Geoffrey A. Manley

Spontaneous otoacoustic emissions (SOAEs) are indicators of active processes in the inner ear and are found in all classes of land vertebrates. In the Australian bobtail lizard, earlier work showed that otoacoustic emissions are generated by an active motility process in the hair-cell bundle. This is likely to be driven by calcium-sensitive mechanisms implicated in other non-mammalian hair cell systems. If so, it should be fundamentally influenced by the extracellular calcium concentration. In in vitro studies, the rate of force generation in hair cell stereovilli is linked to the extracellular calcium concentration. In such preparations, low-calcium solutions, buffered by the calcium chelator BAPTA, were reported to change the frequency of hair cell bundle oscillations. In the present study, BAPTA was iontophoresed into the endolymph of the bobtail skink in vivo, and SOAEs were monitored. Application of BAPTA resulted in a prolonged downward shift in the frequency of individual SOAE spectral peaks. Recovery took more than 1 h, consistent with a slow clearance of BAPTA from endolymph. SOAE peak amplitudes were most often enhanced, suggesting there was no functional disruption of tip links. The direction and degree of frequency shifts were consistent with in vitroand in vivo data showing the effects of changing calcium concentrations in the endolymph directly.

Spontaneous otoacoustic emissions (SOAEs) are accepted as being indicators of an active process in the inner ear and have been observed in all groups of land vertebrates. Previous studies have indicated that there may be more than one cellular substrate driving the active processes in different groups of vertebrates. To investigate the cellular substrate in non-mammals and to relate the findings to studies in mammalian ears, we injected AC and DC currents of amplitudes generally below 5 microA into scala media of the bobtail skink Tiliqua rugosa and recorded their influences on SOAEs. Injected AC current has been shown previously to induce emissions [electrically induced otoacoustic emissions (EEOAEs)] in mammals and lizards. AC current in the appropriate frequency range entrained SOAEs but was relatively ineffective at increasing their magnitude compared with the dependence on current strength of EEOAEs generated at non-SOAE frequencies. The effects of DC current were polarity-dependent and changed over time with prolonged stimulation. Whereas positive current caused a small increase in SOAE frequency and a fall in magnitudes, negative DC current induced a decrease in SOAE frequency of more than 30%, accompanied by changes in level that were strongly time-dependent. All changes were slowly reversible. The effects observed in this species of lizard strongly resemble those observed in frogs and chinchillas. The similarity is interesting in view of the putatively different cellular mechanisms driving the active process in mammals and non-mammals.

The last two decades have produced a great deal of evidence that in the mammalian organ of Corti outer hair cells undergo active shape changes that are part of a “cochlear amplifier” mechanism that increases sensitivity and frequency selectivity of the hearing epithelium. However, many signs of active processes have also been found in nonmammals, raising the question as to the ancestry and commonality of these mechanisms. Active movements would be advantageous in all kinds of sensory hair cells because they help signal detection at levels near those of thermal noise and also help to overcome fluid viscosity. Such active mechanisms therefore presumably arose in the earliest kinds of hair cells that were part of the lateral line system of fish. These cells were embedded in a firm epithelium and responded to relative motion between the hair bundle and the hair cell, making it highly likely that the first active motor mechanism was localized in the hair-cell bundle. In terrestrial nonmammals, there are many auditory phenomena that are best explained by the presence of a cochlear amplifier, indicating that in this respect the mammalian ear is not unique. The latest evidence supports siting the active process in nonmammals in the hair-cell bundle and in intimate association with the transduction process.

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.