Mapping cardiac pacemaker circuits: Methodological puzzles of the sinoatrial node optical mapping

Circulation Research

Volumn 106, Issue 2, 2010, Pages 255-271

  Efimov, Igor R ^a   Fedorov, Vadim V ^a   Joung, Boyoung ^b   Lin, Shien Fong ^b  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium; Optical mapping; Sinoatrial exit block; Sinoatrial node

Indexed keywords

ACTION POTENTIAL; CALCIUM CELL LEVEL; ELECTROCARDIOGRAPHY; HEART ELECTROPHYSIOLOGY; HEART MUSCLE; MEMBRANE CURRENT; MICROELECTRODE; PRIORITY JOURNAL; REVIEW; SIGNAL PROCESSING; SINUS NODE;

ANIMALS; CALCIUM; ELECTROCARDIOGRAPHY; ELECTROPHYSIOLOGY; HEART CONDUCTION SYSTEM; HUMANS; MODELS, CARDIOVASCULAR; MYOCARDIAL CONTRACTION; MYOCARDIUM; SINOATRIAL NODE;

EID: 76349106146     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.109.209841     Document Type: Review

References (104)

1. Keith A, Flack M. The form and nature of the muscular connection between the primary divisions of the vertebrate heart. J Anat Physiol. 1907;41:172-189.
2. Tawara S. Das Reizleitungssystem des Saugetierherzens: Eine Anatomische-Histologische Studie Uber Das Atrioventrikularbundel Und Die Purkinjeschen Faden. 1906. Jena, Germany: Verlag von Gustav Fischer.
3. Lewis T, Oppenheimer A, Oppenheimer BS. The site of origin of the mammalian heart beat: the pacemaker in the dog. Heart. 1910;II: 147-169
4. Wybauw. Archives Internationales de Physiologie. 1910;x:78.
5. Mangoni ME, Nargeot J. Genesis and regulation of the heart automa-ticity. Physiol Rev. 2008;88:919-982.
6. Lakatta EG, DiFrancesco D. What keeps us ticking: a funny current, a calcium clock, or both? J Mol Cell Cardiol. 2009;47:157-170.
7. Rosen MR. 15th annual Gordon K. Moe Lecture. Biological pace-making: in our lifetime? Heart Rhythm. 2005;2:418-428.
8. Efimov IR, Nikolski VP, Salama G. Optical imaging of the heart. Circ Res. 2004;95:21-33.
9. Baxter WT, Mironov SF, Zaitsev AV, Jalife J, Pertsov AM. Visualizing excitation waves inside cardiac muscle using transillumination. Biophys J. 2001;80:516-530.
10. Bray MA, Wikswo JP. Examination of optical depth effects on fluorescence imaging of cardiac propagation. Biophys J. 2003;85:4134-4145.
11. Bishop MJ, Rodriguez B, Qu F, Efimov IR, Gavaghan DJ, Trayanova NA. The role of photon scattering in optical signal distortion during arrhythmia and defibrillation. Biophys J. 2007;93:3714-3726.
12. Fedorov VV, Schuessler RB, Hemphill M, Ambrosi CM, Chang R, Voloshina AS, Brown K, Hucker WJ, Efimov IR. Structural and functional evidence for discrete exit pathways that connect the canine sino-atrial node and atria. Circ Res. 2009;104:915-923.
13. Joung B, Tang L, Maruyama M, Han S, Chen Z, Stucky M, Jones LR, Fishbein MC, Weiss JN, Chen PS, Lin SF. Intracellular calcium dynamics and acceleration of sinus rhythm by beta-adrenergic stimulation. Circulation. 2009;119:788-796.
14. James TN. Anatomy of the human sinus node. Anat Rec. 1961;141: 109-139.
15. James TN. Structure and function of the sinus node, AV node and His bundle of the human heart: part I-structure. Prog Cardiovasc Dis. 2002;45:235-267.
16. Truex RC, Smythe MQ, Taylor MJ. Reconstruction of the human sino-atrial node. Anat Rec. 1967;159:371-378.
17. James T. The connecting pathways between the sinus node and the A-V node and between the right and left atrium of the human heart. Am Heart J. 1963;66:498-508.
18. Eyster JAE, Meek WJ. Experiments on the origin and propagation of the impulse in the heart: point of primary negativity in the mammalian heart and the spread of negativity to other regions. Heart. 1913;5:119-136.
19. Meek WJ, Eyster J.A.E. The effect of vagal stimulation and of colling on the location of the pacemaker within the sino-auricular node. Am J Physiol. 1914;34:368-383.
20. Trautwein W, Zink K. [Membrane and action potentials of single myo-cardial fibers of cold and warmblooded animals.]. Pflugers Arch. 1952; 256:64-84.
21. de Carvalho AP, de Mello WC, Hoffman BF. Electrophysiological evidence for specialized fiber types in rabbit atrium. Am J Physiol. 1959;196:483-488.
22. Sano T, Yamagishi S. Spread of excitation from the sinus node. Circ Res. 1965;16:423-430.
23. Efimov IR, Fahy GJ, Cheng YN, Van Wagoner DR, Tchou PJ, Mazgalev TN. High resolution fluorescent imaging of rabbit heart does not reveal a distinct atrioventricular nodal anterior input channel (fast pathway) during sinus rhythm. J Cardiovasc Electrophysiol. 1997;8: 295-306.
24. Boyett MR, Honjo H, Yamamoto M, Nikmaram MR, Niwa R, Kodama I. Downward gradient in action potential duration along conduction path in and around the sinoatrial node. Am J Physiol. 1999;276:H686-H698.
25. Vinogradova TM, Fedorov VV, Yuzyuk TN, Zaitsev AV, Rosensh-traukh LV. Local cholinergic suppression of pacemaker activity in the rabbit sinoatrial node. J Cardiovasc Pharmacol. 1998;32:413-424.
26. Bleeker WK, Mackaay AJ, Masson-Pevet M, Bouman LN, Becker AE. Functional and morphological organization of the rabbit sinus node. Circ Res. 1980;46:11-22.
27. Fedorov VV, Hucker WJ, Dobrzynski H, Rosenshtraukh LV, Efimov IR. Postganglionic Nerve Stimulation Induces Temporal Inhibition of Excitability in the Rabbit Sinoatrial Node. Am J Physiol. 2006;291: H612-H623.
28. Shibata N, Inada S, Mitsui K, Honjo H, Yamamoto M, Niwa R, Boyett MR, Kodama I. Pacemaker shift in the rabbit sinoatrial node in response to vagal nerve stimulation. Exp Physiol. 2001;86:177-184.
29. Bromberg BI, Hand DE, Schuessler RB, Boineau JP. Primary negativity does not predict dominant pacemaker location: implications for sino-atrial conduction. Am J Physiol. 1995;269:H877-H887.
30. Kwong KF, Schuessler RB, Green KG, Laing JG, Beyer EC, Boineau JP, Saffitz JE. Differential expression of gap junction proteins in the canine sinus node. Circ Res. 1998;82:604-612.
31. James TN. Anatomy of the sinus node of the dog. Anat Rec. 1962;143: 251-265.
32. Boineau JP, Canavan TE, Schuessler RB, Cain ME, Corr PB, Cox JL. Demonstration of a widely distributed atrial pacemaker complex in the human heart. Circulation. 1988;77:1221-1237.
33. Verkerk AO, van Ginneken AC, Wilders R. Pacemaker activity of the human sinoatrial node: role of the hyperpolarization-activated current, I (f). Int J Cardiol. 2009;132:318-336.
34. Schuessler RB. Abnormal sinus node function in clinical arrhythmias. J Cardiovasc Electrophysiol. 2003;14:215-217.
35. Durrer D, Dam RTv, Freud GE, Janse MJ, Meijler FL, Arzbaecher RC. Total excitation of the isolated human heart. Circulation. 1970;41: 899-912.
36. Cosio FG, Martin-Penato A, Pastor A, Nunez A, Montero MA, Cantale CP, Schames S. Atrial activation mapping in sinus rhythm in the clinical electrophysiology laboratory: observations during Bachmann's bundle block. J Cardiovasc Electrophysiol. 2004;15:524-531.
37. Boineau JP, Schuessler RB, Mooney CR, Wylds AC, Miller CB, Hudson RD, Borremans JM, Brockus CW. Multicentric origin of the atrial depolarization wave: the pacemaker complex. Relation to dynamics of atrial conduction, P-wave changes and heart rate control. Circulation. 1978;58:1036-1048.
38. Fedorov VV, Glukhov AV, Chang R, Kostecki G, Alferol H, Wuskell J, Loew LM, Moazami N, Efimov IR. The origin of heartbeat in the human sinus node: evidence of sino-atrial exit pathways. Circulation. 2009;119.
39. Tuchin V. Tissue optics: light scattering methods and instruments for medical diagnosis. Bellingham, Wash: SPIE Press; 2007.
40. Efimov IR, Mazgalev TN. High-resolution three-dimensional fluorescent imaging reveals multilayer conduction pattern in the atrioventricular node. Circulation. 1998;98:54-57.
41. Efimov IR, Sidorov VY, Cheng Y, Wollenzier B. Evidence of 3D scroll waves with ribbon-shaped filament as a mechanism of ventricular tachycardia in the isolated rabbit heart. J Cardiovasc Electrophysiol. 1999;10:1452-1462.
42. Janks DL, Roth BJ. Averaging over depth during optical mapping of unipolar stimulation. IEEE Trans Biomed Eng. 2002;49:1051-1054.
43. Nikolski V, Efimov I. Fluorescent imaging of a dual-pathway atrioven-tricular-nodal conduction system. Circ Res. 2001;88:e23-e30.
44. Hyatt CJ, Mironov SF, Vetter FJ, Zemlin CW, Pertsov AM. Optical action potential upstroke morphology reveals near-surface transmural propagation direction. Circ Res. 2005;97:277-284.
45. Toda N, Shimamoto K. The influence of sympathetic stimulation on transmembrane potentials in the S-A node. J Pharmacol Exp Ther. 1968;159:298-305.
46. Brown HF, DiFrancesco D, Noble SJ. How does adrenaline accelerate the heart? Nature. 1979;280:235-236.
47. Baruscotti M, Bucchi A, DiFrancesco D. Physiology and pharmacology of the cardiac pacemaker ("funny") current. Pharmacol Ther. 2005;107: 59-79.
48. Rubenstein DS, Lipsius SL. Mechanisms of automaticity in subsidiary pacemakers from cat right atrium. Circ Res. 1989;64:648-657.
49. Hata T, Noda T, Nishimura M, Watanabe Y. The role of Ca2+ release from sarcoplasmic reticulum in the regulation of sinoatrial node automaticity. Heart Vessels. 1996;11:234-241.
50. Zhou Z, Lipsius SL. Na(+)-Ca2 + exchange current in latent pacemaker cells isolated from cat right atrium. J Physiol. 1993;466:263-285.
51. Rigg L, Terrar DA. Possible role of calcium release from the sarcoplasmic reticulum in pacemaking in guinea-pig sino-atrial node. Exp Physiol. 1996;81:877-880.
52. Li J, Qu J, Nathan RD. Ionic basis of ryanodine's negative chronotropic effect on pacemaker cells isolated from the sinoatrial node. Am J Physiol. 1997;273:H2481-H2489.
53. Ju YK, Allen DG. Intracellular calcium and Na +-Ca2+ exchange current in isolated toad pacemaker cells. J Physiol. 1998;508(pt 1):153-166.
54. Huser J, Blatter LA, Lipsius SL. Intracellular Ca2+ release contributes to automaticity in cat atrial pacemaker cells. J Physiol. 2000;524(pt 2):415-422.
55. Vinogradova TM, Bogdanov KY, Lakatta EG. beta-Adrenergic stimulation modulates ryanodine receptor Ca(2 +) release during diastolic depolarization to accelerate pacemaker activity in rabbit sinoatrial nodal cells. Circ Res. 2002;90:73-79.
56. Vinogradova TM, Bogdanov KY, Lakatta EG. Novel perspectives on the beating rate of the heart. Circ Res. 2002;91:e3.
57. Bogdanov KY, Vinogradova TM, Lakatta EG. Sinoatrial nodal cell ryanodine receptor and Na(+)-Ca(2 +) exchanger: molecular partners in pacemaker regulation. Circ Res. 2001;88:1254-1258.
58. Maltsev VA, Vinogradova TM, Lakatta EG. The emergence of a general theory of the initiation and strength of the heartbeat. J Pharmacol Sci. 2006;100:338-369.
59. Vinogradova TM, Lyashkov AE, Zhu W, Ruknudin AM, Sirenko S, Yang D, Deo S, Barlow M, Johnson S, Caffrey JL, Zhou YY, Xiao RP, Cheng H, Stern MD, Maltsev VA, Lakatta EG. High basal protein kinase A-dependent phosphorylation drives rhythmic internal Ca2 + store oscillations and spontaneous beating of cardiac pacemaker cells. Circ Res. 2006;98:505-514.
60. Verheijck EE, van Kempen MJ, Veereschild M, Lurvink J, Jongsma HJ, Bouman LN. Electrophysiological features of the mouse sinoatrial node in relation to connexin distribution. Cardiovasc Res. 2001;52:40-50.
61. Lei M, Jones SA, Liu J, Lancaster MK, Fung SS, Dobrzynski H, Camelliti P, Maier SK, Noble D, Boyett MR. Requirement of neuronal-and cardiac-type sodium channels for murine sinoatrial node pace-making. J Physiol. 2004;559:835-848.
62. Lancaster MK, Jones SA, Harrison SM, Boyett MR. Intracellular Ca2 + and pacemaking within the rabbit sinoatrial node: heterogeneity of role and control. J Physiol. 2004;556:481-494.
63. Tellez JO, Dobrzynski H, Greener ID, Graham GM, Laing E, Honjo H, Hubbard SJ, Boyett MR, Billeter R. Differential expression of ion channel transcripts in atrial muscle and sinoatrial node in rabbit. Circ Res. 2006;99:1384-1393.
64. Boineau JP, Miller CB, Schuessler RB, Roeske WR, Autry LJ, Wylds AC, Hill DA. Activation sequence and potential distribution maps demonstrating multicentric atrial impulse origin in dogs. Circ Res. 1984;54: 332-347.
65. Schuessler RB, Boineau JP, Wylds AC, Hill DA, Miller CB, Roeske WR. Effect of canine cardiac nerves on heart rate, rhythm, and pacemaker location. Am J Physiol. 1986;250:H630-H644.
66. Honjo H, Inada S, Lancaster MK, Yamamoto M, Niwa R, Jones SA, Shibata N, Mitsui K, Horiuchi T, Kamiya K, Kodama I, Boyett MR. Sarcoplasmic reticulum Ca2+ release is not a dominating factor in sinoatrial node pacemaker activity. Circ Res. 2003;92:e41-e44.
67. Nikmaram MR, Boyett MR, Kodama I, Suzuki R, Honjo H. Variation in effects of Cs +, UL-FS-49, and ZD-7288 within sinoatrial node. Am J Physiol. 1997;272:H2782-H2792.
68. Leitch SP, Sears CE, Brown HF, Paterson DJ. Effects of high potassium and the bradycardic agents ZD7288 and cesium on heart rate of rabbits and guinea pigs. J Cardiovasc Pharmacol. 1995;25:300-306.
69. Denyer JC, Brown HF. Pacemaking in rabbit isolated sino-atrial node cells during Cs+ block of the hyperpolarization-activated current if. J Physiol. 1990;429:401-409.
70. Joung B, Tang L, Han S, Maruyama M, Chen PS, Lin SF. Cellular mechanism underlying sick sinus syndromes in intact canine sinoatrial node. J Am Coll Cardio. 2009;53:A102.
71. Dobrzynski H, Boyett MR, Anderson RH. New insights into pacemaker activity: promoting understanding of sick sinus syndrome. Circulation. 2007;115:1921-1932.
72. Jones SA, Lancaster MK, Boyett MR. Ageing-related changes of con-nexins and conduction within the sinoatrial node. J Physiol. 2004;560: 429-437.
73. Jones SA, Boyett MR, Lancaster MK. Declining into failure: the age-dependent loss of the L-type calcium channel within the sinoatrial node. Circulation. 2007;115:1183-1190.
74. Verkerk AO, Wilders R, Coronel R, Ravesloot JH, Verheijck EE. Ionic remodeling of sinoatrial node cells by heart failure. Circulation. 2003; 108:760-766.
75. Sanders P, Kistler PM, Morton JB, Spence SJ, Kalman JM. Remodeling of sinus node function in patients with congestive heart failure: reduction in sinus node reserve. Circulation. 2004;110:897-903.
76. Elvan A, Wylie K, Zipes DP. Pacing-induced chronic atrial fibrillation impairs sinus node function in dogs. Electrophysiological remodeling. Circulation. 1996;94:2953-2960.
77. Hocini M, Sanders P, Deisenhofer I, Jais P, Hsu LF, Scavee C, Weera-soriya R, Raybaud F, Macle L, Shah DC, Garrigue S, Le Metayer P, Clementy J, Haissaguerre M. Reverse remodeling of sinus node function after catheter ablation of atrial fibrillation in patients with prolonged sinus pauses. Circulation. 2003;108:1172-1175.
78. Benson DW, Wang DW, Dyment M, Knilans TK, Fish FA, Strieper MJ, Rhodes TH, George AL Jr. Congenital sick sinus syndrome caused by recessive mutations in the cardiac sodium channel gene (SCN5A). J Clin Invest. 2003;112:1019-1028.
79. Veldkamp MW, Wilders R, Baartscheer A, Zegers JG, Bezzina CR, Wilde AA. Contribution of sodium channel mutations to bradycardia and sinus node dysfunction in LQT3 families. Circ Res. 2003;92: 976-983.
80. Milanesi R, Baruscotti M, Gnecchi-Ruscone T, DiFrancesco D. Familial sinus bradycardia associated with a mutation in the cardiac pacemaker channel. N Engl J Med. 2006;354:151-157.
81. Mohler PJ, Bennett V. Ankyrin-based cardiac arrhythmias: a new class of channelopathies due to loss of cellular targeting. Curr Opin Cardiol. 2005;20:189-193.
82. Bhuiyan ZA, Van Den Berg MP, van Tintelen JP, Bink-Boelkens MT, Wiesfeld AC, Alders M, Postma AV, van LI, Mannens MM, Wilde AA. Expanding spectrum of human RYR2-related disease: new electrocardiographic, structural, and genetic features. Circulation. 2007;116: 1569-1576.
83. Ogawa M, Zhou S, Tan AY, Song J, Gholmieh G, Fishbein MC, Luo H, Siegel RJ, Karagueuzian HS, Chen LS, Lin SF, Chen PS. Left stellate ganglion and vagal nerve activity and cardiac arrhythmias in ambulatory dogs with pacing-induced congestive heart failure. J Am Coll Cardiol. 2007;50:335-343.
84. Lakatta EG, Maltsev VA, Bogdanov KY, Stern MD, Vinogradova TM. Cyclic variation of intracellular calcium: a critical factor for cardiac pacemaker cell dominance. Circ Res. 2003;92:e45-e50.
85. Yeh YH, Burstein B, Qi XY, Sakabe M, Chartier D, Comtois P, Wang Z, Kuo CT, Nattel S. Funny current downregulation and sinus node dysfunction associated with atrial tachyarrhythmia: a molecular basis for tachycardia-bradycardia syndrome. Circulation. 2009;119:1576-1585.
86. Zicha S, Fernandez-Velasco M, Lonardo G, L'Heureux N, Nattel S. Sinus node dysfunction and hyperpolarization-activated (HCN) channel subunit remodeling in a canine heart failure model. Cardiovasc Res. 2005;66:472-481.
87. Joung B, Lin S-F, Chen Z, Antoun PS, Maruyama M, Han S, Piccirillo G, Stucky M, Zipes DP, Chen PS, Das MK. Mechanisms of sinoatrial node dysfunction in a canine model of pacing-induced atrial fibrillation. Heart Rhythm. September 16, 2009 [Epub ahead of print] PMID: 19914141.
88. Maltsev VA, Lakatta EG. Synergism of coupled subsarcolemmal Ca2 + clocks and sarcolemmal voltage clocks confers robust and flexible pacemaker function in a novel pacemaker cell model. Am J Physiol Heart Circ Physiol. 2009;296:H594-H615.
89. West TC. Ultramicroelectrode recording from the cardiac pacemaker. J Pharmacol Exp Ther. 1955;115:283-290.
90. de Carvalho AP, de Mello WC, Hoffman BF, eds. The Specialized Tissues of the Heart. Amsterdam, The Netherlands: Elsevier; 1961.
91. Kohlhardt M, Figulla HR, Tripathi O. The slow membrane channel as the predominant mediator of the excitation process of the sinoatrial pacemaker cell. Basic Res Cardiol. 1976;71:17-26.
92. Seyama I. Characteristics of the rectifying properties of the sino-atrial node cell of the rabbit. J Physiol. 1976;255:379-397.
93. James TN. Structure and function of the sinus node, AV node and his bundle of the human heart: part II-function. Prog Cardiovasc Dis. 2003;45:327-360.
94. Woods WT, Urthaler F, James TN. Spontaneous action potentials of cells in the canine sinus node. Circ Res. 1976;39:76-82.
95. Wiedmann RT, Tan RC, Joyner RW. Discontinuous conduction at Purkinje-ventricular muscle junction. Am J Physiol. 1996;271:H1507-H1516.
96. Bishop MJ, Bub G, Garny A, Gavaghan DJ, Rodriguez B. An investigation into the role of the optical detection set-up in the recording of cardiac optical mapping signals: A Monte Carlo simulation study. Physica D. 2009;238:1008-1018.
97. Bien H, Parikh P, Entcheva E. Lenses and effective spatial resolution in macroscopic optical mapping. Phys Med Biol. 2007;52:941-960.
98. Sedmera D, Reckova M, Rosengarten C, Torres MI, Gourdie RG, Thompson RP. Optical mapping of electrical activation in the developing heart. Microsc Microanal. 2005;11:209-215.
99. Danik SB, Rosner G, Lader J, Gutstein DE, Fishman GI, Morley GE. Electrical remodeling contributes to complex tachyarrhythmias in connexin43-deficient mouse hearts. FASEB J. 2008;22:1204-1212.
100. Morley GE, Vaidya D. Understanding conduction of electrical impulses in the mouse heart using high-resolution video imaging technology. Microsc Res Tech. 2001;52:241-250.
101. de Diego C, Chen F, Xie LH, Dave AS, Thu M, Rongey C, Weiss JN, Valderrabano M. Cardiac alternans in embryonic mouse ventricles. Am J Physiol Heart Circ Physiol. 2008;294:H433-H440.
102. Chandler NJ, Greener ID, Tellez JO, Inada S, Musa H, Molenaar P, DiFrancesco D, Baruscotti M, Longhi R, Anderson RH, Billeter R, Sharma V, Sigg DC, Boyett MR, Dobrzynski H. Molecular architecture of the human sinus node: insights into the function of the cardiac pacemaker. Circulation. 2009;119:1562-1575.
103. Bogdanov KY, Maltsev VA, Vinogradova TM, Lyashkov AE, Spurgeon HA, Stern MD, Lakatta EG. Membrane potential fluctuations resulting from submembrane Ca2 + releases in rabbit sinoatrial nodal cells impart an exponential phase to the late diastolic depolarization that controls their chronotropic state. Circ Res. 2006;99:979-987.
104. Fedorov VV, Lozinsky IT, Sosunov EA, Anyukhovsky EP, Rosen MR, Balke CW, Efimov IR. Application of blebbistatin as an excitation-contraction uncoupler for electrophysiologic study of rat and rabbit hearts. Heart Rhythm. 2007;4:619-626.