Department of Complexity Science and Engineering, Graduate School of Frontier Science, the University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba, 277-8561, Japan.
Department of Physics, Graduate School of Science, the University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 133-0033, Japan.
BMC Biol. 2022 Jun 15;20(1):130. doi: 10.1186/s12915-022-01336-w.
Animal locomotion requires dynamic interactions between neural circuits, the body (typically muscles), and surrounding environments. While the neural circuitry of movement has been intensively studied, how these outputs are integrated with body mechanics (neuromechanics) is less clear, in part due to the lack of understanding of the biomechanical properties of animal bodies. Here, we propose an integrated neuromechanical model of movement based on physical measurements by taking Drosophila larvae as a model of soft-bodied animals.
We first characterized the kinematics of forward crawling in Drosophila larvae at a segmental and whole-body level. We then characterized the biomechanical parameters of fly larvae, namely the contraction forces generated by neural activity, and passive elastic and viscosity of the larval body using a stress-relaxation test. We established a mathematical neuromechanical model based on the physical measurements described above, obtaining seven kinematic values characterizing crawling locomotion. By optimizing the parameters in the neural circuit, our neuromechanical model succeeded in quantitatively reproducing the kinematics of larval locomotion that were obtained experimentally. This model could reproduce the observation of optogenetic studies reported previously. The model predicted that peristaltic locomotion could be exhibited in a low-friction condition. Analysis of floating larvae provided results consistent with this prediction. Furthermore, the model predicted a significant contribution of intersegmental connections in the central nervous system, which contrasts with a previous study. This hypothesis allowed us to make a testable prediction for the variability in intersegmental connection in sister species of the genus Drosophila.
We generated a neurochemical model based on physical measurement to provide a new foundation to study locomotion in soft-bodied animals and soft robot engineering.
动物运动需要神经回路、身体（通常是肌肉）和周围环境之间的动态相互作用。虽然运动的神经回路已经得到了深入研究，但这些输出如何与身体力学（神经力学）相结合还不太清楚，部分原因是对动物身体的生物力学特性缺乏了解。在这里，我们以果蝇幼虫为软体制动动物模型，提出了一种基于物理测量的综合神经力学运动模型。
我们首先在节段和整体水平上对果蝇幼虫的向前爬行运动进行了运动学分析。然后，我们使用应力松弛试验来对果蝇幼虫的生物力学参数进行了特征描述，即神经活动产生的收缩力，以及幼虫身体的被动弹性和粘性。我们基于上述物理测量建立了一个数学神经力学模型，获得了七个描述爬行运动的运动学值。通过优化神经回路中的参数，我们的神经力学模型成功地定量再现了实验中获得的幼虫运动的运动学。该模型可以再现先前报道的光遗传学研究的观察结果。该模型预测，在低摩擦条件下可以表现出蠕动运动。对漂浮幼虫的分析提供了与这一预测一致的结果。此外，该模型预测了中枢神经系统中节间连接的重要贡献，这与以前的研究形成了对比。这一假设使我们能够对果蝇属的姐妹种中节间连接的可变性做出可测试的预测。
我们基于物理测量生成了一个神经化学模型，为研究软体制动动物和软机器人工程中的运动提供了新的基础。
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