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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 a...

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Autores principales: Varshney, Lav R., Chen, Beth L., Paniagua, Eric, Hall, David H., Chklovskii, Dmitri B.
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3033362/
https://www.ncbi.nlm.nih.gov/pubmed/21304930
http://dx.doi.org/10.1371/journal.pcbi.1001066
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author Varshney, Lav R.
Chen, Beth L.
Paniagua, Eric
Hall, David H.
Chklovskii, Dmitri B.
author_facet Varshney, Lav R.
Chen, Beth L.
Paniagua, Eric
Hall, David H.
Chklovskii, Dmitri B.
author_sort Varshney, Lav R.
collection PubMed
description 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.
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spelling pubmed-30333622011-02-08 Structural Properties of the Caenorhabditis elegans Neuronal Network Varshney, Lav R. Chen, Beth L. Paniagua, Eric Hall, David H. Chklovskii, Dmitri B. PLoS Comput Biol Research Article 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. Public Library of Science 2011-02-03 /pmc/articles/PMC3033362/ /pubmed/21304930 http://dx.doi.org/10.1371/journal.pcbi.1001066 Text en Varshney et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Varshney, Lav R.
Chen, Beth L.
Paniagua, Eric
Hall, David H.
Chklovskii, Dmitri B.
Structural Properties of the Caenorhabditis elegans Neuronal Network
title Structural Properties of the Caenorhabditis elegans Neuronal Network
title_full Structural Properties of the Caenorhabditis elegans Neuronal Network
title_fullStr Structural Properties of the Caenorhabditis elegans Neuronal Network
title_full_unstemmed Structural Properties of the Caenorhabditis elegans Neuronal Network
title_short Structural Properties of the Caenorhabditis elegans Neuronal Network
title_sort structural properties of the caenorhabditis elegans neuronal network
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3033362/
https://www.ncbi.nlm.nih.gov/pubmed/21304930
http://dx.doi.org/10.1371/journal.pcbi.1001066
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