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Research Article

Wiring optimization can relate neuronal structure and function

Beth L. Chen, David H. Hall, and Dmitri B. Chklovskii
  1. *Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724; and
  2. ‡Albert Einstein College of Medicine, Bronx, NY 10461

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PNAS March 21, 2006 103 (12) 4723-4728; https://doi.org/10.1073/pnas.0506806103
Beth L. Chen
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  • For correspondence: chenb@cshl.edu mitya@cshl.edu
David H. Hall
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Dmitri B. Chklovskii
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  • For correspondence: chenb@cshl.edu mitya@cshl.edu
  1. Edited by Charles F. Stevens, Salk Institute for Biological Studies, La Jolla, CA, and approved January 26, 2006 (received for review August 8, 2005)

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Abstract

We pursue the hypothesis that neuronal placement in animals minimizes wiring costs for given functional constraints, as specified by synaptic connectivity. Using a newly compiled version of the Caenorhabditis elegans wiring diagram, we solve for the optimal layout of 279 nonpharyngeal neurons. In the optimal layout, most neurons are located close to their actual positions, suggesting that wiring minimization is an important factor. Yet some neurons exhibit strong deviations from “optimal” position. We propose that biological factors relating to axonal guidance and command neuron functions contribute to these deviations. We capture these factors by proposing a modified wiring cost function.

  • Caenorhabditis elegans
  • optimal placement

Footnotes

  • †To whom correspondence may be addressed. E-mail: chenb{at}cshl.edu or mitya{at}cshl.edu
  • Author contributions: B.L.C. and D.H.H. compiled the new version of the wiring diagram; and B.L.C. and D.B.C. formulated and solved optimization problems and wrote the paper.

  • ↵ ¶Kaiser, M. & Hilgetag, C. C., Society for Neuroscience Meeting, Nov. 12–16, 2005, Washington, D.C., Program No. 137-9.

  • Conflict of interest statement: No conflicts declared.

  • This paper was submitted directly (Track II) to the PNAS office.

  • ↵ §Results of this work were presented at the 2004 Computational and Systems Neuroscience (Cosyne) meeting at Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.

  • © 2006 by The National Academy of Sciences of the USA
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Wiring optimization can relate neuronal structure and function
Beth L. Chen, David H. Hall, Dmitri B. Chklovskii
Proceedings of the National Academy of Sciences Mar 2006, 103 (12) 4723-4728; DOI: 10.1073/pnas.0506806103

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Wiring optimization can relate neuronal structure and function
Beth L. Chen, David H. Hall, Dmitri B. Chklovskii
Proceedings of the National Academy of Sciences Mar 2006, 103 (12) 4723-4728; DOI: 10.1073/pnas.0506806103
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Proceedings of the National Academy of Sciences of the United States of America: 103 (12)
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  • Article
    • Abstract
    • Wiring Cost Minimization in the Dedicated-Wire Model
    • Comparison of the Minimum-Wiring Placement with Actual Layout
    • Robustness of Optimization Results to Small Variations of Parameters
    • What Causes Discrepancies Between Predicted and Actual Neuronal Layouts?
    • Distribution of Synapse Locations Along a Neuron May Not Predict Cell Body Placement
    • Directionality of Synapses Along the Neuron May Bias the Location of Cell Bodies
    • Wiring Optimization Using the Shared-Wire Model
    • Discussion
    • Acknowledgments
    • Note added in proof.
    • Footnotes
    • References
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