Structural Properties of the Caenorhabditis elegans Neuronal Network
Despite recent interest in reconstructing neuronal networks, complete wiring diagrams on the level of individual synapses remain scarce and the insights into function they can provide remain unclear. Even for Caenorhabditis elegans, whose neuronal network is relatively small and stereotypical from animal to animal, published wiring diagrams are neither accurate nor complete and self-consistent. Using materials from White et al. and new electron micrographs we assemble whole, self-consistent gap junction and chemical synapse networks of hermaphrodite C. elegans. We propose a method to visualize the wiring diagram, which reflects network signal flow. We calculate statistical and topological properties of the network, such as degree distributions, synaptic multiplicities, and small-world properties, that help in understanding network signal propagation. We identify neurons that may play central roles in information processing, and network motifs that could serve as functional modules of the network. We explore propagation of neuronal activity in response to sensory or artificial stimulation using linear systems theory and find several activity patterns that could serve as substrates of previously described behaviors. Finally, we analyze the interaction between the gap junction and the chemical synapse networks. Since several statistical properties of the C. elegans network, such as multiplicity and motif distributions are similar to those found in mammalian neocortex, they likely point to general principles of neuronal networks. The wiring diagram reported here can help in understanding the mechanistic basis of behavior by generating predictions about future experiments involving genetic perturbations, laser ablations, or monitoring propagation of neuronal activity in response to stimulation. Connectomics, the generation and analysis of neuronal connectivity data, stands to revolutionize neurobiology just as genomics has revolutionized molecular biology. Indeed, since neuronal networks are the physical substrates upon which neural functions are carried out, their structural properties are intertwined with the organization and logic of function. In this paper, we report a near-complete wiring diagram of the nematode Caenorhabditis elegans and present several analyses of its properties, finding many nonrandom features. We give novel visualizations and compute network statistics to enhance understanding of the reported data. We also use principled systems-theoretic methods to generate hypotheses on how biological function may arise from the reported neuronal network structure. The wiring diagram reported here can further be used to generate predictions about signal propagation in future perturbation, ablation, or artificial stimulation experiments.