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 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.

Excitatory and inhibitory neural regulation of canine pyloric smooth muscle

1990 ◽  
Vol 259 (1) ◽  
pp. G125-G133 ◽  
Author(s):  
F. Vogalis ◽  
K. M. Sanders
Keyword(s):  
Action Potentials ◽  
Slow Component ◽  
Circular Muscle ◽  
Muscle Layer ◽  
Slow Waves ◽  
Cross Sectional ◽  
Intrinsic Innervation ◽  
Circular Layer ◽  
Neuromuscular Apparatus ◽  
Excitatory Junction Potentials

Studies were performed to characterize the intrinsic innervation of the circular muscle layer of the canine pylorus. Cross-sectional strips of muscle were studied with intracellular recording techniques, and junction potentials were elicited with transmural nerve stimulation. Neurally mediated responses were recorded from cells at several points through the thickness of the circular layer. Excitatory junction potentials (EJPs) increased and inhibitory junction potentials (IJPs) decreased in amplitude with distance from the myenteric border of the circular muscle. Atropine blocked EJPs throughout the circular layer, demonstrating that excitatory inputs are primarily cholinergic. The gradient in IJP amplitude persisted after blockade of EJPs. Three components of IJPs were identified: 1) a fast, apamin-sensitive component that reached a peak and decayed within approximately 1 s; 2) a slower, apamin-insensitive component that reached a peak within 800 ms but decayed slowly over 5 s; and 3) a very slow component that reached a maximum in 7-10 s. Junctional potentials affected the pattern of myogenic electrical activity. Transmural stimulation could evoke premature slow waves in the myenteric portion of the circular layer but when excitatory inputs were blocked, IJPs greatly reduced the amplitude of slow waves. EJPs elicited action potentials in submucosal portion of circular muscles, and IJPs hyperpolarized these cells. The influence of intrinsic nerves on contractile patterns of pyloric muscles was also characterized. These data demonstrate that a neuromuscular apparatus exists within the gastroduodenal junction for 1) local regulation of slow waves and 2) independent control of the myenteric and submucosal regions of the circular layer.

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.

Outward currents in longitudinal colonic muscle cells contribute to spiking electrical behavior

1992 ◽  
Vol 263 (1) ◽  
pp. C237-C245 ◽  
Author(s):  
K. D. Thornbury ◽  
S. M. Ward ◽  
K. M. Sanders
Keyword(s):  
Action Potentials ◽  
Circular Muscle ◽  
Outward Current ◽  
Muscle Cells ◽  
Electrical Behavior ◽  
Patch Clamp Technique ◽  
Potential Oscillations ◽  
Voltage Dependent ◽  
Longitudinal Muscles ◽  
K Currents

Electrical events in longitudinal and circular muscles of the colon are different. Longitudinal muscles generate action potentials superimposed upon small depolarizations termed myenteric potential oscillations and circular muscles generate slow wave events that persist for several seconds. Differences between circular and longitudinal muscles may be related to the potassium channels these cells express. We have studied Ca(2+)-dependent and voltage-dependent K currents of isolated longitudinal cells with the whole cell patch-clamp technique. Test depolarizations positive to -40 mV yielded a transient inward current followed by a large sustained outward current. Blockade of the inward Ca2+ current reduced the amplitude of the outward current. Outward current was also reduced by tetraethylammonium (TEA; 1 mM), suggesting that a component of the outward current is Ca2+ dependent. After blockade of the Ca(2+)-dependent outward current, a voltage- and time-dependent component of outward current remained. The activation and inactivation properties and sensitivity to TEA and 4-aminopyridine (4-AP) were characterized. The voltage-dependent outward current in longitudinal cells had different properties than the voltage-dependent K currents in circular muscle cells (i.e., more negative inactivation, less sensitivity to 4-AP). TEA (1-5 mM) increased the amplitude and frequency of action potentials in intact longitudinal muscles; 4-AP (1 mM) had little effect on electrical activity of longitudinal muscles. The data suggest that differences in electrical behavior of the 2 muscle layers may be related to the expression of different species of K channels.

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.

Canine colonic circular muscle generates action potentials without the pacemaker component

1994 ◽  
Vol 72 (1) ◽  
pp. 70-81 ◽  
Author(s):  
Louis W. C. Liu ◽  
Jan D. Huizinga
Keyword(s):  
Smooth Muscle ◽  
Calcium Channel ◽  
Action Potentials ◽  
Interstitial Cells Of Cajal ◽  
Longitudinal Muscle ◽  
Circular Muscle ◽  
Muscle Cells ◽  
Interstitial Cells ◽  
Slow Waves ◽  
Cells Of Cajal

Two dominant types of action potentials in canine colon are slow wave type action potentials (slow waves) and spike-like action potentials (SLAPs). The slow waves, originating at the submuscular surface where a network of interstitial cells of Cajal (ICCs) is found, possess a pacemaker component. Activation of the pacemaker component is insensitive to voltage changes and L-type calcium channel blockers, and is postulated to involve a metabolic clock sensitive to cyclic AMP. SLAPs are more prominent in the longitudinal muscle. To understand the contribution circular muscle cells make to the generation of these action potentials, a circular muscle preparation (devoid of the submuscular ICC – smooth muscle network, longitudinal muscle, and myenteric plexus) was developed. Circular muscle preparations were spontaneously quiescent, with a resting membrane potential of −62.9 ± 0.6 mV. Ba2+ (0.5 mM) depolarized the cells to −51.8 ± 0.6 mV and induced electrical oscillations with a frequency, duration, amplitude, and rate of rise equal to 6.6 ± 0.4 cpm, 2.2 ± 0.2 s, 19.4 ± 0.9 mV, and 21.8 ± 1.7 mV/s, respectively. In most cases, Ba2+-induced oscillations were preceded by a prepotential of 4.4 ± 0.3 mV, with a rate of rise of 1.1 ± 0.1 mV/s. Ba2+-induced oscillations were abolished by 1 μM D600 as well as by repolarization of 6–12 mV. Addition of 0.1 μM Bay K8644 in the presence of Ba2+ further depolarized circular muscle cells to −42.4 ± 0.8 mV and increased the oscillation frequency to 16.8 ± 1.8 cpm. The electrical oscillations induced in circular muscle preparations by Ba2+ and Bay K8644 were similar to the SLAPs exhibited by the isolated longitudinal muscle layer, indicating that generation of SLAPs is an intrinsic property of smooth muscle cells. Forskolin (1 μM), previously shown to dramatically decrease the frequency but not the amplitude of slow waves in preparations including the submuscular ICC network, decreased the amplitude of the Ba2+-induced oscillations in circular muscle preparations without changing the frequency. These results provide strong evidence for the hypothesis that the submuscular ICC – smooth muscle network is essential for the initiation of the pacemaker component of the colonic slow waves. The mechanism for regulating the frequency of slow waves is different from that responsible for the Ba2+-induced oscillations in circular muscle preparations. Circular muscle cells are shown to be excitable and capable of generating oscillatory activity dominated by L-type calcium channel activity, which is regulated by K+ conductance.Key words: interstitial cells of Cajal, smooth muscle, dog colon, barium chloride, potassium conductance, Bay K8644, pacemaking 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.

Cholinergic nerve-mediated excitation in the guinea pig choledochoduodenal junction activated by distension

1994 ◽  
Vol 267 (5) ◽  
pp. G938-G946 ◽  
Author(s):  
F. Vogalis ◽  
R. R. Bywater ◽  
G. S. Taylor
Keyword(s):  
Smooth Muscle ◽  
Guinea Pig ◽  
Action Potential ◽  
Action Potentials ◽  
Discharge Rate ◽  
Circular Muscle ◽  
Muscle Layer ◽  
Circular Muscle Layer ◽  
Circular Layer ◽  
Longitudinal Layer

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)

Electrical coupling of longitudinal and circular intestinal muscle

1984 ◽  
Vol 246 (5) ◽  
pp. G618-G626 ◽  
Author(s):  
L. Elden ◽  
A. Bortoff
Keyword(s):  
Longitudinal Muscle ◽  
Electrical Coupling ◽  
Circular Muscle ◽  
Muscle Cells ◽  
Methyl Blue ◽  
Current Spread ◽  
Hyperpolarizing Response ◽  
Partition Method ◽  
High Degree ◽  
Longitudinal Layer

Space constants (lambda) were determined for longitudinal-circular muscle strips of cat jejunum by the partition method. Pulses of hyperpolarizing current spread along the major axes of circular muscle cells. In the absence of electrical coupling lambda measured from the longitudinal side of the strips should have been approximately 20 times shorter than lambda measured from the circular side. Median values were found to be statistically the same, 2.4 mm for the longitudinal side (n = 13) and 2.9 mm for the circular (n = 25). Methyl blue, iontophoretically injected into cells on the longitudinal side after recording large hyperpolarizing responses, was found in muscle cells located superficially in the longitudinal layer. The radial lambda for longitudinal muscle, determined from the change in magnitude of the hyperpolarizing response as the microelectrode was advanced through the layer, was 0.27 mm. This is too large to cause differences in depth of recording to significantly affect the circumferential lambda in this layer. These data provide evidence for a high degree of electrical coupling between the two muscle layers of cat jejunum.

Pacemaker potentials generated by interstitial cells of Cajal in the murine intestine

2005 ◽  
Vol 288 (3) ◽  
pp. C710-C720 ◽  
Author(s):  
Yoshihiko Kito ◽  
Sean M. Ward ◽  
Kenton M. Sanders
Keyword(s):  
Interstitial Cells Of Cajal ◽  
Circular Muscle ◽  
Muscle Cells ◽  
Interstitial Cells ◽  
Slow Waves ◽  
Pacemaker Activity ◽  
Dependent Manner ◽  
Plateau Potential ◽  
Pacemaker Potentials ◽  
Cells Of Cajal

Pacemaker potentials were recorded in situ from myenteric interstitial cells of Cajal (ICC-MY) in the murine small intestine. The nature of the two components of pacemaker potentials (upstroke and plateau) were investigated and compared with slow waves recorded from circular muscle cells. Pacemaker potentials and slow waves were not blocked by nifedipine (3 μM). In the presence of nifedipine, mibefradil, a voltage-dependent Ca2+ channel blocker, reduced the amplitude, frequency, and rate of rise of upstroke depolarization (d V/d tmax) of pacemaker potentials and slow waves in a dose-dependent manner (1–30 μM). Mibefradil (30 μM) changed the pattern of pacemaker potentials from rapidly rising, high-frequency events to slowly depolarizing, low-frequency events with considerable membrane noise (unitary potentials) between pacemaker potentials. Caffeine (3 mM) abolished pacemaker potentials in the presence of mibefradil. Pinacidil (10 μM), an ATP-sensitive K+ channel opener, hyperpolarized ICC-MY and increased the amplitude and d V/d tmax without affecting frequency. Pinacidil hyperpolarized smooth muscle cells and attenuated the amplitude and d V/d tmax of slow waves without affecting frequency. The effects of pinacidil were blocked by glibenclamide (10 μM). These data suggest that slow waves are electrotonic potentials driven by pacemaker potentials. The upstroke component of pacemaker potentials is due to activation of dihydropyridine-resistant Ca2+ channels, and this depolarization entrains pacemaker activity to create the plateau potential. The plateau potential may be due to summation of unitary potentials generated by individual or small groups of pacemaker units in ICC-MY. Entrainment of unitary potentials appears to depend on Ca2+ entry during upstroke depolarization.

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