Feedback between motion and sensation provides nonlinear boost in run-and-tumble navigation.

Feedback between motion and sensation provides nonlinear boost in run-and-tumble navigation.
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DOI:
10.1371/journal.pcbi.1005429
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发表时间:
2017-03
影响因子:
4.3
通讯作者:
Emonet T
Emonet T
中科院分区:
生物学2区
文献类型:
--
作者:
Long J;Zucker SW;Emonet T

文献摘要

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许多生物通过交替直线运动(运行)与随机重新定向(翻滚)来导航梯度,只要引诱信号增加,就会暂时抑制翻滚。这引起了运动和感觉之间的功能耦合,因为翻滚的概率是由生物体的内部状态控制的,而生物体的内部状态又取决于先前的信号水平。虽然负反馈倾向于将这种内部状态保持在接近适应水平,但当梯度上的运动降低翻滚概率时,会出现正反馈,从而进一步促进梯度上的漂移。重要的是,这种正反馈会导致内部状态的大幅波动,使分析方法变得复杂。以前的研究集中在当负反馈主导动态时会发生什么。相比之下,我们在这里表明,有很大一部分生理相关的参数空间,其中正反馈可以占主导地位,即使梯度相对较浅。我们演示了如何出现大的瞬态,因为非正常的动态(非正交特征向量附近的一个稳定的固定点)固有的正反馈,并进一步确定一个基本的非线性,强烈放大其效果。最重要的是,这种扩增是不对称的,在有利的方向上延伸,而在其他方向上延伸。其结果是一个“棘轮式”的梯度攀登行为,漂移速度可以接近一半的最大运行速度的有机体。因此,我们的研究结果表明,经典的缺点运行和翻滚导航浪费运行在错误的方向,可以减轻利用非正常的动态隐含在运行和翻滚的策略。无数的细菌、幼虫甚至更大的生物体(和机器人)通过交替的直线运动(奔跑)和随机的重新定向事件(翻滚)来在梯度中导航。翻滚概率的控制基于先前遇到的信号。这种“跑-跌”策略的一个缺点是,偶尔在错误的方向上跑是浪费。在这里,我们表明,有一个操作制度内的有机体的内部参数空间的运行和翻滚导航可以是非常有效的。我们描述了行为和感知信号之间的正反馈如何导致一种非平衡动力学,生物体在向错误的方向移动并在正确的方向延伸运动后迅速翻滚。对于一个遥远的来源,那么,有机体可以很快找到它。
Many organisms navigate gradients by alternating straight motions (runs) with random reorientations (tumbles), transiently suppressing tumbles whenever attractant signal increases. This induces a functional coupling between movement and sensation, since tumbling probability is controlled by the internal state of the organism which, in turn, depends on previous signal levels. Although a negative feedback tends to maintain this internal state close to adapted levels, positive feedback can arise when motion up the gradient reduces tumbling probability, further boosting drift up the gradient. Importantly, such positive feedback can drive large fluctuations in the internal state, complicating analytical approaches. Previous studies focused on what happens when the negative feedback dominates the dynamics. By contrast, we show here that there is a large portion of physiologically-relevant parameter space where the positive feedback can dominate, even when gradients are relatively shallow. We demonstrate how large transients emerge because of non-normal dynamics (non-orthogonal eigenvectors near a stable fixed point) inherent in the positive feedback, and further identify a fundamental nonlinearity that strongly amplifies their effect. Most importantly, this amplification is asymmetric, elongating runs in favorable directions and abbreviating others. The result is a “ratchet-like” gradient climbing behavior with drift speeds that can approach half the maximum run speed of the organism. Our results thus show that the classical drawback of run-and-tumble navigation—wasteful runs in the wrong direction—can be mitigated by exploiting the non-normal dynamics implicit in the run-and-tumble strategy. Countless bacteria, larvae and even larger organisms (and robots) navigate gradients by alternating periods of straight motion (runs) with random reorientation events (tumbles). Control of the tumble probability is based on previously-encountered signals. A drawback of this run-and-tumble strategy is that occasional runs in the wrong direction are wasteful. Here we show that there is an operating regime within the organism’s internal parameter space where run-and-tumble navigation can be extremely efficient. We characterize how the positive feedback between behavior and sensed signal results in a type of non-equilibrium dynamics, with the organism rapidly tumbling after moving in the wrong direction and extending motion in the right ones. For a distant source, then, the organism can find it fast.