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Electrophysiology of colonic smooth muscle

Kenton M. Sander, Terence K. Smith

10.1002/cphy.cp060107

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 Reported Values for Resting Membrane Potential
1.2 Contribution of Electrogenic Pump to Resting Potential
2 Excitable Events in Colonic Muscles
2.1 Slow Electrical Oscillations
2.2 Slow Waves
2.3 Myenteric Potential Oscillations
2.4 Action Potentials
3 Excitation‐Contraction Coupling
4 Electropharmacology of Endogenous Substances
4.1 Cholinergic Agonists
4.2 Adrenergic Agonists
4.3 Peptides
4.4 Paracrine Substances
4.5 Effects of Spontaneous Neural Activity and Transmural and Extrinsic Nerve Stimulation
5 Propagation of Electrical Events
5.1 Electrical Coupling in Colonic Muscles
5.2 Propagation of Slow Waves
5.3 Propagation of Myenteric Potential Oscillations
5.4 Electrical Coupling Between Circular and Longitudinal Muscle Layers
5.5 Propagation of Fast Transients and Action Potentials
6 Summary
Figure 1. Figure 1.

Effects of ouabain and low K+ on resting membrane potentials (RMP) through thickness of circular muscle. Under control conditions intracellular recordings from circular muscle cells through thickness of circular layer demonstrate significant gradient in resting potential (filled squares, n = 9, see Fig. 8). When muscles exposed to either ouabain (10−6 M, open triangles, n = 6) or K+‐free Krebs solution (open circles, n = 3), cells depolarized. Submucosal cells (0% distance) depolarized much more than cells near myenteric border (100% distance), such that after either treatment cells throughout circular layer were polarized between −40 and −55 mV. These treatments, known to inhibit Na+‐K+‐ATPase, essentially abolished resting potential gradient through circular layer.
Figure 2. Figure 2.

Slow waves recorded through thickness of circular muscle. Submucosal circular muscle (SCM) cells displayed characteristic regular slow‐wave activity, consisting of upstroke depolarization and sustained plateau phase. As slow waves propagated away from submucosal surface, upstroke velocity decreased, and this event became indistinguishable within 40%‐60% of distance through circular layer. Resting potential decreased, and amplitude of slow wave decreased such that regular slow‐wave activity was usually not detectable in myenteric circular muscle (MCM) cells. Cable properties of circular syncytium appear to prevent slow waves from invading longitudinal muscle layer (LM).
Figure 3. Figure 3.

Characteristics of colonic slow waves. A: first time derivative (dV/dt) of record in B. This series of slow waves demonstrates variability in waveform that can be observed in many preparations. Long‐duration event lasted ∼30 s, whereas short events were ∼5 s in duration. Long‐duration event is used as example to illustrate features of colonic slow waves. Prepotential is slow depolarization that precedes slow waves in many preparations. Upstroke is relatively rapid phase that reaches peak depolarization of ∼40 mV. Then membrane potential repolarizes slightly into plateau phase that can vary from few seconds to ≥30 s. Some cells demonstrate oscillations in membrane potential at peak of plateau; usually these occur at beginning or end of this phase. Plateau potential then repolarizes back to resting or most polarized level. Sometimes slight afterhyperpolarization can be observed after these events. In A differentiation shows relative rate of rise of upstroke event. Upstroke velocities of next few events are decreased by slow waves of long duration. B: spontaneous oscillations in membrane potential (Vm), referred to as slow waves, recorded with intracellular microelectrodes from canine colonic circular muscle. RMP, resting membrane potential.
Figure 4. Figure 4.

Maximum level of depolarization achieved during slow waves recorded by intracellular techniques from several cells through thickness of canine circular muscle. Although amplitude of slow wave decays significantly as slow waves propagate through circular layer, maximum level of depolarization remains relatively constant because of decrease in resting potential (see Fig. 1). This phenomenon may enable membrane potentials of cells throughout thickness of circular layer to surpass mechanical threshold during each slow‐wave cycle and facilitate excitation‐contraction coupling and coordination.
Figure 5. Figure 5.

Effects of acetylcholine (ACh) on canine colonic circular muscle. Each panel shows electrical activity in top trace with mechanical activity in bottom trace. Electrical recordings were made with sucrose‐gap technique. A: regular electrical events without detectable mechanical events. B: addition of ACh (2 × 10−7 M) increased duration of some slow waves. Mechanical activity occurred in absence of action potentials. C: response to perfusion of constant level of ACh (5 × 10−7 M), which induced pattern of slow waves consisting of long‐duration event followed by several shortduration events. These slow waves were each associated with phasic contraction, amplitude and duration of which was related to slow‐wave duration. D: washout of ACh.

From Huizinga et al. 33
Figure 6. Figure 6.

Effects of micropressure ejection of acetylcholine (ACh). A: series of slow waves recorded by intracellular electrode. At each arrow ACh stimuli of three different intensities were applied via microelectrode positioned close to impaled cell. These caused next slow wave to increase in amplitude and duration. Stimulation with ACh in this manner could also evoke premature slow waves if stimulus was applied early within cycle. B: responses of same cell to ACh applied after muscle had been treated with atropine.
Figure 7. Figure 7.

Five classes of slow‐wave patterns observed in circular muscle of proximal colon in Krebs solution. Class A slow waves were regular and of minimum duration (2–6 s). Class B slow waves were of quite irregular durations; long‐duration events (10–40 s) were randomly interspersed with much shorter duration events. Class C slow waves were rectangular in shape and of generally longer duration (6–14 s) than class A slow waves. Class D pattern consisted of slow waves of large and regular duration (16–20 s) interspersed with short‐duration slow waves. Class E slow waves were regular and long in duration.
Figure 8. Figure 8.

Effects of transmural nerve stimulation. A: in Krebs solution, transmural stimulation caused, after brief latency, an increase in slow‐wave duration and amplitude. B: in atropine, stimulation caused inhibitory junction potential that increased amplitude and duration of next slow wave. After this depressed slow wave, a slow wave of increased amplitude and duration occurred. C: all of these responses were blocked by tetrodotoxin (TTX).
Figure 9. Figure 9.

Effect of removing thin strip of submucosal circular muscle on slow‐wave activity. A: slow waves recorded from intact, cross‐sectional strip demonstrated characteristic decay between submucosal border and B: at 33% of distance through circular muscle. C: another strip from same animal was dissected to remove narrow strip of muscle along submucosal border. Normal resting potentials and slow waves were recorded from the excised strip. D: slow‐wave activity was not observed in remainder of circular layer. These data suggest that pacemaker for slow waves lies along submucosal border of circular layer.
Figure 10. Figure 10.

Synchronous slow waves through thickness of circular layer. Two cells were impaled along line orthogonal to submucosal border, one adjacent to submucosa and another at 40% point. Slow waves occurred in both cells essentially simultaneously. Two traces have been lined up on their resting potentials to display this point. Although amplitude of slow wave decays with distance, frequency and duration of events are perfectly matched. Fast components such as upstroke and plateau oscillations are filtered as slow wave propagates.
Figure 11. Figure 11.

Temporal relationship between slow waves through circular muscle. With fast sweep speed, several slow waves recorded from several cells through thickness of circular layer are displayed. Distance from submucosal border is shown in percent. Events were recorded in pairs, recording from submucosal cell and cell in bulk of circular layer simultaneously. Figure made by lining tracings up on resting potentials and using upstroke of submucosal slow wave as temporal reference. τ0.5 (time to reach half amplitude of slow wave) propagates at rate consistent with electrotonic propagation.
Figure 12. Figure 12.

Summation of slow waves and myenteric potential oscillations (MPO) in circular muscle cells of canine colon. Distances through circular layer were normalized as percent (0%, submucosal border; 100%, myenteric border). A: near myenteric border of circular layer, oscillatory activity at average frequency of 22 cycles/min was observed. C‐F: at sites farther into circular layer, second oscillation was observed. These slow waves increased in amplitude and became dominant event in submucosal half of circular muscle. Amplitude of MPO decreased with distance such that these events were not observed in submucosal quarter of circular layer. Note also gradient in resting membrane potential as function of distance (reference resting membrane potentials shown at right of each trace). Scale at bottom right is relevant to each trace.
Figure 13. Figure 13.

Characterization of myenteric potential oscillations (MPO) in canine colon without interference from slow waves. In intact strips slow waves and MPO summate and produce complicated pattern of electrical activity (see Fig. 12). Left: simpler electrical pattern was obtained by removing submucosal pacemaker cells to remove slow‐wave activity from bulk of circular layer. Right: nine of these preparations were used to study decay of MPO as function of distance. These events decayed exponentially from site of origin near myenteric border. Relative distances are given in percent, and resting potentials at each are given at right of each trace. Scale at bottom right applies to each trace.
Figure 14. Figure 14.

Temporal relationship between electrical activities of two longitudinal cells (A and B) and longitudinal and circular cell just across the myenteric border from each other (C and D). Relatively good phasic relationship existed between electrical events recorded at serosal (A) and myenteric (B) sides of longitudinal muscle. These two traces were recorded from two cells during simultaneous impalements. Some phase shift noted between events recorded at two sites. Phasic relationship was stronger between circular and longitudinal cells just across myenteric border from one another. C and D traces were also made with simultaneous impalements. Nevertheless there was enough phase shift with time to make it impossible to state that events in one layer preceded events in other layer.
Figure 15. Figure 15.

Model of organization of electrical activity in canine colon. Top: cross section of muscularis with types of electrical activity that can be recorded from various points. Slow waves originate at submucosal (SM) border and propagate with decrement through circular layer (CM). Myenteric potential oscillations (MPO) originate at myenteric border and propagate with decrement into circular and longitudinal layers (LM). In longitudinal muscle MPO often initiates action potentials. In circular muscle MPO summates with slow waves. Bottom: this is conceptualized as two oscillators of different frequencies joined by passive cable. Regulation of outputs of pacemakers might occur by neural control of cells within pacemaker region. Regulation at these sites can affect frequency and amplitude of oscillations. Neural and hormonal regulation may also affect cable properties of syncytium connecting pacemaker cells. This would affect length constant of syncytium and therefore affect degree of summation of slow waves and MPO. Neural regulation in longitudinal layer probably affects ability of these cells to generate action potentials in response to propagating MPO.


Figure 1.

Effects of ouabain and low K+ on resting membrane potentials (RMP) through thickness of circular muscle. Under control conditions intracellular recordings from circular muscle cells through thickness of circular layer demonstrate significant gradient in resting potential (filled squares, n = 9, see Fig. 8). When muscles exposed to either ouabain (10−6 M, open triangles, n = 6) or K+‐free Krebs solution (open circles, n = 3), cells depolarized. Submucosal cells (0% distance) depolarized much more than cells near myenteric border (100% distance), such that after either treatment cells throughout circular layer were polarized between −40 and −55 mV. These treatments, known to inhibit Na+‐K+‐ATPase, essentially abolished resting potential gradient through circular layer.



Figure 2.

Slow waves recorded through thickness of circular muscle. Submucosal circular muscle (SCM) cells displayed characteristic regular slow‐wave activity, consisting of upstroke depolarization and sustained plateau phase. As slow waves propagated away from submucosal surface, upstroke velocity decreased, and this event became indistinguishable within 40%‐60% of distance through circular layer. Resting potential decreased, and amplitude of slow wave decreased such that regular slow‐wave activity was usually not detectable in myenteric circular muscle (MCM) cells. Cable properties of circular syncytium appear to prevent slow waves from invading longitudinal muscle layer (LM).



Figure 3.

Characteristics of colonic slow waves. A: first time derivative (dV/dt) of record in B. This series of slow waves demonstrates variability in waveform that can be observed in many preparations. Long‐duration event lasted ∼30 s, whereas short events were ∼5 s in duration. Long‐duration event is used as example to illustrate features of colonic slow waves. Prepotential is slow depolarization that precedes slow waves in many preparations. Upstroke is relatively rapid phase that reaches peak depolarization of ∼40 mV. Then membrane potential repolarizes slightly into plateau phase that can vary from few seconds to ≥30 s. Some cells demonstrate oscillations in membrane potential at peak of plateau; usually these occur at beginning or end of this phase. Plateau potential then repolarizes back to resting or most polarized level. Sometimes slight afterhyperpolarization can be observed after these events. In A differentiation shows relative rate of rise of upstroke event. Upstroke velocities of next few events are decreased by slow waves of long duration. B: spontaneous oscillations in membrane potential (Vm), referred to as slow waves, recorded with intracellular microelectrodes from canine colonic circular muscle. RMP, resting membrane potential.



Figure 4.

Maximum level of depolarization achieved during slow waves recorded by intracellular techniques from several cells through thickness of canine circular muscle. Although amplitude of slow wave decays significantly as slow waves propagate through circular layer, maximum level of depolarization remains relatively constant because of decrease in resting potential (see Fig. 1). This phenomenon may enable membrane potentials of cells throughout thickness of circular layer to surpass mechanical threshold during each slow‐wave cycle and facilitate excitation‐contraction coupling and coordination.



Figure 5.

Effects of acetylcholine (ACh) on canine colonic circular muscle. Each panel shows electrical activity in top trace with mechanical activity in bottom trace. Electrical recordings were made with sucrose‐gap technique. A: regular electrical events without detectable mechanical events. B: addition of ACh (2 × 10−7 M) increased duration of some slow waves. Mechanical activity occurred in absence of action potentials. C: response to perfusion of constant level of ACh (5 × 10−7 M), which induced pattern of slow waves consisting of long‐duration event followed by several shortduration events. These slow waves were each associated with phasic contraction, amplitude and duration of which was related to slow‐wave duration. D: washout of ACh.

From Huizinga et al. 33


Figure 6.

Effects of micropressure ejection of acetylcholine (ACh). A: series of slow waves recorded by intracellular electrode. At each arrow ACh stimuli of three different intensities were applied via microelectrode positioned close to impaled cell. These caused next slow wave to increase in amplitude and duration. Stimulation with ACh in this manner could also evoke premature slow waves if stimulus was applied early within cycle. B: responses of same cell to ACh applied after muscle had been treated with atropine.



Figure 7.

Five classes of slow‐wave patterns observed in circular muscle of proximal colon in Krebs solution. Class A slow waves were regular and of minimum duration (2–6 s). Class B slow waves were of quite irregular durations; long‐duration events (10–40 s) were randomly interspersed with much shorter duration events. Class C slow waves were rectangular in shape and of generally longer duration (6–14 s) than class A slow waves. Class D pattern consisted of slow waves of large and regular duration (16–20 s) interspersed with short‐duration slow waves. Class E slow waves were regular and long in duration.



Figure 8.

Effects of transmural nerve stimulation. A: in Krebs solution, transmural stimulation caused, after brief latency, an increase in slow‐wave duration and amplitude. B: in atropine, stimulation caused inhibitory junction potential that increased amplitude and duration of next slow wave. After this depressed slow wave, a slow wave of increased amplitude and duration occurred. C: all of these responses were blocked by tetrodotoxin (TTX).



Figure 9.

Effect of removing thin strip of submucosal circular muscle on slow‐wave activity. A: slow waves recorded from intact, cross‐sectional strip demonstrated characteristic decay between submucosal border and B: at 33% of distance through circular muscle. C: another strip from same animal was dissected to remove narrow strip of muscle along submucosal border. Normal resting potentials and slow waves were recorded from the excised strip. D: slow‐wave activity was not observed in remainder of circular layer. These data suggest that pacemaker for slow waves lies along submucosal border of circular layer.



Figure 10.

Synchronous slow waves through thickness of circular layer. Two cells were impaled along line orthogonal to submucosal border, one adjacent to submucosa and another at 40% point. Slow waves occurred in both cells essentially simultaneously. Two traces have been lined up on their resting potentials to display this point. Although amplitude of slow wave decays with distance, frequency and duration of events are perfectly matched. Fast components such as upstroke and plateau oscillations are filtered as slow wave propagates.



Figure 11.

Temporal relationship between slow waves through circular muscle. With fast sweep speed, several slow waves recorded from several cells through thickness of circular layer are displayed. Distance from submucosal border is shown in percent. Events were recorded in pairs, recording from submucosal cell and cell in bulk of circular layer simultaneously. Figure made by lining tracings up on resting potentials and using upstroke of submucosal slow wave as temporal reference. τ0.5 (time to reach half amplitude of slow wave) propagates at rate consistent with electrotonic propagation.



Figure 12.

Summation of slow waves and myenteric potential oscillations (MPO) in circular muscle cells of canine colon. Distances through circular layer were normalized as percent (0%, submucosal border; 100%, myenteric border). A: near myenteric border of circular layer, oscillatory activity at average frequency of 22 cycles/min was observed. C‐F: at sites farther into circular layer, second oscillation was observed. These slow waves increased in amplitude and became dominant event in submucosal half of circular muscle. Amplitude of MPO decreased with distance such that these events were not observed in submucosal quarter of circular layer. Note also gradient in resting membrane potential as function of distance (reference resting membrane potentials shown at right of each trace). Scale at bottom right is relevant to each trace.



Figure 13.

Characterization of myenteric potential oscillations (MPO) in canine colon without interference from slow waves. In intact strips slow waves and MPO summate and produce complicated pattern of electrical activity (see Fig. 12). Left: simpler electrical pattern was obtained by removing submucosal pacemaker cells to remove slow‐wave activity from bulk of circular layer. Right: nine of these preparations were used to study decay of MPO as function of distance. These events decayed exponentially from site of origin near myenteric border. Relative distances are given in percent, and resting potentials at each are given at right of each trace. Scale at bottom right applies to each trace.



Figure 14.

Temporal relationship between electrical activities of two longitudinal cells (A and B) and longitudinal and circular cell just across the myenteric border from each other (C and D). Relatively good phasic relationship existed between electrical events recorded at serosal (A) and myenteric (B) sides of longitudinal muscle. These two traces were recorded from two cells during simultaneous impalements. Some phase shift noted between events recorded at two sites. Phasic relationship was stronger between circular and longitudinal cells just across myenteric border from one another. C and D traces were also made with simultaneous impalements. Nevertheless there was enough phase shift with time to make it impossible to state that events in one layer preceded events in other layer.



Figure 15.

Model of organization of electrical activity in canine colon. Top: cross section of muscularis with types of electrical activity that can be recorded from various points. Slow waves originate at submucosal (SM) border and propagate with decrement through circular layer (CM). Myenteric potential oscillations (MPO) originate at myenteric border and propagate with decrement into circular and longitudinal layers (LM). In longitudinal muscle MPO often initiates action potentials. In circular muscle MPO summates with slow waves. Bottom: this is conceptualized as two oscillators of different frequencies joined by passive cable. Regulation of outputs of pacemakers might occur by neural control of cells within pacemaker region. Regulation at these sites can affect frequency and amplitude of oscillations. Neural and hormonal regulation may also affect cable properties of syncytium connecting pacemaker cells. This would affect length constant of syncytium and therefore affect degree of summation of slow waves and MPO. Neural regulation in longitudinal layer probably affects ability of these cells to generate action potentials in response to propagating MPO.

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Article Title: Electrophysiology of colonic smooth muscle
 

How to Cite

Kenton M. Sander, Terence K. Smith. Electrophysiology of colonic smooth muscle. Compr Physiol 2011, Supplement 16: Handbook of Physiology, The Gastrointestinal System, Motility and Circulation: 251-271. First published in print 1989. doi: 10.1002/cphy.cp060107