Medial olivocochlear efferent inhibition of basilar-membrane responses to clicks: evidence for two modes of cochlear mechanical excitation

Conceptualizations of mammalian cochlear mechanics are based on basilar-membrane (BM) traveling waves that scale with frequency along the length of the cochlea, are amplified by outer hair cells (OHCs), and excite inner hair cells and auditory-nerve (AN) fibers in a simple way. However, recent experimental work has shown medial-olivocochlear (MOC) inhibition of AN responses to clicks that do not fit with this picture. To test whether this AN-initial-peak (ANIP) inhibition might result from hitherto unrecognized aspects of the traveling-wave or MOC-evoked inhibition, MOC effects on BM responses to clicks in the basal turns of guinea pig and chinchilla cochleae were measured. MOC stimulation inhibited BM click responses in a time and level dependent manner. Inhibition was not seen during the first half-cycle of the responses, but built up gradually, and ultimately increased the responses' decay rates. MOC stimulation also produced small phase leads in the response wave forms, but had little effect on the instantaneous frequency or the waxing and waning of the responses. These data, plus recent AN data, support the hypothesis that the MOC-evoked inhibitions of the traveling wave and of the ANIP response are separate phenomena, and indicate that the OHCs can affect at least two separate modes of excitation in the mammalian cochlea.     

Time-frequency analysis of auditory-nerve-fiber and basilar-membrane click responses reveal glide irregularities and non-characteristic-frequency skirts

Although many properties of click responses can be accounted for by a single, frequency-dispersive traveling wave exciting a single, characteristic-frequency (CF) resonance, some properties, such as waxing and waning cannot. Joint time-frequency distributions (TFDs) were used to help understand click responses of cat single auditory-nerve (AN) fibers (CFs<4 kHz) and published measurements of chinchilla basilar-membrane (BM) motion. For CFs> 800 Hz, the peak energy of the response decreased in latency and frequency as the level increased, as expected. However, at high levels the trend reversed for AN, but not BM, responses. Normalized TFDs, which show the frequency with the peak energy at each response time, revealed glides, as previously reported. Classical theory predicts smooth, upward glides. Instead, at low CFs there were downward glides, and at other CFs glides had substantial irregularities. Finally, click skirts, defined as the longest-latency part of click responses, sometimes showed deviations from CF for above-threshold sound levels. Most of these phenomena are not explained by a single, frequency-dispersive traveling wave exciting a single CF resonance, but they can be accounted for by the interaction of two (or more) excitation drives with different latencies and frequency contents.     

Vowel enhancement effects in cochlear-implant users

Auditory enhancement of certain frequencies can occur through prior stimulation of surrounding frequency regions. The underlying neural mechanisms are unknown, but may involve stimulus-driven changes in cochlear gain via the medial olivocochlear complex (MOC) efferents. Cochlear implants (CIs) bypass the cochlea and stimulate the auditory nerve directly. If the MOC plays a critical role in enhancement then CI users should not exhibit this effect. Results using vowel stimuli, with and without preceding sounds designed to enhance formants, provided evidence of auditory enhancement in both normal-hearing listeners and CI users, suggesting that vowel enhancement is not mediated solely by cochlear effects.     

Medial efferent effects on auditory-nerve responses to tail-frequency tones. I. Rate reduction.

One way medial efferents are thought to inhibit responses of auditory-nerve fibers (ANFs) is by reducing the gain of the cochlear amplifier thereby reducing motion of the basilar membrane. If this is the only mechanism of medial efferent inhibition, then medial efferents would not be expected to inhibit responses where the cochlear amplifier has little effect, i.e., at sound frequencies in the tails of tuning curves. Inhibition at tail frequencies was tested for by obtaining randomized rate-level functions from cat ANFs with high characteristic frequencies (CF > or = 5 kHz), stimulated with tones two or more octaves below CF. It was found that electrical stimulation of medial efferents can indeed inhibit ANF responses to tail-frequency tones. The amplitude of efferent inhibition depended on both sound level (largest near to threshold) and frequency (largest two to three octaves below CF). On average, inhibition of high-CF ANFs responding to 1 kHz tones was around 5 dB. Although an efferent reduction of basilar-membrane motion cannot be ruled out as the mechanism producing the inhibition of ANF responses to tail frequency tones, it seems more likely that efferents produce this effect by changing the micromechanics of the cochlear partition.     

Dual traveling waves in an inner ear model with two degrees of freedom

We calculate traveling waves in the mammalian cochlea, which transduces acoustic vibrations into neural signals. We use a WKB-based mechanical model with both the tectorial membrane (TM) and basilar membrane (BM) coupled to the fluid to calculate motions along the length of the cochlea. This approach generates two wave numbers that manifest as traveling waves with different modes of motion between the BM and TM. The waves add differently on each mass, producing distinct tuning curves and different characteristic frequencies (CFs) for the TM and the BM. We discuss the effect of TM stiffness and coupling on the waves and tuning curves. We also consider how the differential motions between the masses could influence the cochlear amplifier and how mode conversion could take place in the cochlea.     

Auditory steady-state responses to chirp stimuli based on cochlear traveling wave delay

This study investigates the use of chirp stimuli to compensate for the cochlear traveling wave delay. The temporal dispersion in the cochlea is given by the traveling time, which in this study is estimated from latency-frequency functions obtained from (1) a cochlear model, (2) tone-burst auditory brain stem response (ABR) latencies, (3) and narrow-band ABR latencies. These latency-frequency functions are assumed to reflect the group delay of a linear system that modifies the phase spectrum of the applied stimulus. On the basis of this assumption, three chirps are constructed and evaluated in 49 normal-hearing subjects. The auditory steady-state responses to these chirps and to a click stimulus are compared at two levels of stimulation (30 and 50 dB nHL) and a rate of 90s. The chirps give shorter detection time and higher signal-to-noise ratio than the click. The shorter detection time obtained by the chirps is equivalent to an increase in stimulus level of 20 dB or more. The results indicate that a chirp is a more efficient stimulus than a click for the recording of early auditory evoked responses in normal-hearing adults using transient sounds at a high rate of stimulation.     

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.     

Rate and timing cues associated with the cochlear amplifier: level discrimination based on monaural cross-frequency coincidence detection.

The perceptual significance of the cochlear amplifier was evaluated by predicting level-discrimination performance based on stochastic auditory-nerve (AN) activity. Performance was calculated for three models of processing: the optimal all-information processor (based on discharge times), the optimal rate-place processor (based on discharge counts), and a monaural coincidence-based processor that uses a non-optimal combination of rate and temporal information. An analytical AN model included compressive magnitude and level-dependent-phase responses associated with the cochlear amplifier, and high-, medium-, and low-spontaneous-rate (SR) fibers with characteristic frequencies (CFs) spanning the AN population. The relative contributions of nonlinear magnitude and nonlinear phase responses to level encoding were compared by using four versions of the model, which included and excluded the nonlinear gain and phase responses in all possible combinations. Nonlinear basilar-membrane (BM) phase responses are robustly encoded in near-CF AN fibers at low frequencies. Strongly compressive BM responses at high frequencies near CF interact with the high thresholds of low-SR AN fibers to produce large dynamic ranges. Coincidence performance based on a narrow range of AN CFs was robust across a wide dynamic range at both low and high frequencies, and matched human performance levels. Coincidence performance based on all CFs demonstrated the "near-miss" to Weber's law at low frequencies and the high-frequency "mid-level bump." Monaural coincidence detection is a physiologically realistic mechanism that is extremely general in that it can utilize AN information (average-rate, synchrony, and nonlinear-phase cues) from all SR groups.     

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.     

One source for distortion product otoacoustic emissions generated by low- and high-level primaries

Distortion product otoacoustic emissions (DPOAE) elicited by tones below 60-70 dB sound pressure level (SPL) are significantly more sensitive to cochlear insults. The vulnerable, low-level DPOAE have been associated with the postulated active cochlear process, whereas the relatively robust high-level DPOAE component has been attributed to the passive, nonlinear macromechanical properties of the cochlea. However, it is proposed that the differences in the vulnerability of DPOAEs to high and low SPLs is a natural consequence of the way the cochlea responds to high and low SPLs. An active process boosts the basilar membrane (BM) vibrations, which are attenuated when the active process is impaired. However, at high SPLs the contribution of the active process to BM vibration is small compared with the dominating passive mechanical properties of the BM. Consequently, reduction of active cochlear amplification will have greatest effect on BM vibrations and DPOAEs at low SPLs. To distinguish between the "two sources" and the "single source" hypotheses we analyzed the level dependence of the notch and corresponding phase discontinuity in plots of DPOAE magnitude and phase as functions of the level of the primaries. In experiments where furosemide was used to reduce cochlear amplification, an upward shift of the notch supports the conclusion that both the low- and high-level DPOAEs are generated by a single source, namely a nonlinear amplifier with saturating I/O characteristic.     

Testing coherent reflection in chinchilla: Auditory-nerve responses predict stimulus-frequency emissions

Coherent-reflection theory explains the generation of stimulus-frequency and transient-evoked otoacoustic emissions by showing how they emerge from the coherent "backscattering" of forward-traveling waves by mechanical irregularities in the cochlear partition. Recent published measurements of stimulus-frequency otoacoustic emissions (SFOAEs) and estimates of near-threshold basilar-membrane (BM) responses derived from Wiener-kernel analysis of auditory-nerve responses allow for comprehensive tests of the theory in chinchilla. Model predictions are based on (1) an approximate analytic expression for the SFOAE signal in terms of the BM traveling wave and its complex wave number, (2) an inversion procedure that derives the wave number from BM traveling waves, and (3) estimates of BM traveling waves obtained from the Wiener-kernel data and local scaling assumptions. At frequencies above 4 kHz, predicted median SFOAE phase-gradient delays and the general shapes of SFOAE magnitude-versus-frequency curves are in excellent agreement with the measurements. At frequencies below 4 kHz, both the magnitude and the phase of chinchilla SFOAEs show strong evidence of interference between short- and long-latency components. Approximate unmixing of these components, and association of the long-latency component with the predicted SFOAE, yields close agreement throughout the cochlea. Possible candidates for the short-latency SFOAE component, including wave-fixed distortion, are considered. Both empirical and predicted delay ratios (long-latency SFOAE delay/BM delay) are significantly less than 2 but greater than 1. Although these delay ratios contradict models in which SFOAE generators couple primarily into cochlear compression waves, they are consistent with the notion that forward and reverse energy propagation in the cochlea occurs predominantly by means of traveling pressure-difference waves. The compelling overall agreement between measured and predicted delays suggests that the coherent-reflection model captures the dominant mechanisms responsible for the generation of reflection-source otoacoustic emissions.     

New Evidence of Active Tuning in Cochlea

The wonderful performance of hearing systems is mainly attributed to the tuning tiltering of basilar membrane （BM）. Although theory of the cochlear mechanism has been greatly developed since the 1970s and the amplification or sensitivity of the cochlea has been concluded due to the out hair cells, the mechanics underlying the sharp-tuning or frequency selectivity of cochlea remains a puzzle. We use the cochlear translation function derived from the data of an experiment of the BM in vivo to calculate basilar responses to tone bursts, and find that there are resonant peaks with the characteristic frequency at the corresponding place in the initial and terminal part of the responses. However, when the translation function is shallower, there will be no resonant peaks in the responses. The result indicates that the sharp tuning is due to existence of the active resonant tuning mechanism.     

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.     

A computational model of afferent neural activity from the cochlea to the dorsal acoustic stria

The first comprehensive computational model of the precortical mammalian auditory system to include afferent neural processing up to the level of the dorsal acoustic stria (DAS) is described. The model consists of two scissile stages simulating (1) the cochlea and auditory nerve (AN) and (2) the dorsal cochlear nucleus (DCN). The model derives its input from a 128-channel cochlear filterbank. Cochlear transduction, rectification, logarithmic compression, and two-tone suppression functions are performed at the first stage of the simulation. The 512 artificial neurons employed model the cell at the level of transmembrane potential and have interconnections that follow closely those reported in recent anatomical and physiological studies of the cat AN and DCN. The responses of the model to pure-tone stimuli (at various sound-pressure levels) and noise stimuli (at various levels and bandwidths) are reported in detail and compare well with published results. The model is being used to investigate the representation of initial English stop consonants (differing in voice-onset time) in the DAS; this work is briefly described.     

Representation of the vowel /epsilon/ in normal and impaired auditory nerve fibers: model predictions of responses in cats

The temporal response of auditory-nerve (AN) fibers to a steady-state vowel is investigated using a computational auditory-periphery model. The model predictions are validated against a wide range of physiological data for both normal and impaired fibers in cats. The model incorporates two parallel filter paths, component 1 (C1) and component 2 (C2), which correspond to the active and passive modes of basilar membrane vibration, respectively, in the cochlea. The outputs of the two filters are subsequently transduced by two separate functions, added together, and then low-pass filtered by the inner hair cell (IHC) membrane, which is followed by the IHC-AN synapse and discharge generator. The C1 response dominates at low and moderate levels and is responsible for synchrony capture and multiformant responses seen in the vowel responses. The C2 response dominates at high levels and contributes to the loss of synchrony capture observed in normal and impaired fibers. The interaction between C1 and C2 responses explains the behavior of AN fibers in the transition region, which is characterized by two important observations in the vowel responses: First, all components of the vowel undergo the C1/C2 transition simultaneously, and second, the responses to the nonformant components of the vowel become substantial.     

The mechanical waveform of the basilar membrane. III. Intensity effects

Mechanical responses in the basal turn of the guinea-pig cochlea were measured with broad-band noise stimuli and expressed as input-output cross-correlation functions. The experiments were performed over the full range of stimulus intensities in order to try to understand the influence of cochlear nonlinearity on frequency selectivity, tuning, signal compression and the impulse response. The results are interpreted within the framework of a nonlinear, locally active, three-dimensional model of the cochlea. The data have been subjected to inverse analysis in order to recover the basilar-membrane (BM) impedance, a parameter function that, when inserted into the (linearized version of that) model, produces a model response that is similar to the measured response. This paper reports details about intensity effects for noise stimulation, in particular, the way the BM impedance varies with stimulus intensity. In terms of the underlying cochlear model, the decrease of the "activity component" in the BM impedance with increasing stimulus level is attributed to saturation of transduction in the outer hair cells. In the present paper this property is brought into a quantitative form. According to the theory [the EQ-NL theorem, de Boer, Audit. Neurosci. 3, 377-388 (1997)], the BM impedance is composed of two components, both intrinsically independent of stimulus level. One is the passive impedance Zpass and the other one is the "extra" impedance Zextra. The latter impedance is to be multiplied by a real factor gamma (0 < or = gamma < or = 1) that depends on stimulus level. This concept about the composition of the BM impedance is termed the "two-component theory of the BM impedance." In this work both impedances are entirely derived from experimental data. The dependence of the factor gamma on stimulus level can be derived by using a unified form of the outer-hair-cell transducer function. From an individual experiment, the two functions Zpass and Zextra are determined, and an approximation (Zpass + gamma Zextra) to the BM impedance constructed. Next, the model response (the "resynthesized" response) corresponding to this "artificial" impedance is computed. The same procedure is executed for several stimulus-level values. For all levels, the results show a close correspondence with the original experimental data; this includes correct prediction of the compression of response amplitudes, the reduction of frequency selectivity, the shift in peak frequency and, most importantly, the preservation of timing in the impulse response. All these findings illustrate the predictive power of the underlying model.     

Outer hair cell active force generation in the cochlear environment

Outer hair cells are critical to the amplification and frequency selectivity of the mammalian ear acting via a fine mechanism called the cochlear amplifier, which is especially effective in the high-frequency region of the cochlea. How this mechanism works under physiological conditions and how these cells overcome the viscous (mechanical) and electrical (membrane) filtering has yet to be fully understood. Outer hair cells are electromotile, and they are strategically located in the cochlea to generate an active force amplifying basilar membrane vibration. To investigate the mechanism of this cell's active force production under physiological conditions, a model that takes into account the mechanical, electrical, and mechanoelectrical properties of the cell wall (membrane) and cochlear environment is proposed. It is shown that, despite the mechanical and electrical filtering, the cell is capable of generating a frequency-tuned force with a maximal value of about 40 pN. It is also found that the force per unit basilar membrane displacement stays essentially the same (40 pNnm) for the entire linear range of the basilar membrane responses, including sound pressure levels close to hearing threshold. Our findings can provide a better understanding of the outer hair cell's role in the cochlear amplifier.     

Transmission of cochlear distortion products as slow waves: a comparison of experimental and model data

There is a long-lasting question of how distortion products (DPs) arising from nonlinear amplification processes in the cochlea are transmitted from their generation sites to the stapes. Two hypotheses have been proposed: (1) the slow-wave hypothesis whereby transmission is via the transverse pressure difference across the cochlear partition and (2) the fast-wave hypothesis proposing transmission via longitudinal compression waves. Ren with co-workers have addressed this topic experimentally by measuring the spatial vibration pattern of the basilar membrane (BM) in response to two tones of frequency f(1) and f(2). They interpreted the observed negative phase slopes of the stationary BM vibrations at the cubic distortion frequency f(DP) = 2f(1) - f(2) as evidence for the fast-wave hypothesis. Here, using a physically based model, it is shown that their phase data is actually in accordance with the slow-wave hypothesis. The analysis is based on a frequency-domain formulation of the two-dimensional motion equation of a nonlinear hydrodynamic cochlea model. Application of the analysis to their experimental data suggests that the measurement sites of negative phase slope were located at or apical to the DP generation sites. Therefore, current experimental and theoretical evidence supports the slow-wave hypothesis. Nevertheless, the analysis does not allow rejection of the fast-wave hypothesis.     

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.     

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.