Comprehensive Physiology Wiley Online Library
For Librarians For Authors Editors About

Electrophysiology of the gastric musculature

Kenton M. Sanders, Nelson G. Publicover

10.1002/cphy.cp060105

Source: Supplement 16: Handbook of Physiology, The Gastrointestinal System, Motility and Circulation

Originally published: 1989

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Resting Membrane Potential
1.1 Contribution of Diffusion Potential
1.2 Contribution of Electrogenic Pumps
2 Excitable Events in Gastric Muscles
2.1 Gastric Slow Waves
2.2 Action Potentials
2.3 Electrical Arrhythmias
2.4 Electrical Events of Fundus
2.5 Electrical Activity of Muscularis Mucosa
2.6 Electrical Activity of Amphibian Stomach
3 Excitation‐Contraction Coupling
3.1 Mechanical Threshold
3.2 Anatomical Variation of Voltage‐Tension Relationship
3.3 Voltage Dependence of Ca2+ Channels
4 Electropharmacology of Endogenous Substances
4.1 Adrenergic Agonists
4.2 Cholinergic Agonists
4.3 Peptides
4.4 Prostaglandins
5 Propagation of Electrical Events
5.1 Cell‐to‐Cell Coupling
5.2 Passive Characteristics of Gastric Syncytium
5.3 Measurements of Conduction Velocity
5.4 Use of Conduction‐ Velocity Measurements to Determine Site of Slow‐Wave Origin
5.5 Myogenic Regulation of Propagation
6 Models of Excitability and Propagation
6.1 Relaxation‐Oscillator Models
6.2 Cable Models
7 Directions for Future Research
Figure 1. Figure 1.

Derivation of the shape of gastric slow waves from differential potentials. A: with calomel electrodes applied to surfaces of canine stomachs, differential records of peristaltic waves were recorded. Three waves were identified that were designated as R, S, and T waves. They were similar in shape to corresponding records of cardiac activity except the duration of the complex was 5–8 s. B: approximate shape of gastric slow wave was deduced by integrating differential waveforms. Essential characteristics of the slow wave (upstroke and plateau phases) as recorded by intracellular techniques were apparent from integrated extracellular potentials.

Adapted from Bozler 19
Figure 2. Figure 2.

Recording of gastric slow wave with intracellular electrode from antral circular muscle cell. Various parameters that have been quantitated are upstroke amplitude, time constant of the foot of the upstroke (τf), maximum upstroke velocity (dV/dt), plateau amplitude, slow‐wave duration, area under waveform, and resting membrane potential.

From Bauer et al. 10
Figure 3. Figure 3.

Intracellular potentials recorded from different regions of canine stomach. Variations in resting membrane potential, slow‐wave shape and frequency, and presence of action potentials were observed in isolated tissues from different anatomical regions of the stomach.

From Szurszewski et al. 123
Figure 4. Figure 4.

Slow waves through thickness of circular muscle. Simultaneous intracellular recordings were made from myenteric (electrode A) and submucosal (electrode B) circular muscle cells. Myenteric cells (trace A) were more polarized and generated more robust slow waves than did submucosal cells (trace B). Slow waves always occurred first in myenteric cells, suggesting they originated in the serosal half of muscularis and then propagated through the thickness of circular cells to submucosal cells.

Adapted from Bauer et al. 10
Figure 5. Figure 5.

Dependence of gastric slow wave on external Ca2+. A: slow wave (upper trace) and time derivative (lower trace) recorded intracellularly from canine antral circular cell in Krebs‐Ringer buffer (2.5 mM Ca2+). B: while maintaining impalement, solution bathing muscle was changed to one containing 0.93 mM Ca2+. Reduced [Ca2+] decreased the amplitudes of upstroke and plateau phases and decreased the upstroke velocity.

Courtesy of David Blonfield
Figure 6. Figure 6.

Beginning, middle, and end portions of 17‐min episode of tachygastria in a chronically instrumented dog. Top trace in each panel was recorded by an extracellular electrode 4 cm proximal to pylorus. Bottom trace in each panel was recorded by an electrode 2 cm proximal to pylorus. At beginning of top panel, slow waves were recorded at a typical frequency for canine stomachs. These events were propagating in a broad direction. Then, episode of tachygastria began. Frequency increased to 12.5 cycles/min, and direction of propagation reversed. This suggests that an ectopic, dominant pacemaker developed in distal antrum. At end of episode, pause occurred in electrical activity, which was probably analogous to pacemaker recovery time.

From Code and Marlett 31
Figure 7. Figure 7.

Mechanical (top traces) and intracellular electrical (bottom traces) activities recorded from a muscle of a patient with tachygastria. A: spontaneous activity in Krebs solution. B: activity after indomethacin treatment. Record in B is very similar to types of recordings obtained from normal human or canine muscles. C: abnormal activity recorded from muscle before indomethacin (A) was restored by exogenous prostaglandin E2 (PGE2). Data are consistent with the hypothesis that abnormally high slow‐wave frequencies (tachygastria) can be caused by overabundance of endogenous PGE2.

From Sanders 101
Figure 8. Figure 8.

Mechanical threshold. Two voltage‐tension curves were generated from canine fundus and antrum muscles by depolarizing the preparations with elevated external K+. Both muscles displayed a threshold voltage that had to be surpassed to initiate contraction. Above the mechanical threshold, small depolarizations of membrane potential resulted in large increases in force. Fundus muscles developed tension at more polarized levels than did antral muscles. Not shown in figure is voltage‐tension relationship for corpus muscles that demonstrated a mechanical threshold intermediate to that of fundus and antrum muscles.

From Morgan et al. 82
Figure 9. Figure 9.

Spontaneous mechanical and electrical activity of canine muscularis mucosa. In both A and B, top traces are records of mechanical activity and bottom traces are records of intracellular electrical activity. Faster sweep speed in B shows diastolic depolarization leading up to each spike and the fact that upstroke depolarizations precede mechanical responses.

From Morgan et al. 81
Figure 10. Figure 10.

Slow wave recorded from circular muscle of Bufo marinus. These “slow spikes,” as they were referred to by Mangel and Prosser 78, have many characteristics similar to their mammalian counterparts. There is a relatively rapid upstroke depolarization, followed by a partial repolarization and then a shoulder or plateau phase that persists for several seconds before repolarization to resting potential. Muscle was maintained by constant perfusion of amphibian Ringer's solution (in mM: K+, 2.95; Na+, 124.6; Ca2+, 1.5; Mg2+, 1.0; Cl−, 98; , 30; , 2.3; glucose, 11). The recording was made at 22°C. pH was maintained at 7.3–7.4 by bubbling Ringer's solution with 95% CO2‐5% O2.

Courtesy of Paul Shonnerd
Figure 11. Figure 11.

Relationship between slow‐wave amplitude and contractile force. Top: slow‐wave activity recorded by sucrose‐gap technique. Bottom: mechanical responses. Trace c, slow wave when muscle was exposed to Krebs‐Ringer buffer, which did not produce a contraction. Traces 1 and 2, slow waves in response to 0.5 × 10−8 M acetylcholine. These concentrations enhanced slow‐wave amplitude but failed to elicit mechanical responses. At concentrations of acetylcholine >1.5 × 10−8 M (traces 3–7), enhanced slow‐wave amplitude was associated with concentration‐dependent mechanical responses, mgf, Milligrams force.

From Szurszewski 121
Figure 12. Figure 12.

Spontaneous mechanical (A) and electrical (B) events recorded simultaneously from canine antral circular muscle. Slow‐wave event apparently crossed the mechanical threshold twice during its time course (hypothetical mechanical threshold shown by dotted line), producing a biphasic contractile response.
Figure 13. Figure 13.

Numerical simulation of spread of potential in 2 dimensions. Passive spread of current from point source in a 2‐dimensional syncytium was modeled by numerical simulation. Cells in syncytium modeled as short cables 129 were interconnected by junctional resistances. Each intersection in figure represents 1 cell. The 2 dimensions in the plane of figure represent dimensions of a tissue. Third dimension (out of the plane of figure) represents simulated voltage response after current injection of 10 μA for 1 ms.
Figure 14. Figure 14.

Technique to determine site of slow‐wave origin in 2‐dimensional syncytium. If site and time of slow‐wave origin are unknown, only differences in arrival times (i.e., latencies) of a slow wave at 2 or more recording locations can be measured. As shown in A, a single latency between two electrodes (filled circles) could be produced by events originating at any point along a curve similar in shape to a hyperbola. To pinpoint the site of slow‐wave origin in 2 dimensions, a third electrode is necessary (B). By combining latencies between two pairs of electrodes, site of slow‐wave origin can be determined from intersection of latency curves. For example, if a slow wave arrived simultaneously at the 2 leftmost electrodes in B (time 0) and arrived with a latency of 0.5 time units at the lower electrodes, then the site of origin would be the point denoted by triangle. In both panels, 1 time unit is the time (in arbitrary units) for an event to propagate distance between each pair of adjacent electrodes. Open circles, axes labels.

From Publicover and Sanders 98
Figure 15. Figure 15.

Effects of frequency on conduction velocity. A: conduction velocity (CV) in the x‐axis (parallel to circular fibers) of canine antral muscle plotted as a function of interval between evoked slow waves. B: CV in the y‐axis (perpendicular to circular fibers) as a function of intervals between the same series of slow waves. Each point in both graphs represents an individual measurement of CV during a series of evoked events where intervals between stimuli were randomly selected between 12 s (maximum pacing frequency) and 55 s (intrinsic frequency). Data were fit with exponential function by using nonlinear regression. Strong dependence between slow‐wave frequency and CV was observed in the y‐axis over the physiological frequency range.

From Publicover and Sanders 99
Figure 16. Figure 16.

Patterns of slow‐wave activity. Slow waves were evoked via direct muscle stimulation and recorded with an intracellular microelectrode. In this cell, 3 patterns of slow‐wave activity were evoked by varying stimulus frequency. At 3.5 cycles/min (CPM), each slow wave was identical, with waveforms similar to spontaneous events (A). At 4.2 CPM, plateau phase of alternating slow waves was reduced in amplitude and duration (B). At 5.4 CPM, plateaus of alternating events were completely abolished and upstrokes were significantly reduced (C). At frequencies above 5.4 CPM, pattern of slow‐wave activity became irregular (not shown).

From Publicover and Sanders 100
Figure 17. Figure 17.

Relaxation‐oscillator simulations. These series of simulations were performed on a digital computer by using Equations 1 and 2 (see text), along with the predictor‐corrector method of numerical integration. Parameters (see equations) were selected in an attempt to approximate as much as possible the waveform, duration, and frequency of intracellularly recorded slow waves. In A, frequency of slow waves was selected to be 1–2/min, as found in isolated sheets of antral tissue. Key parameters used during the simulation were a1 = 6 and k = 6. No coupling was induced between oscillators. In B, frequency was increased to 5–6/min as found in vivo. This was achieved by using a1 = 1.0 and b4 = 0.02. C shows same oscillator as illustrated in B except it has been coupled to a string of oscillators with lower intrinsic frequency. Second oscillator in chain was simulated by a1 = 0.9 and in third oscillator by a1 = 0.8. All bidirectional coupling coefficients were set to 0.2. Comparison of B and C demonstrates that there is frequency pulling between coupled oscillators. D shows second oscillator in the chain of coupled oscillators. Events in D are phase locked to those in C, showing phase difference representing spatial spread of excitation.


Figure 1.

Derivation of the shape of gastric slow waves from differential potentials. A: with calomel electrodes applied to surfaces of canine stomachs, differential records of peristaltic waves were recorded. Three waves were identified that were designated as R, S, and T waves. They were similar in shape to corresponding records of cardiac activity except the duration of the complex was 5–8 s. B: approximate shape of gastric slow wave was deduced by integrating differential waveforms. Essential characteristics of the slow wave (upstroke and plateau phases) as recorded by intracellular techniques were apparent from integrated extracellular potentials.

Adapted from Bozler 19


Figure 2.

Recording of gastric slow wave with intracellular electrode from antral circular muscle cell. Various parameters that have been quantitated are upstroke amplitude, time constant of the foot of the upstroke (τf), maximum upstroke velocity (dV/dt), plateau amplitude, slow‐wave duration, area under waveform, and resting membrane potential.

From Bauer et al. 10


Figure 3.

Intracellular potentials recorded from different regions of canine stomach. Variations in resting membrane potential, slow‐wave shape and frequency, and presence of action potentials were observed in isolated tissues from different anatomical regions of the stomach.

From Szurszewski et al. 123


Figure 4.

Slow waves through thickness of circular muscle. Simultaneous intracellular recordings were made from myenteric (electrode A) and submucosal (electrode B) circular muscle cells. Myenteric cells (trace A) were more polarized and generated more robust slow waves than did submucosal cells (trace B). Slow waves always occurred first in myenteric cells, suggesting they originated in the serosal half of muscularis and then propagated through the thickness of circular cells to submucosal cells.

Adapted from Bauer et al. 10


Figure 5.

Dependence of gastric slow wave on external Ca2+. A: slow wave (upper trace) and time derivative (lower trace) recorded intracellularly from canine antral circular cell in Krebs‐Ringer buffer (2.5 mM Ca2+). B: while maintaining impalement, solution bathing muscle was changed to one containing 0.93 mM Ca2+. Reduced [Ca2+] decreased the amplitudes of upstroke and plateau phases and decreased the upstroke velocity.

Courtesy of David Blonfield


Figure 6.

Beginning, middle, and end portions of 17‐min episode of tachygastria in a chronically instrumented dog. Top trace in each panel was recorded by an extracellular electrode 4 cm proximal to pylorus. Bottom trace in each panel was recorded by an electrode 2 cm proximal to pylorus. At beginning of top panel, slow waves were recorded at a typical frequency for canine stomachs. These events were propagating in a broad direction. Then, episode of tachygastria began. Frequency increased to 12.5 cycles/min, and direction of propagation reversed. This suggests that an ectopic, dominant pacemaker developed in distal antrum. At end of episode, pause occurred in electrical activity, which was probably analogous to pacemaker recovery time.

From Code and Marlett 31


Figure 7.

Mechanical (top traces) and intracellular electrical (bottom traces) activities recorded from a muscle of a patient with tachygastria. A: spontaneous activity in Krebs solution. B: activity after indomethacin treatment. Record in B is very similar to types of recordings obtained from normal human or canine muscles. C: abnormal activity recorded from muscle before indomethacin (A) was restored by exogenous prostaglandin E2 (PGE2). Data are consistent with the hypothesis that abnormally high slow‐wave frequencies (tachygastria) can be caused by overabundance of endogenous PGE2.

From Sanders 101


Figure 8.

Mechanical threshold. Two voltage‐tension curves were generated from canine fundus and antrum muscles by depolarizing the preparations with elevated external K+. Both muscles displayed a threshold voltage that had to be surpassed to initiate contraction. Above the mechanical threshold, small depolarizations of membrane potential resulted in large increases in force. Fundus muscles developed tension at more polarized levels than did antral muscles. Not shown in figure is voltage‐tension relationship for corpus muscles that demonstrated a mechanical threshold intermediate to that of fundus and antrum muscles.

From Morgan et al. 82


Figure 9.

Spontaneous mechanical and electrical activity of canine muscularis mucosa. In both A and B, top traces are records of mechanical activity and bottom traces are records of intracellular electrical activity. Faster sweep speed in B shows diastolic depolarization leading up to each spike and the fact that upstroke depolarizations precede mechanical responses.

From Morgan et al. 81


Figure 10.

Slow wave recorded from circular muscle of Bufo marinus. These “slow spikes,” as they were referred to by Mangel and Prosser 78, have many characteristics similar to their mammalian counterparts. There is a relatively rapid upstroke depolarization, followed by a partial repolarization and then a shoulder or plateau phase that persists for several seconds before repolarization to resting potential. Muscle was maintained by constant perfusion of amphibian Ringer's solution (in mM: K+, 2.95; Na+, 124.6; Ca2+, 1.5; Mg2+, 1.0; Cl−, 98; , 30; , 2.3; glucose, 11). The recording was made at 22°C. pH was maintained at 7.3–7.4 by bubbling Ringer's solution with 95% CO2‐5% O2.

Courtesy of Paul Shonnerd


Figure 11.

Relationship between slow‐wave amplitude and contractile force. Top: slow‐wave activity recorded by sucrose‐gap technique. Bottom: mechanical responses. Trace c, slow wave when muscle was exposed to Krebs‐Ringer buffer, which did not produce a contraction. Traces 1 and 2, slow waves in response to 0.5 × 10−8 M acetylcholine. These concentrations enhanced slow‐wave amplitude but failed to elicit mechanical responses. At concentrations of acetylcholine >1.5 × 10−8 M (traces 3–7), enhanced slow‐wave amplitude was associated with concentration‐dependent mechanical responses, mgf, Milligrams force.

From Szurszewski 121


Figure 12.

Spontaneous mechanical (A) and electrical (B) events recorded simultaneously from canine antral circular muscle. Slow‐wave event apparently crossed the mechanical threshold twice during its time course (hypothetical mechanical threshold shown by dotted line), producing a biphasic contractile response.



Figure 13.

Numerical simulation of spread of potential in 2 dimensions. Passive spread of current from point source in a 2‐dimensional syncytium was modeled by numerical simulation. Cells in syncytium modeled as short cables 129 were interconnected by junctional resistances. Each intersection in figure represents 1 cell. The 2 dimensions in the plane of figure represent dimensions of a tissue. Third dimension (out of the plane of figure) represents simulated voltage response after current injection of 10 μA for 1 ms.



Figure 14.

Technique to determine site of slow‐wave origin in 2‐dimensional syncytium. If site and time of slow‐wave origin are unknown, only differences in arrival times (i.e., latencies) of a slow wave at 2 or more recording locations can be measured. As shown in A, a single latency between two electrodes (filled circles) could be produced by events originating at any point along a curve similar in shape to a hyperbola. To pinpoint the site of slow‐wave origin in 2 dimensions, a third electrode is necessary (B). By combining latencies between two pairs of electrodes, site of slow‐wave origin can be determined from intersection of latency curves. For example, if a slow wave arrived simultaneously at the 2 leftmost electrodes in B (time 0) and arrived with a latency of 0.5 time units at the lower electrodes, then the site of origin would be the point denoted by triangle. In both panels, 1 time unit is the time (in arbitrary units) for an event to propagate distance between each pair of adjacent electrodes. Open circles, axes labels.

From Publicover and Sanders 98


Figure 15.

Effects of frequency on conduction velocity. A: conduction velocity (CV) in the x‐axis (parallel to circular fibers) of canine antral muscle plotted as a function of interval between evoked slow waves. B: CV in the y‐axis (perpendicular to circular fibers) as a function of intervals between the same series of slow waves. Each point in both graphs represents an individual measurement of CV during a series of evoked events where intervals between stimuli were randomly selected between 12 s (maximum pacing frequency) and 55 s (intrinsic frequency). Data were fit with exponential function by using nonlinear regression. Strong dependence between slow‐wave frequency and CV was observed in the y‐axis over the physiological frequency range.

From Publicover and Sanders 99


Figure 16.

Patterns of slow‐wave activity. Slow waves were evoked via direct muscle stimulation and recorded with an intracellular microelectrode. In this cell, 3 patterns of slow‐wave activity were evoked by varying stimulus frequency. At 3.5 cycles/min (CPM), each slow wave was identical, with waveforms similar to spontaneous events (A). At 4.2 CPM, plateau phase of alternating slow waves was reduced in amplitude and duration (B). At 5.4 CPM, plateaus of alternating events were completely abolished and upstrokes were significantly reduced (C). At frequencies above 5.4 CPM, pattern of slow‐wave activity became irregular (not shown).

From Publicover and Sanders 100


Figure 17.

Relaxation‐oscillator simulations. These series of simulations were performed on a digital computer by using Equations 1 and 2 (see text), along with the predictor‐corrector method of numerical integration. Parameters (see equations) were selected in an attempt to approximate as much as possible the waveform, duration, and frequency of intracellularly recorded slow waves. In A, frequency of slow waves was selected to be 1–2/min, as found in isolated sheets of antral tissue. Key parameters used during the simulation were a1 = 6 and k = 6. No coupling was induced between oscillators. In B, frequency was increased to 5–6/min as found in vivo. This was achieved by using a1 = 1.0 and b4 = 0.02. C shows same oscillator as illustrated in B except it has been coupled to a string of oscillators with lower intrinsic frequency. Second oscillator in chain was simulated by a1 = 0.9 and in third oscillator by a1 = 0.8. All bidirectional coupling coefficients were set to 0.2. Comparison of B and C demonstrates that there is frequency pulling between coupled oscillators. D shows second oscillator in the chain of coupled oscillators. Events in D are phase locked to those in C, showing phase difference representing spatial spread of excitation.

References
 1. Abe, Y., and T. Tomita. Cable properties of smooth muscle. J. Physiol. Lond. 196: 87–100, 1968.
 2. Adrian, R. H. Potassium chloride movement and the membrane potential of frog muscle. J. Physiol. Lond. 151: 154–185, 1960.
 3. Aickin, C. C., and A. F. Brading. Advances in the understanding of transmembrane ionic gradients and permeabilities in smooth muscle obtained by using ion‐selective micro‐electrodes. Experientia Basel 41: 879–887, 1985.
 4. Akwari, O. E., K. A. Kelly, J. H. Steinbach, and C. F. Code. Electric pacing of intact and transected canine small intestine and its computer model. Am. J. Physiol. 229: 1188–1197, 1975.
 5. Alvarez, W. C., and L. J. Mahoney. Action current in stomach and intestine. Am. J. Physiol. 58: 476–493, 1922.
 6. Anderson, N. C. Limitations and possibilities in smooth muscle voltage‐clamp. In: Excitation‐Contraction Coupling in Smooth Muscle, edited by R. Casteels. Amsterdam: Elsevier/North Holland, 1977, p. 81–89.
 7. Armstrong, C. M., and L. Binstock. Anomalous rectification in the squid giant axon injected with tetraethylammonium chloride. J. Gen. Physiol. 48: 859–872, 1965.
 8. Bass, P., C. F. Code, and E. H. Lambert. Electric activity of gastroduodenal junction. Am. J. Physiol. 201: 587–592, 1961.
 9. Bauer, A. J., N. G. Publicover, and K. M. Sanders. Origin and spread of slow waves in canine gastric antral circular muscle. Am. J. Physiol. 249 (Gastrointest. Liver Physiol. 12): G800–G806, 1985.
 10. Bauer, A. J., J. B. Reed, and K. M. Sanders. Slow wave heterogeneity within the circular muscle of the canine gastric antrum. J. Physiol. Lond. 366: 221–232, 1985.
 11. Bauer, A. J., and K. M. Sanders. Gradient in excitation‐contraction coupling in canine gastric antral circular muscle. J. Physiol. Lond. 369: 283–294, 1985.
 12. Bauer, A. J., and K. M. Sanders. Passive and active membrane properties of canine gastric antral circular muscles. Am. J. Physiol. 251 (Cell Physiol. 20): C268–C273, 1986.
 13. Beaumont, W. Experiments and Observations on Gastric Juice, and the Physiology of Digestion. (Facsimile of the original edition of 1833 together with a biographical essay, “A Pioneer American Physiologist” by Sir William Osier.) New York: Dover, 1959.
 14. Bennett, A., J. J. Misiewicz, and S. L. Waller. Analysis of the motor effects of gastrin and pentagastrin on the human alimentary tract in vitro. Gut 8: 470–474, 1967.
 15. Bolton, T. B. On the nature of the oscillations of the membrane potential (slow waves) produced by acetylcholine or carbachol in intestinal smooth muscle. J. Physiol. Lond. 216: 403–418, 1971.
 16. Bolton, T. B. Effects of electrogenic sodium pumping on the membrane potential of longitudinal smooth muscle from terminal ileum of guinea‐pig. J. Physiol. Lond. 228: 693–712, 1973.
 17. Bolton, T. B., T. Tomita, and G. Vassort. Voltage clamp and the measurement of ionic conductances in smooth muscle. In: Smooth Muscle: An Assessment of Current Knowledge, edited by E. Bülbring, A. F. Brading, A. W. Jones, and T. Tomita. Austin: Univ. of Texas Press, 1981, p. 47–63.
 18. Bortoff, A. Myogenic control of intestinal motility. Physiol. Rev. 56: 418–434, 1976.
 19. Bozler, E. The action potentials of the stomach. Am. J. Physiol. 144: 693–700, 1945.
 20. Brading, A. F. Maintenance of ionic composition, Br. Med. Bull. 35: 227–234, 1979.
 21. Brading, A. F. Ionic distribution and mechanisms of transmembrane ion movements in smooth muscle. In: Smooth Muscle: An Assessment of Current Knowledge, edited by E. Bülbring, A. F. Brading, A. W. Jones, and T. Tomita. Austin: Univ. of Texas Press, 1981, p. 65–92.
 22. Brown, D. A., and P. R. Adams. Muscarinic suppression of a novel voltage‐sensitive K+ current in a vertebrate neurone. Nature Lond. 283: 673–676, 1980.
 23. Bury, V., and K. Boev. Studies on the transmembrane ion currents in the smooth‐muscle cells of the gastric fundus. Experientia Basel 36: 216–218, 1980.
 24. Cameron, A. J., S. F. Phillips, and W. H. J. Summerskill. Comparison of effects of gastrin, cholecystokinin‐pancreozymin, secretin, and glucagon on human stomach muscle in vitro. Gastroenterology 59: 539–545, 1970.
 25. Cannon, W. B. The movements of the stomach studied by means of the röntgen rays. Am. J. Physiol. 1: 13–14, 1898.
 26. Cannon, W. B. The movements of the stomach studied by means of the röntgen rays. Am. J. Physiol. 1: 359–382, 1898.
 27. Carlson, H. C., C. F. Code, and R. A. Nelson. Motor action of the canine gastroduodenal junction: a cineradiographic, pressure and electric study. Am. J. Dig. Dis. 11: 155–172, 1966.
 28. Casteels, R. Membrane potential in smooth muscle cells. In: Smooth Muscle: An Assessment of Current Knowledge, edited by E. Bülbring, A. F. Brading, A. W. Jones, and T. Tomita. Austin: Univ. of Texas Press, 1981, p. 105–126.
 29. Casteels, R., and H. Kuriyama. Membrane potential and ion content in the smooth muscle of the guinea‐pig's taenia coli at different external potassium concentrations. J. Physiol. Lond. 184: 120–130, 1966.
 30. Clay, J. R., M. R. Guevara, and A. Shrier. Phase resetting of the rhythmic activity of embryonic heart cell aggregates. Biophys. J. 45: 699–714, 1984.
 31. Code, C. F., and J. A. Marlett. Canine tachygastria. Mayo Clin. Proc. 49: 325–332, 1974.
 32. Cole, K. S., and H. J. Curtis. Electrical impedance of squid giant axon during activity. J. Gen. Physiol. 22: 649–670, 1938.
 33. Connor, J. A. On exploring the basis for slow potential oscillations in the mammalian stomach and intestine. J. Exp. Biol. 81: 153–173, 1979.
 34. Connor, J. A., D. L. Kreulen, C. L. Prosser, and R. J. Weigel. Interaction between longitudinal and circular muscle in intestine of cat. J. Physiol. Lond. 273: 665–689, 1977.
 35. Connor, J. A., C. L. Prosser, and W. A. Weems. A study of pacemaker activity in intestinal smooth muscle. J. Physiol. Lond. 240: 671–701, 1974.
 36. Cooke, A. R., and J. Christensen. Motor functions of the stomach. In: Gastrointestinal Disease: Pathophysiology, Diagnosis, Management (2nd ed.), edited by M. H. Sleisenger and J. S. Fordtran. Philadelphia, PA: Saunders, 1978, p. 629–640.
 37. Daniel, E. E. The electrical and contractile activity of the pyloric region in dogs and the effects of drugs. Gastroenterology 49: 403–418, 1965.
 38. Daniel, E. E., and K. M. Chapman. Electrical activity of the gastrointestinal tract as an indication of mechanical activity. Am. J. Dig. Dis. 8: 54–102, 1963.
 39. Daniel, E. E., V. P. Daniel, G. Duchon, R. E. Garfield, M. Nichols, S. K. Malhotra, and M. Oki. Is the nexus necessary for cell‐to‐cell coupling of smooth muscle? J. Membr. Biol. 28: 207–239, 1976.
 40. Daniel, E. E., and J. Irwin. Electrical activity of gastric musculature. In: Handbook of Physiology. Alimentary Canal. Motility, edited by C. F. Code. Washington, DC: Am. Physiol. Soc., 1968, sect. IV, vol. 6, chapt. 96, p. 1969–1984.
 41. Daniel, E. E., Y. Sakai, J. E. T. Fox, and V. Posey‐Daniel. Structural basis for function of circular muscle of canine corpus. Can. J. Physiol. Pharmacol. 62: 1304–1314, 1984.
 42. Diamant, N. E., P. K. Rose, and E. J. Davison. Computer simulation of intestinal slow‐wave frequency gradient. Am. J. Physiol. 219: 1684–1690, 1970.
 43. Droogmans, G., and R. Casteels. Membrane potential and ion transport in smooth muscle cells. In: Physiology of Smooth Muscle, edited by E. Bülbring and M. F. Shuba. New York: Raven, 1976, p. 11–18.
 44. El‐Sharkawy, T. Y., K. G. Morgan, and J. H. Szurszewski. Intracellular electrical activity of canine and human gastric smooth muscle. J. Physiol. Lond. 279: 291–307, 1978.
 45. El‐Sharkawy, T. Y., and J. H. Szurszewski. Modulation of canine antral circular smooth muscle by acetylcholine, noradrenaline, and pentagastrin. J. Physiol. Lond. 279: 309–320, 1978.
 46. Fitzhugh, R. Impulses and physiological states in theoretical models of nerve membrane. Biophys. J. 1: 445–466, 1961.
 47. Fujii, K., R. Inoue, K. Yamanaka, and T. Yoshitomi. Effects of calcium antagonists on smooth muscle membranes of the canine stomach. Gen. Pharmacol. 16: 217–221, 1985.
 48. Goldman, D. E. Potential, impedance and rectification in membranes. J. Gen. Physiol. 27: 37–60, 1943.
 49. Gregory, R. A., and H. J. Tracy. The constitution and properties of two gastrins extracted from hog antral mucosa. I. The isolation of two gastrins from hog antral mucosa. II: The properties of two gastrins isolated from hog antral mucosa. Gut 5: 103–114, 1964.
 50. Gullikson, G. W., H. Okuda, M. Shimizu, and P. Bass. Electrical arrhythmias in gastric antrum of the dog. Am. J. Physiol. 239 (Gastrointest. Liver Physiol. 2): G59–G68, 1980.
 51. Hara, Y., and Y. Ito. The electrical activity recorded from smooth muscle of the circular layer of the human stomach. Pfluegers Arch. 382: 145–153, 1979.
 52. Harper, A. A., C. Kidd, and T. Scratcherd. Vago‐vagal reflex effects on gastric and pancreatic secretion and gastrointestinal motility. J. Physiol. Lond. 148: 417–436, 1959.
 53. Hirsch. Centralbl. Klin. Med. xiii: 994, 1892.
 54. Hightower, N. C., Jr., and C. F. Code. The quantitative analysis of antral gastric motility records in normal human beings, with a study of the effects of neostigmine. Mayo Clin. Proc. 25: 697–704, 1950.
 55. Hodgkin, A. L., and P. Horowicz. The influence of potassium and chloride ions on the membrane potential of single muscle fibers. J. Physiol. Lond. 148: 127–160, 1959.
 56. Hodgkin, A. L., and A. F. Huxley. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. Lond. 117: 500–544, 1952.
 57. Hodgkin, A. L., and B. Katz. The effect of sodium ions on the electrical activity of the giant axon of the squid. J. Physiol. Lond. 108: 37–77, 1949.
 58. Hodgkin, A. L., and W. A. H. Rushton. The electrical constants of a crustacean nerve fibre. Proc. R. Soc. Lond. Ser. B 133: 444–479, 1946.
 59. Ichikawa, S., and E. Bozler. Monophasic and diphasic action potentials of the stomach. Am. J. Physiol. 182: 92–96, 1955.
 60. Isenberg, J. I., and M. I. Grossman. Effect of gastrin and SC 15396 on gastric motility in dogs. Gastroenterology 56: 450–455, 1969.
 61. Ito, Y., H. Kuriyama, and Y. Sakamoto. Effects of tetraethylammonium chloride on the membrane activity of guinea‐pig smooth muscle. J. Physiol. Lond. 211: 445–460, 1970.
 62. Jack, J. J. B., D. Noble, and R. W. Tsien. Electric Current Flow in Excitable Cells. London: Oxford Univ. Press, 1975, p. 67–130.
 63. Jacoby, H. I., and C. H. Marshall. Gastric motor‐stimulating activity of gastrin tetrapeptide in dogs. Gastroenterology 56: 80–87, 1969.
 64. Jansson, G. Extrinsic nervous control of gastric motility: an experimental study in the cat. Acta. Physiol. Scand. Suppl. 326: 1–42, 1969.
 65. Johnson, E. A., and M. Lieberman. Heart: excitation and contraction. Annu. Rev. Physiol. 33: 479–532, 1971.
 66. Jones, A. W., and T. Tomita. The longitudinal tissue resistance of the guinea‐pig taenia cell. J. Physiol. Lond. 191: 109–110, 1967.
 67. Kelly, K. A. Effect of gastrin on gastric myo‐electric activity. Am. J. Dig. Dis. 15: 399–405, 1970.
 68. Kelly, K. A. Differential responses of the canine gastric corpus and antrum to electrical stimulation. Am. J. Physiol. 226: 230–234, 1974.
 69. Kelly, K. A. Gastric emptying of liquids and solids: roles of proximal and distal stomach. Am. J. Physiol. 239 (Gastrointest. Liver Physiol. 2): G71–G76, 1980.
 70. Kelly, K. A., and C. F. Code. Canine gastric pacemaker. Am. J. Physiol. 220: 112–118, 1971.
 71. Kelly, K. A., C. F. Code, and L. R. Elveback. Patterns of canine gastric electric activity. Am. J. Physiol. 217: 461–470, 1969.
 72. Kelvin, Lord (W. Thompson). On the theory of the electric telegraph. Proc. R. Soc. 7: 382–399, 1855.
 73. Kerrick, W. G., P. E. Hoar, P. S. Cassidy, L. Bolles, and D. A. Malencik. Calcium‐regulatory mechanisms. Functional classification using skinned fibers. J. Gen. Physiol. 77: 177–190, 1981.
 74. Kim, C. H., F. Azpiroz, and J.‐R. Malagelada. Characteristics of spontaneous and drug‐induced gastric dysrhythmia in a chronic canine model. Gastroenterology 90: 421–427, 1987.
 75. Kuriyama, H., T. Osa, and H. Tasaki. Electrophysiological studies of the antrum muscle fibers of the guinea pig stomach. J. Gen. Physiol. 55: 48–62, 1970.
 76. Kwong, N. K., B. H. Brown, G. E. Whittaker, and H. L. Duthie. Effects of gastrin I, secretin and cholecystokinin‐pancreozymin on the electrical activity, motor activity, and acid output of the stomach in man. Scand. J. Gastroenterol. 7: 161–170, 1972.
 77. Levis, R. A., R. T. Mathias, and R. S. Eisenberg. Electrical properties of sheep Purkinje strands. Biophys. J. 44: 225–248, 1983.
 78. Mangel, A., and C. L. Prosser. Rhythmic electrical activity in stomach and intestine of toad. J. Exp. Biol. 86: 237–248, 1980.
 79. McCoy, E. J., and P. Bass. Chronic electrical activity of gastroduodenal area: effects of food and certain catecholamines. Am. J. Physiol. 205: 439–445, 1963.
 80. Miolan, J. P., and C. Roman. Modification de l'electromyogramme gastrique du chien par stimulation des nerfs extrinseques. J. Physiol. Paris 63: 561–576, 1971.
 81. Morgan, K. G., F. Angel, P. F. Schmalz, and J. H. Szurszewski. Intracellular electrical activity of muscularis mucosae of the dog stomach. Am. J. Physiol. 249 (Gastrointest. Liver Physiol. 12): G256–G263, 1985.
 82. Morgan, K. G., T. C. Muir, and J. H. Szurszewski. The electrical basis for contraction and relaxation in canine fundal smooth muscle. J. Physiol. Lond. 311: 475–488, 1981.
 83. Morgan, K. G., P. F. Schmalz, V. L. W. Go, and J. H. Szurszewski. Effects of pentagastrin, G17, and G34 on the electrical and mechanical activities of canine antral smooth muscle. Gastroenterology 75: 405–412, 1978.
 84. Morgan, K. G., P. F. Schmalz, V. L. W. Go, and J. H. Szurszewski. Electrical and mechnical effects of molecular variants of CCK on antral smooth muscle. Am. J. Physiol. 235 (Endocrinol. Metab. Gastrointest. Physiol. 3): E324–E329, 1978.
 85. Morgan, K. G., P. F. Schmalz, and J. H. Szurszewski. The inhibitory effects of vasoactive intestinal polypeptide on the mechanical and electrical activity of canine antral smooth muscle. J. Physiol. Lond. 282: 437–450, 1978.
 86. Morgan, K. G., and J. H. Szurszewski. Mechanisms of phasic and tonic actions of pentagastrin on canine gastric smooth muscle. J. Physiol. Lond. 301: 229–242, 1980.
 87. Nastuk, W. L., and A. L. Hodgkin. The electrical activity of single muscle fibers. J. Cell. Comp. Physiol. 35: 39–73, 1950.
 88. Nelsen, T. S., and J. C. Becker. Simulation of the electrical and mechanical gradient of the small intestine. Am. J. Physiol. 217: 749–757, 1968.
 89. Nelsen, T. S., E. H. Eigenbrodt, L. A. Keoshian, C. Bunker, and L. Johnson. Alterations in muscular and electrical activity of the stomach following vagotomy. Arch. Surg. 94: 821–835, 1967.
 90. Noble, D., and R. W. Tsien. The kinetics and rectifier properties of the slow potassium current in cardiac Purkinje fibres. J. Physiol. Lond. 195: 185–214, 1968.
 91. Ohba, M., Y. Sakamoto, and T. Tomita. The slow wave in the circular muscle of the guinea‐pig stomach. J. Physiol. Lond. 253: 505–516, 1975.
 92. Ohba, M., Y. Sakamoto, and T. Tomita. Effects of sodium, potassium and calcium ions on the slow wave in the circular muscle of the guinea‐pig stomach. J. Physiol. Lond. 267: 167–180, 1977.
 93. Oki, M., and E. E. Daniel. Ultrastructural basis for electrical coupling in the dog stomach. In: Proc. 4th Int. Symp. Gastrointest. Motil., edited by E. E. Daniel. Vancouver, Canada: Mitchell, 1974, p. 85–95.
 94. Ormsbee, H. S., III, G. R. Mason, and P. Bass. Effects of pyloroplasty on the electrical activity of the canine gastroduodenal junction. In: Proc. 5th Int. Symp. Gastrointest. Motil., edited by G. Vantrappen. Herentals, Belgium: Typoff, 1975, p. 293–299.
 95. Osa, T., and H. Kuriyama. Membrane properties and decree‐mental conduction of excitation in the fundus of the guinea‐pig stomach. Jpn. J. Physiol. 20: 626–639, 1970.
 96. Papasova, M. P., T. Nagai, and C. L. Prosser. Two‐component slow waves in smooth muscle of cat stomach. Am. J. Physiol. 214: 695–702, 1968.
 97. Prosser, C. L., W. A. Weems, and J. A. Connor. Types of slow rhythmic activity in gastrointestinal muscles. In: Physiology of Smooth Muscle, edited by E. Bülbring and M. F. Shuba. New York: Raven, 1976, p. 99–109.
 98. Publicover, N. G., and K. M. Sanders. A technique to locate the pacemaker in smooth muscle. J. Appl. Physiol. 57: 1586–1590, 1984.
 99. Publicover, N. G., and K. M. Sanders. Myogenic regulation of propagation in gastric smooth muscle. Am. J. Physiol. 248 (Gastrointest. Liver Physiol. 11): G512–G520, 1985.
 100. Publicover, N. G., and K. M. Sanders. Effects of frequency on the wave form of propagated slow waves in canine gastric antral muscle. J. Physiol. Lond. 371: 179–189, 1986.
 101. Sanders, K. M. Role of prostaglandins in regulating gastric motility. Am. J. Physiol. 247 (Gastrointest. Liver Physiol. 10): G117–G126, 1984.
 102. Sanders, K. M., A. J. Bauer, and N. G. Publicover. Regulation of gastric antral slow wave frequency by prostaglandins. Proc. 9th Int. Symp. Gastrointest. Motil., edited by C. Roman. Lancaster, UK: MTP, 1984, p. 77–85.
 103. Sanders, K. M., R. Menguy, W. Chey, C. You, K. Lee, K. Morgan, D. Kreulen, P. Schmalz, T. Muir, and J. H. Szurszewski. One explanation for human antral tachygastria (Abstract). Gastroenterology 76: 1234, 1979.
 104. Sanders, K. M., P. Schmalz, and J. H. Szurszewski. Effect of neurotensin on mechanical and intracellular electrical activity of the canine stomach. Am. J. Physiol. 243 (Gastrointest. Liver Physiol. 6): G404–G409, 1982.
 105. Sanders, K. M., and J. H. Szurszewski. Does endogenous prostaglandin affect gastric antral motility? Am. J. Physiol. 241 (Gastrointest. Liver Physiol. 4): G191–G195, 1981.
 106. Sarna, S. K. Gastrointestinal electrical activity: terminology. Gastroenterology. 68: 1631–1635, 1975.
 107. Sarna, S. K. Models of smooth muscle electrical activity. In: Methods in Pharmacology: Smooth Muscle, edited by E. Daniel and D. M. Paton. New York: Plenum, 1975, vol. 3, p. 519–540.
 108. Sarna, S. K., K. L. Bowes, and E. E. Daniel. Post‐operative gastric electrical control activity (ECA) in man. In: Proc. 4th Int. Symp. Gastrointest. Motil, edited by E. E. Daniel. Vancouver, Canada: Mitchell, 1973, p. 73–83.
 109. Sarna, S. K., K. L. Bowes, and E. E. Daniel. Gastric pacemakers. Gastroenterology 70: 226–231, 1976.
 110. Sarna, S. K., and E. E. Daniel. Electrical stimulation of gastric electrical control activity. Am. J. Physiol. 225: 125–131, 1973.
 111. Sarna, S. K., and E. E. Daniel. Vagal control of gastric electrical control activity and motility. Gastroenterology 68: 301–308, 1975.
 112. Sarna, S. K., E. E. Daniel, and Y. J. Kingma. Simulation of slow‐wave electrical activity of small intestine. Am. J. Physiol. 22: 166–175, 1971.
 113. Sarna, S. K., E. E. Daniel, and Y. J. Kingma. Simulation of the electric‐control activity of the stomach by an array of relaxation oscillators. Am. J. Dig. Dis. 17: 299–310, 1972.
 114. Sato, A. Electrophysiological studies on the working mechanism of muscle walls of the stomach. Jpn. J. Physiol. 10: 359–373, 1960.
 115. Shuman, N., A. V. Somlyo, and A. P. Somlyo. Quantitative electron probe microanalysis of biological thin sections: methods and validity. Ultramicroscopy 1: 317–339, 1976.
 116. Singer, J. J., and J. V. Walsh, Jr. Large conductance Ca++‐activated K+ channels in smooth muscle membrane. Biophys. J. 45: 68–70, 1984.
 117. Specht, P. C., and A. Bortoff. Propagation and electrical entrainment of intestinal slow waves. Am. J. Dig. Dis. 17: 311–316, 1972.
 118. Stanfield, P. R. Tetraethylammonium ions and the potassium permeability of excitable cells. Rev. Physiol. Biochem. Pharmacol. 97: 1–67, 1983.
 119. Sturek, M., and K. Hermsmeyer. Calcium and sodium channels in spontaneously contracting vascular muscle cells. Science Wash. DC 233: 475–478, 1986.
 120. Sugawara, K., J. Isaza, J. Curt, and E. R. Woodward. The effect of pentagastrin on gastric motility following vagotomy. J. Surg. Res. 10: 73–80, 1970.
 121. Szurszewski, J. H. Mechanism of action of pentagastrin and acetylcholine on the longitudinal muscle of the canine antrum. J. Physiol. Lond. 252: 335–361, 1975.
 122. Szurszewski, J. H. A study of the canine gastric action potential in the presence of tetraethylammonium chloride. J. Physiol. Lond. 277: 91–102, 1978.
 123. Szurszewski, J. H. Electrical basis for gastrointestinal motility. In: Physiology of the Gastrointestinal Tract, edited by L. R. Johnson. New York: Raven, 1981, p. 1435–1465.
 124. Taylor, A. B., D. L. Kreulen, and C. L. Prosser. Electron microscopy of the connective tissues between longitudinal and circular muscle of small intestine of cat. Am. J. Anat. 150: 427–442, 1977.
 125. Telander, R. L., K. G. Morgan, D. L. Kreulen, P. F. Schmalz, K. A. Kelly, and J. H. Szurszewski. Human gastric atony with tachygastria and gastric retention. Gastroenterology 75: 497–501, 1978.
 126. Thuneberg, L. Interstitial cells of Cajal: intestinal pacemaker cells? Adv. Anat. Embryol. Cell Biol. 71: 1–130, 1982.
 127. Tiegs, O. W. The nerve net of plane muscle, and its relation to automatic rhythmic movements. Aust. J. Exp. Biol. Med. Sci. 2: 157–166, 1925.
 128. Tomita, T. Membrane capacity and resistance of mammalian smooth muscle. J. Theor. Biol. 12: 216–227, 1966.
 129. Tomita, T. Electrical properties of mammalian smooth muscle. In: Smooth Muscle, edited by E. Bülbring, A. F. Brading, A. W. Jones, and T. Tomita. Baltimore, MD: Williams & Wilkins, 1970, p. 197–243.
 130. Van der Pol, B. Biological rhythms considered as relaxation oscillations. Acta Med. Scand. Suppl. 108: 76–88, 1940.
 131. Van der Pol, B., and J. Van der Mark. The heartbeat considered as a relaxation oscillation, and an electrical model of the heart. Philos. Mag. Suppl. 6: 763–775, 1926.
 132. Van Harn, G. L. Frog stomach smooth muscle characteristics. Am. J. Physiol. 215: 1351–1358, 1968.
 133. Walsh, J. V., and J. J. Singer. Calcium action potentials in single freshly isolated smooth muscle cells. Am. J. Physiol. 239 (Cell Physiol. 8): C162–C174, 1980.
 134. Walsh, J. V., and J. J. Singer. Voltage clamp of single freshly dissociated smooth muscle cells: current‐voltage relationships for three currents. Pfluegers Arch. 390: 207–210, 1981.
 135. Weber, J., Jr., and S. Kohatsu. Pacemaker localization and electrical conduction patterns in the canine stomach. Gastroenterology 59: 717–726, 1970.
 136. Wilbur, B. G., and K. A. Kelly. Effect of proximal gastric, complete gastric, and truncal vagotomy on canine gastric electric activity, motility, and emptying. Ann. Surg. 178: 295–303, 1973.
 137. You, C. H., W. Y. Chey, K. Y. Lee, and R. Menguy. Tachygastria in adult subjects: a clinical entity (Abstract). Gastroenterology 76: 1272, 1979.
 138. Zipes, D. P. Specific arrhythmias: diagnosis and treatment. In: Heart Disease, edited by E. Braunwald. Philadelphia, PA: Saunders, 1984, p. 683–743.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Electrophysiology of the gastric musculature
 

How to Cite

Kenton M. Sanders, Nelson G. Publicover. Electrophysiology of the gastric musculature. Compr Physiol 2011, Supplement 16: Handbook of Physiology, The Gastrointestinal System, Motility and Circulation: 187-216. First published in print 1989. doi: 10.1002/cphy.cp060105