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.

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.

Slow waves actively propagate at submucosal surface of circular layer in canine colon

1990 ◽  
Vol 259 (2) ◽  
pp. G258-G263 ◽  
Author(s):  
K. M. Sanders ◽  
R. Stevens ◽  
E. Burke ◽  
S. W. Ward
Keyword(s):  
Wave Propagation ◽  
Slow Wave ◽  
Proximal Colon ◽  
Slow Waves ◽  
Pacemaker Cells ◽  
Transverse Axis ◽  
Active Mechanism ◽  
Conduction Velocities ◽  
Circular Layer ◽  
Thin Band

Colonic slow waves originate from pacemaker cells along the submucosal surface of the circular layer in the dog proximal colon. These events propagate in a nonregenerative manner into the bulk of the circular layer. Conduction velocities consistent with an active mechanism for slow-wave propagation in the longitudinal and circumferential axes of the colon have been reported. Experiments were performed using intracellular recording techniques on canine colonic muscles to determine the regenerative pathway for slow-wave propagation. In a thin band of muscle adjacent to the submucosal border of the circular layer, slow-wave amplitude was independent of distance from a pacing source, and events propagated at a rate of approximately 17 mm/s in the long axis of the circular fibers and 6 mm/s in the transverse axis of the circular fibers. These findings suggest that slow waves propagate in a regenerative manner in this region. Slow waves decayed as they conducted through regions from which the pacemaker cells had been removed with space constants of a few millimeters. Thus the integrity of the thin pacemaker region along submucosal surface is critical for propagation of slow waves and the organization of motility into segmental contractions.

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.

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 slow-wave activity from the circular layer of cat terminal antrum

1991 ◽  
Vol 261 (1) ◽  
pp. G78-G82
Author(s):  
L. M. Renzetti ◽  
M. B. Wang ◽  
J. P. Ryan
Keyword(s):  
Slow Wave ◽  
Circular Muscle ◽  
Muscle Cells ◽  
Muscle Layer ◽  
Wave Activity ◽  
Slow Waves ◽  
Slow Wave Activity ◽  
Plateau Phase ◽  
Circular Layer ◽  
Upstroke Velocity

Intracellular recording techniques were used to characterize the electrical slow-wave activity through the thickness of the circular muscle layer of the cat terminal antrum. Muscle strips were pinned out in cross section to the floor of a recording chamber perfused with Krebs buffer. Circular muscle cells from the myenteric to the submucosal border then were impaled with 20- to 40-M omega glass microelectrodes, and slow-wave activity was recorded. Slow waves from the myenteric side of the circular layer consisted of an upstroke depolarization, a prominent plateau phase, and a downstroke repolarization. Slow-wave characteristics for cells along the myenteric border were Em, -74.2 +/- 1.3 mV; duration, 5.3 +/- 0.5 s; upstroke amplitude, 29.4 +/- 3.4 mV; upstroke velocity, 0.20 +/- 0.03 V/s; and frequency, 5.8 +/- 0.5/min. Slow waves from muscle cells along the submucosal side of the preparation lacked a discernible plateau phase. Slow waves from submucosal border cells had the following characteristics: Em, -80.4 +/- 1.4 mV (P less than 0.01); duration, 3.5 +/- 0.4 s (P less than 0.01); upstroke amplitude, 44.0 +/- 2.4 mV (P less than 0.01); upstroke velocity, 0.56 +/- 0.06 V/s (P less than 0.01); and frequency, 4.2 +/- 0.4/min (P less than 0.05). Slow waves were not affected by 10(-7)M tetrodotoxin and 10(-6)M atropine or by removal of the longitudinal muscle layer. Slow-wave activity within each region was maintained after dissecting the circular layer into submucosal and myenteric segments. The results suggest that two distinct slow waves exist within the circular muscle layer of the cat terminal antrum.(ABSTRACT TRUNCATED AT 250 WORDS)

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.

Electrical coupling and pacemaker activity in colonic smooth muscle

1988 ◽  
Vol 255 (5) ◽  
pp. C653-C660 ◽  
Author(s):  
J. D. Huizinga ◽  
A. Shin ◽  
E. Chow
Keyword(s):  
Slow Wave ◽  
Electrical Coupling ◽  
Circular Muscle ◽  
Input Resistance ◽  
Wave Activity ◽  
Slow Wave Activity ◽  
Pacemaker Activity ◽  
Isolated Cells ◽  
Current Spread ◽  
Length Constant

The effect of heptanol on electrical coupling between submucosal circular muscle cells of the dog colon and consequences for slow-wave activity were investigated. Electrotonic potentials showed exponential decay giving a length constant of 2.6 +/- 0.5 mm and a time constant of 157 +/- 48 ms. Heptanol reversibly abolished electrotonic current spread, and subsequently no slow-wave activity was recorded. The length constant decreased to less than 0.2 mm. The input resistance increased from 3 to 36 M omega, suggesting a change from tissue syncytium to electrically isolated cells. D600 (5 X 10(-6) M) also abolished slow wave activity but had opposite effects on electrotonic current spread. The data are consistent with the hypothesis that heptanol reversibly inhibits intercellular coupling, resulting in loss of spread of extracellularly applied current, uncoupling of cells, and loss of pacemaker activity. Regulation of intercellular communication may be important in the control of intestinal motility.

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.

Correlation between electrical and morphological properties of canine pyloric circular muscle

1991 ◽  
Vol 260 (3) ◽  
pp. G390-G398 ◽  
Author(s):  
F. Vogalis ◽  
S. M. Ward ◽  
K. M. Sanders
Keyword(s):  
Single Cells ◽  
Electrical Coupling ◽  
Circular Muscle ◽  
Muscle Layer ◽  
Morphological Properties ◽  
Morphological Examination ◽  
Isolated Cells ◽  
Time Constants ◽  
Morphological Studies ◽  
Cable Properties

Electrical slow waves decay in amplitude as they conduct from the myenteric to the submucosal regions of the circular muscle layer in the canine pyloric sphincter. We used the partitioned chamber method to study the passive and active properties of pyloric muscles, and we found that length constants of circular muscles of myenteric region were significantly longer than muscles near the submucosal surface. These data suggested differences in either membrane resistance, junctional resistance, or cytoplasmic resistance. The first parameter was evaluated by measuring time constants in intact tissues and single cells isolated from the submucosal and myenteric regions. Membrane time constants were not different in the two regions, nor were differences found in the input resistances of isolated cells. Morphological studies failed to demonstrate differences in cell diameters in the two regions suggesting that cytoplasmic resistances are similar. These findings suggest that the different cable properties in the two regions may be due to differences in electrical coupling. Morphological examination revealed similar numbers of gap junctions between cells in the two regions, but large differences were noted in the size of muscular bundles. Muscles of the myenteric region were arranged into large, tightly packed bundles, whereas muscles of the submucosal region consisted of small bundles with an extensive extracellular space filled with connective tissue. We suggest that the difference in cable properties may be due to differences in electrical coupling between bundles. These data suggest that submucosal muscles function more like a multiunit smooth muscle, whereas myenteric muscles behave as a single unit.

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.

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