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Structural Properties of the Caenorhabditis elegans Neuronal Network

Varshney, Lav R. and Chen, Beth L. and Paniagua, Eric and Hall, David H. and Chklovskii, Dmitri B. (2011) Structural Properties of the Caenorhabditis elegans Neuronal Network. PLoS Computational Biology, 7 (2). Art. No. e1001066. ISSN 1553-734X. PMCID PMC3033362. https://resolver.caltech.edu/CaltechAUTHORS:20110314-142918338

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Abstract

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.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1371/journal.pcbi.1001066 DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3033362/PubMed CentralArticle
Additional Information:© 2011 Varshney et al. 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 credited. Received June 25, 2010; Accepted December 21, 2010; Published February 3, 2011. Editor: Olaf Sporns, Indiana University, United States of America. Funding: LRV was supported by the NSF Graduate Research Fellowship and NSF Grants 0325774, 0836720, and 0729069. BLC was the recipient of an Arnold and Mabel Beckman Graduate Student Fellowship of the Watson School of Biological Sciences. DBC was supported by National Institute of Mental Health Grant 69838, the Swartz Foundation, and a Klingenstein Foundation Award. The Center for C. elegans Anatomy is supported by National Institutes of Health Grant RR 12596 (to DHH). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank John White and Jonathan Hodgkin for the generous donation of the MRC/LMB archival documents and experimental materials to Hall’s laboratory at AECOM, without which this study would not have been possible. We also thank Markus Reigl for providing some of the software used in this study. We thank Sanjoy K. Mitter, Scott Emmons, Leon Avery, Mark Goldman, Cori Bargmann, Alexander Teplyaev, Shawn Lockery and Gonzalo de Polavieja for helpful discussions and for commenting on the manuscript. Author Contributions: Conceived and designed the experiments: BLC DHH DBC. Performed the experiments: BLC DHH. Analyzed the data: LRV BLC EP DBC. Contributed reagents/materials/analysis tools: LRV BLC EP DHH DBC. Wrote the paper: LRV DBC.
Funders:
Funding AgencyGrant Number
NSFCCF-0325774
NSFCCF-0836720
NSFCCF-0729069
Arnold and Mabel Beckman FoundationUNSPECIFIED
NIH69838
Swartz FoundationUNSPECIFIED
Klingenstein FoundationUNSPECIFIED
NIHRR 12596
National Institute of Mental Health (NIMH)UNSPECIFIED
NSF Graduate Research FellowshipUNSPECIFIED
Issue or Number:2
PubMed Central ID:PMC3033362
Record Number:CaltechAUTHORS:20110314-142918338
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20110314-142918338
Official Citation:Varshney LR, Chen BL, Paniagua E, Hall DH, Chklovskii DB (2011) Structural Properties of the Caenorhabditis elegans Neuronal Network. PLoS Comput Biol 7(2): e1001066. doi:10.1371/journal.pcbi.1001066
Usage Policy: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 credited.
ID Code:22868
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:15 Mar 2011 21:23
Last Modified:12 Feb 2020 20:04

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