The Biophysical Origin of Traveling-Wave Dispersion in the Cochlea

Sound processing begins at the peripheral auditory system, where it undergoes a highly complex transformation and spatial separation of the frequency components inside the cochlea. This sensory signal processing constitutes a neurophysiological basis for psychoacoustics. Wave propagation in the cochlea, as shown by measurements of basilar membrane velocity and auditory nerve responses to sound, has demonstrated significant frequency modulation (dispersion), in addition to tonotopic gain and active amplification. The physiological and physical basis for this dispersion remains elusive. In this article, a simple analytical model is presented, along with experimental validation using physiological measurements from guinea pigs, to identify the origin of traveling-wave dispersion in the cochlea. We show that dispersion throughout the cochlea is fundamentally due to the coupled fluid-structure interaction between the basilar membrane and the scala fluids. It is further influenced by the variation in physical and geometrical properties of the basilar membrane, the sensitivity or gain of the hearing organ, and the relative dominance of the compression mode at about one-third octave beyond the best frequency.     

Fast Reverse Propagation of Sound in the Living Cochlea

The auditory sensory organ, the cochlea, not only detects but also generates sounds. Such sounds, otoacoustic emissions, are widely used for diagnosis of hearing disorders and to estimate cochlear nonlinearity. However, the fundamental question of how the otoacoustic emission exits the cochlea remains unanswered. In this study, emissions were provoked by two tones with a constant frequency ratio, and measured as vibrations at the basilar membrane and at the stapes, and as sound pressure in the ear canal. The propagation direction and delay of the emission were determined by measuring the phase difference between basilar membrane and stapes vibrations. These measurements show that cochlea-generated sound arrives at the stapes earlier than at the measured basilar membrane location. Data also show that basilar membrane vibration at the emission frequency is similar to that evoked by external tones. These results conflict with the backward-traveling-wave theory and suggest that at low and intermediate sound levels, the emission exits the cochlea predominantly through the cochlear fluids.     

Linear and nonlinear models of the basilar membrane motion

A linear and a nonlinear transmission line model of the basilar membrane is described. The motion of the basilar membrane model has been simulated by numerical methods and compared with physiological data for several types of sound stimuli. It is shown that a linear model exhibits a frequency modulation in its impulse response that is in accordance with physiological data. The nonlinear model displays a sharpened frequency response for lower sound intensities. Futhermore, a nonlinear model explains why hearing damage imposed by short, high-intensity, sounds is extended to the low-frequency regions of the cochlea.     

Localization of the cochlear amplifier in living sensitive ears

Background

To detect soft sounds, the mammalian cochlea increases its sensitivity by amplifying incoming sounds up to one thousand times. Although the cochlear amplifier is thought to be a local cellular process at an area basal to the response peak on the spiral basilar membrane, its location has not been demonstrated experimentally.

Methodology and Principal Findings

Using a sensitive laser interferometer to measure sub-nanometer vibrations at two locations along the basilar membrane in sensitive gerbil cochleae, here we show that the cochlea can boost soft sound-induced vibrations as much as 50 dB/mm at an area proximal to the response peak on the basilar membrane. The observed amplification works maximally at low sound levels and at frequencies immediately below the peak-response frequency of the measured apical location. The amplification decreases more than 65 dB/mm as sound levels increases.

Conclusions and Significance

We conclude that the cochlea amplifier resides at a small longitudinal region basal to the response peak in the sensitive cochlea. These data provides critical information for advancing our knowledge on cochlear mechanisms responsible for the remarkable hearing sensitivity, frequency selectivity and dynamic range.     

The ultrastructure of the cochlear basilar membrane of the guinea pig

The ultrastructure of the basilar membrane of the guinea pig cochlea is analysed. Measurements were made of the thickness of fibrillar and homogeneous layers along the cochlea of the width of bundles and spaces between them, and the distribution density of fibrils in the bundles. The analysis of the obtained characteristics has demonstrated that the homogeneous ground substance significantly contributes to the buildup of longitudinal stiffness of the basilar membrane.     

Responses to sound of the basilar membrane of the mammalian cochlea.

Recent evidence shows that the frequency-specific non-linear properties of auditory nerve and inner hair cell responses to sound, including their sharp frequency tuning, are fully established in the vibration of the basilar membrane. In turn, the sensitivity, frequency selectivity and non-linear properties of basilar membrane responses probably result from an influence of the outer hair cells.     

Quantitative characteristics of the basilar membrane in the mammalian cochlea

The variations in width and height of the basilar membrane along the cochlea in four species of laboratory animals: white rat, guinea pig, chinchilla and cat have been investigated. The results obtained have been used to calculate the height/width ratio along the cochlea, suggested by Bruns as an estimate of basilar membrane stiffness. The given characteristic is practically identical in all species studied despite the differences in the frequency ranges of auditory reception and, therefore, cannot be used either for characterizing the basilar membrane stiffness or for frequency mapping the cochlea of mammals.     

Finite element modelling of human auditory periphery including a feed-forward amplification of the cochlea

A three-dimensional finite element model is developed for the simulation of the sound transmission through the human auditory periphery consisting of the external ear canal, middle ear and cochlea. The cochlea is modelled as a straight duct divided into two fluid-filled scalae by the basilar membrane (BM) having an orthotropic material property with dimensional variation along its length. In particular, an active feed-forward mechanism is added into the passive cochlear model to represent the activity of the outer hair cells (OHCs). An iterative procedure is proposed for calculating the nonlinear response resulting from the active cochlea in the frequency domain. Results on the middle-ear transfer function, BM steady-state frequency response and intracochlear pressure are derived. A good match of the model predictions with experimental data from the literatures demonstrates the validity of the ear model for simulating sound pressure gain of middle ear, frequency to place map, cochlear sensitivity and compressive output for large intensity input. The current model featuring an active cochlea is able to correlate directly the sound stimulus in the ear canal with the vibration of BM and provides a tool to explore the mechanisms by which sound pressure in the ear canal is converted to a stimulus for the OHCs.     

Modeling the active process of the cochlea: phase relations, amplification, and spontaneous oscillation.

The high sensitivity and sharp frequency selectivity of acoustical signal transduction in the cochlea suggest that an active process pumps energy into the basilar membrane's oscillations. This function is generally attributed to outer hair cells, but its exact mechanism remains uncertain. Several classical models of amplification represent the load upon the basilar membrane as a single mass. Such models encounter a fundamental difficulty, however: the phase difference between basilar-membrane movement and the force generated by outer hair cells inhibits, rather than amplifies, the modeled basilar-membrane oscillations. For this reason, modelers must introduce artificially either negative impedance or an appropriate phase shift, neither of which is justified by physical analysis of the system. We consider here a physical model based upon the recent demonstration that the basilar membrane and reticular lamina can move independently, albeit with elastic coupling through outer hair cells. The mechanical model comprises two resonant masses, representing the basilar membrane and the reticular lamina, coupled through an intermediate spring, the outer hair cells. The spring's set point changes in response to displacement of the reticular lamina, which causes deflection of the hair bundles, variation of outer hair cell length and, hence, force production. Depending upon the frequency of the acoustical input, the basilar membrane and reticular lamina can oscillate either in phase or in counterphase. In the latter instance, the force produced by hair cells leads basilar-membrane oscillation, energy is pumped into basilar-membrane movement, and an external input can be strongly amplified. The model is also capable of producing spontaneous oscillation. In agreement with experimental observations, the model describes mechanical relaxation of the basilar membrane after electrical stimulation causes outer hair cells to change their length.     

Consequences of Location-Dependent Organ of Corti Micro-Mechanics

The cochlea performs frequency analysis and amplification of sounds. The graded stiffness of the basilar membrane along the cochlear length underlies the frequency-location relationship of the mammalian cochlea. The somatic motility of outer hair cell is central for cochlear amplification. Despite two to three orders of magnitude change in the basilar membrane stiffness, the force capacity of the outer hair cell’s somatic motility, is nearly invariant over the cochlear length. It is puzzling how actuators with a constant force capacity can operate under such a wide stiffness range. We hypothesize that the organ of Corti sets the mechanical conditions so that the outer hair cell’s somatic motility effectively interacts with the media of traveling waves—the basilar membrane and the tectorial membrane. To test this hypothesis, a computational model of the gerbil cochlea was developed that incorporates organ of Corti structural mechanics, cochlear fluid dynamics, and hair cell electro-physiology. The model simulations showed that the micro-mechanical responses of the organ of Corti are different along the cochlear length. For example, the top surface of the organ of Corti vibrated more than the bottom surface at the basal (high frequency) location, but the amplitude ratio was reversed at the apical (low frequency) location. Unlike the basilar membrane stiffness varying by a factor of 1700 along the cochlear length, the stiffness of the organ of Corti complex felt by the outer hair cell remained between 1.5 and 0.4 times the outer hair cell stiffness. The Y-shaped structure in the organ of Corti formed by outer hair cell, Deiters cell and its phalange was the primary determinant of the elastic reactance imposed on the outer hair cells. The stiffness and geometry of the Deiters cell and its phalange affected cochlear amplification differently depending on the location.     

Explanation of octave and diplacusis effects

The study is based on the model of sound perception that involves two systems of measuring the frequency of the sound being perceived. The system of analyzing the periodicity of spike sequence in axons of neurons innervating the internal auditory hair cells excited by the running wave is less precise, but it provides the estimation of the frequency of any periodical sounds. Exact measurement of the frequency of the sinusoidal sound occurs from the spikes in axons of neurones innervating the internal hair cells of the auditory reception field, which uses the entire train of waves excited by this sound in the critical layer of the waveguide of the internal ear cochlea, which corresponds to the frequency of the sound. The octave effect is explained in terms of the fact that the spectrum of frequencies of speech sounds, singing and music coincides with the region of the audibility range in which the impulses of the auditory nerve fibers are synchronized by incoming signals. The octave similarity, i.e., the similarity in the sounding of harmonic signals, whose frequencies relate as even numbers (2:1, etc.), is explained by an unambiguous match between the sound frequency and pulse rate in auditory fibers coming from the auditory reception field. The presence in the brain posterior tubercles of multipeak neurons whose peaks are in octave ratio, confirm the crucial role of the system of exact measurement of frequency in the phenomenon of octave similarity. The phenomenon of diplacusis, which is particularly pronounced in persons with Menier disease, is caused by changes in the position of the auditory reception field in the diseased ear as compared with the healthy ear. The alternating switching of reception from one ear to the other is related to a disturbance of the unitary image of pitch.     

Pitch and Timbre Interfere When Both Are Parametrically Varied

Pitch and timbre perception are both based on the frequency content of sound, but previous perceptual experiments have disagreed about whether these two dimensions are processed independently from each other. We tested the interaction of pitch and timbre variations using sequential comparisons of sound pairs. Listeners judged whether two sequential sounds were identical along the dimension of either pitch or timbre, while the perceptual distances along both dimensions were parametrically manipulated. Pitch and timbre variations perceptually interfered with each other and the degree of interference was modulated by the magnitude of changes along the un-attended dimension. These results show that pitch and timbre are not orthogonal to each other when both are assessed with parametrically controlled variations.     

Neural mechanisms underlying acoustic behaviour of the frog Pseudophryne semimarmorata (Anura: Leptodactylidae)

Pseudophryne semimarmorata lacks a columella and tympanic membrane. However, at least males are relatively sensitive to sound. The mating call in this species can be inhibited by certain acoustic stimuli. The range of stimuli that inhibited calling was compared with that which evoked neural activity in midbrain auditory units. One of three types of unit which can be distinguished on the basis of best frequency, the high frequency unit, is presumed to be derived from the basilar papilla. High frequency units responded to the same range of sounds that inhibited calling. It is suggested that production of the mating call is initiated by a neural pacemaker, and sufficient neural input to this centre from the basilar papilla inhibits the pacemaker.     

A comparison of models for sharpening of the frequency selectivity in the coachlea

The mechanical tuning of the basilar membrane has not been shown to be sharp enough to explain the very narrow tuning curves observed in primary auditory fibers. A mechanism for sharpening of the frequency selectivity or an unknown second filter is therefore assumed to exist in the cochlea. In the present paper, several theories for frequency selectivity sharpening in the cochlea are studied with the aid of a basilar membrane model. It is shown that the model proposed by Zwislocki (1974) for interaction between inner and outer hair cells results in the greatest increase in selectivity. It is also shown that nonlinear basilar membrane motion may very well explain the discrepancy between mechanical and neural tuning. Besides an increased selectivity at low sound intensities due to an increased low-frequency cut-off slope in the frequency transfer function, nonlinear basilar membrane motion also results in an increased high-frequency cut-off slope not present in other models for frequency selectivity sharpening.     

Supporting Evidence from Single Unit Experiments for the Cochlea as an Addressed Delay Line

WE have already outlined the principles of a theory of cochlear organization^{1, 2} whereby acoustic signal components in the low and mid frequency range—-that is to say, frequencies for which good or moderate phase locking of unit response is possible—are detected by the cochlea using an approximate cross-correlation mechanism which operates on the time varying signal displayed along the basilar membrane, the latter acting as an acoustic exponential delay line. The running correlations are performed using fixed patterns of control fibres addressed to the outer hair cells, the pattern of addressing for each control fibre group corresponding to an instantaneous wave pattern for a specific frequency defined by the location of the fibre system along the length of the membrane. The fibres of each control system synapse with the afferent dendrites associated with a definite inner hair cell and act as a frequency sensitive gate, the inner hair cell of the assembly providing generator current related to signal amplitude.     

早期声音暴露对蝙蝠中脑下丘听神经元频率调谐特性发育的影响

本实验对鼠耳蝠出生后不同时期进行纯音暴露,采用常规电生理不方法研究出生后早期声音暴露出蝙蝠中脑下丘听神经元频率调谐特性发育的影响及影响的临界期。结果表明,出生后第１,３周开始声暴露的实验组,其神经元调于暴露声频段的数量较对照组和出生后第５周开始声暴露的实验组明显增多,且音调筑构出现扭曲,神经元频率调谐曲线的Ｑ１０－ｄＢ值也较高。     

Response of a membrane in a cochlear model to continuous and transient sounds]

Using enlarged mechanical models of the cochlea and true stimuli sinusoidal or transient, the authors give photographics documents which point out in objective way the "basilar" membrane responses. With pure tones, the membrane vibrates along its entire length no matter what the frequency. With transients, there is a maximum displacement in varying sites but always near the base.     

Spatial cross-correlation

We propose in this paper a new class of model processes for the extraction of spectral information from the neural representation of acoustic signals in mammals. We are concerned particularly with mechanisms for detecting the phase-locked activity of auditory neurons in response to frequencies and intensities of sound associated with speech perception. Recent psychophysical tests on deaf human subjects implanted with intracochlear stimulating electrodes as an auditory prosthesis have produced results which are in conflict with the predictions of the classical place-pitch and periodicity-pitch theories. In our model, the detection of synchronicity between two phase-locked signals derived from sources spaced a finite distance apart on the basilar membrane can be used to extract spectral information from the spatiotemporal pattern of basilar membrane motion. Computer simulations of this process suggest an optimal spacing of about 0.3–0.4 of the wavelength of the frequency to be detected. This interval is consistent with a number of psychophysical, neurophysiological, and anatomical observations, including the results of high resolution frequency-mapping of the anteroventral cochlear nucleus which are presented here. One particular version of this model, invoking the binaurally sensitive cells of the medial superior olive as the critical detecting elements, has properties which are useful in accounting for certain complex binaural psychophysical observations.     

Reverberation challenges the temporal representation of the pitch of complex sounds

Accurate neural coding of the pitch of complex sounds is an essential part of auditory scene analysis; differences in pitch help segregate concurrent sounds, while similarities in pitch can help group sounds from a common source. In quiet, nonreverberant backgrounds, pitch can be derived from timing information in broadband high-frequency auditory channels and/or from frequency and timing information carried in narrowband low-frequency auditory channels. Recording from single neurons in the cochlear nucleus of anesthetized guinea pigs, we show that the neural representation of pitch based on timing information is severely degraded in the presence of reverberation. This degradation increases with both increasing reverberation strength and channel bandwidth. In a parallel human psychophysical pitch-discrimination task, reverberation impaired the ability to distinguish a high-pass harmonic sound from noise. Together, these findings explain the origin of perceptual difficulties experienced by both normal-hearing and hearing-impaired listeners in reverberant spaces.