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The basilar membrane (BM) of the mammalian cochlea constitutes a spiraling acellular ribbon that is intimately attached to the organ of Corti. Its graded stiffness, increasing from apex to the base of the cochlea provides the mechanical basis for sound frequency analysis. Despite its central role in auditory signal transduction, virtually nothing is known about the BM’s structural development. Using polarized light microscopy, the present study characterized the architectural transformations of freshly dissected BM at time points during postnatal development and maturation. The results indicate that the BM structural elements increase progressively in size, becoming radially aligned and more tightly packed with maturation and reach the adult structural signature by postnatal day 20 (P20). The findings provide insight into structural details and developmental changes of the mammalian BM, suggesting that BM is a dynamic structure that changes throughout the life of an animal.

Cochlear hair cells convert sound vibration into electrical potential, and loss of these cells diminishes auditory function. In response to mechanical stimuli, piezoelectric materials generate electricity, suggesting that they could be used in place of hair cells to create an artificial cochlear epithelium. Here, we report that a piezoelectric membrane generated electrical potentials in response to sound stimuli that were able to induce auditory brainstem responses in deafened guinea pigs, indicating its capacity to mimic basilar membrane function. In addition, sound stimuli were transmitted through the external auditory canal to a piezoelectric membrane implanted in the cochlea, inducing it to vibrate. The application of sound to the middle ear ossicle induced voltage output from the implanted piezoelectric membrane. These findings establish the fundamental principles for the development of hearing devices using piezoelectric materials, although there are many problems to be overcome before practical application.

Mammals detect sound through mechanosensitive cells of the cochlear organ of Corti that rest on the basilar membrane (BM). Motions of the BM and organ of Corti have been studied at the cochlear base in various laboratory animals, and the assumption has been that the cochleas of all mammals work similarly. In the classic view, the BM attaches to a stationary osseous spiral lamina (OSL), the tectorial membrane (TM) attaches to the limbus above the stationary OSL, and the BM is the major moving element, with a peak displacement near its center. Here, we measured the motion and studied the anatomy of the human cochlear partition (CP) at the cochlear base of fresh human cadaveric specimens. Unlike the classic view, we identified a soft-tissue structure between the BM and OSL in humans, which we name the CP “bridge.” We measured CP transverse motion in humans and found that the OSL moved like a plate hinged near the modiolus, with motion increasing from the modiolus to the bridge. The bridge moved almost as much as the BM, with the maximum CP motion near the bridge–BM connection. BM motion accounts for 100% of CP volume displacement in the classic view, but accounts for only 27 to 43% in the base of humans. In humans, the TM–limbus attachment is above the moving bridge, not above a fixed structure. These results challenge long-held assumptions about cochlear mechanics in humans. In addition, animal apical anatomy (in SI Appendix) doesn’t always fit the classic view.

Auditory sensory outer hair cells are thought to amplify sound-induced basilar membrane vibration through a feedback mechanism to enhance hearing sensitivity. For optimal amplification, the outer hair cell-generated force must act on the basilar membrane at an appropriate time at every cycle. However, the temporal relationship between the outer hair cell-driven reticular lamina vibration and the basilar membrane vibration remains unclear. By measuring sub-nanometer vibrations directly from outer hair cells using a custom-built heterodyne low-coherence interferometer, we demonstrate in living gerbil cochleae that the reticular lamina vibration occurs after, not before, the basilar membrane vibration. Both tone- and click-induced responses indicate that the reticular lamina and basilar membrane vibrate in opposite directions at the cochlear base and they oscillate in phase near the best-frequency location. Our results suggest that outer hair cells enhance hearing sensitivity through a global hydromechanical mechanism, rather than through a local mechanical feedback as commonly supposed. What is the quietest sound the ear can detect? All sounds begin as vibrating air molecules, which enter the ear and cause the eardrum to vibrate. We can detect vibrations that move the eardrum by a distance of less than one picometer. That’s one thousandth of a nanometer, or about 100 times smaller than a hydrogen atom. But how does the ear achieve this level of sensitivity? Vibrations of the eardrum cause three small bones within the middle ear to vibrate. The vibrations then spread to the cochlea, a fluid-filled spiral structure in the inner ear. Tiny hair cells lining the cochlea move as a result of the vibrations. There are two types of hair cells: inner and outer. Outer hair cells amplify the vibrations. It is this amplification that enables us to detect such small movements of the eardrum. Inner hair cells then convert the amplified vibrations into electrical signals, which travel via the auditory nerve to the brain. The bases of outer hair cells are connected to a structure called the basilar membrane, while their tops are anchored to a structure called the reticular lamina. It was generally assumed that outer hair cells amplify vibrations of the basilar membrane via a local positive feedback mechanism that requires the hair cells to vibrate first. But by comparing the timing of reticular lamina and basilar membrane vibrations in gerbils, He et al. show that this is not the case. Outer hair cells vibrate after the basilar membrane, not before. This indicates that outer hair cells use a mechanism other than commonly assumed local feedback to amplify sounds. The results presented by He et al. change our understanding of how the cochlea works, and may help bioengineers to design better hearing aids and cochlea implants. Millions of patients worldwide who suffer from hearing loss may ultimately stand to benefit.

The traveling wave phenomenon in the artificial basilar membrane (ABM) plays a crucial role in the frequency selectivity and electromechanical signal generation of cochlear implants. Continuous measurement of traveling wave propagation remains challenging due to its rapid spatial displacement variation and the requirement for biomimetic conditions in liquid environments. To address this, we developed a laser Doppler optical scanning system with high spatiotemporal resolution, combined with a fixation device replicating cochlear boundary constraints, and successfully captured the traveling wave propagation process. The traveling wave characteristics of the ABM, including propagation time, velocity, frequency selectivity, and local resonance, are revealed. Experimental results indicate that fluid-mass loading and coupling effects significantly reduce the resonance frequency from 9.3–15.4 kHz in air to 1.9–4.9 kHz in liquid and decrease the propagation velocity from 199.20 m/s to 61.78 m/s under our typical experimental conditions. By correlating spatial modes and local resonances with theoretical analysis, we observe that as the resonance frequency increases, the traveling wave propagates faster, reducing propagation delay. The quantification of traveling wave propagation characteristics provides a critical theoretical and experimental foundation for improving the tonotopic accuracy and biological fidelity of cochlear implants.

Background Despite significant anatomical variation amongst patients, cochlear implant frequency-mapping has traditionally followed a patient-independent approach. Basilar membrane (BM) length is required for patient-specific frequency-mapping, however cochlear duct length (CDL) measurements generally extend to the apical tip of the entire cochlea or have no clearly defined end-point. By characterizing the length between the end of the BM and the apical tip of the entire cochlea (helicotrema length), current CDL models can be corrected to obtain the appropriate BM length. Synchrotron radiation phase-contrast imaging has made this analysis possible due to the soft-tissue contrast through the entire cochlear apex. Methods Helicotrema linear length and helicotrema angular length measurements were performed on synchrotron radiation phase-contrast imaging data of 14 cadaveric human cochleae. On a sub-set of six samples, the CDL to the apical tip of the entire cochlea (CDL TIP ) and the BM length (CDL BM ) were determined. Regression analysis was performed to assess the relationship between CDL TIP and CDL BM . Results The mean helicotrema linear length and helicotrema angular length values were 1.6 ± 0.9 mm and 67.8 ± 37.9 degrees, respectively. Regression analysis revealed the following relationship between CDL TIP and CDL BM : CDL BM  = 0.88(CDL TIP ) + 3.71 ( R 2  = 0.995). Conclusion This is the first known study to characterize the length of the helicotrema in the context of CDL measurements. It was determined that the distance between the end of the BM and the tip of the entire cochlea is clinically consequential. A relationship was determined that can predict the BM length of an individual patient based on their respective CDL measured to the apical tip of the cochlea.

Low-frequency hearing is critically important for speech and music perception, but no mechanical measurements have previously been available from inner ears with intact low-frequency parts. These regions of the cochlea may function in ways different from the extensively studied high-frequency regions, where the sensory outer hair cells produce force that greatly increases the sound-evoked vibrations of the basilar membrane. We used laser interferometry in vitro and optical coherence tomography in vivo to study the low-frequency part of the guinea pig cochlea, and found that sound stimulation caused motion of a minimal portion of the basilar membrane. Outside the region of peak movement, an exponential decline in motion amplitude occurred across the basilar membrane. The moving region had different dependence on stimulus frequency than the vibrations measured near the mechanosensitive stereocilia. This behavior differs substantially from the behavior found in the extensively studied high-frequency regions of the cochlea.

Frequency tuning in the cochlea is determined by the passive mechanical properties of the basilar membrane and active feedback from the outer hair cells, sensory-effector cells that detect and amplify sound-induced basilar membrane motions. The sensory hair bundles of the outer hair cells are imbedded in the tectorial membrane, a sheet of extracellular matrix that overlies the cochlea's sensory epithelium. The tectorial membrane contains radially organized collagen fibrils that are imbedded in an unusual striated-sheet matrix formed by two glycoproteins, α-tectorin (Tecta) and β-tectorin (Tectb). In Tectb −/− mice the structure of the striated-sheet matrix is disrupted. Although these mice have a low-frequency hearing loss, basilar-membrane and neural tuning are both significantly enhanced in the high-frequency regions of the cochlea, with little loss in sensitivity. These findings can be attributed to a reduction in the acting mass of the tectorial membrane and reveal a new function for this structure in controlling interactions along the cochlea.

Purpose A probe that binds to unfixed collagen fibrils was used to image the shapes and fibrous properties of the TM and BM. The probe (CNA35) is derived from the bacterial adhesion protein CNA. We present confocal images of hydrated gerbil TM, BM, and other cochlear structures stained with fluorescently labeled CNA35. A primary purpose of this article is to describe the use of the CNA35 collagen probe in the cochlea. Methods Recombinant poly-histidine-tagged CNA35 was expressed in Escherichia coli , purified by cobalt-affinity chromatography, fluorescence labeled, and further purified by gel filtration chromatography. Cochleae from freshly harvested gerbil bullae were irrigated with and then incubated in CNA35 for periods ranging from 2 h — overnight. The cochleae were fixed, decalcified, and dissected. Isolated cochlear turns were imaged by confocal microscopy. Results The CNA35 probe stained the BM and TM, and volumetric imaging revealed the shape of these structures and the collagen fibrils within them. The limbal zone of the TM stained intensely. In samples from the cochlear base, intense staining was detected on the side of the TM that faces hair cells. In the BM pectinate zone, staining was intense at the upper and lower boundaries. The BM arcuate zone was characterized by a prominent longitudinal collagenous structure. The spiral ligament, limbus and lamina stained for collagen, and within the spiral limbus the habenula perforata were outlined with intense staining. Conclusion The CNA35 probe provides a unique and useful view of collagenous structures in the cochlea.

A spiral‐artificial basilar membrane (S‐ABM) sensor is reported that mimics the basilar membrane (BM) of the human cochlea and can detect sound by separating it into 24 sensing channels based on the frequency band. For this, an analytical function is proposed to design the width of the BM so that the frequency bands are linearly located along the length of the BM. To fabricate the S‐ABM sensor, a spiral‐shaped polyimide film is used as a vibrating membrane, with maximum displacement at locations corresponding to specific frequency bands of sound, and attach piezoelectric sensor modules made of poly(vinylidene fluoride‐trifluoroethylene) film on top of the polyimide film to measure the vibration amplitude at each channel location. As the result, the S‐ABM sensor implements a characteristic frequency band of 96‐12,821 Hz and 24‐independent critical bands. Using real‐time signals from discriminate channels, it is demonstrated that the sensor can rapidly identify the operational noises from equipment processes as well as vehicle sounds from environmental noises on the road. The sensor can be used in a variety of applications, including speech recognition, dangerous situation recognition, hearing aids, and cochlear implants, and more. The spiral‐artificial basilar membrane (S‐ABM) sensor is a biomimetic acoustic sensor consisting of an artificial basilar membrane (ABM) that discriminates sound into frequency bands, 24 independent critical bands, and piezoelectric sensor modules that generates an electrical signal by the vibration of the S‐ABM. An early detection system is developed that can detect and distinguish potential hazards that may occur in industrial processes and driving situations through the sensor.