In vivo evidence for a cochlear amplifier in the hair-cell bundle of lizards

Vertebrate sensory hair cells achieve high sensitivity and frequency selectivity by adding self-generated mechanical energy to low-level signals. This allows them to detect signals that are smaller than thermal molecular motion and to achieve significant resonance amplitudes and frequency selectivity despite the viscosity of the surrounding fluid. In nonmammals, a great deal of in vitro evidence indicates that the active process responsible for this amplification is intimately associated with the hair cells' transduction channels in the stereovillar bundle. Here, we provide in vivo evidence of hair-cell bundle involvement in active processes. Electrical stimulation of the inner ear of a lizard at frequencies typical for this hearing organ induced low-level otoacoustic emissions that could be modulated by low-frequency sound. The unique modulation pattern permitted the tracing of the active process involved to the stereovillar bundles of the sensory hair cells. This supports the notion that, in nonmammals, the cochlear amplifier in the hair cells is driven by a bundle motor system.

Comparing in vitro, in situ, and in vivo experimental data in a three-dimensional model of mammalian cochlear mechanics

Normal mammalian hearing is refined by amplification of the motion of the cochlear partition. This partition, comprising the organ of Corti sandwiched between the basilar and tectorial membranes, contains the outer hair cells that are thought to drive this amplification process. Force generation by outer hair cells has been studied extensively in vitro and in situ, but, to understand cochlear amplification fully, it is necessary to characterize the role played by each of the components of the cochlear partition in vivo. Observations of cochlear partition motion in vivo are severely restricted by its inaccessibility and sensitivity to surgical trauma, so, for the present study, a computer model has been used to simulate the operation of the cochlea under different experimental conditions. In this model, which uniquely retains much of the three-dimensional complexity of the real cochlea, the motions of the basilar and tectorial membranes are fundamentally different during in situ- and in vivo-like conditions. Furthermore, enhanced outer hair cell force generation in vitro leads paradoxically to a decrease in the gain of the cochlear amplifier during sound stimulation to the model in vivo. These results suggest that it is not possible to extrapolate directly from experimental observations made in vitro and in situ to the normal operation of the intact organ in vivo.

Active hair-bundle movements can amplify a hair cell’s response to oscillatory mechanical stimuli

To enhance their mechanical sensitivity and frequency selectivity, hair cells amplify the mechanical stimuli to which they respond. Although cell-body contractions of outer hair cells are thought to mediate the active process in the mammalian cochlea, vertebrates without outer hair cells display highly sensitive, sharply tuned hearing and spontaneous otoacoustic emissions. In these animals the amplifier must reside elsewhere. We report physiological evidence that amplification can stem from active movement of the hair bundle, the hair cell’s mechanosensitive organelle. We performed experiments on hair cells from the sacculus of the bullfrog. Using a two-compartment recording chamber that permits exposure of the hair cell’s apical and basolateral surfaces to different solutions, we examined active hair-bundle motion in circumstances similar to those in vivo. When the apical surface was bathed in artificial endolymph, many hair bundles exhibited spontaneous oscillations of amplitudes as great as 50 nm and frequencies in the range 5 to 40 Hz. We stimulated hair bundles with a flexible glass probe and recorded their mechanical responses with a photometric system. When the stimulus frequency lay within a band enclosing a hair cell’s frequency of spontaneous oscillation, mechanical stimuli as small as ±5 nm entrained the hair-bundle oscillations. For small stimuli, the bundle movement was larger than the stimulus. Because the energy dissipated by viscous drag exceeded the work provided by the stimulus probe, the hair bundles powered their motion and therefore amplified it.

Cochlear mechanisms from a phylogenetic viewpoint

The hearing organ of the inner ear was the last of the paired sense organs of amniotes to undergo formative evolution. As a mechanical sensory organ, the inner-ear hearing organ's function depends highly on its physical structure. Comparative studies suggest that the hearing organ of the earliest amniote vertebrates was small and simple, but possessed hair cells with a cochlear amplifier mechanism, electrical frequency tuning, and incipient micromechanical tuning. The separation of the different groups of amniotes from the stem reptiles occurred relatively early, with the ancestors of the mammals branching off first, approximately 320 million years ago. The evolution of the hearing organ in the three major lines of the descendents of the stem reptiles (e.g., mammals, birds-crocodiles, and lizards-snakes) thus occurred independently over long periods of time. Dramatic and parallel improvements in the middle ear initiated papillar elongation in all lineages, accompanied by increased numbers of sensory cells with enhanced micromechanical tuning and group-specific hair-cell specializations that resulted in unique morphological configurations. This review aims not only to compare structure and function across classification boundaries (the comparative approach), but also to assess how and to what extent fundamental mechanisms were influenced by selection pressures in times past (the phylogenetic viewpoint).