Hearing at speech frequencies is different from what we thought

The mechanics of hearing is understood better at high frequencies than at low frequencies (f < 4 kHz), in part because many experimental animals do not hear well at low frequencies (e.g. mice). This is unfortunate because low frequencies are the most important for human speech. The cochlea analyses sound into component frequencies with high-frequency responses peaking at one end of the cochlea and low-frequency responses peaking at the other. This frequency selectivity is established, in part, by the basilar membrane (BM) whose stiffness changes along the length of the cochlea. Past conceptions of cochlear function have focused on BM motion, partly because of the BM’s important stiffness role, but also because BM motion could be measured in the relatively accessible high-frequency region of the cochlea. Cochlear motion measurements have been difficult to do because the cochlea is encased in bone and opening this bone can cause damage. In the high-frequency region, the cochlea’s sensitivity and frequency selectivity is achieved by mechanical amplification of 100 or more, produced by molecular motors in outer hair cells. In BM motion, this amplification is focused within half an octave of the cochlear location most sensitive to a particular frequency. This results in narrow, band-pass responses that are approximately V-shaped. Since cochlear anatomy changes only gradually from high-frequency to low-frequency regions, and human psychophysics shows only gradual changes across frequency, it has been assumed that the cochlea works the same way at low frequencies as it does at high frequencies. Previous measurements from lowfrequency cochlear regions were consistent with the gradual-change view, in that low-frequency tuning was band-pass (although broader than high-frequency tuning) and there was amplification (although only a factor of 10). However, for most of these measurements a hole was made in the cochlea which changes cochlear hydrodynamics. Dong & Cooper (2006) showed that when the hole was resealed, the tuning changed from band-pass to close to low-pass (termed ‘low-pass-like’), but these experiments did not show whether making the hole had caused damage. A breakthrough in measuring cochlear mechanical responses in the low-frequency region has come from a new technique: vibration measurements using optical coherence tomography at wavelengths that penetrate bone. In this issue of The Journal of Physiology, Recio-Spinoso & Oghalai (2017), using this technique, have shown in a never-opened cochlea that the mechanical response is low-pass-like, and surprisingly, there are frequencies with gains of 300, which is similar to gains in high-frequency regions. Not only is the low-pass-like tuning different from BM band-pass tuning at high frequencies, the frequency distribution of the gain is different. In the low-frequency region, Recio-Spinoso and Oghalai found that the highest gain is at the high-frequency edge of the response, well above the frequency of the largest response. At lower frequencies where the response amplitude is largest, the gain is much less. In short, these results are very different from the traditional view of cochlear mechanics derived from BM motion. There are two reasons for this difference. One is the difference in frequency regions, low versus high. The other is that the new measurements are from near the reticular lamina (RL) at the top of the organ of Corti, whereas the BM is at the bottom of the organ of Corti. Recent measurements from cochlear high-frequency regions found that near-RL motion is amplified more, and tuned differently, compared to BM motion (Lee et al. 2016; Ren et al. 2016). The near-RL motion in low-frequency regions has some interesting similarities with the near-RL motion in high-frequency regions: both have several-octave-wide regions with moderate gains and a higher-frequency region with a much larger gain. The mechanical factors that produce these near-RL motions are poorly understood and new, more detailed mechanical models are needed to interpret them. Nonetheless, the new measurements show that high-frequency BM motion is not a good guide for understanding cochlear mechanics. RL motion is different from BM motion and arguably, RL motion is more important because it is closer to the motion that drives inner hair cell (IHC) stereocilia and excites auditory nerve fibres. The low-pass-like mechanical response in the low-frequency region is different from the band-pass tuning of low-frequency auditory nerve fibres. This reveals the presence of a high-pass filter between the mechanical motion and the auditory nerve response. Several mechanisms may be involved: (1) IHC stereocilia are deflected by fluid thrust resulting in a hydro-mechanical high-pass filter, (2) adaptation in the IHC stereocilia deflection to channel-current response creates a high-pass filter, and (3) ion channels in IHC cell walls may also provide high-pass filtering. How much each contributes is unknown. Much needs to be learned about lowfrequency hearing, particularly because of its importance for speech. The new measurements make it clear that cochlear mechanics in low-frequency regions is different in important ways from the longstanding conception based on highfrequency BM motion.