Molecular mechanisms of sound amplification in the mammalian cochlea

Abstract

Mammalian hearing depends on the enhanced mechanical properties of the basilar membrane within the cochlear duct. The enhancement arises through the action of outer hair cells that act like force generators within the organ of Corti. Simple considerations show that underlying mechanism of somatic motility depends on local area changes within the lateral membrane of the cell. The molecular basis for this phenomenon is a dense array of particles that are inserted into the basolateral membrane and that are capable of sensing membrane potential field. We show here that outer hair cells selectively take up fructose, at rates high enough to suggest that a sugar transporter may be part of the motor complex. The relation of these findings to a recent candidate for the molecular motor is also discussed.T he inner ear of mammals has evolved to analyze sounds over a wide range of frequencies. In humans this range covers about 8 octaves, but it can be both more restricted (hearing in mice covers only 3.5 octaves) or, as in some cetaceans, extend over 10 octaves and use infrasound. Auditory specialists such as the echolocating bats may employ frequencies well into the ultrasonic. When considering how a hearing organ of the size of a pea or even smaller can perform such engineering feats, cochlear construction provides the clues. The cochlea in all these diverse mammalian species shows a remarkable conservation of design. A common feature of all mammalian cochleae is that, within the duct, the basilar membrane supports a propagated traveling wave. In mammals, the basilar membrane performs as a mechanical selector of sound frequencies and maps component frequencies in a complex sound onto a position in the duct. A second feature found throughout mammalian cochleae is the presence of two morphologically distinct sets of hair cells, inner (IHCs) and outer hair cells (OHCs). The cells lie within the organ of Corti, which runs along the full length of the basilar membrane and is shown in cross section in Fig. 1a. Hence the linkage between basilar membrane motion and the deflection of the sensory hair bundles of hair cells recodes sound frequency and intensity into a firing pattern of the afferents of the auditory nerve. The basilar membrane thus acts as a preconditioner of the sound signal. Other vertebrate genera use modified designs of hearing organ (using, for example, local filtering based on electrical resonance of their membranes or mechanical resonance of their hair cell stereocilia). The mammalian cochlear design ensures that even high frequencies can be detected by using material and mechanical properties of the macroscopic structures of the cochlea (1).A wide range of measurements have now shown that the basilar membrane has a mechanical pattern of vibration that is under physiological control. Optimally, threshold sound detection elicits a peak deflection of about 0.3 nm. This exceeds what a membrane of the same mechanical construction can achieve and an energy source is necessarily involved. Indeed, it was suspected mo...

Cochlear Outer Hair Cell Motility

“…To test for the presence of this protein in isolated cells OHCs, glucose in the external solution was isosmotically replaced with fructose. OHCs reversibly shortened, compatible with the proposal that water was moving into the cells along with transported fructose (15,111). The uptake was compatible with transport with a Michaelis constant K m of 16 mM and comparable to that found for the fructose transporter GLUT5 in other systems.…”

Enhancement of sensitivity gain and frequency tuning by coupling of active hair bundles

“…Two mechanisms have been suggested. First, outer hair cell electromotility, which involves cell body contractions (9), could be an important element of the amplifier in the mammalian cochlea (10)(11)(12). Second, the hair bundle, which is the mechanosensitive organelle at the apical surface of the hair cell, could generate forces and movements that contribute to amplification (13)(14)(15).…”

A 2-D silicon cochlea with an improved automatic quality factor control-loop

“…The outer hair cells (OHCs) are instrumental in the active behaviour of the biological cochlea [2]. Many researchers have shown that the OHCs poise themselves on or close to a dynamical nonlinearity known as a Hopf bifurcation and that this is the source of the nonlinear amplification observed in the biological cochlea ( [3], [4], [5] and [6]).…”