Neuromechanical wave resonance in jellyfish swimming

Neuromechanical wave resonance in jellyfish swimming
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DOI:
10.1073/pnas.2020025118
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发表时间:
2021-03-16
影响因子:
11.1
通讯作者:
Miller,Laura A.
Miller,Laura A.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Hoover,Alexander P.;Xu,Nicole W.;Miller,Laura A.

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为了使生物体具有强大的运动能力,它们的神经肌肉组织必须适应不断变化的环境。在水母中,当边缘起搏器激发整个钟状运动神经网络的动作电位时,游泳健全性就出现了,这是肌肉组织收缩的信号。肌肉激活波的速度是由动作电位的通过时间决定的。然而,被动弹性材料的性质也会影响紧急运动学,其时间尺度与神经肌肉组织无关。在这个多模态研究中,我们研究了这两个时间尺度在转弯过程中的相互作用。建立了水母的三维计算流固相互作用模型,利用双向肌肉激活波驱动钟形缘,确定了由此产生的紧急运动学。激活波的速度接近于材料波的速度,在最佳和最差表现者之间的转弯速度相差76倍。只有在激活波速度接近物质波速度时,才会发生边缘超伸,提示共振。这种过度伸展导致了34倍不对称的漩涡环的循环在内部和外部的转弯。实验记录的激活速度证实水母在此范围内驱动,采用粒子图像测速技术的流动可视化验证了数值模型的相应流体动力学。这表明神经机械波共振在生物体运动系统的稳健性中起着重要作用,并在柔性生物体的进化中呈现出一种未被发现的约束。了解这些动力学对于开发软体机器人和生物工程泵中的执行器至关重要。
For organisms to have robust locomotion, their neuromuscular organization must adapt to constantly changing environments. In jellyfish, swimming robustness emerges when marginal pacemakers fire action potentials throughout the bell’s motor nerve net, which signals the musculature to contract. The speed of the muscle activation wave is dictated by the passage times of the action potentials. However, passive elastic material properties also influence the emergent kinematics, with time scales independent of neuromuscular organization. In this multimodal study, we examine the interplay between these two time scales during turning. A three-dimensional computational fluid–structure interaction model of a jellyfish was developed to determine the resulting emergent kinematics, using bidirectional muscular activation waves to actuate the bell rim. Activation wave speeds near the material wave speed yielded successful turns, with a 76-fold difference in turning rate between the best and worst performers. Hyperextension of the margin occurred only at activation wave speeds near the material wave speed, suggesting resonance. This hyperextension resulted in a 34-fold asymmetry in the circulation of the vortex ring between the inside and outside of the turn. Experimental recording of the activation speed confirmed that jellyfish actuate within this range, and flow visualization using particle image velocimetry validated the corresponding fluid dynamics of the numerical model. This suggests that neuromechanical wave resonance plays an important role in the robustness of an organism’s locomotory system and presents an undiscovered constraint on the evolution of flexible organisms. Understanding these dynamics is essential for developing actuators in soft body robotics and bioengineered pumps.