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Biophysics of the inner ear and beyond

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Number 1 Reichenbach, T. & Hudspeth, A.J. 2014. The Physics of Hearing: Fluid Mechanics and the Active Process of the Inner Ear. Reports on Progress in Physics 10.1088/0034-4885/77/7/076601 Abstract Most sounds of interest consist of complex, time-dependent admixtures of tones of diverse frequencies and variable amplitudes. To detect and process these signals, the ear employs a highly nonlinear, adaptive, real-time spectral analyzer: the cochlea. Sound excites vibration of the eardrum and the three miniscule bones of the middle ear, the last of which acts as a piston to initiate oscillatory pressure changes within the liquid-filled chambers of the cochlea. The basilar membrane, an elastic band spiralling along the cochlea between two of these chambers, responds to these pressures by conducting a largely independent traveling wave for each frequency component of the input. Because the basilar membrane is graded in mass and stiffness along its length, however, each traveling wave grows in magnitude and decreases in wavelength until it peaks at a specific, frequency-dependent position: low frequencies propagate to the cochlear apex, whereas high frequencies culminate at the base. The oscillations of the basilar membrane deflect hair bundles, the mechanically sensitive organelles of the ear’s sensory receptors, the hair cells. As mechanically sensitive ion channels open and close, each hair cell responds with an electrical signal that is chemically transmitted to an afferent nerve fibre and thence into the brain. In addition to transducing mechanical inputs, hair cells amplify them by two means. Channel gating endows a hair bundle with negative stiffness, an instability that interacts with the motor protein myosin-1c to produce a mechanical amplifier and oscillator. Acting through the piezoelectric membrane protein prestin, electrical responses also cause outer hair cells to elongate and shorten, thus pumping energy into the basilar membrane’s movements. The two forms of motility constitute an active process that amplifies mechanical inputs, sharpens frequency discrimination, and confers a compressive nonlinearity on responsiveness. These features arise because the active process operates near a Hopf bifurcation, the generic properties of which explain several key features of hearing. Moreover, when the gain of the active process rises sufficiently in ultraquiet circumstances, the system traverses the bifurcation and even a normal ear actually emits sound. The remarkable properties of hearing thus stem from the propagation of traveling waves on a nonlinear and excitable medium.

Number 2 Reichenbach, T & Hudspeth, A. J. 2010. A Ratchet Mechanism for Amplification in Low-frequency Mammalian Hearing. PNAS Vol.107. No 11. 4973-4978. Summary The sensitivity and frequency selectivity of hearing result from tuned amplification by an active process in the mechanoreceptive hair cells. In most vertebrates, the active process stems from the active motility of hair bundles. The mammalian cochlea exhibits an additional form of mechanical activity termed electromotility: its outer hair cells (OHCs) change length upon electrical stimulation. The relative contributions of these two mechanisms to the active process in the mammalian inner ear is the subject of intense current debate. Here, we show that active hair-bundle motility and electromotility can together implement an efficient mechanism for amplification that functions like a ratchet: Sound-evoked forces, acting on the basilar membrane, are transmitted to the hair bundles, whereas electromotility decouples active hair-bundle forces from the basilar membrane. This unidirectional coupling can extend the hearing range well below the resonant frequency of the basilar membrane. It thereby provides a concept for low frequency hearing that accounts for a variety of unexplained experimental observations from the cochlear apex, including the shape and phase behaviour of apical tuning curves, their lack of significant nonlinearities, and the shape changes of threshold tuning curves of auditory-nerve fibres along the cochlea. The ratchet mechanism constitutes a general design principle for implementing mechanical amplification in engineering applications.

Number 3 Reichenbach, T., Stefanovic, A., Nin, F., & Hudspeth, A. J. 2012. Waves on Reissner’s Membrane: A Mechanism for the Propagation of Otoacoustic Emissions from the Cochlea. Cell Reports 1 374-384 April 2012. Summary Sound is detected and converted into electrical signals within the ear. The cochlea not only acts as a passive detector of sound, however, but can also produce tones itself. These otoacoustic emissions are a striking manifestation of the cochlea’s mechanical active process. A controversy remains of how these mechanical signals propagate back to the middle ear, from which they are emitted as sound. Here, we combine theoretical and experimental studies to show that mechanical signals can be transmitted by waves on Reissner’s membrane, an elastic structure within the cochlea. We develop a theory for wave propagation on Reissner’s membrane and its role in otoacoustic emissions. Employing a scanning laser interferometer, we measure traveling waves on Reissner’s membrane in the gerbil, guinea pig, and chinchilla. The results are in accord with the theory and thus support a role for Reissner’s membrane in otoacoustic emissions.

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