Mechanical network equivalence between the katydid and mammalian inner ears

PLoS Comput Biol. 2024 Dec 13;20(12):e1012641. doi: 10.1371/journal.pcbi.1012641. eCollection 2024 Dec.

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.

MeSH terms

  • Animals
  • Cochlea / anatomy & histology
  • Cochlea / physiology
  • Computational Biology
  • Computer Simulation
  • Ear, Inner* / anatomy & histology
  • Ear, Inner* / physiology
  • Hearing* / physiology
  • Insecta / physiology
  • Mammals* / physiology
  • Models, Biological
  • X-Ray Microtomography

Grants and funding

This research was part of the project "The Insect Cochlea" funded by the European Research Council, Grant ERCCoG-2017–773067 to FMZ; and was also funded by the Natural Environment Research Council (NERC), grant DEB-1937815 to FMZ. CW and ÒG received a salary from the NERC grant DEB-1937815. LRD was funded and received a salary from the Leverhulme Trust Early Career Fellowship grant (ECF-2021-199). GKT was supported by a Major Research Grant from Jesus College, Oxford. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.