Theory of Condensed Matter Group, Department of Physics, Cavendish Laboratory, University of Cambridge, Cambridge CB3 0HE, United Kingdom.
J Neurosci. 2013 Apr 10;33(15):6380-7. doi: 10.1523/JNEUROSCI.3784-12.2013.
There is increasing interest in topological analysis of brain networks as complex systems, with researchers often using neuroimaging to represent the large-scale organization of nervous systems without precise cellular resolution. Here we used graph theory to investigate the neuronal connectome of the nematode worm Caenorhabditis elegans, which is defined anatomically at a cellular scale as 2287 synaptic connections between 279 neurons. We identified a small number of highly connected neurons as a rich club (N = 11) interconnected with high efficiency and high connection distance. Rich club neurons comprise almost exclusively the interneurons of the locomotor circuits, with known functional importance for coordinated movement. The rich club neurons are connector hubs, with high betweenness centrality, and many intermodular connections to nodes in different modules. On identifying the shortest topological paths (motifs) between pairs of peripheral neurons, the motifs that are found most frequently traverse the rich club. The rich club neurons are born early in development, before visible movement of the animal and before the main phase of developmental elongation of its body. We conclude that the high wiring cost of the globally integrative rich club of neurons in the C. elegans connectome is justified by the adaptive value of coordinated movement of the animal. The economical trade-off between physical cost and behavioral value of rich club organization in a cellular connectome confirms theoretical expectations and recapitulates comparable results from human neuroimaging on much larger scale networks, suggesting that this may be a general and scale-invariant principle of brain network organization.
人们对大脑网络作为复杂系统的拓扑分析越来越感兴趣，研究人员经常使用神经影像学来表示神经系统的大规模组织，而无需精确的细胞分辨率。在这里，我们使用图论来研究线虫秀丽隐杆线虫的神经元连接组，该连接组在细胞尺度上定义为 279 个神经元之间的 2287 个突触连接。我们确定了一小部分高度连接的神经元作为丰富俱乐部（N = 11），它们以高效和高连接距离相互连接。丰富俱乐部神经元几乎完全由运动回路的中间神经元组成，对于协调运动具有已知的功能重要性。丰富俱乐部神经元是连接器枢纽，具有高介数中心度，并且与不同模块中的节点具有许多模块间连接。在识别对之间的最短拓扑路径（模体）时，发现最频繁遍历丰富俱乐部的模体。丰富俱乐部神经元在动物可见运动之前和其身体主要发育伸长阶段之前的早期发育中产生。我们得出的结论是，线虫连接组中高度整合的丰富俱乐部神经元的高布线成本是由动物协调运动的适应性价值所证明的。在细胞连接组中，丰富俱乐部组织的物理成本和行为价值之间的经济权衡符合理论预期，并重现了来自人类神经影像学的可比结果，表明这可能是大脑网络组织的一般和标度不变原则。
