Mechanosensitive enteric neurons in the guinea pig gastric corpus

Mazzuoli‐Weber, Gemma; Schemann, Michael

doi:10.3389/fncel.2015.00430

Cited by 24 publications

(39 citation statements)

References 54 publications

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“…3 out of 34 porcine ISMP MEN responded to both mechanical stimuli. This agrees with the data from other species and gastrointestinal regions 16,43 . This finding reinforces the translational aspect of our MEN concept across regions and species.…”

Section: Discussionsupporting

confidence: 93%

“…Furthermore, this finding emphasized that the response was specific. Similar positive relations between stimulus strength and neuronal activity have already been shown for compression stimuli (intraganglionic volume injection and von Frey hair probing) as well as for stretch stimuli 14,16,19 .…”

Section: Discussionsupporting

confidence: 78%

“…In our hands, this rather reflects the conservation of crucial pathways in the ENS across species. Previously, we have already observed similar behaviour of MEN irrespective of whether we recorded from human, guinea pig or mouse myenteric neurons 14,16,23 . In this respect, the pig is just another model and does not seem superior to the guinea pig, in particular since there are large differences between the anatomy of porcine and human colon.…”

Section: Discussionsupporting

confidence: 64%

“…This would also mean that the NOS-expressing MEN rather project within the ISMP and do not project to the mucosa as NO increases secretion by a direct activation of epithelial cells 45 . It is noteworthy, that stretch sensitive MEN in the guinea pig gastric myenteric plexus were also mostly nitrergic 16 .…”

Section: Discussionmentioning

confidence: 86%

“…In addition to compression, the sensitivity of myenteric neurons to tensile forces have been also shown 16,22,23 . Moreover, recordings of ion secretion in response to tissue distensions suggested the existence of stretch activated ion channels on enteric neurons other than capsaicin-sensitive neurons 27 .…”

Section: Discussionmentioning

confidence: 99%

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Compression and stretch sensitive submucosal neurons of the porcine and human colon

Filzmayer

Elfers

Michel

et al. 2020

Sci Rep

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The pig is commonly believed to be a relevant model for human gut functions-however, there are only a few comparative studies and none on neural control mechanisms. To address this lack we identified as one central aspect mechanosensitive enteric neurons (MEN) in porcine and human colon. We used neuroimaging techniques to record responses to tensile or compressive forces in submucous neurons. Compression and stretch caused Ca-transients and immediate spike discharge in 5-11% of porcine and 15-24% of human enteric neurons. The majority of these MEN exclusively responded to either stimulus quality but about 9% responded to both. Most of the MEN expressed choline acetyltransferase and substance P; nitric oxide synthase-positive MEN primarily occurred in distal colon. The findings reveal common features of MEN in human and pig colon which we interpret as a result of species-independent evolutionary conservation rather than a specific functional proximity between the two species. The enteric nervous system (ENS), which is integrated into the wall of the gastrointestinal tract (GIT) from the oesophagus to the anal sphincter, enables the GIT to generate reflex activity independent from central influences 1-3. The ENS is organized in two complex neuronal networks called the submucosal plexus (SMP) and the myenteric plexus (MP). In both, the pig and human the SMP consists of two layers interconnected by interganglionic nerve fiber tracts 4,5. The SMP regulates mostly epithelial functions, such as secretion and absorption, as well as blood flow, cell proliferation and immune responses. The distinct parts of the SMP are called inner SMP (ISMP) and outer SMP (OSMP) with the ISMP being located closely to the lamina muscularis mucosae, whereas the OSMP is located on the luminal side of the circular muscle layer 6. In the porcine and human colon mainly neurons in the ISMP predominantly project to the mucosa 7-9 , and hence likely regulate epithelial functions 10. Enteric neurons can be activated by various stimuli, including chemical stimuli as well as mechanical distortion 11-17. During muscle contraction and relaxation enteric neurons are constantly exposed to distorting forces 16,18. Remarkably, even enteric neurons classically defined as interneurons or motoneurons are mechanosensitive, suggesting that mechanosensitive enteric neurons (MEN) are multifunctional 14,15,19. With intracellular recording techniques it has been shown that MEN in the MP respond to distension as well as to mucosal distortion 20-22. An important step forward was the use of imaging techniques, as they allowed to record simultaneously from a larger set of neurons and were also a prerequisite to study enteric neurons in larger animals 14-17,23,24. Using von Frey hair probing and intraganglionic volume injection, compression sensitive MEN have been identified in the MP of the guinea pig gastric corpus, ileum and colon 14,16,23 as well as in mouse ileum and colon 15. Furthermore, von Frey hair probing was used to identify compression sensitive MEN in isol...

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Section: Discussionsupporting

confidence: 93%

Section: Discussionsupporting

confidence: 78%