Rotation of the propagation and gain functions enables the mammalian cochlea to operate as a wideband, hydromechanical laser analyzer.     

A nonlinear filter-bank model of the guinea-pig cochlear nerve: rate responses

The aim of this study is to produce a functional model of the auditory nerve (AN) response of the guinea-pig that reproduces a wide range of important responses to auditory stimulation. The model is intended for use as an input to larger scale models of auditory processing in the brain-stem. A dual-resonance nonlinear filter architecture is used to reproduce the mechanical tuning of the cochlea. Transduction to the activity on the AN is accomplished with a recently proposed model of the inner-hair-cell. Together, these models have been shown to be able to reproduce the response of high-, medium-, and low-spontaneous rate fibers from the guinea-pig AN at high best frequencies (BFs). In this study we generate parameters that allow us to fit the AN model to data from a wide range of BFs. By varying the characteristics of the mechanical filtering as a function of the BF it was possible to reproduce the BF dependence of frequency-threshold tuning curves, AN rate-intensity functions at and away from BF, compression of the basilar membrane at BF as inferred from AN responses, and AN iso-intensity functions. The model is a convenient computational tool for the simulation of the range of nonlinear tuning and rate-responses found across the length of the guinea-pig cochlear nerve.