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 high 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 found 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 which predicted that this motion induces hair-bundle-stimulating fluid velocity, and is due to an anatomical asymmetry seen in many reptile and bird species. These results suggest 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. SIGNIFICANCEWe present the most comprehensive picture of tissue-scale mechanics in a reptile hearing organ to-date: sound-evoked displacement responses within the basilar papilla of the tokay gecko (Gekko gecko) both ex vivo and in vivo, across the animals auditory frequency range, and along all three spatial dimensions. We find that place-frequency tuning is not present in the mechanics of the tissue as it is in mammals. Instead, this organ relies on an untuned rocking mechanism to stimulate hair bundles. A mathematical model shows that this may be at play in other reptile and bird species, indicating a unifying mechanism of hearing in the class Reptilia in which hair bundle mechanics play the leading role in frequency tuning.