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Regional complexity in enteric neuron wiring reflects diversity of motility patterns in the mouse large intestine

  1. Zhiling Li
  2. Marlene M Hao
  3. Chris Van den Haute
  4. Veerle Baekelandt
  5. Werend Boesmans  Is a corresponding author
  6. Pieter Vanden Berghe  Is a corresponding author
  1. University of Leuven, Belgium
  2. University of Melbourne, Australia
Research Article
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Cite this article as: eLife 2019;8:e42914 doi: 10.7554/eLife.42914

Abstract

The enteric nervous system controls a variety of gastrointestinal functions including intestinal motility. The minimal neuronal circuit necessary to direct peristalsis is well-characterized but several intestinal regions display also other motility patterns for which the underlying circuits and connectivity schemes that coordinate the transition between those patterns are poorly understood. We investigated whether in regions with a richer palette of motility patterns, the underlying nerve circuits reflect this complexity. Using Ca2+ imaging, we determined the location and response fingerprint of large populations of enteric neurons upon focal network stimulation. Complemented by neuronal tracing and volumetric reconstructions of synaptic contacts, this shows that the multifunctional proximal colon requires specific additional circuit components as compared to the distal colon, where peristalsis is the predominant motility pattern. Our study reveals that motility control is hard-wired in the enteric neural networks and that circuit complexity matches the motor pattern portfolio of specific intestinal regions.

Article and author information

Author details

  1. Zhiling Li

    Laboratory for Enteric NeuroScience (LENS), University of Leuven, Leuven, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  2. Marlene M Hao

    Department of Anatomy and Neuroscience, University of Melbourne, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  3. Chris Van den Haute

    Laboratory for Neurobiology and Gene Therapy, Department of Neurosciences, University of Leuven, Leuven, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  4. Veerle Baekelandt

    Laboratory for Neurobiology and Gene Therapy, Department of Neurosciences, University of Leuven, Leuven, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  5. Werend Boesmans

    Laboratory for Enteric NeuroScience (LENS), University of Leuven, Leuven, Belgium
    For correspondence
    werend.boesmans@kuleuven.be
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2426-0451
  6. Pieter Vanden Berghe

    Laboratory for Enteric NeuroScience (LENS), University of Leuven, Leuven, Belgium
    For correspondence
    pieter.vandenberghe@med.kuleuven.be
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0009-2094

Funding

Fonds Wetenschappelijk Onderzoek (G.0921.15)

  • Werend Boesmans
  • Pieter Vanden Berghe

Hercules Foundation (AKUL/15/37)

  • Werend Boesmans
  • Pieter Vanden Berghe

Chinese Scholarship Council (201408370078)

  • Zhiling Li

KULeuven (C32/15/031)

  • Veerle Baekelandt

Hercules Foundation (AKUL/11/37)

  • Werend Boesmans
  • Pieter Vanden Berghe

Fonds Wetenschappelijk Onderzoek (SBO/S006617N)

  • Veerle Baekelandt

Postdoctoral fellowship of the Fund for Scientific Research Flanders

  • Marlene M Hao

Fund for Scientific Research Flanders (G.0921.15 SBO/S006617N)

  • Pieter Vanden Berghe

IWT (SBO/130065)

  • Pieter Vanden Berghe

Hercules Foundation (AKUL/13/37)

  • Werend Boesmans
  • Pieter Vanden Berghe

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experiments were approved by the animal ethics committee of the KU Leuven guidelines for the use and care of animals (specific license numbers: P192-2013; P017-2013; P021-2015)

Reviewing Editor

  1. David D Ginty, Harvard Medical School, United States

Publication history

  1. Received: October 17, 2018
  2. Accepted: February 11, 2019
  3. Accepted Manuscript published: February 12, 2019 (version 1)

Copyright

© 2019, Li 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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