Neural mechanism of optimal limb coordination in crustacean swimming

Neural mechanism of optimal limb coordination in crustacean swimming
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甲壳动物游泳中最佳肢体协调的神经机制

DOI:
10.1073/pnas.1323208111
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发表时间:
2014
期刊:
Proceedings of the National Academy of Sciences
影响因子:
--
通讯作者:
T. J. Lewis
T. J. Lewis
中科院分区:
--
文献类型:
--
作者:
Calvin Zhang;R. Guy;B. Mulloney;Qinghai Zhang;T. J. Lewis

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尽管人们普遍认为神经回路是为了优化行为而进化的,但很少有研究清楚地确定了优化行为背后的神经机制。甲壳类动物游泳中不同的肢体协调和相对简单的神经协调回路使我们能够证明甲壳类动物游泳中的肢体间协调在生物力学上是最佳的,以及潜在的神经回路结构如何强有力地引起这种协调。因此,我们提供了一个具体的例子,说明最佳行为是如何从神经回路的解剖结构中产生的。此外,我们的研究结果表明,甲壳类动物在游泳过程中肢体协调的神经回路的连通性可能是自然选择的结果,有利于更有效和高效的游泳。神经科学的一个基本挑战是理解生物学上显著的运动行为是如何从底层神经回路的特性中产生的。小龙虾、磷虾、对虾、龙虾和其他长尾甲壳类动物通过有节奏地移动四肢游泳,这些四肢被称为游泳体。在动物大小和划水频率的整个生物范围内,相邻游泳者的运动保持着大约四分之一周期的相位差,更多的后肢引领循环。我们使用计算流体动力学模型来表明,这种频率不变的划水模式是甲壳类动物游泳中所有生物学相关雷诺数范围内最有效和机械效率最高的划水节奏。然后我们表明,游泳协调的神经回路组织为产生这种泳姿模式提供了一个强大的机制。具体地说,波状肢体协调是由驱动每个肢体运动的局部中心模式生成电路(cpg)的半中心结构、局部cpg之间连接的不对称网络拓扑结构和实验测量的局部cpg的相位响应特性相结合而产生的。因此,甲壳类动物的游泳系统是一个具体的例子,其中神经回路的结构以一种稳健的方式导致了最优行为。此外,我们考虑了局部cpg之间所有可能的连接拓扑,并表明自然连接模式最鲁棒地产生了生物力学上最优的卒中模式。鉴于甲壳类动物游泳的高代谢成本,我们的研究结果表明,自然选择促使游泳动物的神经回路朝着产生最佳行为的连接拓扑方向发展。
Significance Despite the general belief that neural circuits have evolved to optimize behavior, few studies have clearly identified the neural mechanisms underlying optimal behavior. The distinct limb coordination in crustacean swimming and the relative simplicity of the neural coordinating circuit have allowed us to show that the interlimb coordination in crustacean swimming is biomechanically optimal and how the structure of underlying neural circuit robustly gives rise to this coordination. Thus, we provide a concrete example of how an optimal behavior arises from the anatomical structure of a neural circuit. Furthermore, our results suggest that the connectivity of the neural circuit underlying limb coordination during crustacean swimming may be a consequence of natural selection in favor of more effective and efficient swimming. A fundamental challenge in neuroscience is to understand how biologically salient motor behaviors emerge from properties of the underlying neural circuits. Crayfish, krill, prawns, lobsters, and other long-tailed crustaceans swim by rhythmically moving limbs called swimmerets. Over the entire biological range of animal size and paddling frequency, movements of adjacent swimmerets maintain an approximate quarter-period phase difference with the more posterior limbs leading the cycle. We use a computational fluid dynamics model to show that this frequency-invariant stroke pattern is the most effective and mechanically efficient paddling rhythm across the full range of biologically relevant Reynolds numbers in crustacean swimming. We then show that the organization of the neural circuit underlying swimmeret coordination provides a robust mechanism for generating this stroke pattern. Specifically, the wave-like limb coordination emerges robustly from a combination of the half-center structure of the local central pattern generating circuits (CPGs) that drive the movements of each limb, the asymmetric network topology of the connections between local CPGs, and the phase response properties of the local CPGs, which we measure experimentally. Thus, the crustacean swimmeret system serves as a concrete example in which the architecture of a neural circuit leads to optimal behavior in a robust manner. Furthermore, we consider all possible connection topologies between local CPGs and show that the natural connectivity pattern generates the biomechanically optimal stroke pattern most robustly. Given the high metabolic cost of crustacean swimming, our results suggest that natural selection has pushed the swimmeret neural circuit toward a connection topology that produces optimal behavior.
一个单独的局部模式生成电路控制小龙虾中每个游泳足的运动。
DOI: 10.1152/jn.1993.70.6.2620
发表时间: 1993
影响因子: 2.5
作者:
Murchison,D;Chrachri,A;Mulloney,B
通讯作者: Mulloney,B
小龙虾游泳足系统局部模式生成电路中的五种类型的非尖峰中间神经元。
DOI: 10.1152/jn.00079.2013
发表时间: 2013
影响因子: 2.5
作者:
Smarandache-Wellmann,Carmen;Weller,Cynthia;WrightJr,TerrenceM;Mulloney,Brian
通讯作者: Mulloney,Brian