The review is both timely and relevant, as recent findings have shown the tectorial membrane plays a more dynamic role in hearing than hitherto suspected, and that many forms of deafness can result ...from mutations in tectorial membrane proteins.
Main themes covered are the molecular composition, the structural organization and properties of the tectorial membrane, the role of the tectorial membrane as a second resonator and a structure within which there is significant longitudinal coupling, and how mutations in tectorial membrane proteins cause deafness in mice and men.
Findings from experimental models imply that the tectorial membrane plays multiple, critical roles in hearing. These include coupling elements along the length of the cochlea, supporting a travelling wave and ensuring the gain and timing of cochlear feedback are optimal. The clinical findings suggest stable, moderate-to-severe forms of hereditary hearing loss may be diagnostic of a mutation in TECTA, a gene encoding one of the major, noncollagenous proteins of the tectorial membrane.
It was first suggested by Gold in 1948 1 that the exquisite sensitivity and frequency selectivity of the mammalian cochlea is due to an active process referred to as the cochlear amplifier. It is ...thought that this process works by pumping energy to augment the otherwise damped sound-induced vibrations of the basilar membrane 2–4, a mechanism known as negative damping. The existence of the cochlear amplifier has been inferred from comparing responses of sensitive and compromised cochleae 5 and observations of acoustic emissions 6, 7 and through mathematical modeling 8, 9. However, power amplification has yet to be demonstrated directly. Here, we prove that energy is indeed produced in the cochlea on a cycle-by-cycle basis. By using laser interferometry 10, we show that the nonlinear component of basilar-membrane responses to sound stimulation leads the forces acting on the membrane. This is possible only in active systems with negative damping 11. Our finding provides the first direct evidence for power amplification in the mammalian cochlea. The finding also makes redundant current hypotheses of cochlear frequency sharpening and sensitization that are not based on negative damping.
The sensory hair cells of amniote hearing organs are usually distributed in tonotopic array from low to high frequencies and are very sensitively and sharply tuned to acoustic stimulation. Frequency ...tuning and tonotopicity of non-mammalian auditory hair cells is due largely to intrinsic properties of the hair cells 1, but frequency tuning and tonotopic organisation of the mammalian cochlea has an extrinsic basis in the basilar membrane (BM); a spiralling ribbon of collagen-rich extracellular matrix that decreases in stiffness from the high-frequency base of the cochlea to the low-frequency apex 2,3. Sensitive frequency tuning is due to amplification, which specifically boosts low-level input to the mechanosensitive hair cells at their tonotopic location to overcome viscous damping 1–3. In non-mammalian hearing organs, at least, amplification is attributed to calcium-mediated hair bundle motion 1. In the mammalian cochlea, amplification is the remit of the sensory-motor outer hair cells (OHCs), located within the organ of Corti to exercise maximum mechanical effect on the motion of the BM and transmit cochlear responses to the adjacent sensory inner hair cells (IHCs) and, consequently, to the auditory nerve 1–3 (Figure 1A). OHCs behave like piezoelectric actuators, developing forces along their long axis in response to changes in membrane potential 2. These forces are due to voltage-dependent conformational changes in the motor molecule prestin, which is densely distributed in the OHC lateral membranes 2.
Distortion product otoacoustic emissions (DPOAEs) were recorded from guinea pigs in response to simultaneous increases in the levels of high frequency primary tones in the presence of a low frequency ...biasing tone of 30 Hz at 120 dB SPL. The DPOAE amplitudes plotted as functions of the biasing tone phase angle show distinctive repeatable minima, which are identical to the amplitude notches observed for the distortion products at the output of a single saturating non-linearity. The number of the amplitude minima grows with increasing order of the DPOAE, a feature that is also reproduced by the model. The model of DPOAE generation due to a single saturating non-linearity does not explain the experimentally observed asymmetry of the response of the DPOAEs to rising and falling half cycles of the biasing tone. This asymmetry is attributed to a hypothetical mechanism, which adjusts the operating point of the outer hair cell’s mechanoelectrical transducer. Experimental data were consistent with a hypothesis that, for the parameters of stimulation used in this study, both lower and upper sideband DPOAEs are dominated by emission generated from a single and spatially localized place in the cochlea.
The round window (RW) membrane provides pressure relief when the cochlea is excited by sound. Here, we report measurements of cochlear function from guinea pigs when the cochlea was stimulated at ...acoustic frequencies by movements of a miniature magnet which partially occluded the RW. Maximum cochlear sensitivity, corresponding to subnanometre magnet displacements at neural thresholds, was observed for frequencies around 20 kHz, which is similar to that for acoustic stimulation. Neural response latencies to acoustic and RW stimulation were similar and taken to indicate that both means of stimulation resulted in the generation of conventional travelling waves along the cochlear partition. It was concluded that the relatively high impedance of the ossicles, as seen from the cochlea, enabled the region of the RW not occluded by the magnet, to act as a pressure shunt during RW stimulation. We propose that travelling waves, similar to those owing to acoustic far-field pressure changes, are driven by a jet-like, near-field component of a complex pressure field, which is generated by the magnetically vibrated RW. Outcomes of research described here are theoretical and practical design principles for the development of new types of hearing aids, which use near-field, RW excitation of the cochlea.
Morphometry of the lamina reticularis of the guinea pig cochlea was performed using scanning electron microscopy. Seventy-four geometrical parameters of the lamina reticularis, the bundles of ...stereocilia, and individual stereocilia, in all rows of hair cells and within the individual hair cells, were measured at ten equally spaced locations along the longitudinal direction of the cochlea. Variations of the parameters versus the longitudinal coordinate were statistically analyzed and fitted with polynomials (constant, linear, or quadratic). Our data show that a unique set of geometrical parameters of inner and outer hair cells is typical for every frequency-dependent position at the lamina reticularis. Morphology of the outer hair cell structures varies more than respective parameters of the inner hair cells. Mechanical modeling using the obtained geometrical parameters provides a novel glance at the mechanical characteristics with respect to the cochlear tonotopy.
A laser-diode forms the basis of a displacement sensitive homodyne interferometer suitable for measurements from poorly reflective surfaces. The compact and cost-effective interferometer utilizes the ...self-mixing effect when laser light reflected from a moving target re-enters the laser cavity and causes phase dependent changes of the lasing intensity. A piezo positioner was used to displace the interferometer with known frequency and amplitude as a basis for real-time calibration of the interferometer's sensitivity. The signal-processing algorithm is described that allows measurements in presence of high amplitude noise leading to variation of the interferometer's operating point. Measurements of sound-induced basilar membrane displacements were made in the intact cochleae of rodents by focusing the laser beam of the interferometer through the transparent round window membrane. The interferometer provides a viable means for making subnanometre mechanical measurements from structures in the inner ears of small mammals, where opening of the cochlea is not practicable.
The mammalian inner ear contains sense organs responsible for detecting sound, gravity and linear acceleration, and angular acceleration. Of these organs, the cochlea is involved in hearing, while ...the sacculus and utriculus serve to detect linear acceleration. Recent evidence from birds and mammals, including humans, has shown that the sacculus, a hearing organ in many lower vertebrates, has retained some of its ancestral acoustic sensitivity. Here we provide not only more evidence for the retained acoustic sensitivity of the sacculus, but we also found that acoustic stimulation of the sacculus has behavioral significance in mammals. We show that the amplitude of an elicited auditory startle response is greater when the startle stimuli are presented simultaneously with a low-frequency masker, including masker tones that are outside the sensitivity range of the cochlea. Masker-enhanced auditory startle responses were also observed in otoconia-absent Nox3 mice, which lack otoconia but have no obvious cochlea pathology. However, masker enhancement was not observed in otoconia-absent Nox3 mice if the low-frequency masker tones were outside the sensitivity range of the cochlea. This last observation confirms that otoconial organs, most likely the sacculus, contribute to behavioral responses to low-frequency sounds in mice.
1 School of Life Sciences, University of Sussex, Brighton, United Kingdom; and 2 Department of Developmental Neurobiology, St. Jude Children's Research Hospital, Memphis, Tennessee
Submitted 31 ...October 2007;
accepted in final form 30 January 2008
Electrically evoked otoacoustic emissions are sounds emitted from the inner ear when alternating current is injected into the cochlea. Their temporal structure consists of short- and long-delay components and they have been attributed to the motile responses of the sensory-motor outer hair cells of the cochlea. The nature of these motile responses is unresolved and may depend on either somatic motility, hair bundle motility, or both. The short-delay component persists after almost complete elimination of outer hair cells. Outer hair cells are thus not the sole generators of electrically evoked otoacoustic emissions. We used prestin knockout mice, in which the motor protein prestin is absent from the lateral walls of outer hair cells, and Tecta ENT/ ENT mice, in which the tectorial membrane, a structure with which the hair bundles of outer hair cells normally interact, is vestigial and completely detached from the organ of Corti. The amplitudes and delay spectra of electrically evoked otoacoustic emissions from Tecta ENT/ ENT and Tecta +/+ mice are very similar. In comparison with prestin +/+ mice, however, the short-delay component of the emission in prestin –/– mice is dramatically reduced and the long-delay component is completely absent. Emissions are completely suppressed in wild-type and Tecta ENT/ ENT mice at low stimulus levels, when prestin-based motility is blocked by salicylate. We conclude that near threshold, the emissions are generated by prestin-based somatic motility.
Address for reprint requests and other correspondence: I. Russell, University of Sussex, School of Life Sciences, Falmer, Brighton, BN1 9RE, UK (E-mail: i.j.russell{at}sussex.ac.uk )
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