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

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.

1990 ◽  
Vol 259 (2) ◽  
pp. G264-G273 ◽  
Author(s):  
S. M. Ward ◽  
K. M. Sanders

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.


1990 ◽  
Vol 258 (3) ◽  
pp. G484-G491 ◽  
Author(s):  
P. J. Sabourin ◽  
Y. J. Kingma ◽  
K. L. Bowes

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.


1990 ◽  
Vol 259 (2) ◽  
pp. G258-G263 ◽  
Author(s):  
K. M. Sanders ◽  
R. Stevens ◽  
E. Burke ◽  
S. W. Ward

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.


1965 ◽  
Vol 209 (6) ◽  
pp. 1254-1260 ◽  
Author(s):  
Alex Bortoff

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.


1991 ◽  
Vol 261 (1) ◽  
pp. G78-G82
Author(s):  
L. M. Renzetti ◽  
M. B. Wang ◽  
J. P. Ryan

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)


1988 ◽  
Vol 255 (6) ◽  
pp. C828-C834 ◽  
Author(s):  
T. K. Smith ◽  
J. B. Reed ◽  
K. M. Sanders

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.


1989 ◽  
Vol 256 (4) ◽  
pp. G779-G784 ◽  
Author(s):  
K. M. Sanders ◽  
E. P. Burke ◽  
R. J. Stevens

The hypothesis that methylene blue has a direct effect on colonic muscle cells was tested. Intracellular recordings were made from cross-sectional preparations of canine proximal colon. Cells through the circular layer were impaled and membrane potentials ranging from -81 mV at the submucosal surface to -46 mV at the myenteric border were recorded. Methylene blue (10(-5) M) depolarized cells near the submucosal border by an average of 43 mV and slow-wave activity ceased. The loss of slow-wave activity could be explained by the depolarizing effects of methylene blue rather than a specific effect of methylene blue on the pacemaker mechanism. Other experiments suggested that the depolarizing effects of methylene blue were not confined to muscle cells within the submucosal pacemaker region. Depolarization of cells was noted throughout the circular layer, but the magnitude of the depolarization decreased with distance from the submucosal border. After methylene blue, the gradient in resting potential across the circular layer was greatly reduced or abolished. The data suggest that methylene blue is not necessarily a specific probe for interstitial cells and has direct effects on smooth muscle cells in the canine proximal colon. This effect is similar to treatments that are known to block the electrogenic sodium pump.


1987 ◽  
Vol 252 (3) ◽  
pp. C290-C299 ◽  
Author(s):  
T. K. Smith ◽  
J. B. Reed ◽  
K. M. Sanders

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.


1992 ◽  
Vol 262 (2) ◽  
pp. G298-G307 ◽  
Author(s):  
K. D. Keef ◽  
S. M. Ward ◽  
R. J. Stevens ◽  
B. W. Frey ◽  
K. M. Sanders

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.


1994 ◽  
Vol 267 (5) ◽  
pp. G938-G946 ◽  
Author(s):  
F. Vogalis ◽  
R. R. Bywater ◽  
G. S. Taylor

The electrical basis of propulsive contractions in the guinea pig choledochoduodenal junction (CDJ), which are triggered by distension, was investigated using intracellular microelectrode recording techniques. The isolated CDJ was placed in a continuously perfused tissue chamber at 37 degrees C. Membrane potential was recorded from smooth muscle cells in either the ampulla or in the upper CDJ (upper junction) regions, which were immobilized by pinning. Distension of the upper junction (20-30 s) by increasing intraductal hydrostatic pressure (mean elevation: 2.0 +/- 0.3 kPa, n = 13) triggered "transient depolarizations" (TDs: < 5 mV in amplitude and 2-5 s in duration) and action potentials in the circular muscle layer of the ampulla. The frequency of TDs in the ampulla was increased from 2.2 +/- 0.2 to 15.9 +/- 2.2 min-1 (n = 13) during distension. Simultaneous impalements of cells in the longitudinal and circular muscle layers in the ampulla revealed that subthreshold TDs in the circular layer were associated with an increased rate of action potential discharge in the longitudinal layer. Atropine (Atr; 1.4 x 10(-6) M) and tetrodotoxin (TTX; 3.1 x 10(-6) M blocked the distension-evoked increase in TD frequency, without affecting the frequency of ongoing TDs. The sulfated octapeptide of cholecystokinin (1-5 x 10(-8) M) increased the amplitude of TDs recorded in the circular muscle layer of the ampulla and increased action potential discharge rate. In separate recordings, radial stretch of the ampulla region increased the rate of discharge of action potentials in the smooth muscle of the upper junction.(ABSTRACT TRUNCATED AT 250 WORDS)


Sign in / Sign up

Export Citation Format

Share Document