Tuned vibration modes in a miniature hearing organ: Insights from the bushcricket

Abstract

Bushcrickets (katydids) rely on only 20 to 120 sensory units located in their forelegs to sense sound. Situated in tiny hearing organs less than 1 mm long (40× shorter than the human cochlea), they cover a wide frequency range from 1 kHz up to ultrasounds, in tonotopic order. The underlying mechanisms of this miniaturized frequency-place map are unknown. Sensory dendrites in the hearing organ (crista acustica [CA]) are hypothesized to stretch, thereby driving mechanostransduction and frequency tuning. However, this has not been experimentally confirmed. Using optical coherence tomography (OCT) vibrometry, we measured the relative motion of structures within and adjacent to the CA of the bushcricketMecopoda elongata. We found different modes of nanovibration in the CA that have not been previously described. The two tympana and the adjacent septum of the foreleg that enclose the CA were recorded simultaneously, revealing an antiphasic lever motion strikingly reminiscent of vertebrate middle ears. Over the entire length of the CA, we were able to separate and compare vibrations of the top (cap cells) and base (dorsal wall) of the sensory tissue. The tuning of these two structures, only 15 to 60 μm (micrometer) apart, differed systematically in sharpness and best frequency, revealing a tuned periodic deformation of the CA. The relative motion of the two structures, a potential drive of transduction, demonstrated sharper tuning than either of them. The micromechanical complexity indicates that the bushcricket ear invokes multiple degrees of freedom to achieve frequency separation with a limited number of sensory cells.