Transducer-Based Force Generation Explains Active Process in Drosophila Hearing

BACKGROUND Like vertebrate hair cells, Drosophila auditory neurons are endowed with an active, force-generating process that boosts the macroscopic performance of the ear. The underlying force generator may be the molecular apparatus for auditory transduction, which, in the fly as in vertebrates, seems to consist of force-gated channels that occur in series with adaptation motors and gating springs. This molecular arrangement explains the active properties of the sensory hair bundles of inner-ear hair cells, but whether it suffices to explain the active macroscopic performance of auditory systems is unclear. RESULTS To relate transducer dynamics and auditory-system behavior, we have devised a simple model of the Drosophila hearing organ that consists only of transduction modules and a harmonic oscillator that represents the sound receiver. In vivo measurements show that this model explains the ear's active performance, quantitatively capturing displacement responses of the fly's antennal sound receiver to force steps, this receiver's free fluctuations, its response to sinusoidal stimuli, nonlinearity, and activity and cycle-by-cycle amplification, and properties of electrical compound responses in the afferent nerve. CONCLUSIONS Our findings show that the interplay between transduction channels and adaptation motors accounts for the entire macroscopic phenomenology of the active process in the Drosophila auditory system, extending transducer-based amplification from hair cells to fly ears and demonstrating that forces generated by transduction modules can suffice to explain active processes in ears.