Mechanical network equivalence between the katydid and mammalian inner ears

Emine Celiker, Charlie Woodrow, Òscar Guadayol, Leonidas-Romanos Davranoglou, Christian M Schlepütz, Beth Mortimer, Graham K Taylor, Stuart Humphries and Fernando Montealegre-Z

PLOS Computational Biology, 2024, vol. 20, issue 12, 1-17

Abstract: Mammalian hearing operates on three basic steps: 1) sound capturing, 2) impedance conversion, and 3) frequency analysis. While these canonical steps are vital for acoustic communication and survival in mammals, they are not unique to them. An equivalent mechanism has been described for katydids (Insecta), and it is unique to this group among invertebrates. The katydid inner ear resembles an uncoiled cochlea, and has a length less than 1 mm. Their inner ears contain the crista acustica, which holds tonotopically arranged sensory cells for frequency mapping via travelling waves. The crista acustica is located on a curved triangular surface formed by the dorsal wall of the ear canal. While empirical recordings show tonotopic vibrations in the katydid inner ear for frequency analysis, the biophysical mechanism leading to tonotopy remains elusive due to the small size and complexity of the hearing organ. In this study, robust numerical simulations are developed for an in silico investigation of this process. Simulations are based on the precise katydid inner ear geometry obtained by synchrotron-based micro-computed tomography, and empirically determined inner ear fluid properties for an accurate representation of the underlying mechanism. We demonstrate that the triangular structure below the hearing organ drives the tonotopy and travelling waves in the inner ear, and thus has an equivalent role to the mammalian basilar membrane. This reveals a stronger analogy between the inner ear basic mechanical networks of two organisms with ancient evolutionary differences and independent phylogenetic histories.Author summary: Katydids (Insecta) have a unique hearing system among invertebrates because, similar to mammals, they exhibit outer, middle, and inner ear components. The katydid inner ear resembles an uncoiled mammalian cochlea. Although much smaller in size (∼700 μm), the katydid inner ear possesses a tonotopic frequency-discriminating sensory epithelium like the mammalian cochlea. Yet, the mechanical equivalence between the workings of the two inner ears has not been investigated experimentally, due to the minuscule dimension and tightly integrated inner ear components of the katydid ear. In this study, comprehensive numerical simulations are developed using accurate 3D ear models to investigate such an equivalence. The results reveal that similar to the mammalian basilar membrane, the triangular structure holding the katydid hearing organ drives the movements of the mechanosensors, so that the minuscule katydid inner ear functions with a similar biophysical mechanism as the mammalian cochlea. This provides a unique opportunity to infer processes difficult to measure in the mammalian cochlea through an analogous model auditory system.

Date: 2024
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Persistent link: https://EconPapers.repec.org/RePEc:plo:pcbi00:1012641

DOI: 10.1371/journal.pcbi.1012641

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