Regional complexity in enteric neuron wiring reflects diversity of motility patterns in the mouse large intestine
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.
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Author details
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)
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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