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Electrophysiology of the intestinal musculature

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Abstract

The sections in this article are:

1 Properties of Single Intestinal Smooth Muscle Cells
1.1 Complement of Ionic Channels
1.2 Passive Electrical Properties
1.3 Active Properties
1.4 Responses to Receptor Activation
2 Electrical and Mechanical Activity in Vitro of Intestinal Smooth Muscle Tissues
2.1 Active and Passive Electrical Properties
2.2 Nerve‐Evoked Responses: Excitatory and Inhibitory Junction Potentials
2.3 Receptor‐Evoked Responses
3 Summary
Figure 1. Figure 1.

Electrophysiological properties of single isolated smooth muscle cell from longitudinal muscle of rabbit jejunum. Recordings of membrane potential show responses to rectangular depolarizing and hyperpolarizing current pulses (A, B); recordings of membrane current under voltage clamp (C) were obtained with a low‐resistance patch pipette filled with high‐K+ buffered‐Ca2+ solution. A: when bathed in normal solution (2.5 mM Ca2+, 6 mM K+, 137 mM Na+), the cell discharges action potentials on depolarization and an inward‐current pulse evokes an electrotonic potential; from this, cell input resistance can be calculated. B: cell input resistance is increased and larger action potentials are discharged in Ca2+‐free 20 mM Ba2+ solution. After the action potential, repolarization was to a less negative potential. C: under voltage clamp, stepping from a holding potential of −50 mV to 0 mV potential evoked, after an initial upward capacitive transient, an initial net inward current followed by outward current in normal solution (upper recording). A similar protocol in Ca2+‐free 20 mM Ba2+ solution produced a larger initial peak of inward current and outward current was very small (lower recording). Both Ba2+ and Ca2+ can carry the inward current, but in Ca2+‐free, Ba2+‐containing solution, outward K+ current or repolarization is attenuated; input resistance is increased.

From Bolton et al.
Figure 2. Figure 2.

Action of acetylcholine (Ach) on transient outward current evoked by a depolarizing command pulse under voltage clamp in single isolated cell from longitudinal muscle layer of rabbit jejunum. Recording was done with a low‐resistance pipette containing a high‐K+ solution in which Ca2+ was minimally buffered with ethylene glycol‐bis(β‐aminoeth‐ylether)‐N,N'‐tetraacetic acid (EGTA) (0.08 mM). A: cell was held at −50 mV and stepped to zero potential (lower trace) for 100 ms every 10 s. Initial inward current, unaffected by iontophoretic application of Ach for 1 s, is followed by outward current (upper trace); this has an initial transient component resembling a single spontaneous transient outward current (STOC) (see Fig. ) followed by a more sustained component; Ach application abolishes this transient outward current, which recovers by 61 s. B: expanded traces of averaged records (cont, control, 3 traces; Ach, 2 traces) to show effect of Ach application (left) and net effect of Ach (right) obtained by subtraction.

From Benham and Bolton
Figure 3. Figure 3.

Action of acetylcholine (Ach) on a single cell from longitudinal muscle layer of rabbit jejunum. Recording of membrane potential (upper trace) or membrane current (lower trace) was made with a pipette containing a high‐K+, buffered‐Ca2+ solution. Membrane potential responses to alternate depolarizing and hyperpolarizing current pulses (middle trace) were evoked. At bar, a 2‐s pulse of Ach was iontophoretically applied; this depolarized the cell, and electrotonic potentials at this time became very small; they recovered as cell repolarized. In lower trace, cell was held at −40 mV under voltage clamp (potential trace not shown). Application of 10−5 M Ach in bathing solution evoked an inward current that reached a peak and then declined despite continuing Ach presence. Holding current also showed spontaneous transient outward currents (STOCs) that were abolished by applying Ach. Results suggest that Ach opens additional ionic channels in membrane (note increased current noise in lower trace) that allow inward current to pass, depolarizing the cell. At the same time, Ca2+ stores are discharged and STOCs abolished.

From Benham et al. . Reprinted by permission from Nature, copyright 1985, Macmillan Journals Limited


Figure 1.

Electrophysiological properties of single isolated smooth muscle cell from longitudinal muscle of rabbit jejunum. Recordings of membrane potential show responses to rectangular depolarizing and hyperpolarizing current pulses (A, B); recordings of membrane current under voltage clamp (C) were obtained with a low‐resistance patch pipette filled with high‐K+ buffered‐Ca2+ solution. A: when bathed in normal solution (2.5 mM Ca2+, 6 mM K+, 137 mM Na+), the cell discharges action potentials on depolarization and an inward‐current pulse evokes an electrotonic potential; from this, cell input resistance can be calculated. B: cell input resistance is increased and larger action potentials are discharged in Ca2+‐free 20 mM Ba2+ solution. After the action potential, repolarization was to a less negative potential. C: under voltage clamp, stepping from a holding potential of −50 mV to 0 mV potential evoked, after an initial upward capacitive transient, an initial net inward current followed by outward current in normal solution (upper recording). A similar protocol in Ca2+‐free 20 mM Ba2+ solution produced a larger initial peak of inward current and outward current was very small (lower recording). Both Ba2+ and Ca2+ can carry the inward current, but in Ca2+‐free, Ba2+‐containing solution, outward K+ current or repolarization is attenuated; input resistance is increased.

From Bolton et al.


Figure 2.

Action of acetylcholine (Ach) on transient outward current evoked by a depolarizing command pulse under voltage clamp in single isolated cell from longitudinal muscle layer of rabbit jejunum. Recording was done with a low‐resistance pipette containing a high‐K+ solution in which Ca2+ was minimally buffered with ethylene glycol‐bis(β‐aminoeth‐ylether)‐N,N'‐tetraacetic acid (EGTA) (0.08 mM). A: cell was held at −50 mV and stepped to zero potential (lower trace) for 100 ms every 10 s. Initial inward current, unaffected by iontophoretic application of Ach for 1 s, is followed by outward current (upper trace); this has an initial transient component resembling a single spontaneous transient outward current (STOC) (see Fig. ) followed by a more sustained component; Ach application abolishes this transient outward current, which recovers by 61 s. B: expanded traces of averaged records (cont, control, 3 traces; Ach, 2 traces) to show effect of Ach application (left) and net effect of Ach (right) obtained by subtraction.

From Benham and Bolton


Figure 3.

Action of acetylcholine (Ach) on a single cell from longitudinal muscle layer of rabbit jejunum. Recording of membrane potential (upper trace) or membrane current (lower trace) was made with a pipette containing a high‐K+, buffered‐Ca2+ solution. Membrane potential responses to alternate depolarizing and hyperpolarizing current pulses (middle trace) were evoked. At bar, a 2‐s pulse of Ach was iontophoretically applied; this depolarized the cell, and electrotonic potentials at this time became very small; they recovered as cell repolarized. In lower trace, cell was held at −40 mV under voltage clamp (potential trace not shown). Application of 10−5 M Ach in bathing solution evoked an inward current that reached a peak and then declined despite continuing Ach presence. Holding current also showed spontaneous transient outward currents (STOCs) that were abolished by applying Ach. Results suggest that Ach opens additional ionic channels in membrane (note increased current noise in lower trace) that allow inward current to pass, depolarizing the cell. At the same time, Ca2+ stores are discharged and STOCs abolished.

From Benham et al. . Reprinted by permission from Nature, copyright 1985, Macmillan Journals Limited
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T. B. Bolton. Electrophysiology of the intestinal musculature. Compr Physiol 2011, Supplement 16: Handbook of Physiology, The Gastrointestinal System, Motility and Circulation: 217-250. First published in print 1989. doi: 10.1002/cphy.cp060106