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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.

SUBMITTER: Li Z

PROVIDER: S-EPMC6391068 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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

Li Zhiling Z Hao Marlene M MM Van den Haute Chris C Baekelandt Veerle V Boesmans Werend W Vanden Berghe Pieter P

eLife 20190212

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 circui ...[more]

PMID: 30747710

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Project description:Although microbiota plays a critical role for the normal development and function of host immune systems, the detail of the influence, especially on those in the large intestine (LI), remains unknown. Here, we performed transcriptome analysis using Affymetrix GeneChip on LI of germ-free (GF) and specific pathogen free (SPF) mice of IQI, an inbred strain established from ICR. Experiment Overall Design: Male germ-free (GF) and specific pathogen-free (SPF) IQI/Jic mice were bred and maintained in the laboratory of Central Institute for Experimental Animals (CIEA, Kawasaki, Kanagwa, Japan). GF mice were housed in a Trexler-type flexible film isolator in a standard germ free state and screened on a weekly basis for germ-free status by sampling feces sterilely and culturing on MRS-agar plates under aerobic and anaerobic conditions. All the GF, SPF, ex-GF mice were kept in a 12: 12-h light/dark cycle and at a temperature of 22+-2 ÂºC. Nine week old mice (n=3) were sacrificed by cervical dislocation and the colon was dissected (the colon was not divided into proximal and distal sections and was treated as a single intestinal section). Experiment Overall Design: The SPF mice were provided by the Central Institute for Experimental Animals of Japan. These mice were determined free of the following pathogens (by various techniques including culture, microscopic observation, serological test, and PCR): Dermatophytes, Citrobacter rodentium, Pasteurella pneumotropica, Corynebacterium kutscheri, Pseudomonas aeruginosa, Salmonella spp., Staphylococcus aureus, Mycoplasma pulmonis, Corynebacterium kutscheri, Salmonella typhimurium, Clostridium piliforme, Mycoplasma pulmonis, Mouse hepatitis virus, Sendai virus, Ectromelia virus, Lymphocytic c. virus, Hantavirus, Giardia muris, Spironucleus muris, Syphacia spp., Aspiculuris tetraptera, Ectoparasits, Intestinalprotozoa, Pinworm, Pneumocystis carinii, Helicobacter hepaticus, Helicobacter bilis, EDIM virus(Rotavirus), Pneumonia virus of mice, Minute virus of mice, Mouse adenovirus, Mouse cytomegalovirus, Mouse encephalomyelitis virus, Reovirus type3, and CAR bacillus.

Project description:BACKGROUND: Within the gut the autonomous enteric nervous system (ENS) is able to sense mechanical stimuli and to trigger gut reflex behaviour. We previously proposed a novel sensory circuit in the ENS which consists of multifunctional rapidly adapting mechanosensitive enteric neurons (RAMEN) in the guinea pig. The aim of this study was to validate this concept by studying its applicability to other species or gut regions. METHODOLOGY/PRINCIPAL FINDINGS: We deformed myenteric ganglia in the mouse small and large intestine and recorded spike discharge using voltage sensitive dye imaging. We also analysed expression of markers hitherto proposed to label mouse sensory myenteric neurons in the ileum (NF145kD) or colon (calretinin). RAMEN constituted 22% and 15% of myenteric neurons per ganglion in the ileum and colon, respectively. They encoded dynamic rather than sustained deformation. In the colon, 7% of mechanosensitive neurons fired throughout the sustained deformation, a behaviour typical for slowly adapting echanosensitive neurons (SAMEN). RAMEN and SAMEN responded directly to mechanical deformation as their response remained unchanged after synaptic blockade in low Ca(++)/high Mg(++). Activity levels of RAMEN increased with the degree of ganglion deformation. Recruitment of more RAMEN with stronger stimuli may suggest low and high threshold RAMEN. The majority of RAMEN were cholinergic but most lacked expression of NF145kD or calretinin. CONCLUSIONS/SIGNIFICANCE: We showed for the first time that fundamental properties of mechanosensitive enteric neurons, such as firing pattern, encoding of dynamic deformation, cholinergic phenotype and their proportion, are conserved across species and regions. We conclude that RAMEN are important for mechanotransduction in the ENS. They directly encode dynamic changes in force as their firing frequency is proportional to the degree of deformation of the ganglion they reside in. The additional existence of SAMEN in the colon is likely an adaptation to colonic motor patterns which consist of phasic and tonic contractions.

Dataset Information

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

Publications

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

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