[论文解读] Ciliary flocking and emergent instabilities enable collective agility in a non-neuromuscular animal

Matthew S. Bull, Vivek N. Prakash+1 more|arXiv (Cornell University)|Jul 6, 2021

Micro and Nano Robotics参考文献 53被引用 8

一句话总结

本文表明，*Trichoplax adhaerens*——一种非神经肌肉动物——通过组织尺度的活性-弹性谐振器中涌现的不稳定性，实现纤毛集群化运动，从而达成敏捷的运动。通过将纤毛重定向映射到参数放大谐振器模型，研究揭示了周期性和噪声激励如何产生线速度行进波，从而在无神经元或肌肉的情况下实现快速、灵敏的响应。

ABSTRACT

Effective organismal behavior responds appropriately to changes in the surrounding environment. Attaining this delicate balance of sensitivity and stability is a hallmark of the animal kingdom. By studying the locomotory behavior of a simple animal ( extit{Trichoplax adhaerens}) without muscles or neurons, here, we demonstrate how monociliated epithelial cells work collectively to give rise to an agile non-neuromuscular organism. Via direct visualization of large ciliary arrays, we report the discovery of sub-second ciliary reorientations under a rotational torque that is mediated by collective tissue mechanics and the adhesion of cilia to the underlying substrate. In a toy model, we show a mapping of this system onto an "active-elastic resonator". This framework explains how perturbations propagate information in this array as linear speed traveling waves in response to mechanical stimulus. Next, we explore the implications of parametric driving in this active-elastic resonator and show that such driving can excite mechanical 'spikes'. These spikes in collective mode amplitudes are consistent with a system driven by parametric amplification and a saturating nonlinearity. We conduct extensive numerical experiments to corroborate these findings within a polarized active-elastic sheet. These results indicate that periodic and stochastic forcing are valuable for increasing the sensitivity of collective ciliary flocking. We support these theoretical predictions via direct experimental observation of linear speed traveling waves which arise from the hybridization of spin and overdamped density waves. We map how these ciliary flocking dynamics result in agile motility via coupling between an amplified resonator and a tuning (Goldstone-like) mode of the system. This sets the stage for how activity and elasticity can self-organize into behavior which benefits the organism as a whole.

研究动机与目标

• 理解非神经肌肉动物如何在无神经元或肌肉的情况下实现敏捷、快速的定向改变。
• 研究上皮组织中集体纤毛重定向与波传播的物理机制。
• 确定参数放大与非线性弹性如何在纤毛动力学中实现敏感性与稳定性。
• 将组织建模为支持长波长、欠阻尼行进波的活性-弹性谐振器。
• 探索此类生物动力学作为具身智能中储层的计算潜力。

提出的方法

• 通过高速成像直接观测纤毛阵列在机械扭矩作用下的亚秒级重定向。
• 构建一个将纤毛动力学映射到参数驱动的活性-弹性谐振器的简化模型。
• 对二维极化活性-弹性薄片进行数值模拟，以验证波传播与不稳定性动力学。
• 分析周期性与随机激励下的参数共振，以解释机械脉冲的放大现象。
• 采用混合自旋-过阻尼密度波框架，解释无惯性效应下的线速度行进波。
• 应用储层计算原理，评估系统通过非线性动力学进行信息处理的潜力。

实验结果

研究问题

• RQ1 *Trichoplax adhaerens* 的纤毛阵列如何在无神经控制的情况下实现亚秒级重定向？
• RQ2 在非惯性、过阻尼的纤毛系统中，何种物理机制可实现线速度行进波的传播？
• RQ3 活性-弹性谐振器中的参数放大如何增强对机械刺激的敏感性？
• RQ4 涌现的不稳定性与非线性性如何在非神经肌肉系统中实现敏捷且稳定的运动行为？
• RQ5 该组织的集体动力学能否被解释为具身系统中的一种物理储层计算？

主要发现

• 亚秒级纤毛重定向由集体组织力学与基底黏附介导，实现快速的方向改变。
• 该系统表现为一个活性-弹性谐振器，通过参数放大支持欠阻尼、长波长的行进波。
• 周期性与噪声性参数驱动激发了集体模态振幅的机械脉冲，与饱和非线性一致。
• 线速度行进波源于自旋波与过阻尼密度波的混合，实现在无惯性条件下的信息传播。
• 系统表现出类似戈德斯通模式的特性，与放大谐振器耦合，实现组织尺度上的敏捷、灵敏响应。
• 数值模拟证实，即使在强阻尼条件下，参数放大仍能稳定并增强波的传播。