Nigel P. Cooper

Efferent‐mediated control of basilar membrane motion

Medial olivocochlear efferent (MOCE) neurones innervate the outer hair cells (OHCs) of the mammalian cochlea, and convey signals that are capable of controlling the sensitivity of the peripheral auditory system in a frequency‐specific manner. Recent methodological developments have allowed the effects of the MOCE system to be observed in vivo at the level of the basilar membrane (BM). These observations have confirmed earlier theories that at least some of the MOCEs effects are mediated via the cochleas mechanics, with the OHCs acting as the mechanical effectors. However, the new observations have also provided some unexpected twists: apparently, the MOCEs can enhance the BMs responses to some sounds while inhibiting its responses to others, and they can alter the BMs response to a single sound using at least two separate mechanisms. Such observations put new constraints on the way in which the cochleas mechanics, and the OHCs in particular, are thought to operate.

Separate mechanical processes underlie fast and slow effects of medial olivocochlear efferent activity

Sound‐evoked vibrations of the basilar membrane (BM) in anaesthetised guinea‐pigs are shown to be affected over two distinct time scales by electrical stimulation of the medial olivocochlear efferent system: one is fast (10–100 ms), the other much slower (10–100 s). For low and moderate level tones near the BMs characteristic frequency, both fast and slow effects inhibited BM motion. However, fast inhibition was accompanied by phase leads, while slow inhibition was accompanied by phase lags. These findings are consistent with a hypothesis that both fast and slow effects decrease sound amplification in the cochlea. However, the opposing directions of the phase changes indicate that separate mechanical processes must underlie fast and slow effects. One plausible interpretation of these findings is that efferent slow effects are caused by outer‐hair‐cell stiffness decreases, while efferent fast effects are caused by reductions in ‘negative damping’.

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 gerbils 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.

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.

Vibration of beads placed on the basilar membrane in the basal turn of the cochlea.

Interferometric recordings of sound-evoked vibrations in the basal turn and hook regions of the guinea-pig cochlea are used to show that reflective microbeads (i) follow the motion of the structures on which they are placed, and (ii) do not affect this motion dramatically. Extrapolating these findings to other types of reflective or radioactive material lends support to the findings of numerous studies of cochlear mechanics.

Mathematical modeling of the radial profile of basilar membrane vibrations in the inner ear

Motivated by recent experimental results, an explanation is sought for the asymmetry in the radial profile of basilar membrane vibrations in the inner ear. A sequence of one-dimensional beam models is studied which take into account variations in the bending stiffness of the basilar membrane as well as the potential presence of structural hinges. The results suggest that the main cause of asymmetry is likely to be differences between the boundary conditions at the two extremes of the basilar membranes width. This has fundamental implications for more detailed numerical simulations of the entire cochlea.

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.

Comparison of nonlinear mammalian cochlear-partition models

Various simple mathematical models of the dynamics of the organ of Corti in the mammalian cochlea are analyzed and their dynamics compared. The specific models considered are phenomenological Hopf and cusp normal forms, a recently proposed description combining active hair-bundle motility and somatic motility, a reduction thereof, and finally a model highlighting the importance of the coupling between the nonlinear transduction current and somatic motility. It is found that for certain models precise tuning to any bifurcation is not necessary and that a compressively nonlinear response over a range similar to experimental observations and that the normal form of the Hopf bifurcation is not the only description that reproduces compression and tuning similar to experiment.

Nonlinear models of development, amplification and compression in the mammalian cochlea

This paper reviews current understanding and presents new results on some of the nonlinear processes that underlie the function of the mammalian cochlea. These processes occur within mechano-sensory hair cells that form part of the organ of Corti. After a general overview of cochlear physiology, mathematical modelling results are presented in three parts. First, the dynamic interplay between ion channels within the sensory inner hair cells is used to explain some new electrophysiological recordings from early development. Next, the state of the art is reviewed in modelling the electro-motility present within the outer hair cells (OHCs), including the current debate concerning the role of cell body motility versus active hair bundle dynamics. A simplified model is introduced that combines both effects in order to explain observed amplification and compression in experiments. Finally, new modelling evidence is presented that structural longitudinal coupling between OHCs may be necessary in order to capture all features of the observed mechanical responses.

Masking of sounds by a background noise – cochlear mechanical correlates

•  Basilar membrane responses to tone and noise stimuli presented simultaneously were measured in chinchillas and a gerbil. Overall responses increase monotonically with stimulus level in a compressive manner. •  Response components elicited by the weaker stimulus, whether tone or noise, were reduced by the stronger one. That is, the suppressor stimulus could be either the tone or the noise. Suppression by noise stimuli occurred only when the tone frequency was in the non‐linear region of the basilar membrane recording site. •  Basilar membrane responses to click and noise stimuli were also recorded in some experiments. The click response component was suppressed by the noise. •  Mutual suppression, meaning the simultaneous suppression of the tone and noise response components, was also observed under certain stimulus conditions. •  Detection thresholds of the tone stimuli increased in a near‐linear fashion with noise level increments.