Experimental and Theoretical Explorations of Traveling Waves and Tuning in the Bushcricket Ear

Abstract

The ability to detect airborne sound is essential for many animals. Examples from the inner ear of mammals and bushcrickets demonstrate that similar detection strategies evolved in taxonomically distant species. Both mammalian and bushcricket ears possess a narrow strip of sensory tissue that exhibits an anatomical gradient and traveling wave motion responses used for frequency discrimination. We measured pressure and motion in the bushcricket ear to investigate physical properties, stiffness, and mass, which govern the mechanical responses to sound. As in the mammalian cochlea, sound-induced fluid pressure and motion responses were tonotopically organized along the longitudinal axis of the crista acustica, the bushcricket's hearing organ. The fluid pressure at the crista and crista motion were used to calculate the acoustic impedance of the organ-bounded fluid mass (Z mass ). We used a theoretical wave analysis of wavelength data from a previous study to predict the crista acustica stiffness. The wave analysis also predicts Z mass , and that result agreed reasonably well with the directly measured Z mass , lending support to the theoretical wave analysis. The magnitude of the crista stiffness was similar to basilar membrane stiffness in mammals, and as in mammals, the stiffness decreased from the high-frequency to the low-frequency region. At a given location, the stiffness increased with increasing frequency, corresponding to increasing curvature of the traveling wave (decreasing wavelength), indicating that longitudinal coupling plays a substantial role in determining crista stiffness. This is in contrast to the mammalian ear, in which stiffness is independent of frequency and longitudinal coupling is relatively small.

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

“…The tonotopy and phase patterns in Fig. 3 are consistent with previous reports of CA vibrations (12,19). The overall tuning and tonotopy of the DW are similar to those of the CC, but we also found systematic differences between the tuning of the two structures in the 5-to 25-kHz frequency range.…”

“…Viewing through the glass coverslip allowed us to identify the underlying structures and perform mechanical measurements, and it is a common method in mammal hearing research (42). As was the case in previous bushcricket studies (19), there are no signs that removing the cuticle adversely affected auditory sensitivity. The population data in are combined from animals with an intact cuticle and animals with the cuticle removed.…”

“…Spatial phase gradients in tone-evoked vibrations indicate the existence of waves traveling from the distal, high-frequency end to the proximal end of the CA ( 16 ). Whereas traveling waves in the mammalian cochlea accumulate several cycles of phase delay ( 18 ), the total phase accumulation in the bushcricket CA is only 0.5 to 1 cycle ( 19 ). The exact mechanisms that drive transduction and tonotopy in the CA are undefined.…”

Comparative micromechanics of bushcricket ears with and without a specialized auditory fovea region in the crista acustica

“…The auditory fovea in the bushcricket A. fenestrata is also generated by an area of a halted anatomical gradient in the medial crista acustica [16,19]. It was shown that in bushcricket ears the mechanical response is stiffness dependent [50] and anatomical features like the dendritic height correspond to mechanical changes in frequency responses [51]. Mechanical anchors along the dendrites, called ciliary roots, contribute to the found stiffness changes.…”

Bridging the Gap Between Mammal and Insect Ears – A Comparative and Evolutionary View of Sound-Reception

“…The elongated and linear arranged auditory epithelium of the bush cricket, crista acustica, resembles the biophysical properties of an uncoiled mammalian cochlea (Udayashankar et al, 2012(Udayashankar et al, , 2014. Like the basilar membrane of the mammalian cochlea, the crista acustica has graded changes in its stiffness and mass to make it tonotopic (Hummel et al, 2017;Olson and Nowotny, 2019). A specially evolved adaptation in hearing organs is an overrepresentation of key ecologically important frequencies along the length of epithelium, called an auditory fovea found in some mammals (Müller et al, 1992;Neuweiler and Schmidt, 1993;Kössl, 1997), birds (Köppl et al, 1993;Corfield et al, 2011) and insects (Scherberich et al, 2016(Scherberich et al, , 2017.…”