Dynamics of Cochlear Nonlinearity.

Dynamic aspects of cochlear mechanical compression were studied by recording basilar membrane (BM) vibrations evoked by tone pairs ("beat stimuli") in the 11-19 kHz region of the gerbil cochlea. The frequencies of the stimulus components were varied to produce a range of "beat rates" at or near the characteristic frequency (CF) of the BM site under study, and the amplitudes of the components were balanced to produce near perfect periodic cancellations, visible as sharp notches in the envelope of the BM response. We found a compressive relation between instantaneous stimulus intensity and BM response magnitude that was strongest at low beat rates (e.g., 10-100 Hz). At higher beat rates, the amount of compression reduced progressively (i.e. the responses became linearized), and the rising and falling flanks of the response envelope showed increasing amounts of hysteresis; the rising flank becoming steeper than the falling flank. This hysteresis indicates that cochlear mechanical compression is not instantaneous, and is suggestive of a gain control mechanism having finite attack and release times. In gain control terms, the linearization that occurs at higher beat rates occurs because the instantaneous gain becomes smoothened, or low-pass filtered, with respect to the magnitude fluctuations in the stimulus. In terms of peripheral processing, the linearization corresponds to an enhanced coding, or decompression, of rapid amplitude modulations. These findings are relevant both to those who wish to understand the underlying mechanisms and those who need a realistic model of nonlinear processing by the auditory periphery.

Masking of sounds by a background noise--cochlear mechanical correlates.

In the search for cochlear correlates of auditory masking by noise stimuli, we recorded basilar membrane (BM) vibrations evoked by either tone or click signals in the presence of varying levels of background noise. The BM vibrations were recorded from basal regions in healthy cochleae of anaesthetized chinchilla and gerbil. Non-linear interactions that could underpin various aspects of psychophysical masking data, including both compression and suppression at the BM level, were observed. The suppression effects, whereby the amplitude of the responses to each stimulus component could be reduced, depended on the relative intensities of the noise and the tones or clicks. Only stimulus components whose frequencies fell inside the non-linear region of the recording site, i.e. around its characteristic frequency (CF), were affected by presentation of the 'suppressing' stimulus (which could be either the tone or the noise). Mutual suppression, the simultaneous reduction of the responses to both tones and noise components, was observed under some conditions, but overall reductions of BM vibration were rarely observed. Moderate- to high-intensity tones suppressed BM responses to low-intensity Gaussian stimuli, including both broadband and narrowband noise. Suppression effects were larger for spectral components of the noise response that were closer to the CF. In this regime, the tone and noise stimuli became the suppressor and probe signals, respectively. This study provides the first detailed observations of cochlear mechanical correlates of the masking effects of noise. Mechanical detection thresholds for tone signals, which were arbitrarily defined using three criteria, are shown to increase in almost direct proportion to the noise level for low and moderately high noise levels, in a manner that resembles the findings of numerous psychophysical observations.

A new auditory threshold estimation technique for low frequencies: proof of concept.

OBJECTIVES: Presently available nonbehavioral methods to estimate auditory thresholds perform less well at frequencies below 1 kHz than at 1 kHz and above. For many uses, such as providing accurate infant hearing aid amplification for low-frequency vowels, an accurate nonbehavioral method to estimate low-frequency thresholds is needed. A novel technique was developed to estimate low-frequency cochlear thresholds based on the use of a previously reported waveform. It was determined how well the method worked by comparing the resulting thresholds to thresholds from onset-response compound action potentials (CAPs) and single-auditory-nerve (AN)- fibers in cats. A long-term goal is to translate this technique for use in humans. DESIGN: An electrode near the cochlea records a combination of cochlear microphonic (CM) and neural responses. In response to low-frequency, near threshold-level tones, the CM is almost sinusoidal whereas the neural responses occur preferentially at one phase of the tone. If the tone is presented again but with its polarity reversed, the neural response keeps the same shape, but shifts ½ cycle in time. Averaging responses to tones presented separately at opposite polarities overlaps and interleaves the neural responses and yields a waveform in which the CM is canceled and the neural response appears twice each tone cycle, that is, the resulting neural response is mostly at twice the tone frequency. The resultant waveform is referred to as "the auditory nerve overlapped waveform" (ANOW). In this study, ANOW level functions were measured in anesthetized cats from 10 to 80 dB SPL in 10 dB steps using tones between 0.3 and 1 kHz. As a response metric, the magnitude of the ANOW component was calculated at twice the tone frequency (ANOW2f). The ANOW threshold was the sound level where the interpolated ANOW2f crossed a statistical criterion that was higher than 95% of the noise floor distribution. ANOW thresholds were compared with onset-CAP thresholds from the same recordings and single-AN-fiber thresholds from the same animals. RESULTS: ANOW and onset-CAP level functions were obtained for 0.3 to 1 kHz tones, and single-AN-fiber responses from cats. Except at 1 kHz, typical ANOW thresholds were mostly 10 to 20 dB more sensitive than onset-CAP thresholds and 10 to 20 dB less sensitive than the most sensitive single-AN-fiber thresholds. CONCLUSIONS: ANOW provides frequency-specific estimates of cochlear neural thresholds over a frequency range that is important for hearing but is not well accessed by nonbehavioral, objective methods. Results suggest that with further targeted development, the ANOW low-frequency threshold estimation technique can be useful both clinically in humans and in basic-science animal experiments.

Basilar-membrane interference patterns from multiple internal reflection of cochlear traveling waves.

At low stimulus levels, basilar-membrane (BM) mechanical transfer functions in sensitive cochleae manifest a quasiperiodic rippling pattern in both amplitude and phase. Analysis of the responses of active cochlear models suggests that the rippling is a mechanical interference pattern created by multiple internal reflection within the cochlea. In models, the interference arises when reverse-traveling waves responsible for stimulus-frequency otoacoustic emissions (SFOAEs) reflect off the stapes on their way to the ear canal, launching a secondary forward-traveling wave that combines with the primary wave produced by the stimulus. Frequency-dependent phase differences between the two waves then create the rippling pattern measurable on the BM. Measurements of BM ripples and SFOAEs in individual chinchilla ears demonstrate that the ripples are strongly correlated with the acoustic interference pattern measured in ear-canal pressure, consistent with a common origin involving the generation of SFOAEs. In BM responses to clicks, the ripples appear as temporal fine structure in the response envelope (multiple lobes, waxing and waning). Analysis of the ripple spacing and response phase gradients provides a test for the role of fast- and slow-wave modes of reverse energy propagation within the cochlea. The data indicate that SFOAE delays are consistent with reverse slow-wave propagation but much too long to be explained by fast waves.

The frequency limit of outer hair cell motility measured in vivo.

Outer hair cells (OHCs) in the mammalian ear exhibit electromotility, electrically driven somatic length changes that are thought to mechanically amplify sound-evoked vibrations. For this amplification to work, OHCs must respond to sounds on a cycle-by-cycle basis even at frequencies that exceed the low-pass corner frequency of their cell membranes. Using in vivo optical vibrometry we tested this theory by measuring sound-evoked motility in the 13-25 kHz region of the gerbil cochlea. OHC vibrations were strongly rectified, and motility exhibited first-order low-pass characteristics with corner frequencies around 3 kHz- more than 2.5 octaves below the frequencies the OHCs are expected to amplify. These observations lead us to suggest that the OHCs operate more like the envelope detectors in a classical gain-control scheme than like high-frequency sound amplifiers. These findings call for a fundamental reconsideration of the role of the OHCs in cochlear function and the causes of cochlear hearing loss.

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.

Gerbil middle-ear sound transmission from 100 Hz to 60 kHz.

Middle-ear sound transmission was evaluated as the middle-ear transfer admittance H(MY) (the ratio of stapes velocity to ear-canal sound pressure near the umbo) in gerbils during closed-field sound stimulation at frequencies from 0.1 to 60 kHz, a range that spans the gerbil's audiometric range. Similar measurements were performed in two laboratories. The H(MY) magnitude (a) increased with frequency below 1 kHz, (b) remained approximately constant with frequency from 5 to 35 kHz, and (c) decreased substantially from 35 to 50 kHz. The H(MY) phase increased linearly with frequency from 5 to 35 kHz, consistent with a 20-29 micros delay, and flattened at higher frequencies. Measurements from different directions showed that stapes motion is predominantly pistonlike except in a narrow frequency band around 10 kHz. Cochlear input impedance was estimated from H(MY) and previously-measured cochlear sound pressure. Results do not support the idea that the middle ear is a lossless matched transmission line. Results support the ideas that (1) middle-ear transmission is consistent with a mechanical transmission line or multiresonant network between 5 and 35 kHz and decreases at higher frequencies, (2) stapes motion is pistonlike over most of the gerbil auditory range, and (3) middle-ear transmission properties are a determinant of the audiogram.

Vibration hotspots reveal longitudinal funneling of sound-evoked motion in the mammalian cochlea.

The micromechanical mechanisms that underpin tuning and dynamic range compression in the mammalian inner ear are fundamental to hearing, but poorly understood. Here, we present new, high-resolution optical measurements that directly map sound-evoked vibrations on to anatomical structures in the intact, living gerbil cochlea. The largest vibrations occur in a tightly delineated hotspot centering near the interface between the Deiters' and outer hair cells. Hotspot vibrations are less sharply tuned, but more nonlinear, than basilar membrane vibrations, and behave non-monotonically (exhibiting hyper-compression) near their characteristic frequency. Amplitude and phase differences between hotspot and basilar membrane responses depend on both frequency and measurement angle, and indicate that hotspot vibrations involve longitudinal motion. We hypothesize that structural coupling between the Deiters' and outer hair cells funnels sound-evoked motion into the hotspot region, under the control of the outer hair cells, to optimize cochlear tuning and compression.

An experimental study into the acousto-mechanical effects of invading the cochlea.

The active and nonlinear mechanical processing of sound that takes place in the mammalian cochlea is fundamental to our sense of hearing. We have investigated the effects of opening the cochlea in order to make experimental observations of this processing. Using an optically transparent window that permits laser interferometric access to the apical turn of the guinea-pig cochlea, we show that the acousto-mechanical transfer functions of the sealed (i.e. near intact) cochlea are considerably simpler than those of the unsealed cochlea. Comparison of our results with those of others suggests that most previous investigations of apical cochlear mechanics have been made under unsealed conditions, and are therefore likely to have misrepresented the filtering of low-frequency sounds in the cochlea. The mechanical filtering that is apparent in the apical turns of sealed cochleae also differs from the filtering seen in individual auditory nerve fibres with similar characteristic frequencies. As previous studies have shown the neural and mechanical tuning of the basal cochlea to be almost identical, we conclude that the strategies used to process low frequency sounds in the apical turns of the cochlea might differ fundamentally from those used to process high frequency sounds in the basal turns.

Mechanical preprocessing of amplitude-modulated sounds in the apex of the cochlea.

Sound-evoked vibrations of individual Hensen's cells in the apical turn of a living guinea pig cochlea were recorded using a displacement-sensitive laser interferometer. The mechanical responses to amplitude-modulated (AM) tones were investigated, and are shown to be physiologically vulnerable. In the healthy cochlea, the AM responses are demodulated strongly at both moderate and high sound pressure levels. In the less healthy and postmortem cochlea, AM demodulation is weaker and is only seen at high stimulus levels. The physiologically vulnerable component of the demodulation is considered to be an analogue of the baseline position shifts that can be seen in the apical cochlea's responses to pure-tone stimuli, and is likely to originate in the cellular motility of the cochlea's outer hair cells.