1. Neuroscience
Download icon

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
  • Cited 18
  • Views 3,323
  • Annotations
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.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for each of the figures.

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)
  4. Version of Record published: February 26, 2019 (version 2)

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.

Metrics

  • 3,323
    Page views
  • 411
    Downloads
  • 18
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Neuroscience
    Casey Paquola et al.
    Tools and Resources Updated

    Neuroimaging stands to benefit from emerging ultrahigh-resolution 3D histological atlases of the human brain; the first of which is ‘BigBrain’. Here, we review recent methodological advances for the integration of BigBrain with multi-modal neuroimaging and introduce a toolbox, ’BigBrainWarp’, that combines these developments. The aim of BigBrainWarp is to simplify workflows and support the adoption of best practices. This is accomplished with a simple wrapper function that allows users to easily map data between BigBrain and standard MRI spaces. The function automatically pulls specialised transformation procedures, based on ongoing research from a wide collaborative network of researchers. Additionally, the toolbox improves accessibility of histological information through dissemination of ready-to-use cytoarchitectural features. Finally, we demonstrate the utility of BigBrainWarp with three tutorials and discuss the potential of the toolbox to support multi-scale investigations of brain organisation.

    1. Neuroscience
    Gabriella R Sterne et al.
    Tools and Resources Updated

    Neural circuits carry out complex computations that allow animals to evaluate food, select mates, move toward attractive stimuli, and move away from threats. In insects, the subesophageal zone (SEZ) is a brain region that receives gustatory, pheromonal, and mechanosensory inputs and contributes to the control of diverse behaviors, including feeding, grooming, and locomotion. Despite its importance in sensorimotor transformations, the study of SEZ circuits has been hindered by limited knowledge of the underlying diversity of SEZ neurons. Here, we generate a collection of split-GAL4 lines that provides precise genetic targeting of 138 different SEZ cell types in adult Drosophila melanogaster, comprising approximately one third of all SEZ neurons. We characterize the single-cell anatomy of these neurons and find that they cluster by morphology into six supergroups that organize the SEZ into discrete anatomical domains. We find that the majority of local SEZ interneurons are not classically polarized, suggesting rich local processing, whereas SEZ projection neurons tend to be classically polarized, conveying information to a limited number of higher brain regions. This study provides insight into the anatomical organization of the SEZ and generates resources that will facilitate further study of SEZ neurons and their contributions to sensory processing and behavior.