Stretch‐dependent sensitization of post‐junctional neural effectors in colonic muscles
Open accessAbstract
Background The colon undergoes distension‐induced changes in motor activity as luminal contents or feces increase wall pressure. Input from enteric motor neurons regulates this motility. Here we examined stretch‐dependent responses in circular muscle strips of murine colon. Methods Length ramps (6–31 μ m s−1) were applied in the axis of the circular muscle layer in a controlled manner until 5 mN isometric force was reached. Key Results Length ramps produced transient membrane potential hyperpolarizations and attenuation of action potential (AP) complexes. Responses were reproducible when ramps were applied every 30 s. Stretch‐dependent hyperpolarization was blocked by TTX, suggesting AP‐dependent release of inhibitory neurotransmitter(s). Atropine did not potentiate stretch‐induced hyperpolarizations, but increased compliance of the circular layer.Nω‐nitro‐l‐arginine (l‐NNA) inhibited stretch‐dependent hyperpolarization and decreased muscle compliance, suggesting release of NO mediates stretch‐dependent inhibition. Control membrane potential was restored by the NO donor sodium nitorprusside. Stretch‐dependent hyperpolarizations were blocked by l‐methionine, an inhibitor of stretch‐dependent K+(SDK) channels in colonic muscles. Loss of interstitial cells of Cajal, elicited by Kit neutralizing antibody, also inhibited responses to stretch. In presence of l‐NNA and apamin, stretch responses became excitatory and were characterized by membrane depolarization and increased AP firing. A neurokinin‐1 receptor antagonist inhibited this stretch‐dependent increase in excitability. Conclusions and Inferences Our data show that stretch‐dependent responses in colonic muscles require tonic firing of enteric inhibitory neurons, but reflex activation of neurons does not appear to be necessary. NO causes activation of SDK channels, and stretch of muscles further activates these channels, explaining the inhibitory response to stretch in colonic muscle strips.
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Studies in murine and guinea pig models show that enteric neurons are activated or inhibited by luminal stretch with resultant motility changes.
“Studies in murine and guinea pig models show that enteric neurons are activated or inhibited by luminal stretch with resultant motility changes. 56”
From Hypermobile Ehlers–Danlos syndrome and disorders of the gastrointestinal tract: What the gastroenterologist needs to know (2022) · cites this paper as [56]
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- [9]Won K-J Sanders KM Ward SM Stretch induced changes in pacemaker frequency are mediated through ICC in the murine gastric antrum Proc Natl Acad Sci U S A 2005 102 14913 14918 16204383 PMC1253552
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- Authors
- Won, K. ‐., Sanders, K. M., & Ward, S. M.
- Affiliations
- University of Nevada, Reno (US)
- Corresponding author
- Ward, S. M.
- Venue
- Neurogastroenterology & Motility
- Publisher
- Wiley
- Published
- 2013-01-02
- Volume
- 25
- Issue
- 2
- Pages
- e101-13
- ISSN
- 1350-1925 (ISSN-L)
- 1365-2982
- PMC
- PMC3552106
- OpenAlex
- W1487089942
- Cited by
- 12
- References
- 52
- Citations by year
- 2025: 1 · 2024: 2 · 2022: 1 · 2021: 1 · 2019: 1 · 2018: 1 · 2017: 1 · 2016: 1 · 2015: 1 · 2014: 2
- FWCI
- 1.26
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Neurogastroenterology & Motility (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (P01DK041315, DK57236, DK41315, R01DK057236)
- Topics
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Health Sciences › Medicine › Surgery › Congenital gastrointestinal and neural anomalies
- Keywords
- nitric oxide, interstitial cells of Cajal, membrane potential, action potential firing, neurokinin-1 receptor, colonic distension
- MeSH terms
- Animals, Colon, Compliance, Electrophysiology, Membrane Potentials, Mice, Inbred BALB C, Muscle, Smooth, Neurons, Potassium Channels, Enteric Nervous System, Mice, Interstitial Cells of Cajal
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