A cellular and regulatory map of the cholinergic nervous system of C.elegans

  1. Laura Pereira
  2. Paschalis Kratsios
  3. Esther Serrano-Saiz
  4. Hila Sheftel
  5. Avi E Mayo
  6. David H Hall
  7. John G White
  8. Brigitte LeBoeuf
  9. L Rene Garcia
  10. Uri Alon
  11. Oliver Hobert  Is a corresponding author
  1. Howard Hughes Medical Institute, Columbia University, United States
  2. Weizmann Institute of Science, Israel
  3. Albert Einstein College of Medicine, United States
  4. MRC Laboratory of Molecular Biology, United Kingdom
  5. Texas A&M University, United States
  6. Howard Hughes Medical Institute, Texas A&M University, United States

Abstract

Nervous system maps are of critical importance for understanding how nervous systemsdevelop and function. We systematically map here all cholinergic neuron types in the male and hermaphrodite C.elegans nervous system. We find that acetylcholine is the most broadly used neurotransmitter and we analyze its usage relative to other neurotransmitters within the context of the entire connectome and within specific network motifs embedded in the connectome. We reveal several dynamic aspects of cholinergic neurotransmitter identity, including a sexually dimorphic glutamatergic to cholinergic neurotransmitter switch in a sex-shared interneuron. An expression pattern analysis of ACh-gated anion channels furthermore suggests that ACh may also operate very broadly as an inhibitory neurotransmitter. As a first application of this comprehensive neurotransmitter map, we identify transcriptional control mechanisms that control cholinergic neurotransmitter identity and cholinergic circuit assembly.

Article and author information

Author details

  1. Laura Pereira

    Department of Biological Sciences, Department of Biochemistry and Molecular Biophysics, Howard Hughes Medical Institute, Columbia University, New York, United States
    Competing interests
    No competing interests declared.
  2. Paschalis Kratsios

    Department of Biological Sciences, Department of Biochemistry and Molecular Biophysics, Howard Hughes Medical Institute, Columbia University, New york, United States
    Competing interests
    No competing interests declared.
  3. Esther Serrano-Saiz

    Department of Biological Sciences, Department of Biochemistry and Molecular Biophysics, Howard Hughes Medical Institute, Columbia University, New York, United States
    Competing interests
    No competing interests declared.
  4. Hila Sheftel

    Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    No competing interests declared.
  5. Avi E Mayo

    Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    No competing interests declared.
  6. David H Hall

    Department of Neuroscience, Albert Einstein College of Medicine, New York, United States
    Competing interests
    No competing interests declared.
  7. John G White

    MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    No competing interests declared.
  8. Brigitte LeBoeuf

    Department of Biology, Texas A&M University, College Station, United States
    Competing interests
    No competing interests declared.
  9. L Rene Garcia

    Department of Biology, Howard Hughes Medical Institute, Texas A&M University, College Station, United States
    Competing interests
    No competing interests declared.
  10. Uri Alon

    Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    No competing interests declared.
  11. Oliver Hobert

    Department of Biological Sciences, Department of Biochemistry and Molecular Biophysics, Howard Hughes Medical Institute, Columbia University, New York, United States
    For correspondence
    or38@columbia.edu
    Competing interests
    Oliver Hobert, Reviewing editor, eLife.

Reviewing Editor

  1. Kang Shen, Howard Hughes Medical Institute, Stanford University, United States

Version history

  1. Received: October 20, 2015
  2. Accepted: December 22, 2015
  3. Accepted Manuscript published: December 25, 2015 (version 1)
  4. Version of Record published: February 18, 2016 (version 2)

Copyright

© 2015, Pereira 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. Laura Pereira
  2. Paschalis Kratsios
  3. Esther Serrano-Saiz
  4. Hila Sheftel
  5. Avi E Mayo
  6. David H Hall
  7. John G White
  8. Brigitte LeBoeuf
  9. L Rene Garcia
  10. Uri Alon
  11. Oliver Hobert
(2015)
A cellular and regulatory map of the cholinergic nervous system of C.elegans
eLife 4:e12432.
https://doi.org/10.7554/eLife.12432

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https://doi.org/10.7554/eLife.12432

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