Comprehensive Physiology Wiley Online Library

Electrophysiology of the gastric musculature

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
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.
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.
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.
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
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
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.
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.
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 , 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
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 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
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
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
Figure 17. Figure 17.

Relaxation‐oscillator simulations. These series of simulations were performed on a digital computer by using Equations and (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


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.


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.


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.


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


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


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.


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.


Figure 10.

Slow wave recorded from circular muscle of Bufo marinus. These “slow spikes,” as they were referred to by Mangel and Prosser , 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


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 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


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


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


Figure 17.

Relaxation‐oscillator simulations. These series of simulations were performed on a digital computer by using Equations and (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.

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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