RT Journal Article SR Electronic T1 A biologically accurate model of directional hearing in the parasitoid fly Ormia ochracea JF bioRxiv FD Cold Spring Harbor Laboratory SP 2021.09.15.460520 DO 10.1101/2021.09.15.460520 A1 Max R. Mikel-Stites A1 Mary K. Salcedo A1 John J. Socha A1 Paul E. Marek A1 Anne E. Staples YR 2021 UL http://biorxiv.org/content/early/2021/10/07/2021.09.15.460520.abstract AB This manuscript was compiled on October 5, 2021 Although most binaural organisms localize sound sources using neurological structures to amplify the sounds they hear, some animals use mechanically coupled hearing organs instead. One of these animals, 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 0.5 mm, which is less than 1/100th of the wavelength of the sound emitted by the crickets that it parasitizes. In 1995, Miles et al. developed a model of hearing mechanics in O. ochracea, which works well for incoming sound angles of less than ±30°, but suffers from reduced accuracy (up to 60% error) at higher angles. Even with this limitation, it has served as the basis for multiple bio-inspired microphone designs for decades. Here, we present critical improvements to the classic O. ochracea hearing model based on information from 3D reconstructions of O. ochracea’s tympana. The 3D images reveal that the tympanal organ has curved lateral faces in addition to the flat front-facing prosternal membranes represented in the Miles 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. The 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.Significance Statement The ability to identify the location of sound sources is critical to organismal survival and for technologies that minimize unwanted background noise, such as directional microphones for hearing aids. Because of its exceptional auditory system, the parasitoid fly Ormia ochracea has served as an important model for binaural hearing and a source of bioinspiration for building tiny directional microphones with outsized sound localization abilities. Here, we performed 3D imaging of the fly’s tympanal organs and used the morphological information to improve the current model for hearing in O. ochracea. This model greatly expands the range of biological accuracy from ±30° to all incoming sound angles, providing a new avenue for studies of binaural hearing and further inspiration for fly-inspired technologies.Competing Interest StatementThe authors have declared no competing interest.ITDInteraural Time DelayIADInteraural Amplitude Difference (sometimes called the Interaural IntensitmlTDMechanical Interaural Time DelaymlADMechanical Interaural Amplitude Difference