Somatic motility and hair bundle mechanics, are both necessary for cochlear amplification?

Abstract

Hearing organs have evolved to detect sounds across several orders of magnitude of both intensity and frequency. Detection limits are at the atomic level despite the energy associated with sound being limited thermodynamically. Several mechanisms have evolved to account for the remarkable frequency selectivity, dynamic range, and sensitivity of these various hearing organs, together termed the active process or cochlear amplifier. Similarities between hearing organs of disparate species provides insight into the factors driving the development of the cochlear amplifier. These properties include: a tonotopic map, the emergence of a two hair cell system, the separation of efferent and afferent innervations, the role of the tectorial membrane, and the shift from intrinsic tuning and amplification to a more end organ driven process. Two major contributors to the active process are hair bundle mechanics and outer hair cell electromotility, the former present in all hair cell organs tested, the latter only present in mammalian cochlear outer hair cells. Both of these processes have advantages and disadvantages, and how these processes interact to generate the active process in the mammalian system is highly disputed. A hypothesis is put forth suggesting that hair bundle mechanics provides amplification and filtering in most hair cells, while in mammalian cochlea, outer hair cell motility provides the amplification on a cycle by cycle basis driven by the hair bundle that provides frequency selectivity (in concert with the tectorial membrane) and compressive nonlinearity. Separating components of the active process may provide additional sites for regulation of this process.

Figure 1

Evolution of hearing organs. An evolutionary tree of the various organisms discussed in this review shows that insects and amphibians are furthest from mammals, and stem reptiles (red) are the closest. Adapted from (Manley, Koppl, 1998).

Figure 2

Principles of mammalian hair cell mechanisms. (A) Stereocilia at the apex of the hair cell are responsible for mechanotransduction. Positive deflection of stereocilia (black) causes an opening of the mechanotransduction channels leading to an influx of cations into the cell. The calcium component of the current drives an adaptation process, a reduction in current during a constant stimulus that is thought to underlie force generation by the hair bundle. Negative deflection of the stereocilia (red) causes transduction channels to close, triggering reverse adaptation back to the resting level. Asterisks indicate potential sites of force generation. (B) Somatic motility occurs in the lateral membrane of the hair cell (cross-hatched area). A hyperpolarization of membrane voltage leads to an increase in the lateral membrane surface area, hence an expansion of the hair cell. A depolarization in membrane voltage leads to a decrease in lateral membrane surface area and a contraction of the hair cell. (C) Cochlear mechanisms at work in the mammalian cochlea include active hair bundle motions coupled through the tectorial membrane (black arrow) and somatic motility (blue arrows) which feedback onto basilar membrane motion (red arrow).

Figure 3

Comparison of threshold and tuning curves across vertebrate species. (A) Audiograms were obtained from (Fay, 1988) for all species except the bobtail skink which came from (Manley, 2000a) and the bush cricket from (Stumpner, Molina, 2006). All curves are behavioral audiograms except for the bobtail skink and the bush cricket which are neural audiograms. (B) Tuning curves for each organism were chosen with center frequencies near their lowest threshold in order to compare the shapes of tuning curves across species, therefore the sharpness of tuning (Q_10DB) cannot be strictly compared here because these values vary depending on center frequencies in different species. Center frequencies for the tuning curves and data sources are as follows: chinchilla 8.1 kHz (Ruggero et al., 1990), guinea pig 7 kHz (Pickles, 1984), mouse 10 kHz (Taberner, Liberman, 2005), chicken 1.7 kHz (Salvi et al., 1992), barn owl 4.2 kHz (Köppl, 1997), bobtail skink 1.2 kHz (Manley et al., 1988), turtle 330 Hz (Crawford, Fettiplace, 1980), frog 751 Hz (Stiebler, Narins, 1990), bush cricket 20kHz (Stumpner, Molina, 2006).

Figure 4

Schematic representation of the unifying theory of cochlear amplification. (A) In some vertebrates, like turtle basilar papilla shown here, intrinsic mechanisms within the hair cell are enough to produce sharp tuning and amplification without basilar membrane tuning. Iso-intensity responses of the hair cell (blue) and basilar membrane (red) are schematized for 3 different intensity levels. Red arrows indicate direction of sound stimulation. (B) Hair cells of the mammalian cochlea alone are not able to feedback onto the basilar membrane, however the hair bundle has some intrinsic tuning properties providing it with compressive non-linearily and some tuning as compared to corresponding basilar membrane motion. (C) The introduction of a tectorial membrane further sharpens tuning with some amplification provided by the concerted effort of multiple hair bundles that can feedback onto basilar membrane. (D) The addition of somatic motility provides further gain to the system, which is fed back onto the basilar membrane. The gain is necessary to bring the motion above the level of the noise (cross-hatched area) in the system to make the stimulus detectable.