Mechanisms underlying nutrient-induced segmentation in isolated guinea pig small intestine

2007 ◽  
Vol 292 (4) ◽  
pp. G1162-G1172 ◽  
Author(s):  
R. M. Gwynne ◽  
J. C. Bornstein
Keyword(s):  
Small Intestine ◽  
Guinea Pig ◽  
Motor Neurons ◽  
Slow Wave ◽  
Neural Circuit ◽  
Circular Muscle ◽  
Decanoic Acid ◽  
Slow Waves ◽  
Longitudinal Position

Mechanisms underlying nutrient-induced segmentation within the gut are not well understood. We have shown that decanoic acid and some amino acids induce neurally dependent segmentation in guinea pig small intestine in vitro. This study examined the neural mechanisms underlying segmentation in the circular muscle and whether the timing of segmentation contractions also depends on slow waves. Decanoic acid (1 mM) was infused into the lumen of guinea pig duodenum and jejunum. Video imaging was used to monitor intestinal diameter as a function of both longitudinal position and time. Circular muscle electrical activity was recorded by using suction electrodes. Recordings from sites of segmenting contractions showed they are always associated with excitatory junction potentials leading to action potentials. Recordings from sites oral and anal to segmenting contractions revealed inhibitory junction potentials that were time locked to those contractions. Slow waves were never observed underlying segmenting contractions. In paralyzed preparations, intracellular recording revealed that slow-wave frequency was highly consistent at 19.5 (SD 1.4) cycles per minute (c/min) in duodenum and 16.6 (SD 1.1) c/min in jejunum. By contrast, the frequencies of segmenting contractions varied widely (duodenum: 3.6–28.8 c/min, median 10.8 c/min; jejunum: 3.0–27.0 c/min, median 7.8 c/min) and sometimes exceeded slow-wave frequencies for that region. Thus nutrient-induced segmentation contractions in guinea pig small intestine do not depend on slow-wave activity. Rather they result from a neural circuit producing rhythmic localized activity in excitatory motor neurons, while simultaneously activating surrounding inhibitory motor neurons.

scholarly journals The myogenic component in distention-induced peristalsis in the guinea pig small intestine

2001 ◽  
Vol 280 (3) ◽  
pp. G491-G500 ◽  
Author(s):  
Graeme Donnelly ◽  
Timothy D. Jackson ◽  
Krista Ambrous ◽  
Jing Ye ◽  
Adeel Safdar ◽  
...  
Keyword(s):  
Small Intestine ◽  
Guinea Pig ◽  
Slow Wave ◽  
Action Potentials ◽  
Slow Waves ◽  
Intraluminal Pressure ◽  
Control Activity ◽  
Potential Oscillations ◽  
Frequency Gradient

In an in vitro model for distention-induced peristalsis in the guinea pig small intestine, the electrical activity, intraluminal pressure, and outflow of contents were studied simultaneously to search for evidence of myogenic control activity. Intraluminal distention induced periods of nifedipine-sensitive slow wave activity with superimposed action potentials, alternating with periods of quiescence. Slow waves and associated high intraluminal pressure transients propagated aborally, causing outflow of content. In the proximal small intestine, a frequency gradient of distention-induced slow waves was observed, with a frequency of 19 cycles/min in the first 1 cm and 11 cycles/min 10 cm distally. Intracellular recording revealed that the guinea pig small intestinal musculature, in response to carbachol, generated slow waves with superimposed action potentials, both sensitive to nifedipine. These slow waves also exhibited a frequency gradient. In addition, distention and cholinergic stimulation induced high-frequency membrane potential oscillations (∼55 cycles/min) that were not associated with distention-induced peristalsis. Continuous distention produced excitation of the musculature, in part neurally mediated, that resulted in periodic occurrence of bursts of distally propagating nifedipine-sensitive slow waves with superimposed action potentials associated with propagating intraluminal pressure waves that caused pulsatile outflow of content at the slow wave frequency.

Myogenic mechanism for peristalsis in the cat esophagus

1999 ◽  
Vol 277 (2) ◽  
pp. G306-G313 ◽  
Author(s):  
Harold G. Preiksaitis ◽  
Nicholas E. Diamant
Keyword(s):  
Muscle Contraction ◽  
Slow Wave ◽  
Circular Muscle ◽  
Smooth Muscle Contraction ◽  
Slow Waves ◽  
Mechanical Activity ◽  
Control Mechanisms ◽  
Slow Wave Oscillations

A myogenic control system (MCS) is a fundamental determinant of peristalsis in the stomach, small bowel, and colon. In the esophagus, attention has focused on neuronal control, the potential for a MCS receiving less attention. The myogenic properties of the cat esophagus were studied in vitro with and without nerves blocked by 1 μM TTX. Muscle contraction was recorded, while electrical activity was monitored by suction electrodes. Spontaneous, nonperistaltic, electrical, and mechanical activity was seen in the longitudinal muscle and persisted after TTX. Spontaneous circular muscle activity was minimal, and peristalsis was not observed without pharmacological activation. Direct electrical stimulation (ES) in the presence of bethanechol or tetraethylammonium chloride (TEA) produced slow-wave oscillations and spike potentials accompanying smooth muscle contraction that progressed along the esophagus. Increased concentrations of either drug in the presence of TTX produced slow waves and spike discharges, accompanied by peristalsis in 5 of 8 TEA- and 2 of 11 bethanechol-stimulated preparations without ES. Depolarization of the muscle by increasing K+ concentration also produced slow waves but no peristalsis. We conclude that the MCS in the esophagus requires specific activation and is manifest by slow-wave oscillations of the membrane potential, which appear to be necessary, but are not sufficient for myogenic peristalsis. In vivo, additional control mechanisms are likely supplied by nerves.

Voltage sensitivity of slow wave frequency in isolated circular muscle strips from guinea pig gastric antrum

1999 ◽  
Vol 276 (2) ◽  
pp. G518-G528 ◽  
Author(s):  
S.-M. Huang ◽  
S. Nakayama ◽  
S. Iino ◽  
T. Tomita
Keyword(s):  
Smooth Muscle ◽  
Guinea Pig ◽  
Slow Wave ◽  
Circular Muscle ◽  
Gastric Antrum ◽  
Slow Waves ◽  
Wave Frequency ◽  
Voltage Sensitivity ◽  
Dependent Manner ◽  
Circular Smooth Muscle

In circular muscle preparations isolated from the guinea pig gastric antrum, regular spontaneous electrical activity (slow waves) was recorded. Under normal conditions (6 mM K+), the frequency and shape of the slow waves were similar to those observed in ordinary stomach smooth muscle preparations. When the resting membrane potential was hyperpolarized and depolarized by changing the extracellular K+ concentration (2–18 mM), the frequency of slow waves decreased and increased, respectively. Application of cromakalim hyperpolarized the cell membrane and reduced the frequency of slow waves in a dose-dependent manner. Cromakalim (3 μM) hyperpolarized the membrane, and slow waves ceased in most preparations. In the presence of cromakalim, subsequent increases in the extracellular K+ concentration restored the frequency of slow waves accompanied by depolarization. Also, glibenclamide completely antagonized this effect of cromakalim. In smooth muscle strips containing both circular and longitudinal muscle layers, such changes in the slow wave frequency were not observed. It was concluded that the maneuver of isolating circular smooth muscle altered the voltage dependence of the slow wave frequency.

Ascending enteric reflex: multiple neurotransmitter systems and interactions

1989 ◽  
Vol 256 (3) ◽  
pp. G540-G545 ◽  
Author(s):  
P. Holzer
Keyword(s):  
Small Intestine ◽  
Substance P ◽  
Guinea Pig ◽  
Motor Neurons ◽  
Circular Muscle ◽  
Neural Pathways ◽  
Neurotransmitter Systems ◽  
Cholinergic Interneurons

Isolated segments of the guinea pig small intestine were used to examine the transmitter circuitry of the neural pathways subserving the ascending enteric reflex (AER) contraction of the circular muscle. Inflation of an intraluminal balloon provided the distension stimulus for the AER. The ascending contraction was reduced to 5% of its original amplitude by atropine and to 10% by hexamethonium, which indicates that cholinergic interneurons and cholinergic motor neurons constitute the main AER pathway. However, in the continued presence of atropine or hexamethonium for 60 min, the AER recovered to approximately 30% of its original amplitude. The atropine-resistant AER was blocked by hexamethonium and the tachykinin antagonist spantide [( D-Arg1,D-Trp7,9, Leu11]-substance P) suggesting that it involved cholinergic interneurons and tachykinin-utilizing motor neurons. The hexamethonium-resistant AER was abolished by atropine but left unaffected by spantide, suggesting the participation of as yet unidentified interneurons and cholinergic motor neurons. These findings demonstrate that the AER is mediated by multiple neural pathways with different transmitters and that adaptive interactions between these pathways take place after blockade of one of its neurotransmitters systems.

Slow wave and spike action potentials recorded in cell cultures from the muscularis externa of the guinea pig small intestine

1999 ◽  
Vol 77 (8) ◽  
pp. 598-605 ◽  
Author(s):  
Rosa Espinosa-Luna ◽  
Stephen M Collins ◽  
Luis M Montaño ◽  
Carlos Barajas-López
Keyword(s):  
Small Intestine ◽  
Guinea Pig ◽  
Cell Cultures ◽  
Slow Wave ◽  
Action Potentials ◽  
Critical Mass ◽  
Slow Waves ◽  
Intracellular Recordings ◽  
Spontaneous Movements ◽  
Muscularis Externa

Intracellular recordings were obtained to investigate whether slow wave and spike type action potentials are present in cell cultures of the muscularis externa from the guinea pig small intestine. The muscularis externa of the small intestine was dissociated by using specific purified enzymes and gentle mechanical dissociation. Cells were plated on cover slips and maintained in culture for up to 4 weeks. Dissociated cells obtained in this way reorganized themselves in a few days to form small cell clumps showing spontaneous movements. Intracellular recordings of these clumps displayed both spike and slow wave type action potentials. Spikes were observed on top of some slow waves and were abolished by the addition of nifedipine or the removal of extracellular calcium. Slow waves, however, were nifedipine insensitive and temperature sensitive, and were abolished by octanol (a gap junction blocker) and forskolin (an adenyl cyclase activator). Slow waves were never observed in small clumps (<50 µm), suggesting that a critical mass of cells might be required for their generation. These observations demonstrated for the first time the presence of nifedipine-insensitive slow waves in cell cultures of the muscularis externa from the guinea pig small intestine. Cell cultures allow rigorous control of the immediate environment for the cells and this should facilitate future studies on the molecular and cellular mechanisms responsible for the slow waves in the gastrointestinal tract.Key words: smooth muscle, slow waves, spiking activity, gastrointestinal tract, gut, small intestine, electrophysiology, pacemaker activity, guinea pig.

Serotonin and cholecystokinin mediate nutrient-induced segmentation in guinea pig small intestine

2013 ◽  
Vol 304 (8) ◽  
pp. G749-G761 ◽  
Author(s):  
Melina Ellis ◽  
Jordan D. Chambers ◽  
Rachel M. Gwynne ◽  
Joel C. Bornstein
Keyword(s):  
Small Intestine ◽  
Guinea Pig ◽  
Time Course ◽  
Pyridoxal Phosphate ◽  
Neural Circuit ◽  
Contractile Activity ◽  
Computational Simulation ◽  
Decanoic Acid ◽  
Receptor Antagonists ◽  
Cck Receptor Antagonists

Segmentation is an important process in nutrient mixing and absorption; however, the mechanisms underlying this motility pattern are poorly understood. Segmentation can be induced by luminal perfusion of fatty acid in guinea pig small intestine in vitro and mimicked by the serotonin (5-HT) reuptake inhibitor fluoxetine (300 nM) and by cholecystokinin (CCK). Serotonergic and CCK-related mechanisms underlying nutrient-induced segmentation were investigated using selective 5-HT and CCK receptor antagonists on isolated segments of small intestine luminally perfused with 1 mM decanoic acid. Motility patterns were analyzed using video imaging and spatiotemporal maps. Segmenting activity mediated by decanoic acid was depressed following luminal application of the 5-HT receptor antagonists granisetron (5-HT3, 1 μM) and SB-207266 (5-HT4, 10 nM) and the CCK receptor antagonists devazepide (CCK-1, 300 nM) and L-365260 (CCK-2, 300 nM), but these antagonists did not further depress segmentation when combined. The P2 receptor antagonist pyridoxal phosphate-6-azophenyl-2′,4′-disulfonate (10 μM) had no effect on activity. Serosal application of 5-HT antagonists had little effect on segmentation in the duodenum but reduced activity in the jejunum when granisetron and SB-207266 were applied together. These results reveal that 5-HT3 and 5-HT4 receptors, as well as CCK-1 and CCK-2 receptors, are critical in regulating decanoic acid-induced segmentation. Computational simulation indicated that these data are consistent with decanoic acid activating two pathways in the mucosa that converge within the enteric neural circuitry, while contraction-induced release of 5-HT from the mucosa provides feedback into the neural circuit to set the time course of the overall contractile activity.

Pacemaker activity in septal structures of canine colonic circular muscle

1990 ◽  
Vol 259 (2) ◽  
pp. G264-G273 ◽  
Author(s):  
S. M. Ward ◽  
K. M. Sanders
Keyword(s):  
Slow Wave ◽  
Electrical Coupling ◽  
Circular Muscle ◽  
Proximal Colon ◽  
Slow Waves ◽  
Pacemaker Activity ◽  
Electrical Measurements ◽  
Morphological Studies ◽  
Circular Layer ◽  
And Function

Morphological and electrophysiological experiments were performed to characterize the pacemaker areas of the circular muscle in the canine proximal colon. Morphological studies showed interstitial cells of Cajal lining the submucosal surface of the circular layer and the septal structures that separate the circular layer into bundles. Electrical measurements suggested that slow waves may propagate into the thickness of the circular muscle in a regenerative manner along the surface of these septa. Removal of the submucosal pacemaker region blocked generation of slow waves in nonseptal regions of the circular muscle, but slow-wave activity continued in the circular muscle near septa. These data suggest that slow-wave pacemaker activity is not limited to a two-dimensional surface at the submucosal surface but extends into the interior of the circular layer along septal invaginations. Experiments were also performed to determine the dominance of pacemaker activity (i.e., septal vs. submucosal), and examples were found in which both areas appeared to initiate slow waves in intact muscles. Other studies showed that slow waves could propagate across septa, suggesting some form of electrical coupling between circular muscle bundles. This study provides a more complete view of the structure and function of pacemaker areas in the canine proximal colon.

Some species differences in the intrinsic factor stimulation of B12 uptake by small intestine in vitro

1959 ◽  
Vol 197 (4) ◽  
pp. 926-928 ◽  
Author(s):  
T. Hastings Wilson ◽  
Elliott W. Strauss
Keyword(s):  
Small Intestine ◽  
Guinea Pig ◽  
Species Differences ◽  
Intrinsic Factor ◽  
Vitamin B ◽  
Guinea Pig Ileum ◽  
Rat Intestine ◽  
Intrinsic Factors ◽  
Stimulation Of

Sacs of everted small intestine from a variety of animals were incubated in bicarbonate-saline containing vitamin B12 with and without intrinsic factor (IF). B12 uptake by rat intestine was stimulated only by its own intrinsic factor. Guinea pig ileum responded to all intrinsic factors tested (guinea pig, rat, hog, hamster, human being and rabbit). The intestines of hamster and rabbit were intermediate in specificity, responding to some, but not all, of the IF preparations. Species differences occur in both the intestine and intrinsic factor preparations. The guinea pig ileum was suggested as a possible assay for both hog and human IF.

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