A stochastic neuronal model predicts random search behaviors at multiple spatial scales in C. elegans

  1. William M Roberts
  2. Steven B Augustine
  3. Kristy J Lawton
  4. Theodore H Lindsay
  5. Tod R Thiele
  6. Eduardo J Izquierdo
  7. Serge Faumont
  8. Rebecca A Lindsay
  9. Matthew Cale Britton
  10. Navin Pokala
  11. Cornelia I Bargmann
  12. Shawn R Lockery  Is a corresponding author
  1. University of Oregon, United States
  2. University of Pennsylvania, United States
  3. Reed College, United States
  4. California Institute of Technology, United States
  5. University of Toronto, Canada
  6. Indiana University, United States
  7. Children's Hospital Los Angeles, United States
  8. University of Minnesota, United States
  9. New York Institiute of Technology, United States
  10. Howard Hughes Medical Institute, Rockefeller University, United States

Abstract

Random search is a behavioral strategy used by organisms from bacteria to humans to locate food that is randomly distributed and undetectable at a distance. We investigated this behavior in the nematode Caenorhabditis elegans, an organism with a small, well-described nervous system. Here we formulate a mathematical model of random search abstracted from the C. elegans connectome and fit to a large-scale kinematic analysis of C. elegans behavior at submicron resolution. The model predicts behavioral effects of neuronal ablations and genetic perturbations, as well as unexpected aspects of wild type behavior. The predictive success of the model indicates that random search in C. elegans can be understood in terms of a neuronal flip-flop circuit involving reciprocal inhibition between two populations of stochastic neurons. Our findings establish a unified theoretical framework for understanding C. elegans locomotion and a testable neuronal model of random search that can be applied to other organisms.

Article and author information

Author details

  1. William M Roberts

    Institute of Neuroscience, University of Oregon, Eugene, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Steven B Augustine

    School of Nursing, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Kristy J Lawton

    Biology Department, Reed College, Portland, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Theodore H Lindsay

    Division of biology and biological engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Tod R Thiele

    Department of Biological Sciences, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  6. Eduardo J Izquierdo

    Cognitive Science Program, Indiana University, Bloomington, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Serge Faumont

    Institute of Neuroscience, University of Oregon, Eugene, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Rebecca A Lindsay

    Department of Ophthalmology, The Vision Center, Children's Hospital Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Matthew Cale Britton

    Department of Neurology, University of Minnesota, Minneapolis, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Navin Pokala

    Department of Life Sciences, New York Institiute of Technology, Old Westbury, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Cornelia I Bargmann

    Howard Hughes Medical Institute, Rockefeller University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Shawn R Lockery

    Institute of Neuroscience, University of Oregon, Eugene, United States
    For correspondence
    shawn@uoregon.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

Version history

  1. Received: October 26, 2015
  2. Accepted: January 19, 2016
  3. Accepted Manuscript published: January 29, 2016 (version 1)
  4. Version of Record published: March 8, 2016 (version 2)
  5. Version of Record updated: October 11, 2018 (version 3)

Copyright

© 2016, Roberts et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. William M Roberts
  2. Steven B Augustine
  3. Kristy J Lawton
  4. Theodore H Lindsay
  5. Tod R Thiele
  6. Eduardo J Izquierdo
  7. Serge Faumont
  8. Rebecca A Lindsay
  9. Matthew Cale Britton
  10. Navin Pokala
  11. Cornelia I Bargmann
  12. Shawn R Lockery
(2016)
A stochastic neuronal model predicts random search behaviors at multiple spatial scales in C. elegans
eLife 5:e12572.
https://doi.org/10.7554/eLife.12572

Share this article

https://doi.org/10.7554/eLife.12572

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