Rocking without a tune: Ex vivo and in vivo responses to sound in the basilar papilla of the tokay gecko

Like mammals, some reptiles possess sensitive and frequency-selective hearing at mid-to high-kilohertz frequencies. Both groups employ a place-frequency map within the inner ear to encode sound stimuli, but the mechanisms by which they achieve tuned nerve activation along the cochlea are believed to be distinct. To investigate the mechanical origins of auditory sensation in the reptiles, we measured sound-evoked displacement responses in the hearing organ of the tokay gecko (Gekko gecko), known as the basilar papilla. Using optical coherence tomography, we were able to resolve sub-nanometer-scale vibrations throughout the organ both in vivo and ex vivo. We saw that tuning was not present in the tissue-scale mechanics at any position within the organ; it instead exhibits an untuned rotational motion. We developed a mathematical model that predicted that this motion induces hair-bundle-stimulating fluid displacement and is due to an anatomical asymmetry seen in many reptile species. These results are consistent with the theory that hair-bundle-level mechanics are primarily responsible for tuning in the tokay gecko cochlea, and we argue that our proposed mechanisms generalize to many other species across the Reptilia class.