Basic Sciences Division, Fred Hutchinson Cancer Center, Seattle, Washington, United States of America.
Molecular and Cellular Biology Program, University of Washington, Seattle, Washington, United States of America.
PLoS Comput Biol. 2024 Mar 4;20(3):e1011906. doi: 10.1371/journal.pcbi.1011906. eCollection 2024 Mar.
Adult animals display robust locomotion, yet the timeline and mechanisms of how juvenile animals acquire coordinated movements and how these movements evolve during development are not well understood. Recent advances in quantitative behavioral analyses have paved the way for investigating complex natural behaviors like locomotion. In this study, we tracked the swimming and crawling behaviors of the nematode Caenorhabditis elegans from postembryonic development through to adulthood. Our principal component analyses revealed that adult C. elegans swimming is low dimensional, suggesting that a small number of distinct postures, or eigenworms, account for most of the variance in the body shapes that constitute swimming behavior. Additionally, we found that crawling behavior in adult C. elegans is similarly low dimensional, corroborating previous studies. Further, our analysis revealed that swimming and crawling are distinguishable within the eigenworm space. Remarkably, young L1 larvae are capable of producing the postural shapes for swimming and crawling seen in adults, despite frequent instances of uncoordinated body movements. In contrast, late L1 larvae exhibit robust coordination of locomotion, while many neurons crucial for adult locomotion are still under development. In conclusion, this study establishes a comprehensive quantitative behavioral framework for understanding the neural basis of locomotor development, including distinct gaits such as swimming and crawling in C. elegans.
成年动物表现出强健的运动能力,但幼年动物如何获得协调的运动能力,以及这些运动能力在发育过程中如何演变,这些问题尚未得到很好的理解。定量行为分析的最新进展为研究复杂的自然行为(如运动)铺平了道路。在这项研究中,我们跟踪了线虫秀丽隐杆线虫从胚胎后发育到成年期的游泳和爬行行为。我们的主成分分析表明,成年秀丽隐杆线虫的游泳行为是低维的,这表明少数独特的姿势,或本征虫,解释了构成游泳行为的大部分身体形状变化。此外,我们发现成年秀丽隐杆线虫的爬行行为也是类似的低维,与之前的研究结果相符。此外,我们的分析表明,游泳和爬行在本征虫空间内是可区分的。值得注意的是,年轻的 L1 幼虫能够产生在成年期看到的游泳和爬行的姿势,尽管经常出现不协调的身体运动。相比之下,晚期 L1 幼虫表现出强烈的运动协调能力,而许多对成年运动至关重要的神经元仍在发育中。总之,这项研究建立了一个全面的定量行为框架,用于理解运动发育的神经基础,包括线虫中的不同步态,如游泳和爬行。