Andrei N. Temchin

The roles of the external, middle, and inner ears in determining the bandwidth of hearing

The view seems to prevail that the frequency range of hearing is determined by the properties of the outer and middle ears. We argue that this view is an oversimplification, in part because the reactive component of cochlear input impedance, which affects the low-frequency sensitivity of the cochlea, is neglected. Further, we use comparisons of audiograms and transfer functions for stapes (or columella) velocity or pressure in scala vestibuli near the stapes footplate to show that the middle ear by itself is not responsible for limiting high-frequency hearing in the few species for which such comparisons are possible. Finally, we propose that the tonotopic organization of the cochlea plays a crucial role in setting the frequency limits of cochlear sensitivity and hence in determining the bandwidth of hearing.

Similarity of Traveling-Wave Delays in the Hearing Organs of Humans and Other Tetrapods

Transduction of sound in mammalian ears is mediated by basilar-membrane waves exhibiting delays that increase systematically with distance from the cochlear base. Most contemporary accounts of such “traveling-wave” delays in humans have ignored postmortem basilar-membrane measurements in favor of indirect in vivo estimates derived from brainstem-evoked responses, compound action potentials, and otoacoustic emissions. Here, we show that those indirect delay estimates are either flawed or inadequately calibrated. In particular, we argue against assertions based on indirect estimates that basilar-membrane delays are much longer in humans than in experimental animals. We also estimate in vivo basilar-membrane delays in humans by correcting postmortem measurements in humans according to the effects of death on basilar-membrane vibrations in other mammalian species. The estimated in vivo basilar-membrane delays in humans are similar to delays in the hearing organs of other tetrapods, including those in which basilar membranes do not sustain traveling waves or that lack basilar membranes altogether.

Basilar Membrane Vibrations Near the Round Window of the Gerbil Cochlea

Using a laser velocimeter, responses to tones were measured at a basilar membrane site located about 1.2 mm from the extreme basal end of the gerbil cochlea. In two exceptional cochleae in which function was only moderately disrupted by surgical preparations, basilar membrane responses had characteristic frequencies (CFs) of 34–37 kHz and exhibited a CF-specific compressive nonlinearity: Sensitivity near the CF decreased systematically and the response peaks shifted toward lower frequencies with increasing stimulus level. Response phases also changed with increases in stimulus level, exhibiting small relative lags and leads at frequencies just lower and higher than CF, respectively. Basilar membrane responses to low-level CF tones exceeded the magnitude of stapes vibrations by 54–56 dB. Response phases led stapes vibrations by about 90° at low stimulus frequencies; at higher frequencies, basilar membrane responses increasingly lagged stapes vibration, accumulating 1.5 periods of phase lag at CF. Postmortem, nonlinearities were abolished and responses peaked at ~0.5 octave below CF, with phases which lagged and led in vivo responses at frequencies lower and higher than CF, respectively. In conclusion, basilar membrane responses near the round window of the gerbil cochlea closely resemble those for other basal cochlear sites in gerbil and other species.

Threshold Tuning Curves of Chinchilla Auditory Nerve Fibers. II. Dependence on Spontaneous Activity and Relation to Cochlear Nonlinearity

Spontaneous activity and frequency threshold tuning curves were studied in thousands of auditory nerve fibers in chinchilla. The frequency distribution of spontaneous activity rates is strongly bimodal for auditory nerve fibers with characteristic frequency <3 kHz but only mildly bimodal for the entire sample. Spontaneous activity rates and thresholds at the characteristic frequency are inversely related. Auditory-nerve fibers with low spontaneous rate have tuning curves with lower tip-to-tail ratios and more sharply tuned tips than the tuning curves of fibers with high spontaneous rates. It is shown here that this dependence of tuning on spontaneous rates is consistent with a previously unnoticed nonmonotonic dependence on iso-velocity criterion of the frequency tuning of basilar membrane vibrations.

Traveling waves on the organ of corti of the chinchilla cochlea: spatial trajectories of inner hair cell depolarization inferred from responses of auditory-nerve fibers.

Spatial magnitude and phase profiles for inner hair cell (IHC) depolarization throughout the chinchilla cochlea were inferred from responses of auditory-nerve fibers (ANFs) to threshold- and moderate-level tones and tone complexes. Firing-rate profiles for frequencies ≤2 kHz are bimodal, with the major peak at the characteristic place and a secondary peak at 3–5 mm from the extreme base. Response-phase trajectories are synchronous with peak outward stapes displacement at the extreme cochlear base and accumulate 1.5 period lags at the characteristic places. High-frequency phase trajectories are very similar to the trajectories of basilar-membrane peak velocity toward scala tympani. Low-frequency phase trajectories undergo a polarity flip in a region, 6.5–9 mm from the cochlear base, where traveling-wave phase velocity attains a local minimum and a local maximum and where the onset latencies of near-threshold impulse responses computed from responses to near-threshold white noise exhibit a local minimum. That region is the same where frequency-threshold tuning curves of ANFs undergo a shape transition. Since depolarization of IHCs presumably indicates the mechanical stimulus to their stereocilia, the present results suggest that distinct low-frequency forward waves of organ of Corti vibration are launched simultaneously at the extreme base of the cochlea and at the 6.5–9 mm transition region, from where antiphasic reflections arise.

Passive basilar membrane vibrations in gerbil neonates: mechanical bases of cochlear maturation

Using a laser velocimeter, basilar membrane (BM) responses to tones were measured in neonatal gerbils at a site near the round window of the cochlea. In adult gerbils, ‘active’ BM responses at this site are most sensitive at 34–37 kHz and exhibit a compressive non‐linearity. Postmortem, BM responses in adults become ‘passive’, i.e. linear and insensitive, and the best frequency (BF) shifts downwards by about 0.5 octaves. At 14 and 16 days after birth (DAB), BM responses in neonatal gerbils were passive but otherwise very different from postmortem responses in adult gerbils: BF was more than an octave lower, the steep slopes of the phase vs. frequency curves were shifted downwards in frequency by nearly 1 octave, and the maximum phase lags amounted to only 180 deg relative to stapes. BFs and phase lags increased systematically between 14 and 20 DAB, implying drastic alterations of the passive material properties of cochlear tissues and accounting for a large part of the shift in BF that characterizes maturation of auditory nerve responses during the same period.

Middle-ear transmission in humans: wide-band, not frequency-tuned?

Postmortem and in vivo vibration responses to sound of the stapes and the umbo of human ears are surveyed. The magnitudes of umbo velocity responses recorded postmortem decay between 1 and 5 or 10 kHz at rates between 0 and -3 dB/octave. In contrast, the magnitudes of in vivo umbo vibration are relatively invariant over a wide frequency range, amply exceeding the bandwidth of the audiogram according to one report. Similarly, most studies of postmortem stapes vibration report velocities tuned to about 1 kHz, with magnitudes that decay at a rate of about -6 dB/octave at higher frequencies. In contrast, in vivo stapes responses are apparently only mildly tuned. We conjecture that the bandwidth of stapes vibration velocity in humans will eventually be shown to exceed the bandwidth of the audiogram, in line with findings in other amniotic vertebrates.

High-frequency sensitivity of the mature gerbil cochlea and its development

The thresholds of compound action potentials evoked by tone pips were measured in the cochleae of anesthetized gerbils, both in adults and in neonates aged 14, 16, 18, 20 and 30 days, using round-window electrodes. Stapes vibrations were also measured, using a laser velocimeter, in many of the same ears of adults and neonates aged 14, 16, 18 and 20 days to assess cochlear sensitivity in isolation from middle ear effects and to circumvent problems associated with calibration of acoustic stimuli at high frequencies. Whether referenced to sound pressure level in the ear canal or stapes vibration velocity, thresholds in adults were roughly uniform in the entire range of tested frequencies, 1.25–38.5 kHz. In neonates, thresholds decreased systematically as a function of age, with the largest reductions occurring at the highest frequencies. Thresholds remained slightly immature at all frequencies 30 days after birth. The results for adult gerbils are consistent with the recent finding that basilar-membrane responses to characteristic frequency tones normalized to stapes vibrations are as sensitive at sites near the round window as at more apical sites. The results for neonates confirm that the extreme basal region of the cochlea is the last to approach maturity, with substantial development occurring between 20 and 30 days after birth.

Timing of cochlear responses inferred from frequency-threshold tuning curves of auditory-nerve fibers.

Links between frequency tuning and timing were explored in the responses to sound of auditory-nerve fibers. Synthetic transfer functions were constructed by combining filter functions, derived via minimum-phase computations from average frequency-threshold tuning curves of chinchilla auditory-nerve fibers with high spontaneous activity (Temchin et al., 2008), and signal-front delays specified by the latencies of basilar-membrane and auditory-nerve fiber responses to intense clicks (Temchin et al., 2005). The transfer functions predict several features of the phase-frequency curves of cochlear responses to tones, including their shape transitions in the regions with characteristic frequencies of 1 kHz and 3-4 kHz (Temchin and Ruggero, 2010). The transfer functions also predict the shapes of cochlear impulse responses, including the polarities of their frequency sweeps and their transition at characteristic frequencies around 1 kHz. Predictions are especially accurate for characteristic frequencies <1 kHz.

Spatial Irregularities of Sensitivity along the Organ of Corti of the Cochlea

Fine structures of spatial profiles were computed from existing records of cat and chinchilla auditory-nerve fibers on the basis of their characteristic frequencies and cochlear maps. The spatial fine structures of characteristic-frequency thresholds and of “spontaneous” and driven firing rates were mutually correlated, implying the presence of sensitivity fluctuations due to spatial irregularities of presynaptic structures or processes of the inner hair cells and their input. These findings suggest that activity that appears spontaneous is not actually spontaneous and may indicate irregularities of tonotopic mapping in cochlear mechanics.