Comparative Anatomy of the Myenteric Plexus of the Distal Colon in Eight Mammals

The study was designed to investigate the effect of estradiol on the excitatory effect of oxytocin (OT) on colon motility. Female Wistar rats were used, and some of them were ovariectomized (OVX) and treated with vehicle or estradiol (E2). A plastic balloon made of condom was inserted into colon to monitor the change of colonic pressure in vivo. Longitudinal muscle strips of distal colon were prepared to monitor the spontaneous contraction of colon in vitro. Expression of OT receptor (OTR) was investigated by Western blot analysis. Expression of OTR mRNA was detected by RT-PCR. Immunohistochemistry was used to locate OTR. In OVX rats, pretreatment of E2 (4–100 μg/kg sc) dose-dependently increased the excitatory effect of OT on colon motility both in vivo and in vitro and increased the expression of OTR and OTR mRNA in colon. Systemic administration of OT excited the colon motility in vivo in rats at perioda of proestrus and estrus but did not influence it at diestrus period, when the concentration of plasma E2 was lowest in the estrous cycle. Pretreatment of atosiban, the specific OTR antagonist, and TTX, the blocker of voltage-dependent sodium channel on nerve fiber, attenuated the excitatory effect of OT on colon motility. OTR was located in myenteric plexus of colon. These results suggested that E2 increased the excitatory effect of OT on colon motility by upregulating the expression of OTR in myenteric plexus.

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Faculty Opinions recommendation of Enteric glia are targets of the sympathetic innervation of the myenteric plexus in the guinea pig distal colon.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.3760956.4862059 ◽

2010 ◽

Author(s):

Tor Savidge ◽

John H Winston

Keyword(s):

Guinea Pig ◽

Myenteric Plexus ◽

Sympathetic Innervation ◽

Distal Colon ◽

Enteric Glia

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Regional cholinergic differences between distal and proximal colonic myenteric plexus

AJP Gastrointestinal and Liver Physiology ◽

10.1152/ajpgi.1990.258.3.g404 ◽

1990 ◽

Vol 258 (3) ◽

pp. G404-G410 ◽

Cited By ~ 3

Author(s):

W. L. Hasler ◽

S. Kurosawa ◽

O. Y. Chung

Keyword(s):

Myenteric Plexus ◽

Regional Differences ◽

Acetylcholine Release ◽

Longitudinal Muscle ◽

Circular Muscle ◽

Distal Colon ◽

Proximal Colon ◽

Maximal Response ◽

Total Tissue ◽

Cholinergic Response

We investigated differences in myogenic and neural response of proximal vs. distal guinea pig colon in longitudinal and circular muscle. Spontaneous phasic contractions were more intense in distal colon in both layers. Phasic contractile frequency was also greater in distal colon in both layers. In both longitudinal and circular muscle, acetylcholine induced greater contractions in distal than in proximal colon (maximal response: longitudinal, 7.00 +/- 1.04 X 10(4) vs. 3.50 +/- 0.49 X 10(4) N/m2; circular, 3.29 +/- 0.82 X 10(4) vs. 8.92 +/- 1.30 X 10(3) N/m2). Compared with proximal colon, electric field stimulation induced greater atropine-sensitive contractions in distal colon in both muscle layers (maximal response: longitudinal, 4.22 +/- 0.53 X 10(4) vs. 7.53 +/- 1.97 X 10(3) N/m2; circular, 2.14 +/- 0.79 X 10(3) vs. -5.28 +/- 2.04 X 10(2) N/m2). In contrast, there were no regional differences in atropine-insensitive relaxations. Veratridine (10(-5) M) stimulated greater [3H]acetylcholine release from distal longitudinal muscle-myenteric plexus than from proximal preparations (11.44 +/- 2.03 vs. 5.84 +/- 1.26% of total tissue radioactivity). These data suggest the greater contractile responses in the distal colon are because of enhanced cholinergic response to neural stimuli and increased muscle sensitivity to acetylcholine, whereas there are no differences in the inhibitory responses to neural stimuli.

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Mechanisms underlying distension-evoked peristalsis in guinea pig distal colon: is there a role for enterochromaffin cells?

AJP Gastrointestinal and Liver Physiology ◽

10.1152/ajpgi.00101.2011 ◽

2011 ◽

Vol 301 (3) ◽

pp. G519-G527 ◽

Cited By ~ 72

Author(s):

Nick J. Spencer ◽

Sarah J. Nicholas ◽

Lucy Robinson ◽

Melinda Kyloh ◽

Nicholas Flack ◽

...

Keyword(s):

Guinea Pig ◽

Myenteric Plexus ◽

Distal Colon ◽

Solid Content ◽

Submucosal Plexus ◽

Fecal Pellets ◽

Colonic Wall ◽

Ec Cells ◽

Colonic Distension ◽

Muscularis Externa

The mechanisms underlying distension-evoked peristalsis in the colon are incompletely understood. It is well known that, following colonic distension, 5-hydroxytryptamine (5-HT) is released from enterochromaffin (EC) cells in the intestinal mucosa. It is also known that exogenous 5-HT can stimulate peristalsis. These observations have led some investigators to propose that endogenous 5-HT release from EC cells might be involved in the initiation of colonic peristalsis, following distension. However, because no direct evidence exists to support this hypothesis, the aim of this study was to determine directly whether release of 5-HT from EC cells was required for distension-evoked colonic peristalsis. Real-time amperometric recordings of 5-HT release and video imaging of colonic wall movements were performed on isolated segments of guinea pig distal colon, during distension-evoked peristalsis. Amperometric recordings revealed basal and transient release of 5-HT from EC cells before and during the initiation of peristalsis, respectively. However, removal of mucosa (and submucosal plexus) abolished 5-HT release but did not inhibit the initiation of peristalsis nor prevent the propagation of fecal pellets or intraluminal fluid. Maintained colonic distension by fecal pellets induced repetitive peristaltic waves, whose intrinsic frequency was also unaffected by removal of the submucosal plexus and mucosa, although their propagation velocities were slower. In conclusion, the mechanoreceptors and sensory neurons activated by radial distension to initiate peristalsis lie in the myenteric plexus and/or muscularis externa, and their activation does not require the submucosal plexus, release of 5-HT from EC cells, nor the presence of the mucosa. The propagation of peristalsis and propulsion of liquid or solid content along the colon is entrained by activity within the myenteric plexus and/or muscularis externa and does not require sensory feedback from the mucosa, nor neural inputs arising from submucosal ganglia.

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Regulation of excitatory neural input to longitudinal intestinal muscle by myenteric interneurons

AJP Gastrointestinal and Liver Physiology ◽

10.1152/ajpgi.1998.275.5.g973 ◽

1998 ◽

Vol 275 (5) ◽

pp. G973-G978 ◽

Cited By ~ 8

Author(s):

J. R. Grider

Keyword(s):

Substance P ◽

Myenteric Plexus ◽

Neurotransmitter Release ◽

Longitudinal Muscle ◽

Distal Colon ◽

Excitatory Input ◽

Gaba Neurons ◽

Inhibitory Pathways ◽

Neural Input ◽

Rat Distal Colon

The circuit of myenteric interneurons that regulate excitatory input to longitudinal colonic muscle was identified using dispersed ganglia and longitudinal muscle strips with adherent myenteric plexus from rat distal colon. The preparations enabled measurement of neurotransmitter release from interneurons and/or excitatory motoneurons innervating longitudinal muscle. 1,1-Dimethyl-4-phenylpiperizinium (DMPP) and somatostatin were used to activate myenteric neurons in dispersed ganglia and muscle strips, respectively. DMPP-stimulated vasoactive intestinal peptide (VIP) release in dispersed ganglia was inhibited by [Met]enkephalin and bicuculline and augmented by naloxone and GABA, implying that inhibitory opioid and stimulatory GABA neurons regulate the activity of VIP interneurons. In muscle strips, VIP stimulated basal and augmented somatostatin-induced substance P (SP) release; the somatostatin-induced increase in SP release was inhibited by VIP-(10—28) and N G-nitro-l-arginine, implying that excitatory VIP neurons regulate tachykinin motoneurons innervating longitudinal muscle. Somatostatin inhibited [Met]enkephalin and stimulated VIP release; basal and somatostatin-stimulated VIP release were inhibited by [Met]enkephalin and bicuculline and augmented by naloxone and GABA, implying that inhibitory pathways linking somatostatin, opioid, and GABA neurons regulate VIP interneurons, which in turn regulate tachykinin and probably cholinergic motoneurons.

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Electrical rhythmicity and spread of action potentials in longitudinal muscle of guinea pig distal colon

AJP Gastrointestinal and Liver Physiology ◽

10.1152/ajpgi.00345.2001 ◽

2002 ◽

Vol 282 (5) ◽

pp. G904-G917 ◽

Cited By ~ 21

Author(s):

Nick J. Spencer ◽

Grant W. Hennig ◽

Terence K. Smith

Keyword(s):

Guinea Pig ◽

Myenteric Plexus ◽

Action Potentials ◽

Longitudinal Muscle ◽

Circular Muscle ◽

Intrinsic Property ◽

Distal Colon ◽

Separation Distance ◽

Spontaneous Action ◽

Cells Of Cajal

Using simultaneous intracellular recordings, we have characterized 1) electrical activity in the longitudinal muscle (LM) of isolated segments of guinea pig distal colon free to contract spontaneously and 2) extent of propagation of spontaneous action potentials around the circumference of the colon. In all animals, rhythmical spontaneous depolarizations (SDs) were recorded that are usually associated with the generation of action potentials. Recordings from pairs of LM cells, separated by 100 μm in the circumferential axis, revealed that each action potential was phase locked at the two electrodes (mean propagation velocity: 3 mm/s). However, at an increased electrode separation distance of 1 mm circumferentially, action potentials and SDs became increasingly uncoordinated at the two recording sites. No SDs or action potentials ever propagated from one circumferential edge to the other (i.e., 13 mm apart). When LM strips were separated from the myenteric plexus and circular muscle, rhythmically firing SDs and action potentials were still recorded. Atropine (1 μM) or tetrodotoxin (1 μM) either reduced the frequency of SDs or temporily abolished activity, whereas nifedipine (1 μM) always abolished SDs and action potentials. Kit-positive interstitial cells of Cajal were present at the level of the myenteric plexus and circular and longitudinal muscle. In summary, SDs and action potentials in LM propagate over discrete localized zones, usually <1 mm around the circumference of the colon. Furthermore, in contrast to the classic slow wave, rhythmic depolarizations in LM appear to be generated by an intrinsic property of the smooth muscle itself and are critically dependent on opening of L-type Ca2+ channels.

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Correlation of morphology, electrophysiology and chemistry of neurons in the myenteric plexus of the guinea-pig distal colon

Journal of the Autonomic Nervous System ◽

10.1016/s0165-1838(99)00008-9 ◽

1999 ◽

Vol 76 (1) ◽

pp. 45-61 ◽

Cited By ~ 53

Author(s):

A.E.G Lomax ◽

K.A Sharkey ◽

P.P Bertrand ◽

A.M Low ◽

J.C Bornstein ◽

...

Keyword(s):

Guinea Pig ◽

Myenteric Plexus ◽

Distal Colon

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Homeoprotein OTX1 and OTX2 involvement in rat myenteric neuron adaptation after DNBS-induced colitis

PeerJ ◽

10.7717/peerj.8442 ◽

2020 ◽

Vol 8 ◽

pp. e8442

Author(s):

Michela Bistoletti ◽

Giovanni Micheloni ◽

Nicolò Baranzini ◽

Annalisa Bosi ◽

Andrea Conti ◽

...

Keyword(s):

Nitric Oxide ◽

Nervous System ◽

Small Intestine ◽

Nitric Oxide Synthase ◽

Myenteric Plexus ◽

Distal Colon ◽

Myeloperoxidase Activity ◽

Myenteric Neurons ◽

Protein Levels ◽

Oxide Synthase

Background Inflammatory bowel diseases are associated with remodeling of neuronal circuitries within the enteric nervous system, occurring also at sites distant from the acute site of inflammation and underlying disturbed intestinal functions. Homeoproteins orthodenticle OTX1 and OTX2 are neuronal transcription factors participating to adaptation during inflammation and underlying tumor growth both in the central nervous system and in the periphery. In this study, we evaluated OTX1 and OTX2 expression in the rat small intestine and distal colon myenteric plexus after intrarectal dinitro-benzene sulfonic (DNBS) acid-induced colitis. Methods OTX1 and OTX2 distribution was immunohistochemically investigated in longitudinal muscle myenteric plexus (LMMP)-whole mount preparations. mRNAs and protein levels of both OTX1 and OTX2 were evaluated by qRT-PCR and Western blotting in LMMPs. Results DNBS-treatment induced major gross morphology and histological alterations in the distal colon, while the number of myenteric neurons was significantly reduced both in the small intestine and colon. mRNA levels of the inflammatory markers, TNFα, pro-IL1β, IL6, HIF1α and VEGFα and myeloperoxidase activity raised in both regions. In both small intestine and colon, an anti-OTX1 antibody labeled a small percentage of myenteric neurons, and prevalently enteric glial cells, as evidenced by co-staining with the glial marker S100β. OTX2 immunoreactivity was present only in myenteric neurons and was highly co-localized with neuronal nitric oxide synthase. Both in the small intestine and distal colon, the number of OTX1- and OTX2-immunoreactive myenteric neurons significantly increased after DNBS treatment. In these conditions, OTX1 immunostaining was highly superimposable with inducible nitric oxide synthase in both regions. OTX1 and OTX2 mRNA and protein levels significantly enhanced in LMMP preparations of both regions after DNBS treatment. Conclusions These data suggest that colitis up-regulates OTX1 and OTX2 in myenteric plexus both on site and distantly from the injury, potentially participating to inflammatory-related myenteric ganglia remodeling processes involving nitrergic transmission.

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