scholarly journals Regulation and dysregulation of esophageal peristalsis by the integrated function of circular and longitudinal muscle layers in health and disease

2016 ◽  
Vol 311 (3) ◽  
pp. G431-G443 ◽  
Author(s):  
Ravinder K. Mittal

Muscularis propria throughout the entire gastrointestinal tract including the esophagus is comprised of circular and longitudinal muscle layers. Based on the studies conducted in the colon and the small intestine, for more than a century, it has been debated whether the two muscle layers contract synchronously or reciprocally during the ascending contraction and descending relaxation of the peristaltic reflex. Recent studies in the esophagus and colon prove that the two muscle layers indeed contract and relax together in almost perfect synchrony during ascending contraction and descending relaxation of the peristaltic reflex, respectively. Studies in patients with various types of esophageal motor disorders reveal temporal disassociation between the circular and longitudinal muscle layers. We suggest that the discoordination between the two muscle layers plays a role in the genesis of esophageal symptoms, i.e., dysphagia and esophageal pain. Certain pathologies may selectively target one and not the other muscle layer, e.g., in eosinophilic esophagitis there is a selective dysfunction of the longitudinal muscle layer. In achalasia esophagus, swallows are accompanied by the strong contraction of the longitudinal muscle without circular muscle contraction. The possibility that the discoordination between two muscle layers plays a role in the genesis of esophageal symptoms, i.e., dysphagia and esophageal pain are discussed. The purpose of this review is to summarize the regulation and dysregulation of peristalsis by the coordinated and discoordinated function of circular and longitudinal muscle layers in health and diseased states.

2017 ◽  
Vol 05 (03) ◽  
pp. E146-E150 ◽  
Author(s):  
David Rahni ◽  
Takashi Toyonaga ◽  
Yoshiko Ohara ◽  
Francesco Lombardo ◽  
Shinichi Baba ◽  
...  

Background and study aims A 54-year-old man was diagnosed with a rectal tumor extending through the submucosal layer. The patient refused surgery and therefore endoscopic submucosal dissection (ESD) was pursued. The lesion exhibited the muscle retraction sign. After dissecting circumferentially around the fibrotic area by double tunneling method, a myotomy was performed through the internal circular muscle layer, creating a plane of dissection between the internal circular muscle layer and the external longitudinal muscle layer, and a myectomy was completed.The pathologic specimen verified T1b grade 1 sprouting adenocarcinoma with 4350 µm invasion into the submucosa with negative resection margins.


1998 ◽  
Vol 76 (10-11) ◽  
pp. 989-999 ◽  
Author(s):  
Michal Ceregrzyn ◽  
Tsuyoshi Ozaki ◽  
Atsukazu Kuwahara ◽  
Maria Wiechetek

The effects of sodium nitrite (0.1, 1, 10 mM) on mechanical activity of isolated rat stomach fundus muscle and the influence of guanylate cyclase activity inhibitor (methylene blue) and channel inhibitors (tetrodotoxin, charybdotoxin, apamin) were studied. Nitrite evoked dose-dependent relaxation in the longitudinal and circular muscle layers. The lowest effective concentration of sodium nitrite was 0.1 mM, which is comparable with the NOAEL (no observed adverse effect level). Tetrodotoxin (1 µM) markedly inhibited electrically induced contraction and rebound relaxation, but did not influence the nitrite-induced relaxation. Charybdotoxin (100 nM) decreased the relaxation evoked by 10 mM nitrite to 52.3 and 65.7% of control reaction in the circular and longitudinal muscle layer, respectively. Apamin (100 nM) did not influence the nitrite-induced relaxation. Methylene blue (10 µM) decreased relaxation induced by nitrite in the longitudinal and circular muscle layer, respectively, to 66.7 and 54.3% of the response to 1 mM nitrite alone. Relaxation induced by nitrite was decreased in the presence of L-cysteine (5 mM), and in the circular and longitudinal muscle layer reached 29.6 and 23.1%, respectively, of the response to 1 mM nitrite alone. We conclude that the relaxing effect of nitrite on gastric fundus results from its direct action on smooth muscle cells and probably the enteric nervous system is not involved in this action. The nitrite-elicited relaxation depends on activation of guanylate cyclase and high conductance Ca2+-activated potassium channels; however, activation of potassium channels might be a part of or might act in parallel with the mechanism involving the cyclic GMP system. Effects of nitrite observed in the presence of L-cysteine suggest that nitrosothiols are not responsible for nitrite-evoked activation of guanylate cyclase.Key words: nitrite, gastric motility, tetrodotoxin, methylene blue, charybdotoxin, L-cysteine.


1990 ◽  
Vol 258 (3) ◽  
pp. G344-G351 ◽  
Author(s):  
A. Tottrup ◽  
A. Forman ◽  
P. Funch-Jensen ◽  
U. Raundahl ◽  
K. E. Andersson

Smooth muscle strips representing longitudinal and circular muscle layers of the esophagogastric junction (EGJ) and esophageal body (EB) of the human esophagus were prepared. The strips were mounted in organ baths and isometric tension was recorded. Square wave stimulation was applied through platinum electrodes. Only responses abolished by tetrodotoxin (TTX) were considered neurogenic. Strips taken from longitudinal muscle layers of the EB and EGJ contracted during field stimulation. The responses evoked were abolished by atropine, and optimal frequency of stimulation was 40 Hz. In strips taken from the circular muscle layer of the EB, a contraction occurred after cessation of the stimulus. Atropine inhibited 90% of this response; the optimal stimulation frequency was 40 Hz. When a tone was induced in strips from this layer, a TTX-sensitive relaxation was seen during field stimulation. During stimulation of strips from the EGJ circular muscle layer, which was the only preparation developing spontaneous active tone, a relaxation was seen. A small contraction followed after termination of the stimulus. The relaxation, which was nonadrenergic, noncholinergic, reached maximum at 10 Hz. Atropine inhibited 40% of the contraction. The results suggest that in the longitudinal muscle layer of the human lower esophagus field stimulation causes postganglionic nerves to release transmitter(s) acting on muscarinic receptors. The responses of circular muscle layers seem to be mediated through release of at least two transmitters.


1980 ◽  
Vol 86 (1) ◽  
pp. 237-248
Author(s):  
ALLEN MANGEL ◽  
C. LADD PROSSER

The intact stomach of the toad initiates rhythmic slow-spikes of 5–15 s duration and frequency of 3-5 min−1. The spontaneous electrical waves originate in the longitudinal muscle layer; isolated circular muscle is quiescent. Aboral conduction velocity is 0.12–0.9 mm s−1. Reduction of external sodium concentration from 89.5 to 15 mM produced no effect on slow spikes, although further reduction to 1.5 mM increased frequency and decreased amplitude. Slow-spikes were unaffected by ouabain or by incubation in potassium-free solution. When calcium in the medium was reduced, slow-spike amplitude and frequency decreased. Slow-spikes exhibited a change in amplitude of 16 mV per decade change in CaO2+; slow-spikes were eliminated at 10−8 M CaO2+ and by blockers of calcium conductance channels. Intact intestine of toad demonstrated slow-waves which resembled those of mammalian intestine. These were sensitive to changes in external sodium and were eliminated by 1 × 10−4M ouabain. It is suggested that rhythmic slow-spikes of longitudinal smooth muscle of amphibian stomach may result from periodic changes in Ca conductance whereas endogenous electrical waves of intestine may result from rhythmic extrusion of sodium.


1975 ◽  
Vol 228 (6) ◽  
pp. 1887-1892 ◽  
Author(s):  
J Melville ◽  
E Macagno ◽  
J Christensen

The hypothesis examined was that contractions of the longitudinal muscle layer occurin the duodenum which are independent of those of the circular muscle layer and that they induce flow of duodenal contents. A segment of opossum duodenum isolated in vitro was marked and photographed during periods of longitudinal muscle contraction, when the circular muscle layer appeared inactive. The prequency of longitudinal oscillation of the marked points was 20.5 cycles/min. The longitudinal displacement wave spread caudad with an average velocity of 3.27 cm/s. Frequency and velocity of electrical slow waves were determined in similiar duodenal segments. Slow-wave frquencywas 18.9 cycles/min. In a two-dimensional mechanical model, flow induced by simulatedlongitudinal muscle layer appear to be driven by the electrical slow waves of the duodenum. They are capable of inducing a pattern of flow in which ocntents flow betweenthe core and the periphery of the intestinal conduit.


1990 ◽  
Vol 68 (11) ◽  
pp. 1419-1431 ◽  
Author(s):  
I. Berezin ◽  
J. D. Huizinga ◽  
E. E. Daniel

We have carried out a detailed ultrastructural study of the interstitial cells near the myenteric plexus of the canine colon and defined the structural characteristics which distinguish them from other resident non-neural cells. We have also examined the interconnections of these interstitial cells with nerves, the longitudinal muscle, and the circular muscle. In addition, we sought connections between interstitial cells of the myenteric plexus and those described earlier at the inner border of the circular muscle in proximal and distal colon. The interstitial cells of the myenteric plexus were structurally distinctive, and made gap junctions with one another and occasionally with smooth muscle. There seemed to be two subsets of these interstitial cells, one associated with the longitudinal muscle and the other with the circular muscle. Cells of both subsets were often close (≤20 nm) to nerve profiles. The interstitial cells near the longitudinal muscle layer penetrated slightly into the muscle layer, but those near the circular muscle did not and neither set contacted the other. Moveover, interstitial cells of Cajal located near the myenteric plexus were never observed to contact those at the inner border of circular muscle. The interstitial cells of Cajal at the canine colon myenteric plexus are structurally organized to provide independent pacemaking activities for the longitudinal and adjacent circular muscle. Their dense innervation suggests that they mediate neural modulation of intestinal pacemaker activities. Moreover, they lack direct contacts with the interstitial cell network at the inner border of circular muscle, which is essential for the primary pacemaking activity of circular muscle. The structural organization of interstitial cells in canine colon is consistent with their proposed role in pacemaking activity of the two muscle layers.Key words: pacemakers, neuromodulation, interstitial cells of Cajal.


1992 ◽  
Vol 263 (2) ◽  
pp. G269-G276 ◽  
Author(s):  
J. F. Kuemmerle ◽  
G. M. Makhlouf

Opioid receptors were characterized on muscle cells isolated separately from the circular and longitudinal muscle layers of rabbit intestine. Selective radioligands for kappa- ([3H]U69,593), delta- ([3H][D-Pen2,5]enkephalin, DPDPE), and mu- ([3H][D-Ala2,N-Me-Phe4,Gly5-ol]enkephalin, DAGO) opioid receptors were used in conjunction with a technique of receptor protection designed to enrich cells with a specific receptor type. Binding was observed only in cells from the circular muscle layer. Binding was rapid (peak within 2 min), temperature dependent, and concentration dependent. Dissociation constants (Kd) for high-affinity binding sites derived from saturation curves (1.1 +/- 0.3 nM for U69,593, 0.39 +/- 0.04 nM for DPDPE, and 1.9 +/- 0.3 nM for DAGO) were similar to Kd values derived from competition curves. In competition studies, the order of potency with which opioid ligands inhibited binding depended on the radioligand used: U69,593 (Kd 1.5 +/- 0.2 nM) inhibited preferentially the binding of [3H]U69,593, DPDPE (Kd 0.72 +/- 0.16 nM) the binding of [3H]DPDPE and DAGO (Kd 1.2 +/- 0.3 nM) the binding of [3H]DAGO. In each instance the other two ligands were 400-12,000 times less potent. In cells enriched with one receptor type, binding and contraction were observed only with the corresponding selective ligand. The potency of the ligand was slightly enhanced, whereas the potencies of the other two ligands were further reduced (greater than 10,000-fold). We conclude that distinct kappa-, delta-, and mu-opioid receptors are present on muscle cells of the circular but not longitudinal muscle layer of the intestine.


2003 ◽  
Vol 284 (5) ◽  
pp. G768-G775 ◽  
Author(s):  
J. R. Grider

A two-compartment, flat-sheet preparation of rat colon was devised, which enabled exclusive measurement of longitudinal muscle activity during the ascending and descending phases of the peristaltic reflex. A previous study using longitudinal muscle strips revealed the operation of an integrated neuronal circuit consisting of somatostatin, opioid, and VIP/pituitary adenylate cyclase-activating peptide (PACAP)/nitric oxide synthase (NOS) interneurons coupled to cholinergic/tachykinin motor neurons innervating longitudinal muscle strips that could lead to descending contraction and ascending relaxation of this muscle layer. Previous studies in peristaltic preparations have also shown that an increase in somatostatin release during the descending phase causes a decrease in Met-enkephalin release and suppression of the inhibitory effect of Met-enkephalin on VIP/PACAP/NOS motor neurons innervating circular muscle and a distinct set of VIP/PACAP/NOS interneurons. The present study showed that in contrast to circular muscle, longitudinal muscle contracted during the descending phase and relaxed during the ascending phase. Somatostatin antiserum inhibited descending contraction and augmented ascending relaxation of longitudinal muscle, whereas naloxone had the opposite effect. VIP and PACAP antagonists inhibited descending contraction of longitudinal muscle and augmented ascending relaxation. Atropine and tachykinin antagonists inhibited descending contraction of longitudinal muscle. As shown in earlier studies, the same antagonists and antisera produced opposite effects on circular muscle. We conclude that longitudinal muscle contracts and relaxes in reverse fashion to circular muscle during the peristaltic reflex. Longitudinal muscle activity is regulated by excitatory VIP/PACAP/NOS interneurons coupled to cholinergic/tachykinin motor neurons innervating longitudinal muscle.


1982 ◽  
Vol 242 (5) ◽  
pp. G498-G503 ◽  
Author(s):  
B. P. Brown ◽  
S. Anuras ◽  
D. D. Heistad

This study was performed to compare mechanical activity produced by acetylcholine and histamine in longitudinal and circular muscle layers of the portal vein. Peak tension was measured in longitudinal and circular muscle strips from portal veins of rabbits as they were superfused with acetylcholine and histamine (10(-6) to 10(-4) M). Responses to acetylcholine were three to four times greater in longitudinal muscle than in circular muscle; for example, acetylcholine (10(-5) M) produced contractions of 1.6 +/- 0.2 X 10(3) (mean +/- SE) dynes in longitudinal muscle and 0.4 +/- 0.09 X 10(3) dynes in circular muscle. In the same strips, histamine produced similar responses in the two layers: histamine (10(-5) M) produced contractions of 0.4 +/- 0.1 X 10(3) dynes in longitudinal and 0.4 +/- 0.1 X 10(3) dynes in circular muscle. Histological studies of portal vein muscle strips showed that the longitudinal muscle layer is three to four times thicker than the circular muscle layer. Thus, in response to acetylcholine, tension developed in each muscle layer is proportional to the thickness of that layer. In response to histamine, however, longitudinal muscle develops less tension than is predicted by the thickness of the muscle layer. We conclude that longitudinal and circular muscle layers of the rabbit portal vein differ in their responsiveness to histamine.


1987 ◽  
Vol 252 (1) ◽  
pp. G136-G142
Author(s):  
J. D. Huizinga ◽  
E. Chow ◽  
N. E. Diamant ◽  
T. Y. el-Sharkaway

Simultaneous recording of electrical activities from the circular and longitudinal muscle layers of the pig colon was performed in vitro to study possible coordination of activities. The electrical activity of both muscle layers consisted of electrical oscillations with superimposed spikes. The frequency range of the electrical oscillations in the circular muscle was 0.5-3.5 cycles per minute (cpm) and in the longitudinal muscle 24-42 cpm. Coordination of the activities of both muscle layers occurred consistently only after stretch or cholinergic stimulation. Then it occurred in a unique fashion. Each oscillation in the circular muscle layer occurred at the same time as the onset of a burst of oscillations in the longitudinal muscle. In addition, multiple simultaneous recordings of the electrical activities from each muscle layer were obtained showing that within the circular muscle layer electrical oscillations were phase locked in the circumferential direction and along the long axis of the colon. They appeared to propagate in either the oral or aboral direction. In tetrodotoxin (with stretch as stimulus) and also in presence of carbachol, bursts of oscillations in the longitudinal muscle layer were phase locked circumferentially (in the different taeniae) and longitudinally. This study shows that the muscle layers in the colon, which have different myogenic electrical activities, can obtain a high level of coordination.


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