Parasympathetic modulation of sinoatrial node pacemaker activity in rabbit heart: A unifying model

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 276, Issue 6 45-6, 1999, Pages

  Demir, Semahat S ^a   Clark, John W ^b   Giles, Wayne R ^c  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b Rice University   (United States)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

Action potential simulation; Cardiac pacemaker cell; Extrajunctional receptor; Hodgkin Huxley model; Isoprenaline; Junctional receptor; Muscarinic receptors; Phase sensitivity; Phase response curve; Steady state entrainment; Whole cell voltage clamp

Indexed keywords

ACETYLCHOLINE; ISOPRENALINE; MUSCARINIC RECEPTOR;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHOLINERGIC TRANSMISSION; COMPARTMENT MODEL; CONTROLLED STUDY; HYPERPOLARIZATION; MATHEMATICAL MODEL; NONHUMAN; PARASYMPATHETIC NERVE; POTASSIUM CURRENT; PRIORITY JOURNAL; RABBIT; SINUS NODE; VAGUS NERVE STIMULATION; VOLTAGE CLAMP;

EID: 0033001517     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.1999.276.6.h2221     Document Type: Article

References (96)

1. Anumonwo, J., M. Delmar, V. A. D. Michaels, and J. Jalife. Phase resetting and entrainment of pacemaker activity in single sinus nodal cells. Circ. Res. 68: 1138-1153, 1991.
2. Bailey, J., and D. Ollis (Editors). Biochemical Engineering Fundamentals. New York: McGraw-Hill, 1986, chapt. 3, p. 86-156.
3. Bonner, T., N. Buckley, A. Young, and M. Brann. Identification of a family of muscarinic acetylcholine receptor genes. Science 237: 527-532, 1987.
4. 5 muscarinic acetylcholine receptor genes. Neuron 1: 403-410, 1988.
5. Bramich, N., J. Brock, F. Edwards, and G. Hirst. Ionophoretically applied acetylcholine and vagal stimulation in the arrested sinus venosus of the toad, Bufo marinus. J. Physiol. (Lond.) 478: 289-300, 1994.
6. Breitwieser, G., and G. Szabo. Uncoupling of cardiac muscarinic and β-adrenergic receptors from ion channels by a guanine nucleotide analogue. Nature 317: 538-540, 1985.
7. + channel activation as revealed by hydrolysis-resistant GTP analogues. J. Gen. Physiol. 91: 469-493, 1988.
8. Bristow, D., and J. Clark. A mathematical model of the vagally driven primary pacemaker. Am. J. Physiol. 244 (Heart Circ. Physiol. 13): H150-H161, 1983.
9. a. Brown, G., and J. Eccles. The action of a single vagal volley on the rhythm of the heart beat. J. Physiol. (Lond.) 82: 211-240, 1934.
10. Brown, G., and J. Eccles. Further experiments on vagal inhibition of the heart beat. J. Physiol. (Lond.) 82: 242-257, 1934.
11. a. Brown, H., and J. Denyer. Low-dose acetylcholine reduces calcium current in isolated sino-atrial node cells of rabbit (Abstract). J. Physiol. (Lond.) 410: 65P, 1989.
12. Brown, H., D. DiFrancesco, and S. Noble. How does adrenaline accelerate the heart? Nature 280: 235-236, 1979.
13. Bywater, R., G. Campbell, F. Edwards, and G. Hirst. Effects of vagal stimulation and applied acetylcholine on the arrested sinus venosus of the toad. J. Physiol. (Lond.) 425: 1-27, 1990.
14. Campbell, G., F. Edwards, G. Hirst, and J. O'Shea. Effects of vagal stimulation and applied acetylcholine on pacemaker potentials in the guinea-pig heart. J. Physiol. (Lond.) 415: 57-68, 1989.
15. Canale, E., G. Campbell, J. Smalich, and J. Campbell. Cardiac Muscle. Berlin: Springer-Verlag, 1986.
16. 2+ channels. Pflügers Arch. 419: 433-443, 1991.
17. Choate, J., F. Edwards, G. Hirst, and J. O'Shea. Effects of sympathetic nerve stimulation on the sino-atrial node of the guinea-pig. J. Physiol. (Lond.) 471: 707-727, 1993.
18. Choate, J., M. Klemm, and G. Hirst. Sympathetic and parasympathetic neuro-muscular junctions in the guinea-pig sino-atrial node. J. Auton. Nerv. Syst. 44: 1-16, 1993.
19. Demir, S., J. Clark, C. Murphey, and W. Giles. A mathematical model of a rabbit sinoatrial node cell. Am. J. Physiol. 266 (Cell Physiol. 35): C832-C852, 1994.
20. Denyer, J. Isolation and Electrophysiological Characteristics of Rabbit Sino-Atrial Node Cells (Ph.D. thesis). Oxford, UK: Univeristy of Oxford, 1989.
21. + pump in isolated cardiac myocytes. Am. J. Physiol. 251 (Heart Circ. Physiol. 20): H218-H225, 1986.
22. Dexter, F., M. Levy, and Y. Rudy. Mathematical model of the changes in heart rate elicited by vagal stimulation. Circ. Res. 65: 1330-1339, 1989.
23. Dexter, F., G. Saidel, and M. Levy. Mathematical model of dependence of heart rate on tissue concentration of ACh. Am. J. Physiol. 256 (Heart Circ. Physiol. 25): H520-H526, 1989.
24. f and the neuronal modulation of heart rate. In: Cardiac Electrophysiology, edited by D. Zipes and J. Jalife. Philadelphia, PA: Saunders, 1990, chapt. 4, p. 28-35.
25. DiFrancesco, D., P. Ducouret, and R. Robinson. Muscarinic modulation of cardiac rate at low acetylcholine concentrations. Science 243: 669-671, 1989.
26. DiFrancesco, D., and D. Noble. A model of cardiac electrical activity incorporating ionic pumps and concentration changes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 307: 353-398, 1985.
27. DiFrancesco, D., and P. Tortora. Direct activation of cardiac pacemaker channels by intracellular cyclic AMP. Nature 351: 145-147, 1991.
28. f. Pflügers Arch. 410: 139-142, 1987.
29. f) induced by acetylcholine in rabbit sino-atrial node myocytes. J. Physiol. (Lond.) 405: 477-491, 1988.
30. Dokos, S., B. Celler, and N. Lovell. Modification of DiFrancesco-Noble equations to simulate the effects of vagal stimulation on in vivo mammalian sinoatrial node electrical activity. Ann. Biomed. Eng. 21: 321-335, 1993.
31. Dong, E., and B. Reitz. Effect of timing of vagal stimulation on heart rate in the dog. Circ. Res. 27: 635-646, 1970.
32. Edwards, F., N. Bramich, and G. Hirst. Analysis of the effects of vagal stimulation on the sinus venosus of the toad. Philos. Trans. R. Soc. Lond. B Biol. Sci. 341: 149-162, 1993.
33. Egan, T., and S. Noble. Acetylcholine and the mammalian "slow inward" current: a computer investigation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 230: 315-337, 1987.
34. 1 muscarinic receptors increase calcium current and phosphoinositide turnover in guinea-pig ventricular cardiocytes. J. Physiol. (Lond.) 471: 41-60, 1993.
35. + pump current in guinea-pig ventricular myocytes by a cAMP-dependent PKA pathway. J. Physiol. (Lond.) 477: 373-380, 1994.
36. + pump in guniea-pig ventricular myocytes. J. Physiol. (Lond.) 449: 689-704, 1992.
37. Giles, W., and E. Shibata. Autonomic transmitter actions on cardiac pacemaker tissue: a brief review. Federation Proc. 40: 2618-2624, 1981.
38. Glass, L., and M. Mackey. From Clocks to Chaos: The Rhythms of Life. Princeton, NJ: Princeton University Press, 1988.
39. Guevara, M., and H. Jongsma. Phase resetting in a model of sinoatrial nodal membrane: ionic and topological aspects. Am. J. Physiol. 258 (Heart Circ. Physiol. 27): H734-H747, 1990.
40. Guevara, M., and H. Jongsma. Three ways of abolishing automaticity in sinoatrial node: ionic modeling and nonlinear dynamics. Am. J. Physiol. 262 (Heart Circ. Physiol. 31): H1268-H1286, 1992.
41. Hagiwara, N., and H. Irisawa. Modulation by intracellular calcium of the hyperpolarization-activated inward current in rabbit single sino-atrial node cells. J. Physiol. (Lond.) 409: 121-141, 1989.
42. Hagiwara, N., H. Irisawa, and M. Kameyama. Transient-type calcium current contributes to the pace-maker potential in isolated rabbit sino-atrial node cells (Abstract). J. Physiol. (Lond.) 382: 104P, 1987.
43. Hagiwara, N., H. Irisawa, and M. Kameyama. Contribution of two types of calcium currents to the pacemaker potentials of rabbit sino-atrial node cells. J. Physiol. (Lond.) 395: 233-253, 1988.
44. Han, X., Y. Shimoni, and W. Giles. An obligatory role for nitric oxide in autonomic control of mammalian heart rate. J. Physiol. (Lond.) 476: 309-314, 1994.
45. Han, X., Y. Shimoni, and W. Giles. A cellular mechanism for nitric oxide-mediated cholinergic control of mammalian heart rate. J. Gen. Physiol. 106: 45-65, 1995.
46. Hartzell, H. Distribution of muscarinic acetylcholine receptors and presynaptic nerve terminals in the amphibian heart. J. Cell Biol. 86: 6-20, 1980.
47. Hartzell, H. Regulation of cardiac ion channels by catecholamines, acetylcholine and second messenger system. Prog. Biophys. Mol. Biol. 52: 165-247, 1988.
48. Hescheler, J., M. Kameyama, and W. Trautwein. On the mechanism of muscarinic inhibition of the cardiac Ca current. Pflügers Arch. 407: 182-189, 1986.
49. Hutter, O., and W. Trautwein. Effect of vagal stimulation on the sinus venosus of the frog's heart. Nature 176: 512-513, 1955.
50. Hutter, O., and W. Trautwein. Vagal and sympathetic effects on the pacemaker fibers in the sinus venosus of the heart. J. Gen. Physiol. 39: 715-733, 1956.
51. Iacono, G., and M. Vassalle. Acetylcholine increases intracellular sodium activity in sheep cardiac Purkinje fiber. Am. J. Physiol. 256 (Heart Circ. Physiol. 25): H1407-H1416, 1989.
52. Iano, T., M. Levy, and M. Lee. An acceleratory component of the parasympathetic control of heart rate. Am. J. Physiol. 224: 997-1005, 1973.
53. Irisawa, H., H. Brown, and W. Giles. Cardiac pacemaking in the sinoatrial node. Physiol. Rev. 73: 197-227, 1993.
54. + pump function in voltage-clamped ventricular myocytes of the rat heart. Pflügers Arch. 424: 361-363, 1993.
55. Jalife, J., and G. Moe. Phasic effects of vagal stimulation on pacemaker activity of the isolated sinus node of the young cat. Circ. Res. 45: 595-607, 1979.
56. Jalife, J., V. Slenter, J. Salata, and D. Michaels. Dynamic vagal control of pacemaker activity in the mammalian sinoatrial node. Circ. Res. 52: 642-656, 1983.
57. Klemm, M., G. Hirst, and G. Campbell. Structure of autonomic neuromuscular junctions in the sinus venosus of the toad. J. Auton. Nerv. Syst. 39: 139-150, 1992.
58. Kodama, I., and M. Boyett. Regional differences in the electrical activity of the rabbit sinus node. Pflügers Arch. 404: 214-226, 1985.
59. Kronhaus, K. D., J. Spear, and E. Moore. Sinus node extracellular potassium transients following vagal stimulation. Nature 275: 322-324, 1978.
60. Levy, M., P. Martin, T. Iano, and H. Zieske. Paradoxical effect of vagus nerve stimulation on heart rate in dogs. Circ. Res. 25: 303-314, 1969.
61. Mackaay, A., T. Op't Hof, W. Bleeker, H. Jongsma, and L. Bouman. Interaction of adrenaline and acetylcholine on cardiac pacemaker function. Functional inhomogeneity of the rabbit sinus node. J. Pharmacol. Exp. Ther. 214: 417-422, 1980.
62. Michaels, D., E. Matyas, and J. Jalife. A mathematical model of the effects of acetylcholine pulses on sinoatrial pacemaker activity. Circ. Res. 55: 89-101, 1984.
63. Michaels, D., V. Slenter, and J. Salata. A model of dynamic vagus-sinoatrial node interactions. Am. J. Physiol. 245 (Heart Circ. Physiol. 14): H1043-H1053, 1983.
64. + current in amphibian atrial cells. Biophys. J. 45: 20-22, 1984.
65. Murphey, C., and J. Clark. Parasympathetic control of the SA node cell in rabbit heart - a model. In: Activation, Metabolism and Perfusion of the Heart, edited by S. Sideman and R. Beyar. Boston, MA: Martinus Nijhof, 1987, p. 41-59.
66. Nathanson, N. Molecular properties of the muscarinic acetylcholine receptor. Annu. Rev. Neurosci. 10: 195-236, 1987.
67. Noble, D., and S. Noble. A model of sino-atrial node electrical activity based on a modification of the DiFrancesco-Noble (1984) equations. Proc. R. Soc. Lond. B Biol. Sci. 222: 295-304, 1984.
68. Noma, A. GTP-binding proteins couple cardiac muscarinic receptors to potassium channels. Trends Neurosci. 9: 142-143, 1986.
69. + on the resting membrane potential of the rabbit sinoatrial node cell. Jpn. J. Physiol. 25: 287-302, 1975.
70. Opie, L. Intracellular calcium fluxes and sarcoplasmic reticulum. In: The Heart: Physiology and Metabolism. New York: Raven, 1991, chapt. 6, p. 127-146.
71. Osterrieder, W., A. Noma, and W. Trautwein. On the kinetics of the potassium current activated by acetylcholine in the SA node of the rabbit heart. Pflügers Arch. 386: 101-109, 1980.
72. Paulsen, R., J. Clark, P. Murphy, and J. Burdine. Sensitivity analysis and improved identification of a systemic arterial model. IEEE Trans. Biomed. Eng. 29: 164-178, 1982.
73. Peralta, E., A. Ashkenazi, J. Winslow, D. Smith, J. Ramachandran, and D. Capon. Distinct primary structures, ligand-binding properties and tissue-specific expression of four human muscarinic acetylcholine receptors. EMBO J. 6: 3923-3929, 1987.
74. Petit-Jacques, J., P. Bois, J. Bescond, and J. Lenfant. Mechanism of muscarinic control of the high-threshold calcium current in rabbit sino-atrial node myocytes. Pflügers Arch. 423: 21-27, 1993.
75. Purves, R. The time course of cellular responses to iontophoretically applied drugs. J. Theor. Biol. 65: 327-344, 1977.
76. Reid, J. The cardiac pacemaker: effects of regularly spaced nervous input. Am. Heart J. 78: 58-64, 1969.
77. a.Reuveny, E., P. Slesinger, J. Inglese, J. Morales, J. Inigeuzlluhi, R. Lefkowitz, H. Bourne, Y. Jan, and L. Jan. Activation of the cloned muscarinic potassium channel by G protein beta gamma subunits. Nature 370: 143-146, 1994.
78. Roberts, L. A., G. R. Slocum, and D. Riley. Morphological study of the innervation pattern of the rabbit sinoatrial node. Am. J. Anat. 185: 74-88, 1989.
79. + channels in isolated pacemaker cells of the mammalian heart. Nature 303: 250-253, 1983.
80. Schimerlik, M. Structure and regulation of muscarinic receptors. Annu. Rev. Physiol. 51: 217-227, 1989.
81. a.Schreibmayer, W., W. Dessauer, D. Vorobiov, A. Gilman, H. Lester, N. Davidson, and N. Dascal. Inhibition of an inwardly-rectifying K channel by G-protein α-subunits. Nature 380: 624-627, 1996.
82. Seyama, I. Characteristics of the anion channel in the sino-atrial node cell of the rabbit. J. Physiol. (Lond.) 294: 447-460, 1979.
83. Shibata, E., W. Giles, and G. Pollack. Threshold effects of acetylcholine on primary pacemaker cells of the rabbit sino-atrial node. Proc. R. Soc. Lond. B Biol. Sci. 223: 355-378, 1985.
84. Shumaker, J., J. Clark, and W. Giles. A model of phase sensitivity of the pacemaking cell in the bullfrog heart. J. Theor. Biol. 151: 193-230, 1991.
85. Slenter, V., J. Salata, and J. Jalife. Vagal control of pacemaker periodicity and intranodal conduction in the rabbit sinoatrial node. Circ. Res. 54: 436-446, 1984.
86. Spear, J., K. D. Kronhaus, E. Moore, and R. Kline. The effect of brief vagal stimulation on the isolated rabbit sinus node. Circ. Res. 44: 75-88, 1979.
87. Spear, J., and E. Moore. Influence of brief vagal and stellate nerve stimulation on pacemaker activity and conduction within the atrioventricular conduction system of the dog. Circ. Res. 32: 27-41, 1973.
88. Spear, J., and E. Moore. Patterns of atrial responses following vagally induced reentry in the isolated sinus node of the rabbit. In: Neural Mechanisms in Cardiac Arrhythmias. Perspectives in Cardiovascular Research, edited by P. Schwartz, A. Brown, A. Malliani, and A. Zanchetti. New York: Raven, 1978, p. 167-178.
89. Stuesse, S., M. Levy, and H. Zieske. Phase-related sensitivity of the sinoatrial node to vagal stimuli in the isolated rat atrium. Circ. Res. 43: 217-224, 1978.
90. Takano, M., and A. Noma. Distribution of the isoprenaline-induced chloride current in rabbit heart. Pflügers Arch. 420: 223-226, 1992.
91. Toda, N., and T. West. Changes in sino-atrial node transmembrane potentials on vagal stimulation of the isolated rabbit atrium. Nature 205: 808-809, 1965.
92. +, and vagal stimulation in S-A node of the rabbit. Am. J. Physiol. 212: 416-423, 1967.
93. Trautwein, W. Effects of acetylcholine on SA node of the heart. In: Cellular Pacemakers. I. Mechanisms and Pacemaker Generation, edited by D. Carpenter. New York: Wiley, 1981, p. 127-160.
94. f in single cells from rabbit sino-atrial node. J. Physiol. (Lond.) 434: 57-83, 1991.
95. Yatani, A., K. Okabe, J. Codina, L. Birnbaumer, and A. Brown. Heart rate regulation by G proteins acting on the cardiac pacemaker channel. Science 249: 1163-1166, 1990.
96. Yingst, D. Modulation of the Na,K-ATPase by Ca and intracellular proteins. Annu. Rev. Physiol. 50: 291-303, 1988.