Atypical Tuning and Amplification Mechanisms in Gecko Auditory Hair Cells

The auditory papilla of geckos contains two zones of sensory hair cells, one covered by a continuous tectorial membrane affixed to the hair bundles and the other by discrete tectorial sallets each surmounting a transverse row of bundles. Gecko papillae are thought to encode sound frequencies up to 5 kHz, but little is known about the hair cell electrical properties or their role in frequency tuning. We recorded from hair cells in the isolated auditory papilla of the crested gecko, Correlophus ciliatus, and found that in both the nonsalletal region and part of the salletal region, the cells displayed electrical tuning organized tonotopically. Along the salletal zone, occupying the apical two-thirds of the papilla, hair bundle length decreased threefold and stereociliary complement increased 1.5-fold. The two morphological variations predict a 13-fold gradient in bundle stiffness, confirmed experimentally, which, when coupled with salletal mass, could provide passive mechanical resonances from 1 to 6 kHz. Sinusoidal electrical currents injected across the papilla evoked hair bundle oscillations at twice the stimulation frequency, consistent with fast electromechanical responses from hair bundles of two opposing orientations across the papilla. Evoked bundle oscillations were diminished by reducing Ca2+ influx, but not by blocking the mechanotransduction channels or inhibiting prestin action, thereby distinguishing them from known electromechanical mechanisms in hair cells. We suggest the phenomenon may be a manifestation of an electromechanical amplification that augments the passive mechanical tuning of the sallets over the high-frequency region