Graeme K. Yates

Basilar membrane measurements and the travelling wave.

From the original measurements of G. von Békésy (1942) until a few years ago, the basilar membrane was considered to undergo simple passive linear vibration. Recent measurements have completely altered this notion. It is now known that the BM is highly non linear and very sharply tuned. Indeed, BM can now account for most of the properties of the eighth nerve response to sound. The non linearity can be approximated by a hyperbolic function and appears to be part of an active process in the outer hair cell. At the characteristic frequency, CAP threshold (10 dB SPL) corresponds to 0.3 nm motion and the non linearity shows half saturation at 10 nm. The sigmoid shape of the full range BM input-output curve is due to the combination of a less sensitive linear passive component with the added sensitivity of the active non linear function. A hyperbolic input-output function is also present in the cochlear microphonics, and at low frequencies the half saturation value again corresponds to 10 nm BM displacement. With induced threshold loss (e.g. noise trauma) the nonlinearity disappears from the BM, but is still present in the CM. This suggests that the pathology is in the active mechanical feedback process, rather than in the receptor system. It appears that BM mechanics at low amplitudes near the resonant frequency is controlled by a nonlinear mechano-electrical transducer followed by a vulnerable, linear, active mechanism (electro-mechanical?) feeding back in positive phase onto BM vibration.

Diversity of characteristic frequency rate-intensity functions in guinea pig auditory nerve fibres.

Rate-intensity functions at characteristic frequency (CF) were recorded from single fibres in the auditory nerve of anaesthetised guinea pigs. Within the same animal, CF rate-intensity functions, although probably forming a continuum, could be conveniently divided into three groups; (1) Saturating; reach maximum discharge rate within 30 dB of threshold, (2) Sloping-saturation; initially rapid growth in discharge rate leading to a slower growth in discharge rate but not saturating and (3) Straight; approximately constant increase in firing rate per decibel increase in sound pressure up to the maximum sound pressures used. Thresholds for individual fibres were plotted relative to compound action potential thresholds at the appropriate frequency. Fibres with straight CF rate-intensity functions had the highest thresholds. Fibres of the saturating CF sloping-saturation CF rate-intensity type had thresholds intermediate between saturating and straight. There was a close relationship between the type of CF rate-intensity function exhibited by a fibre and its spontaneous discharge rate. Fibres with saturating CF rate-intensity functions generally had high spontaneous discharge rates (greater than 18/s), whereas those with straight CF rate-intensity functions generally had low spontaneous discharge rates (less than 0.5/s). The majority of fibres with sloping-saturation CF rate-intensity functions had spontaneous rates between 0.5/s and 18/s. There was a negative correlation (r = -0.59) between the logarithm of the spontaneous discharge rate and relative threshold at CF with the lowest spontaneous rate fibres having the highest thresholds and vice-versa. This diversity of CF rate-intensity functions has functional implications for both frequency and intensity coding at high sound pressures in the mammalian auditory system.

Basilar membrane nonlinearity determines auditory nerve rate-intensity functions and cochlear dynamic range

In a previous paper (Winter et al., 1990) we demonstrated the existence of a new type of auditory-nerve rate-intensity function, the straight type, as well as a correlation between rate-level type, threshold and spontaneous rate. In this paper we now show that the variation in rate-intensity functions has its origin in the basilar membrane nonlinearity. Comparison of rate-intensity functions at characteristic frequency and at a tail-frequency show that the rate-intensity functions are identical at low firing rates and that the sloping-saturation and straight types deviate from the standard function only at higher firing rates. The frequencies at which the deviations occur, and the change from saturating to sloping-saturation or straight, are closely correlated with the characteristic frequency of the fibre. Using the tail-frequency rate-intensity function as a calibration, it is possible to derive the basilar membrane input-output function at characteristic frequency from the characteristic frequency rate-intensity function. The resulting derived basilar membrane input-output functions are of a simple form and agree well with published direct measurements of basilar membrane motion. They show that the wide dynamic range to which the cochlea responds, about 120 decibels, is compressed by the basilar membrane nonlinearity into a much smaller range of about 30-35 decibels. General characteristics of the derived basilar membrane input-output curves show features which agree well with psychoacoustic studies of loudness estimation.

Outer hair cell receptor current and sensorineural hearing loss

It is argued in this paper that many nonlinear phenomena in audition and many types of sensorineural hearing loss can be explained by a disruption of the mechano-electrical transduction process at the apex of the outer hair cells. This is done using experimental data and a simple model of the active role of outer hair cells in cochlear mechanics based on our previous experiments with acoustic trauma. The causes of sensorineural loss addressed include acoustic trauma, aminoglycoside ototoxicity, intoxication with loop diuretics, hypoxia and Menieres disease. The nonlinear phenomena discussed include loudness compression, two-tone suppression and modulation of cochlear sensitivity by very low-frequency tones. In every case considered the reduction in neural sensitivity was related to the reduction in outer hair cell receptor current in a quantitatively similar way. We conclude that the link is causal.

Basilar membrane nonlinearity and its influence on auditory nerve rate-intensity functions ☆

Previous papers have shown that the shapes of rate-intensity functions of auditory nerve fibres vary with spontaneous rate (Sachs and Abbas 1974; Sachs et al. 1989; Winter et al. 1990; Yates et al. 1990), and that the variation is due to the nonlinear properties of the basilar membrane. This paper examines the basilar membrane nonlinearity and provides a semi-quantitative explanation for it in terms of previous models (Zwicker 1979; Patuzzi et al. 1989) and an analogue model. It thereby provides explanations for the shapes of the basilar membrane input-output curves and for the way in which they vary with trauma. The shapes of the neural rate-intensity functions are quantified and shown to be consistent with the low-threshold data of Geisler et al. (1985). Several nonlinear properties of the cochlea, such as recruitment, are also interpreted.

Cochlear action potential threshold and single unit thresholds.

There is a close correlation between the sound pressure of tone burst required to affect a primary auditory neuron at its characteristic frequency and that which will produce a detectable N1 response at the same frequency. Units with thresholds from 80--0 db SPL (recorded from damaged and undamaged cochleas) were 0--20 dB , respectively, more sensitive than the action potential response.

The origin of the low-frequency microphonic in the first cochlear turn of guinea-pig

Low-frequency microphonic potentials (100 Hz to 2000 Hz) have been measured in the first turn of the guinea pig cochlea before and after a variety of manipulations of the cochlea. These included ablation of the apical turns, iontophoresis of streptomycin, dc current injection into the first turn, acoustic trauma and two-tone interference with pure tones. These manipulations indicate that the low-frequency microphonic measured in the first turn and at the round window is generated predominantly by the hair cells of this region. It is a convenient and relatively uncomplicated indicator of the integrity of the mechano-electrical transduction process of these cells.

Saturation of outer hair cell receptor currents causes two-tone suppression ☆

Zwicker [Biol. Cybern. 35, 243-250, (1979); J. Acoust. Soc. Am. 80, 163-176 (1986)] has previously proposed that many nonlinear phenomena in the mammalian cochlea can be explained by saturation of a positive feedback process which enhances mechanical sensitivity, although the site of the nonlinearity producing this saturation has so far remained obscure. In this paper we present evidence suggesting that the nonlinearity of mechano-electrical transduction in the outer hair cells is the dominant nonlinearity producing two-tone suppression in the mammalian cochlea. In particular, we show that: (i) suppression of the extracellular summating potential (SP), recorded from a particular place within the organ of Corti, has characteristics similar to the suppression of activity in the auditory-nerve; (ii) that SP suppression occurs at approximately constant basilar membrane displacement, inferred from the SP iso-response contours; and that (iii) the onset of SP suppression with suppressor tones on the tail of the frequency tuning curve closely parallels the onset of nonlinearity in the local cochlear microphonic. Since previous studies (Patuzzi et al., 1989) have demonstrated that the vibration of the basilar membrane at its characteristic frequency is very sensitive to changes in outer hair cell receptor current, we consider that interference in outer hair cell currents caused by nonlinearity in mechano-electrical transduction is an adequate explanation of two-tone suppression. This requires that outer hair cell receptor currents deviate from linearity at a suppressor tone level below that required to produce a significant DC receptor potential within the inner hair cells, and that the active process within the cochlea is distributed along a local region of the cochlea, basal of the vibration peak.

Nonlinear input-output functions derived from the responses of guinea-pig cochlear nerve fibres: Variations with characteristic frequency

Rate-versus-level functions (RLFs) were recorded from individual cochlear nerve fibres in anaesthetised guinea-pigs. Variations in the shapes of these functions with frequency were used to derive input-output (IO) relationships for the mechanical preprocessing mechanisms in the cochlea. It was assumed that these preprocessing mechanisms operated linearly at frequencies well below each fibres characteristic frequency (CF). The IO functions derived at each fibres CF provided strong evidence of compressively nonlinear preprocessing in most regions of the cochlea. However, the apparent degree of compression depended on the fibres CF, and hence on the presumed site of cochlear innervation. For fibres with CFs of between 1.5 and 3.6 kHz, the CF derived IO functions grew at rates of around 0.5 dB/dB. For fibres with CFs above 4 kHz, the IO functions were more compressive, with high-intensity asymptotic slopes of around 0.13 dB/dB. In the highest (> or = 10 kHz) CF fibres, the degree of compression depended on the physiological condition of the cochlea; the derived IO functions becoming more linear as the cochlea became less sensitive. The derived IO technique was not well suited to analyse responses evoked by very low frequency (e.g., < 500 Hz) tones. Nonetheless, the CF RLFs from fibres with CFs lower than approximately 1 kHz provided little evidence of mechanical nonlinearity near the apex of the cochlea. These findings imply a longitudinal variation in the mechanisms of cochlear preprocessing, and provide important new tests for functional models of the cochlea.

Changes in cochlear microphonic and neural sensitivity produced by acoustic trauma.

The low-frequency (200 Hz) microphonic potentials at the round window and in the organ of Corti of the first turn of the guinea pig cochlea have been measured before and after acoustic overstimulation. Reductions in the amplitude of this microphonic after loud sound are highly correlated with neural threshold elevation in this region. The fall in the microphonic amplitude appears due to an inactivation of mechano-electrical transduction channels at the apex of the outer hair cells into a closed state. These results are consistent with the idea that the current through the outer hair cells controls the mechanical sensitivity of the organ of Corti, and that the temporary loss of mechanical and neural sensitivity following loud sound is due to a simple inactivation of the mechano-electrical transduction channels.