The sense of hearing is critical for predator detection and communication across the animal kingdom. Vertebrate hearing organs are incredibly diverse, but all rely on mechanosensory hair cells that convert mechanical stimulation of their hair bundles into neurotransmitter release. Studies of hair cells and the mechanics of the sound-sensing organs that contain them have led to remarkable advances in the treatment of sensorineural hearing loss, such as cochlear implants and gene therapies.
The tokay gecko is a vocal lizard famous for its fierce demeanor and vibrant colors (as seen in the image by Sihao Lu of Rockefeller University that appears on the cover of the October 20 issue of Biophysical Journal), as well as its mating call, “tokay,” from which it gets its name. It is a valuable animal model for studying hearing from a comparative perspective, because its hearing organ—the basilar papilla—differs significantly in structure from that of its mammalian homologue— the organ of Corti—but still is capable of resolving sounds at frequencies up to 6 kHz. The papilla also displays tonotopy, a hallmark of the mammalian system in which nerve connections to different positions within the organ respond maximally at different frequencies.
To investigate the mechanisms of auditory sensation in this species, we used optical coherence tomography, a volumetric imaging method that is also capable of measuring displacements at a sub-nanometer scale. This allowed us to obtain the most comprehensive picture of a reptilian hearing organ’s mechanics to date, measuring vibrations in response to sound stimuli across all three dimensions of the papilla both ex vivo and in vivo.
We saw that, contrary to the mammalian system, the organ does not exhibit tuned displacement responses at different positions. Instead, it rocks side to side in an untuned manner, stimulating hair bundles through this rotational motion. Using a computational model, we show that this is caused by an asymmetry in the organ that is prominent across the class Reptilia.
These results are consistent with the long-standing theory that hair bundles are primarily responsible for the tuning seen in nerve responses. That this is true in an animal capable of hearing at reasonably high frequencies strengthens the claim that hair bundle mechanics play a key role in mammalian organs as well. This has been a challenging hypothesis to probe in mammal models; our study shows that it may be more tractably observed in reptiles. For example, genetic or pharmacological manipulations similar to those used in mammal studies could prove valuable in a gecko model, isolating the component of hearing degradation that is due to the hair bundles from the various confounding effects in the organ of Corti.
We dedicate this publication to the memory of Jim Hudspeth, who shaped not only the work herein, but the entire world of auditory science.
—Brian L. Frost, Yuriria Vázquez, Kazuhiro Horii, and Brian A. Fabella