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Electrophysiological and neuromuscular relationships in extramural blood vessels

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Abstract

The sections in this article are:

1 Innervation of Mesenteric Circulation
1.1 Anatomy
2 Mesenteric Artery
2.1 Resting Membrane Potential
2.2 Cell Coupling
2.3 Active Membrane Properties
2.4 Responses to Addition of Autonomic Neurotransmitters
2.5 Responses to Nerve Stimulation
2.6 Pharmacology of Neuroeffector Transmission
2.7 Prejunctional Effects on Neuromuscular Transmission
3 Neuromuscular Relationships in Nonmammalian Artery
4 Mesenteric Vein
4.1 Resting Membrane Potential
4.2 Action Potentials
4.3 Passive Membrane Properties
4.4 Response to Autonomic Transmitter Substances
4.5 Response to Nerve Stimulation
4.6 Pharmacology of Neuroeffector Transmission
5 Portal Vein
5.1 Spontaneous Action Potentials
5.2 Cell Coupling
5.3 Response to Nerve Stimulation
5.4 Response to Neurotransmitters
6 Functional Implications of Neuromuscular Differences Between Artery and Vein
7 Conclusions
Figure 1. Figure 1.

Representation of relationship between adrenergic nerves and mesenteric blood vessels of the rat. c, Capillary; cv, collecting venule; pa, principal artery; pca, precapillary arteriole; pv, principal vein; sa, small artery of microvasculature; sv, small vein; ta, terminal arteriole; Heavy lines, adrenergic nerves; arrows, direction of blood flow. Precapillary arterioles and collecting venules are not innervated.

From Furness and Marshall
Figure 2. Figure 2.

Induction of excitability by tetraethylammonium ion (TEA) in the normally inexcitable vascular smooth muscle from guinea pig superior mesenteric artery. A: control shows resting potential of approx. −58 mV and lack of spontaneous action potentials or responses to intense external electrical stimulation (1‐shock artifact depicted). B: record from same cell impaled in A 5 min after addition of 5 mM TEA, illustrates a large overshooting action potential produced in response to electrical stimulation. C: record from another cell shown at a faster sweep speed. D: record from another muscle exposed to 7.5 mM TEA illustrates partial depolarization and production of spontaneous action potentials. Time scale in B applies to all panels except C; voltage calibration in B applies to all panels; dV/dt calibration in B applies to B‐D.

From Harder and Sperelakis
Figure 3. Figure 3.

Effects of noradrenaline (NA) on membrane potential of single smooth cell of rabbit mesenteric artery. NA was applied between arrows.

From Itoh et al.
Figure 4. Figure 4.

Relationship between contraction and depolarization produced by noradrenaline (NA) and raised external K+ in guinea pig mesenteric artery. Potassium contractions were expressed as percentage of the maximal contraction to NA.

From Bolton et al.
Figure 5. Figure 5.

Effects of acetylcholine (ACh) on various splanchnic vessels in guinea pig. Although ACh initiates a hyperpolarization in both jejunal mesenteric artery and vein, it depolarizes the portal vein. [K]0, extracellular potassium concentration.

Adapted from Takata
Figure 6. Figure 6.

Effect of acetylcholine (ACh) on amplitude of excitatory junction potentials (EJP) in guinea pig jejunal mesenteric artery induced by increasing stimulus intensity. In absence of ACh, amplitude of EJPs increased with 4 steps as stimulus intensity was increased; with ACh (10−9 M), amplitude of EJPs decreased but continued to show stepwise increase in amplitude with increasing stimulus intensity.

From Kuriyama and Suzuki
Figure 7. Figure 7.

Responses to single perivascular nerve stimulus in presence of 3 × 10−6 M tetrodotoxin (TTX) in guinea pig ear artery. A: responses obtained between stimulating electrodes and at distances of 1 and 2 mm from them. Although an action potential is recorded at stimulating electrode, only small slow potential change is observed at 1 mm distance. B: peak amplitude of response against distance from stimulating electrodes in presence and absence of TTX. After exposure to TTX, responses are only obtained near stimulating electrodes.

From Keef and Neild
Figure 8. Figure 8.

Simultaneous recordings of electrical (top tracing) and mechanical (bottom tracing) activities of rat tail artery induced by stimulation of perivascular nerves with single 0.05‐ms pulse. A: stimulation at 40 V produced excitatory junction potential (EJP) and no contraction (left panel). Increasing the stimulus strength to 120 V induces active response on EJP and long sustained depolarization; fast phasic and slow sustained contraction were also observed (right panel). B: in another preparation, stimulation at 88 V elicited slow depolarization and slow contraction that were abolished by prazosin (5 × 10−9 g/ml). EJP was subthreshold and was not affected by prazosin. C: increasing stimulus strength to 90 V initiated fast phasic contraction associated with action potential arising from EJP; a second fast contraction was triggered when slow depolarization reached threshold. Prazosin abolished only second fast contraction.

From Cheung
Figure 9. Figure 9.

Effects of brief electrical stimuli on longitudinal muscle of anterior mesenteric artery of domestic fowl measured by sucrose‐gap method. A: depolarization without action potentials (lower trace) accompanies smooth rise in tension (upper trace) with repetitive stimulation at 5 Hz; act on potentials are associated with small rapid contractions. Upper vertical bar, 1‐g calibration; lower vertical bar, 2‐mV calibration; horizontal calibration, 2 s. B: effects of brief electrical stimuli on preparation in which tone was raised by adding 0.2 mg/ml BaCl2 to physiological saline in presence of hyoscine (10 ng/ml). Upper trace, contractile response. Lower trace, membrane potential response. Electrical stimulation at supramaximal strength was applied for 5 s at 1 Hz (left panel) or 10 Hz (right panel). Complete inhibition of action potentials occurs at the higher frequency of stimulation.

From Bolton ].
Figure 10. Figure 10.

Action potentials and slow waves induced by nerve stimulation, recorded from smooth muscle cells of guinea pig mesenteric vein. A: nerve stimulation (20 Hz, 1 s) induced action potential and slow waves. Train of pulses at 1 Hz (B), 2 Hz (C), or 4 Hz (D) was applied for 1 min. Upper trace in each record, time scale of 1 s.

From Suzuki
Figure 11. Figure 11.

Action potentials and slow depolarization, recorded in small (tertiary) mesenteric vein of distal colon in guinea pig with repetitive stimulation of lumbar colonic nerves. Note increasing amplitude action potentials recorded with higher frequencies. Resting membrane potential —70 mV; stimuli 10 V, 0.2 ms. (O. D. Hottenstein and D. L. Kreulen, unpublished observations.)

Figure 12. Figure 12.

Spontaneous and evoked activity in strip of rabbit portal vein, recorded with sucrose‐gap technique. A: normal ongoing spontaneous activity; B: response to stimulation of intramural noradrenergic nerves; C: response to 0.1 μg/ml of noradrenaline (NA).

From Holman
Figure 13. Figure 13.

Contractile responses of innervated strip of rabbit portal vein to postganglionic nerve stimulation in vitro. A: 4 Hz; B: 8 Hz; C: 16 Hz. Increase in contraction frequency produced by nerve stimulation in this regularly contracting muscle. Heavy bar, stimulation time.

From Johansson and Ljung
Figure 14. Figure 14.

Comparison of membrane potential responses of mesenteric vein and artery to repetitive lumbar colonic nerve stimulation (supramaximal). Greater slow depolarizations occur at both frequencies in vein. Vertical deflections in venous tracing during stimulation are stimulus artifacts; in artery, vertical deflections at 1 Hz are excitatory junction potentials (EJP), whereas at 5 Hz, stimulus artifacts are superimposed upon EJP. Bar, period of stimulation.

Adapted from Hottenstein and Kreulen
Figure 15. Figure 15.

Frequency dependence of the amplitude of slow depolarization in vein and artery of distal colonic mesentery of guinea pig. Seven artery cell and 11 vein cell responses were compared by unpaired t test (P < 0.01).

Adapted from Hottenstein and Kreulen


Figure 1.

Representation of relationship between adrenergic nerves and mesenteric blood vessels of the rat. c, Capillary; cv, collecting venule; pa, principal artery; pca, precapillary arteriole; pv, principal vein; sa, small artery of microvasculature; sv, small vein; ta, terminal arteriole; Heavy lines, adrenergic nerves; arrows, direction of blood flow. Precapillary arterioles and collecting venules are not innervated.

From Furness and Marshall


Figure 2.

Induction of excitability by tetraethylammonium ion (TEA) in the normally inexcitable vascular smooth muscle from guinea pig superior mesenteric artery. A: control shows resting potential of approx. −58 mV and lack of spontaneous action potentials or responses to intense external electrical stimulation (1‐shock artifact depicted). B: record from same cell impaled in A 5 min after addition of 5 mM TEA, illustrates a large overshooting action potential produced in response to electrical stimulation. C: record from another cell shown at a faster sweep speed. D: record from another muscle exposed to 7.5 mM TEA illustrates partial depolarization and production of spontaneous action potentials. Time scale in B applies to all panels except C; voltage calibration in B applies to all panels; dV/dt calibration in B applies to B‐D.

From Harder and Sperelakis


Figure 3.

Effects of noradrenaline (NA) on membrane potential of single smooth cell of rabbit mesenteric artery. NA was applied between arrows.

From Itoh et al.


Figure 4.

Relationship between contraction and depolarization produced by noradrenaline (NA) and raised external K+ in guinea pig mesenteric artery. Potassium contractions were expressed as percentage of the maximal contraction to NA.

From Bolton et al.


Figure 5.

Effects of acetylcholine (ACh) on various splanchnic vessels in guinea pig. Although ACh initiates a hyperpolarization in both jejunal mesenteric artery and vein, it depolarizes the portal vein. [K]0, extracellular potassium concentration.

Adapted from Takata


Figure 6.

Effect of acetylcholine (ACh) on amplitude of excitatory junction potentials (EJP) in guinea pig jejunal mesenteric artery induced by increasing stimulus intensity. In absence of ACh, amplitude of EJPs increased with 4 steps as stimulus intensity was increased; with ACh (10−9 M), amplitude of EJPs decreased but continued to show stepwise increase in amplitude with increasing stimulus intensity.

From Kuriyama and Suzuki


Figure 7.

Responses to single perivascular nerve stimulus in presence of 3 × 10−6 M tetrodotoxin (TTX) in guinea pig ear artery. A: responses obtained between stimulating electrodes and at distances of 1 and 2 mm from them. Although an action potential is recorded at stimulating electrode, only small slow potential change is observed at 1 mm distance. B: peak amplitude of response against distance from stimulating electrodes in presence and absence of TTX. After exposure to TTX, responses are only obtained near stimulating electrodes.

From Keef and Neild


Figure 8.

Simultaneous recordings of electrical (top tracing) and mechanical (bottom tracing) activities of rat tail artery induced by stimulation of perivascular nerves with single 0.05‐ms pulse. A: stimulation at 40 V produced excitatory junction potential (EJP) and no contraction (left panel). Increasing the stimulus strength to 120 V induces active response on EJP and long sustained depolarization; fast phasic and slow sustained contraction were also observed (right panel). B: in another preparation, stimulation at 88 V elicited slow depolarization and slow contraction that were abolished by prazosin (5 × 10−9 g/ml). EJP was subthreshold and was not affected by prazosin. C: increasing stimulus strength to 90 V initiated fast phasic contraction associated with action potential arising from EJP; a second fast contraction was triggered when slow depolarization reached threshold. Prazosin abolished only second fast contraction.

From Cheung


Figure 9.

Effects of brief electrical stimuli on longitudinal muscle of anterior mesenteric artery of domestic fowl measured by sucrose‐gap method. A: depolarization without action potentials (lower trace) accompanies smooth rise in tension (upper trace) with repetitive stimulation at 5 Hz; act on potentials are associated with small rapid contractions. Upper vertical bar, 1‐g calibration; lower vertical bar, 2‐mV calibration; horizontal calibration, 2 s. B: effects of brief electrical stimuli on preparation in which tone was raised by adding 0.2 mg/ml BaCl2 to physiological saline in presence of hyoscine (10 ng/ml). Upper trace, contractile response. Lower trace, membrane potential response. Electrical stimulation at supramaximal strength was applied for 5 s at 1 Hz (left panel) or 10 Hz (right panel). Complete inhibition of action potentials occurs at the higher frequency of stimulation.

From Bolton ].


Figure 10.

Action potentials and slow waves induced by nerve stimulation, recorded from smooth muscle cells of guinea pig mesenteric vein. A: nerve stimulation (20 Hz, 1 s) induced action potential and slow waves. Train of pulses at 1 Hz (B), 2 Hz (C), or 4 Hz (D) was applied for 1 min. Upper trace in each record, time scale of 1 s.

From Suzuki


Figure 11.

Action potentials and slow depolarization, recorded in small (tertiary) mesenteric vein of distal colon in guinea pig with repetitive stimulation of lumbar colonic nerves. Note increasing amplitude action potentials recorded with higher frequencies. Resting membrane potential —70 mV; stimuli 10 V, 0.2 ms. (O. D. Hottenstein and D. L. Kreulen, unpublished observations.)



Figure 12.

Spontaneous and evoked activity in strip of rabbit portal vein, recorded with sucrose‐gap technique. A: normal ongoing spontaneous activity; B: response to stimulation of intramural noradrenergic nerves; C: response to 0.1 μg/ml of noradrenaline (NA).

From Holman


Figure 13.

Contractile responses of innervated strip of rabbit portal vein to postganglionic nerve stimulation in vitro. A: 4 Hz; B: 8 Hz; C: 16 Hz. Increase in contraction frequency produced by nerve stimulation in this regularly contracting muscle. Heavy bar, stimulation time.

From Johansson and Ljung


Figure 14.

Comparison of membrane potential responses of mesenteric vein and artery to repetitive lumbar colonic nerve stimulation (supramaximal). Greater slow depolarizations occur at both frequencies in vein. Vertical deflections in venous tracing during stimulation are stimulus artifacts; in artery, vertical deflections at 1 Hz are excitatory junction potentials (EJP), whereas at 5 Hz, stimulus artifacts are superimposed upon EJP. Bar, period of stimulation.

Adapted from Hottenstein and Kreulen


Figure 15.

Frequency dependence of the amplitude of slow depolarization in vein and artery of distal colonic mesentery of guinea pig. Seven artery cell and 11 vein cell responses were compared by unpaired t test (P < 0.01).

Adapted from Hottenstein and Kreulen
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How to Cite

D. L. Kreulen, K. D. Keef. Electrophysiological and neuromuscular relationships in extramural blood vessels. Compr Physiol 2011, Supplement 16: Handbook of Physiology, The Gastrointestinal System, Motility and Circulation: 1605-1634. First published in print 1989. doi: 10.1002/cphy.cp060144