Biomechanics of Hearing Sensitivity

1991 ◽  
Vol 113 (1) ◽  
pp. 1-13 ◽  
Author(s):  
Sir James Lighthill

This survey lecture on the biomechanics of hearing sensitivity is concerned, not with how the brain in man and other mammals analyzes the data coming to it along auditory nerve fibers, but with the initial capture of that data in the cochlea. The brain, needless to say, can produce all its miracles of interpretation only where it works on good initial data. For frequency selectivity these depend on some remarkable properties of the cochlea as a passive macromechanical system, comprising the basilar membrane with its steeply graded stiffness distribution vibrating within the cochlear fluids. But the biomechanics of hearing sensitivity to low levels of sound (at any particular frequency) calls also into play an active micromechanical system, which during the past few years has progressively been identified as located in the outer hair cells, and which, through a process of positive feedback, amplifies (in healthy ears) that basilar membrane vibration. This in turn offers the inner hair cells an enhanced signal at low sound levels, so that the threshold at which they can generate activity in auditory nerve fibers is, in consequence, very substantially lowered.

2001 ◽  
Vol 81 (3) ◽  
pp. 1305-1352 ◽  
Author(s):  
Luis Robles ◽  
Mario A. Ruggero

In mammals, environmental sounds stimulate the auditory receptor, the cochlea, via vibrations of the stapes, the innermost of the middle ear ossicles. These vibrations produce displacement waves that travel on the elongated and spirally wound basilar membrane (BM). As they travel, waves grow in amplitude, reaching a maximum and then dying out. The location of maximum BM motion is a function of stimulus frequency, with high-frequency waves being localized to the “base” of the cochlea (near the stapes) and low-frequency waves approaching the “apex” of the cochlea. Thus each cochlear site has a characteristic frequency (CF), to which it responds maximally. BM vibrations produce motion of hair cell stereocilia, which gates stereociliar transduction channels leading to the generation of hair cell receptor potentials and the excitation of afferent auditory nerve fibers. At the base of the cochlea, BM motion exhibits a CF-specific and level-dependent compressive nonlinearity such that responses to low-level, near-CF stimuli are sensitive and sharply frequency-tuned and responses to intense stimuli are insensitive and poorly tuned. The high sensitivity and sharp-frequency tuning, as well as compression and other nonlinearities (two-tone suppression and intermodulation distortion), are highly labile, indicating the presence in normal cochleae of a positive feedback from the organ of Corti, the “cochlear amplifier.” This mechanism involves forces generated by the outer hair cells and controlled, directly or indirectly, by their transduction currents. At the apex of the cochlea, nonlinearities appear to be less prominent than at the base, perhaps implying that the cochlear amplifier plays a lesser role in determining apical mechanical responses to sound. Whether at the base or the apex, the properties of BM vibration adequately account for most frequency-specific properties of the responses to sound of auditory nerve fibers.


Author(s):  
Dalian Ding ◽  
Haiyan Jiang ◽  
Senthilvelan Manohar ◽  
Xiaopeng Liu ◽  
Li Li ◽  
...  

2-Hyroxypropyl-beta-cyclodextrin (HPβCD) is being used to treat Niemann-Pick C1, a fatal neurodegenerative disease caused by abnormal cholesterol metabolism. HPβCD slows disease progression, but unfortunately causes severe, rapid onset hearing loss by destroying the outer hair cells (OHC). HPβCD-induced damage is believed to be related to the expression of prestin in OHCs. Because prestin is postnatally upregulated from the cochlear base toward the apex, we hypothesized that HPβCD ototoxicity would spread from the high-frequency base toward the low-frequency apex of the cochlea. Consistent with this hypothesis, cochlear hearing impairments and OHC loss rapidly spread from the high-frequency base toward the low-frequency apex of the cochlea when HPβCD administration shifted from postnatal day 3 (P3) to P28. HPβCD-induced histopathologies were initially confined to the OHCs, but between 4- and 6-weeks post-treatment, there was an unexpected, rapid and massive expansion of the lesion to include most inner hair cells (IHC), pillar cells (PC), peripheral auditory nerve fibers, and spiral ganglion neurons at location where OHCs were missing. The magnitude and spatial extent of HPβCD-induced OHC death was tightly correlated with the postnatal day when HPβCD was administered which coincided with the spatiotemporal upregulation of prestin in OHCs. A second, massive wave of degeneration involving IHCs, PC, auditory nerve fibers and spiral ganglion neurons abruptly emerged 4–6 weeks post-HPβCD treatment. This secondary wave of degeneration combined with the initial OHC loss results in a profound, irreversible hearing loss.


1992 ◽  
Vol 68 (4) ◽  
pp. 1087-1099 ◽  
Author(s):  
M. A. Ruggero ◽  
L. Robles ◽  
N. C. Rich

1. The vibratory response to two-tone stimuli was measured in the basilar membrane of the chinchilla cochlea by means of the Mossbauer technique or laser velocimetry. Measurements were made at sites with characteristic frequency (CF, the frequency at which an auditory structure is most sensitive) of 7-10 kHz, located approximately 3.5 mm from the oval window. 2. Two-tone suppression (reduction in the response to one tone due to the presence of another) was demonstrated for CF probe tones and suppressor tones with frequencies both higher and lower than CF, at moderately low stimulus levels, including probe-suppressor combinations for which responses to the suppressor were lower than responses to the probe tone alone. 3. For a fixed suppressor tone, suppression magnitude decreased as a function of increasing probe intensity. 4. The magnitude of suppression increased monotonically with suppressor intensity. 5. The rate of growth of suppression magnitude with suppressor intensity was higher for suppressors in the region below CF than for those in the region above CF. 6. For low-frequency suppressor tones, suppression magnitude varied periodically, attaining one or two maxima within each period of the suppressor tone. 7. Suppression was frequency tuned: for either above-CF or below-CF suppressor tones, suppression magnitude reached a maximum for probe frequencies near CF. 8. Cochlear damage or death diminished or abolished suppression. There was a clear positive correlation between magnitude of suppression and basilar-membrane sensitivity for responses to CF tones. 9. Suppression tended to be accompanied by small phase lags in responses to CF probe tones. 10. Because all of the features of two-tone suppression at the basilar membrane match qualitatively (and, generally, also quantitatively) the features of two-tone rate suppression in auditory-nerve fibers, it is concluded that neural two-tone rate suppression originates in mechanical phenomena at the basilar membrane. 11. Because the lability of mechanical suppression parallels the loss of sensitivity and frequency tuning due to outer hair cell dysfunction, the present findings suggest that mechanical two-tone suppression arises from an interaction between the outer hair cells and the basilar membrane.


2008 ◽  
Vol 100 (5) ◽  
pp. 2889-2898 ◽  
Author(s):  
Andrei N. Temchin ◽  
Nola C. Rich ◽  
Mario A. Ruggero

Frequency-threshold tuning curves were recorded in thousands of auditory-nerve fibers (ANFs) in chinchilla. Synthetic tuning curves with 21 characteristic frequencies (187 Hz to 19.04 kHz, spaced every 1/3 octave) were constructed by averaging individual tuning curves within 2/3-octave frequency bands. Tuning curves undergo a gradual transition in symmetry at characteristic frequencies (CFs) of 1 kHz and an abrupt change in shape at CFs of 3–4 kHz. For CFs ≤3 kHz, the lower limbs of tuning curves have similar slopes, about −18 dB/octave, but the upper limbs have slopes that become increasingly steep with increasing frequency and CF. For CFs >4 kHz, tuning curves normalized to the CF are nearly identical and consist of three segments. A tip segment, within 30–40 dB of CF threshold, has lower- and upper-limb slopes of −60 and +120 dB/octave, respectively, and is flanked by a low-frequency (“tail”) segment, with shallow slope, and a terminal high-frequency segment with very steep slope (several hundreds of dB/octave). The tuning curves of fibers innervating basal cochlear sites closely resemble basilar-membrane tuning curves computed with low isovelocity criteria. At the apex of the chinchilla cochlea, frequency tuning is substantially sharper for ANFs than for available recordings of organ of Corti vibrations.


1993 ◽  
Vol 70 (3) ◽  
pp. 1054-1075 ◽  
Author(s):  
X. Wang ◽  
M. B. Sachs

1. We have studied auditory responses to a set of speech-related narrowband sounds, single-formant stimuli (SFSs), in populations of auditory nerve fibers (ANFs). An analytic method was developed to extract the envelope of temporal discharge patterns of the ANF responses to nonsinusoidally modulated stimuli, whose spectra have multiple clusters of components. Such responses are often encountered in the auditory system when complex stimuli are used and have traditionally been studied by analyzing the fundamental component of the responses. 2. The envelope modulation in the SFSs is shown to be represented by the response patterns of ANFs. When the whole ANF population is considered, the information on modulation in stimulus envelope does not disappear at the highest sound level tested at all best frequencies (BFs) we studied (1-10 kHz). The representation is the best at medium sound levels and degrades at high sound levels. Low/medium-spontaneous rate (SR) ANFs showed greater envelope modulation in their responses at high sound levels than do high-SR ANFs. The quality of the representation at high sound levels is, on average, proportional to BF threshold of an ANF. On the basis of populations of ANFs with all SRs, the envelope modulation in the SFSs is represented over a wide range of sound levels. 3. We found that low-BF ANFs differ from high-BF ANFs in representing envelope modulation in the SFSs. For ANFs with BFs less than approximately 6 kHz, information on stimulus envelope is not only contained in spectral components near direct current but also in components at the vicinities of frequencies equal to BF and its multiples. In fact, for ANFs with BFs < 3 kHz, the contribution from spectral components centered at BF to overall response modulation is greater than that from spectral components near direct current. These findings indicate that, by using measures solely based on the fundamental component, the amount of modulation in the responses to narrowband stimuli is underestimated for low-BF ANFs. 4. Off-BF stimulation of ANFs with SFSs was found to result in increased envelope modulation in responses at high sound levels. The further away the stimulus is centered relative to unit BF, the greater the modulation it induces, provided that the stimulus is capable of exciting the unit. An SFS centered as close as 15% off unit BF can produce a significant increase in the modulation of responses at very high sound levels.(ABSTRACT TRUNCATED AT 400 WORDS)


2016 ◽  
Vol 113 (35) ◽  
pp. 9910-9915 ◽  
Author(s):  
Tianying Ren ◽  
Wenxuan He ◽  
David Kemp

It is commonly believed that the exceptional sensitivity of mammalian hearing depends on outer hair cells which generate forces for amplifying sound-induced basilar membrane vibrations, yet how cellular forces amplify vibrations is poorly understood. In this study, by measuring subnanometer vibrations directly from the reticular lamina at the apical ends of outer hair cells and from the basilar membrane using a custom-built heterodyne low-coherence interferometer, we demonstrate in living mouse cochleae that the sound-induced reticular lamina vibration is substantially larger than the basilar membrane vibration not only at the best frequency but surprisingly also at low frequencies. The phase relation of reticular lamina to basilar membrane vibration changes with frequency by up to 180 degrees from ∼135 degrees at low frequencies to ∼-45 degrees at the best frequency. The magnitude and phase differences between reticular lamina and basilar membrane vibrations are absent in postmortem cochleae. These results indicate that outer hair cells do not amplify the basilar membrane vibration directly through a local feedback as commonly expected; instead, they actively vibrate the reticular lamina over a broad frequency range. The outer hair cell-driven reticular lamina vibration collaboratively interacts with the basilar membrane traveling wave primarily through the cochlear fluid, which boosts peak responses at the best-frequency location and consequently enhances hearing sensitivity and frequency selectivity.


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