Mechanical network equivalence between the katydid and mammalian inner ears.

IF 3.6 2区 生物学 Q1 BIOCHEMICAL RESEARCH METHODS
PLoS Computational Biology Pub Date : 2024-12-13 eCollection Date: 2024-12-01 DOI:10.1371/journal.pcbi.1012641
Emine Celiker, Charlie Woodrow, Òscar Guadayol, Leonidas-Romanos Davranoglou, Christian M Schlepütz, Beth Mortimer, Graham K Taylor, Stuart Humphries, Fernando Montealegre-Z
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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.

蝈蝈和哺乳动物内耳的机械网络等同性
哺乳动物的听觉有三个基本步骤:1)声音捕捉;2)阻抗转换;3)频率分析。虽然这些基本步骤对哺乳动物的声音交流和生存至关重要,但它们并不是哺乳动物独有的。蝈蝈(昆虫纲)也有类似的机制,这在无脊椎动物中是独一无二的。蝈蝈的内耳类似于未卷曲的耳蜗,长度不到 1 毫米。它们的内耳包含一个听觉器官--听小骨,里面有按音调排列的感觉细胞,可通过行波绘制频率图。耳廓位于耳道背壁形成的弯曲三角形表面上。虽然经验记录显示螽斯内耳的音调振动可用于频率分析,但由于听觉器官体积小、结构复杂,导致音调振动的生物物理机制仍然难以捉摸。本研究开发了稳健的数值模拟,用于对这一过程进行硅学研究。模拟基于同步加速器微型计算机断层扫描获得的蝈蝈内耳精确几何图形,以及根据经验确定的内耳流体特性,以准确呈现潜在机制。我们证明,听觉器官下方的三角形结构驱动着内耳的音调和游动波,因此与哺乳动物的基底膜具有同等作用。这揭示了两种具有古老进化差异和独立系统发育历史的生物的内耳基本机械网络之间更强的相似性。
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来源期刊
PLoS Computational Biology
PLoS Computational Biology BIOCHEMICAL RESEARCH METHODS-MATHEMATICAL & COMPUTATIONAL BIOLOGY
CiteScore
7.10
自引率
4.70%
发文量
820
审稿时长
2.5 months
期刊介绍: PLOS Computational Biology features works of exceptional significance that further our understanding of living systems at all scales—from molecules and cells, to patient populations and ecosystems—through the application of computational methods. Readers include life and computational scientists, who can take the important findings presented here to the next level of discovery. Research articles must be declared as belonging to a relevant section. More information about the sections can be found in the submission guidelines. Research articles should model aspects of biological systems, demonstrate both methodological and scientific novelty, and provide profound new biological insights. Generally, reliability and significance of biological discovery through computation should be validated and enriched by experimental studies. Inclusion of experimental validation is not required for publication, but should be referenced where possible. Inclusion of experimental validation of a modest biological discovery through computation does not render a manuscript suitable for PLOS Computational Biology. Research articles specifically designated as Methods papers should describe outstanding methods of exceptional importance that have been shown, or have the promise to provide new biological insights. The method must already be widely adopted, or have the promise of wide adoption by a broad community of users. Enhancements to existing published methods will only be considered if those enhancements bring exceptional new capabilities.
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