Electrical and mechanical interactions between the muscle layers of canine proximal colon

1990 ◽  
Vol 258 (3) ◽  
pp. G484-G491 ◽  
Author(s):  
P. J. Sabourin ◽  
Y. J. Kingma ◽  
K. L. Bowes
Keyword(s):  
Membrane Potential ◽  
Circular Muscle ◽  
Longitudinal Direction ◽  
Proximal Colon ◽  
Slow Waves ◽  
The Other ◽  
Potential Oscillations ◽  
Circular Layer ◽  
Longitudinal Layer ◽  
Membrane Potential Oscillations

Electrical and mechanical interactions between the two smooth muscle layers of canine colon have been studied using a dual sucrose gap apparatus. Muscle samples were dissected into an L-shape, with one leg cut in the circular direction and the other cut in the longitudinal direction. Longitudinal muscle was removed from the circular leg and circular muscle was removed from the longitudinal leg. The bend of the L contained both layers. The activity of the two layers was studied simultaneously under basal conditions, after stimulation by neostigmine and carbachol, and in the presence of tetrodotoxin. Interactions were more common after stimulation and were marked by modification of one layer's mechanical and electrical activity during increased activity in the other layer. Two patterns were commonly observed. First, during a burst of membrane potential oscillations and spike potentials in the longitudinal layer, slow waves in the circular layer developed spike potentials and some slow waves were also prolonged. Second, during a slow-wave cycle in the circular layer, the amplitude of membrane potential oscillations in the longitudinal layer was increased with an associated increase in the incidence of spike potentials. These interactions were associated with contractions of increased strength, which were similar in both layers. All interactions continued after nerve-conduction blockade by tetrodotoxin.

Effects of membrane potential on electrical slow waves of canine proximal colon

1988 ◽  
Vol 255 (6) ◽  
pp. C828-C834 ◽  
Author(s):  
T. K. Smith ◽  
J. B. Reed ◽  
K. M. Sanders
Keyword(s):  
Membrane Potential ◽  
Circular Muscle ◽  
Input Resistance ◽  
Proximal Colon ◽  
Slow Waves ◽  
Cross Sectional ◽  
Electrical Pulses ◽  
Length Constant ◽  
Circular Layer ◽  
External K

The effects of membrane potential on the waveforms and propagation of slow waves were tested using circular muscles of the canine colon. Studies were conducted with intracellular recording techniques on cross-sectional strips of canine proximal colon. Circular muscle cells near the submucosa generated slow waves that decayed in amplitude as they spread through the circular layer. The membrane potentials of cells were less negative as a function of distance from the submucosal border. Cells near the submucosa were depolarized with elevated external K+ and electrical pulses using the partitioned chamber technique. The waveforms of depolarized submucosal cells were compared with events recorded from cells in the bulk of the circular layer. The waveform changes caused by experimental depolarization were different from the changes in waveform that occur during propagation, suggesting the latter are due to a different mechanism than depolarization. The effects of the membrane potential on syncytial input resistance and length constant were also evaluated. The results of these studies are consistent with the hypothesis that slow-wave propagation across the circular layer in canine proximal colon occurs passively.

Origin and propagation of electrical slow waves in circular muscle of canine proximal colon

1987 ◽  
Vol 252 (2) ◽  
pp. C215-C224 ◽  
Author(s):  
T. K. Smith ◽  
J. B. Reed ◽  
K. M. Sanders
Keyword(s):  
Slow Wave ◽  
Circular Muscle ◽  
Proximal Colon ◽  
Slow Waves ◽  
Thin Strip ◽  
Colon Cells ◽  
Cable Properties ◽  
Wave Event ◽  
Circular Layer ◽  
Longitudinal Layer

Experiments to determine the site of slow-wave origin and the mechanism of propagation were performed on muscles of the canine proximal colon. Cells along the submucosal border of the circular layer had resting membrane potentials (RMP) averaging -78 mV, and slow waves, 40 mV in amplitude. The RMP of cells through the thickness of the circular layer decreased exponentially with distance from the submucosal border, such that RMPs of circular cells at the myenteric border were only -43 mV. Slow waves decreased in amplitude through the thickness such that slow waves could not be detected adjacent to the myenteric border. When a thin strip of muscle along the submucosal border was removed, slow waves were not recorded from the bulk of the circular layer and could not be evoked by acetylcholine. Slow waves were still present in the excised strip. Experiments to determine the rate of slow-wave propagation were also performed. Two cells were impaled, one at the submucosal surface, and another at some distance through the circular layer. Slow waves occurred nearly simultaneously at both sites. What latency was observed could be explained on the basis of electrotonic conduction. The results support the hypothesis that in the canine proximal colon slow waves are generated at the extreme submucosal surface of the circular layer. The bulk of the circular layer does not possess either pacemaker or regenerative mechanisms, and slow waves propagate passively toward the myenteric border. The cable properties of the circular muscle syncytium furnish a barrier to invasion of the longitudinal layer by the slow wave event.

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.

Electrical pacemakers of canine proximal colon are functionally innervated by inhibitory motor neurons

1989 ◽  
Vol 256 (3) ◽  
pp. C466-C477 ◽  
Author(s):  
T. K. Smith ◽  
J. B. Reed ◽  
K. M. Sanders
Keyword(s):  
Electrical Activity ◽  
Motor Neurons ◽  
Circular Muscle ◽  
Proximal Colon ◽  
Nerve Fibers ◽  
Pacemaker Activity ◽  
Intracellular Recordings ◽  
Potential Oscillations ◽  
Circular Layer ◽  
Different Populations

Pacemaker activity in the canine proximal colon occurs at the submucosal and myenteric borders of the circular layer [Am. J. Physiol. 252 (Cell Physiol. 21): C215-C224 and C290-C299, 1987]. The present study investigated the neural regulation of rhythmic electrical activity. Spontaneous inhibitory junction potentials (IJPs) were observed in intracellular recordings from circular muscle cells near the myenteric border. The amplitudes of these events decayed with distance through the circular layer. Stimulation at the myenteric plexus surface evoked IJPs that mimicked the spontaneous events. Stimulation at the submucosal surface evoked IJPs in adjacent cells that were of shorter duration and of different waveform than myenteric IJPs. Amplitudes of IJPs evoked by stimulation near either surface decayed with distance from the site of stimulation. The decay functions for IJPs were essentially identical to the decay of spontaneous slow waves or myenteric potential oscillations. Spontaneous and evoked IJPs affected the amplitudes, durations, and patterns of ongoing rhythmic electrical activity. The data suggest that myenteric and submucosal pacemaker populations may be innervated by different populations of inhibitory nerve fibers. Innervation appears to be heterogeneous with dense populations of inhibitory nerve fibers predominantly located in the pacemaker regions. Neural regulations of pacemaker activity influences rhythmic electrical activity throughout the muscularis.

Electrical transmission of slow waves from longitudinal to circular intestinal muscle

1965 ◽  
Vol 209 (6) ◽  
pp. 1254-1260 ◽  
Author(s):  
Alex Bortoff
Keyword(s):  
Longitudinal Muscle ◽  
Circular Muscle ◽  
Complete Removal ◽  
Intestinal Wall ◽  
Slow Waves ◽  
Electrical Transmission ◽  
Circular Layer ◽  
Spontaneous Rhythmicity ◽  
Longitudinal Layer ◽  
Rhythmical Contractions

Circular muscle from cat intestine exhibits spontaneous rhythmical contractions only when it is attached to longitudinal muscle. Under these conditions electrical slow waves can be recorded from circular muscle, but they disappear following complete removal of the longitudinal layer. If a small patch of longitudinal muscle remains, slow waves can be recorded from adjacent circular muscle. Those recorded lateral to the longitudinal layer are synchronized with slow waves recorded directly from this layer. Their amplitude decreases exponentially with distance, approaching zero at about 12 mm from the lateral edges and about 3 mm from the oral or aboral edge of the longitudinal layer. Slow waves can also be recorded across the entire intestinal wall or across a longitudinal-circular muscle preparation. With this method of recording, the amplitude of the slow waves decreases as the thickness of the circular layer is reduced by stripping away its innermost layers. The amplitude is not increased by replacing these layers. These results indicate that slow waves may be transmitted electrotonically from longitudinal to circular muscle, implying the existence of electrical continuity between the two muscle layers. The transmission of slow waves can account for the coordinated spontaneous rhythmicity exhibited by circular muscle under normal conditions, i.e., when attached to the longitudinal layer.

Changes in electrical and mechanical activity during ontogeny of the canine proximal colon

1996 ◽  
Vol 271 (1) ◽  
pp. G184-G191 ◽  
Author(s):  
S. M. Ward
Keyword(s):  
Membrane Potential ◽  
Circular Muscle ◽  
Electrical Field Stimulation ◽  
Muscle Layer ◽  
Proximal Colon ◽  
Mechanical Activity ◽  
Resting Membrane Potential ◽  
Circular Muscle Layer ◽  
Circular Layer ◽  
Spontaneous Contractions

The ontogenetic development of the circular muscle layer of the canine proximal colon was studied in animals from midway through gestation to 30 days old. With age, there was an increase in resting membrane potential along the submucosal surface and a decrease along the myenteric surface of the circular layer. Coinciding with the changes in membrane potential, slow waves increased in amplitude along the submucosal border and decreased in amplitude along the myenteric border. Muscle strips from animals midway through gestation were mechanically quiescent; however, 1 wk before birth spontaneous activity was observed. Electrical field stimulation of enteric nerves increased spontaneous contractions; this increase in activity was reversed to inhibition by atropine. In the presence of atropine and N omega-nitro-L-arginine or N omega-nitro-L-arginine methyl ester, a noncholinergic excitation was revealed at stimulation frequencies > 5 Hz. The results of these studies provide evidence that the canine proximal colon is spontaneously rhythmic and that a functional innervation to the circular muscle layer exists before birth. The gradient in resting membrane potential across the circular layer is absent at birth but develops within 2-3 wk after parturition.

Colonic Electrical Activity: Concerto for Two Pacemakers

Physiology ◽  
1989 ◽  
Vol 4 (5) ◽  
pp. 176-181
Author(s):  
KM Sanders
Keyword(s):  
Electrical Activity ◽  
Circular Muscle ◽  
Proximal Colon ◽  
Slow Waves ◽  
Potential Oscillations ◽  
Contraction Coupling

In the proximal colon, two discrete pacemaker populations exist: one group of cells generates the 6-cycle/min rhythm known as slow waves;other cells generate a 17-cycle/min rhythm termed myenteric potential oscillations. Summation of these events in the circular muscle provides the signal for escitation-contraction coupling. This article describes the origin and integration of pacemaker activities in the colon.

Electrical activity induced by nitric oxide in canine colonic circular muscle

2002 ◽  
Vol 282 (1) ◽  
pp. G123-G129 ◽  
Author(s):  
K. D. Keef ◽  
U. Anderson ◽  
K. O'Driscoll ◽  
S. M. Ward ◽  
K. M. Sanders
Keyword(s):  
Nitric Oxide ◽  
Circular Muscle ◽  
Cyclopiazonic Acid ◽  
Muscle Layer ◽  
Slow Waves ◽  
Potential Oscillations ◽  
Carbonyl Cyanide ◽  
Mitochondrial Uncouplers ◽  
Cells Of Cajal ◽  
Membrane Potential Oscillations

Nitric oxide generates slow electrical oscillations (SEOs) in cells near the myenteric edge of the circular muscle layer, which resemble slow waves generated by interstitial cells of Cajal (ICCs) at the submucosal edge of this muscle. The properties of SEOs were studied to determine whether these events are similar to slow waves. Rapid frequency membrane potential oscillations (MPOs; 16 ± 1 cycles/min and 9.6 ± 0.2 mV) were recorded from control muscles near the myenteric edge. Sodium nitroprusside (0.3 μM) reduced MPOs and initiated SEOs (1.3 ± 0.3 cycles/min and 13.4 ± 1.4 mV amplitude). SEOs were abolished by the guanylate cyclase inhibitor 1H-[1,2,4]-oxadiazolo-[4,3-a]-quinoxaline-1-one (10 μM). MPOs were abolished by nifedipine (1 μM), whereas SEO frequency increased and the amount of depolarization decreased. BAY K 8644 (1 μM) prolonged SEOs and reduced their frequency. SEOs were abolished by Ni2+ (0.5 mM), low Ca2+ solution (0.1 mM Ca2+), cyclopiazonic acid (10 μM), and the mitochondrial uncouplers antimycin (10 μM) and carbonyl cyanide p-trifluoromethoxyphenylhydrazone (1 μM). Oligomycin (10 μM) was without effect. These effects are similar to those described for colonic slow waves. Our results suggest that nitric oxide-induced SEOs are similar in mechanism to slow waves, an activity not previously thought to be generated by myenteric pacemakers.

Interaction of two electrical pacemakers in muscularis of canine proximal colon

1987 ◽  
Vol 252 (3) ◽  
pp. C290-C299 ◽  
Author(s):  
T. K. Smith ◽  
J. B. Reed ◽  
K. M. Sanders
Keyword(s):  
Action Potentials ◽  
Circular Muscle ◽  
Muscle Cells ◽  
Proximal Colon ◽  
Slow Waves ◽  
Cross Sectional ◽  
Electrical Oscillation ◽  
Discrete Populations ◽  
Longitudinal Muscles ◽  
Longitudinal Layer

Experiments were performed to determine the source of the 20 cycles/min electrical oscillation commonly seen in colonic electrical records, the influence of the 20 cycles/min rhythm on the circular and longitudinal muscle layers, and the interactions between the 20 cycles/min rhythm and slow waves in circular muscle cells. Cross-sectional muscle preparations of the canine proximal colon were used to allow impalement of cells at any point through the thickness of the muscularis. Intracellular recordings from circular muscle cells clearly showed the two characteristic pacemaker frequencies in the colon (6 cycles/min slow waves; 20 cycles/min oscillations). The 20 cycles/min oscillations were recorded from longitudinal and circular muscle cells. Their amplitudes were greatest at the myenteric border. In the longitudinal layer the 20 cycles/min events initiated action potentials; in circular muscle the 20 cycles/min events summed with slow waves. Simultaneous recordings from circular and longitudinal cells across the myenteric border demonstrated that events in the two layers were usually in phase, suggesting that the two layers are electrically coupled and are paced by a common pacemaker. The amplitude of the 20 cycles/min events decayed with distance from the myenteric border in both circular and longitudinal muscles. The data demonstrate that two discrete populations of pacemaker cells generate the spontaneous electrical activity in the colon. Both events appear to passively spread through the circular muscle. It is the summation of these events that appears to serve as the signal for excitation-contraction coupling in circular muscle.

Electrical and mechanical effects of acetylcholine and substance P in subregions of canine colon

1992 ◽  
Vol 262 (2) ◽  
pp. G298-G307 ◽  
Author(s):  
K. D. Keef ◽  
S. M. Ward ◽  
R. J. Stevens ◽  
B. W. Frey ◽  
K. M. Sanders
Keyword(s):  
Substance P ◽  
Circular Muscle ◽  
Muscle Layer ◽  
Proximal Colon ◽  
Slow Waves ◽  
Circular Muscle Layer ◽  
Long Duration ◽  
Low Concentrations ◽  
Excitatory Neurotransmitters ◽  
Circular Layer

Effects of acetylcholine (ACh) and substance P on the electrical and mechanical activities of the circular muscle layer of the canine proximal colon were studied. Because this muscle layer is bordered by two different pacemaker regions, responses from segments containing either a single pacemaker region or no pacemaker region were compared with responses of the complete muscle layer. Concentration-response relationships for ACh and substance P were similar between the various segments, suggesting that receptors for these agonists are expressed throughout the layer. The dominant contractile pattern induced by ACh and substance P in each segment was a 1- to 3-cycle/min rhythm. In a like manner, these agonists also elicited an electrical pattern in which a long-duration slow wave occurred one to three times per minute between short-duration slow waves. Low concentrations of nifedipine (0.01 microM) selectively antagonized the 1- to 3-cycle/min rhythm. In circular muscles with no pacemaker region, ACh (1 microM) caused depolarization, induced oscillations in membrane potential averaging 24 +/- 5 mV in amplitude and 2.9 +/- 0.9 cycles/min in frequency, and generated rhythmic contractions at the same frequency. This "interior" circular muscle was functionally innervated by cholinergic excitatory nerves. Exposure to ACh (1 microM) did not alter the conduction of slow waves through the thickness of the circular layer. In summary, the excitatory neurotransmitters, ACh and substance P, induce a dominant electrical and contractile rhythm throughout the circular muscle layer that is different from the spontaneous rhythms produced at either the myenteric or submucosal border.

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