The mechanical basis of Drosophila audition

Abstract

In Drosophila melanogaster, antennal hearing organs mediate the detection of conspecific songs. Combining laser Doppler vibrometry, acoustic near-field measurements and anatomical analysis, we have investigated the first steps in Drosophila audition, i.e. the conversion of acoustic energy into mechanical vibrations and the subsequent transmission of vibrations to the auditory receptors in the base of the antenna. Examination of the mechanical responses of the antennal structures established that the distal antennal parts (the funiculus and the arista) together constitute a mechanical entity, the sound receiver. Unconventionally, this receiver is asymmetric, resulting in an unusual, rotatory pattern of vibration; in the presence of sound, the arista and the funiculus together rotate about the longitudinal axis of the latter. According to the mechanical response characteristics, the antennal receiver represents a moderately damped simple harmonic oscillator. The receiver's resonance frequency increases continuously with the stimulus intensity, demonstrating the presence of a non-linear stiffness that may be introduced by the auditory sense organ. This surprising, non-linear effect is relevant for close-range acoustic communication in Drosophila; by improving antennal sensitivity at low song intensities and reducing sensitivity when intensity is high, it brings about dynamic range compression in the fly's auditory system.