3D-imaging inspired improvements to hearing model in parasitoid fly Ormia ochracea

Although most binaural organisms localize sound sources using neurological structures to amplify the sounds they hear, some animals use mechanically coupled hearing organs to do so. One example, the parasitoid fly Ormia ochracea, has astoundingly accurate sound localization abilities and can locate objects in the azimuthal plane with a precision of 2°, equal to that of humans. This is accomplished despite an intertympanal distance of only 1.2 mm, which is about 1/100th of the wavelength of the sound emitted by the crickets that it parasitizes. In 1995, Miles et al. developed a model for hearing mechanics in O. Ochracea, which works well for incoming sound angles of less than ±30°, but suffers from reduced accuracy at higher angles. Despite this, it has served as the basis for multiple bio-inspired microphone designs for decades. Here, we present critical modifications to the classic O. ochracea hearing model based on information from 3D reconstructions of O. ochracea's tympana. The 3D images reveal that the tympana have curved lateral faces in addition to the flat front-facing prosternal membranes represented in the 1995 model. To mimic these faces, we incorporated spatially varying spring and damper coefficients that respond asymmetrically to incident sound waves, making a new quasi-two-dimensional (q2D) model. This q2D model has high accuracy (average errors of less than 10%) for the entire range of incoming sound angles. This improved biomechanical hearing model can inform the development of new technologies and may help to play a key role in developing improved hearing aids.

Cues for Directional Hearing in the Fly Ormia ochracea

Insects are often small relative to the wavelengths of sounds they need to localize, which presents a fundamental biophysical problem. Understanding novel solutions to this limitation can provide insights for biomimetic technologies. Such an approach has been successful using the fly Ormia ochracea (Diptera: Tachinidae) as a model. O. ochracea is a parasitoid species whose larvae develop as internal parasites within crickets (Gryllidae). In nature, female flies find singing male crickets by phonotaxis, despite severe constraints on directional hearing due to their small size. A physical coupling between the two tympanal membranes allows the flies to obtain information about sound source direction with high accuracy because it generates interaural time-differences (ITD) and interaural level differences (ILD) in tympanal vibrations that are exaggerated relative to the small arrival-time difference at the two ears, that is the only cue available in the sound stimulus. In this study, I demonstrate that pure time-differences in the neural responses to sound stimuli are sufficient for auditory directionality in O. ochracea.