Myths and realities of the cardiac vagus

Journal of Physiology

Volumn 591, Issue 17, 2013, Pages 4073-4085

  Coote, J H ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; ACETYLCHOLINE M2 RECEPTOR; ACETYLCHOLINESTERASE; CHOLINE ACETYLTRANSFERASE; UNCLASSIFIED DRUG;

ACETYLCHOLINE RELEASE; ACTION POTENTIAL; ACTION POTENTIAL DURATION; ACTION POTENTIAL FORCE; ACTION POTENTIAL RHYTHM; ENZYME HISTOCHEMISTRY; FUNCTIONAL ANATOMY; HEART ATRIUM; HEART CONDUCTION; HEART CONTRACTION; HEART FUNCTION; HEART MUSCLE CELL; HEART MUSCLE EXCITABILITY; HEART MUSCLE POTENTIAL; HEART PHYSIOLOGY; HEART VENTRICLE; HEART VENTRICLE FUNCTION; HUMAN; IMMUNOHISTOCHEMISTRY; NERVE PLEXUS; NODOSE GANGLION; NONHUMAN; PARASYMPATHETIC GANGLION; PARASYMPATHETIC INNERVATION; PARASYMPATHETIC NERVE; PHENOTYPIC VARIATION; PHYSIOLOGY; POSTGANGLIONIC NERVE; PREGANGLIONIC NERVE; PRIORITY JOURNAL; REFRACTORY PERIOD; REVIEW; SYMPATHETIC TONE; VAGUS NERVE; VAGUS NERVE STIMULATION; ANIMAL; INNERVATION;

ANIMALS; HEART VENTRICLES; HUMANS; VAGUS NERVE; VENTRICULAR FUNCTION;

EID: 84883265774     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.257758     Document Type: Review

References (165)

1. Akiyama T & Yamazaki T (2001). Effect of right and left vagal stimulation on left ventricular acetylcholine levels in cat. Acta Physiol Scand 172, 11-16.
2. Akiyama T, Yamazaki T & Ninomiya I (1994). In vivo detection of endogenous acetylcholine release in cat ventricles. Am J Physiol Heart Circ Physiol 266, H854-H860.
3. Ardell JL & Randall WC (1986). Selective vagal innervation of sinoatrial and atrioventricular nodes in the canine heart. Am J Physiol Heart Circ Physiol 251, H764-H773.
4. Armour JA (2008). Potential clinical relevance of the 'little brain' on the mammalian heart. Exp Physiol 93, 165-176.
5. Batulevicius D, Pauziene N & Pauza DH (2005). Architecture and age-related analysis of the neuronal number of the guinea pig intrinsic cardiac nerve plexus. Ann Anat 187, 225-243.
6. Bermani A-W, Bloomquist EI & Montvilo JA (1982). Distribution of pulmonary cholinergic nerves in the rabbit. Thorax 37, 703-710.
7. Billman GE, Hoskins RS, Randall DC, Randall WC, Hamlin RL & Lin YC (1989). Selective vagal postganglionic innervation of the sinoatrial and atrioventricular nodes in the non-human primate. J Auton Nerv Syst 26, 27-36.
8. Blomquist TM, Priola DV & Romero AM (1987). Source of intrinsic innervation of the canine ventricles: a functional study. Am J Physiol Heart Circ Physiol 252, H638-H644.
9. Brack KE, Coote JH & Ng GA (2004). Interaction between direct sympathetic and vagus nerve stimulation on heart rate in the isolated rabbit heart. Exp Physiol 89, 128-139.
10. Brack KE, Coote JH & Ng GA (2006). The effect of direct autonomic nerve stimulation on left ventricular force in the isolated innervated Langendorff perfused rabbit heart. Auton Neurosci 124, 69-80.
11. Brack KE, Coote JH & Ng GA (2011). Vagus nerve stimulation protects against ventricular fibrillation independent of muscarinic receptor activation. Cardiovasc Res 91, 437-447.
12. Brack KE, Patel VH, Coote JH & Ng GA (2007). Nitric oxide mediates the vagal protective effect on ventricular fibrillation via effects on action potential duration restitution in the rabbit heart. J Physiol 583, 695-704.
13. Brack KE, Patel VH, Mantravardi R, Coote JH & Ng GA (2009). Direct evidence of nitric oxide release from neuronal nitric oxide synthase activation in the left ventricle as a result of cervical vagus nerve stimulation. J Physiol 587, 3045-3054.
14. Brack KE, Winter J & Ng GA (2012). Mechanisms underlying the autonomic modulation of ventricular fibrillation initiation-tentative prophylactic properties of vagus nerve stimulation on malignant arrhythmia in heart failure. Heart Fail Rev 18, 389-408.
15. Casadei B (2001). Vagal control of myocardial contractility in humans. Exp Physiol 86, 817-823.
16. Cechetto DF & Saper CB (1987). Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat. J Comp Neurol 262, 27-45.
17. Chang HY, Mashimo H & Goyal RK (2003). Musings of the wanderer: What's new in our understanding of vagal-vagal reflex? IV. Current concepts of vagal efferent projections to the gut. Am J Physiol Gastrointest Liver Physiol 284, G357-G366.
18. Cheng Z & Powley TL (2000). Nucleus ambiguus projections to cardiac ganglia of rat atria: an anterograde tracing study. J Comp Neurol 424, 588-606.
19. Cheng Z, Powley TL, Schwaber JS & Doyle FJ III (1999). Projections of the dorsal motor nucleus of the vagus to cardiac ganglia of rat atria: an anterograde tracing study. J Comp Neurol 410, 320-341.
20. Cheng Z, Zhang H, Guo SZ, Wurster R & Gozal D (2004). Differential control over postganglionic neurones in rat cardiac ganglia by NA and DmnX neurons: anatomical evidence. Am J Physiol Regul Integr Comp Physiol 286, R625-R633.
21. Cheshire WP & Saper CB (2006). The insular cortex and cardiac response to stroke. Neurology 66, 1296-1297.
22. Conlon K, Collins T & Kidd C (1996). Modulation of vagal actions on heart rate produced by inhibition of nitric oxide synthase in the anaesthetized ferret. Exp Physiol 81, 547-550.
23. Conlon K & Kidd C (1999). Neuronal nitric oxide facilitates vagal chronotropic and dromotropic actions on the heart. J Auton Nerv Syst 75, 136-146.
24. Cooper T (1965). Terminal innervation of the heart. In Nervous Control of the Heart, ed. Randall WC, pp. 130-153. Williams and Wilkins, Baltimore.
25. Coote JH (2004). The hypothalamus and cardiovascular regulation. In Neural Mechanisms of Cardiovascular Regulation, ed. Dun NJ, Machado BH & Pilowsky PM, pp. 117-146. Kluver, London.
26. Corbett EK, Batten TF, Kaye JC, Deuchars J & McWilliam PN (1999). Labelling of rat vagal preganglionic neurones by carbocyanine dye DiI applied to the heart. Neuroreport 10, 1177-1181.
27. Corr PB & Gillis RA (1974). Role of vagus nerves in cardiovascular changes induced by coronary occlusion. Circulation 49, 86-97.
28. Crick SJ, Anderson RH, Ho SY & Sheppard MN (1999). Localisation and quantitation of autonomic innervation in the porcine heart. II: endocardium, myocardium and epicardium. J Anat 195, 359-373.
29. Cullis W & Tribe EM (1913). Distribution of nerves in the heart. J Physiol 46, 141-150.
30. Daly I deBurgh & Hebb CO (1952). Pulmonary vasomotor fibres in the cervical vago-sympathetic nerve of the dog. Quart J Exp Physiol 37, 19-43.
31. Daly M deBurgh & Evans DLH (1953). Functional and histological changes in the vagus nerve of the cat after degenerative section at various levels. J Physiol 120, 579-595.
32. Daly M deBurgh & Kirkman E (1989). Differential modulation by pulmonary stretch afferents of some reflex cardioinhibitory responses in the cat. J Physiol 417, 323-241.
33. Darlington DN, Miyamoto M, Keil LC & Dallman MF (1989). Paraventricular stimulation with glutamate elicits bradycardia and pituitary responses. Am J Physiol Regul Integr Comp Physiol 256, R112-R119.
34. Davis F, Francis ETB & King TS (1952). Neurological studies of the cardiac ventricles of mammals. J Anat 86, 130-143.
35. Dawson TA, Li D, Woodward TD, Barber ZE, Wang L & Paterson DJ (2008). Cardiac cholinergic NO-cGMP signaling following acute myocardial infarction and nNOS gene transfer. Am J Physiol Heart Circ Physiol 295, H990-H998.
36. De Geest H, Levy MN & Zieske H (1964). Negative inotropic effect of the vagus nerves upon the canine ventricle. Science 144, 1223-1225.
37. Deighton NM, Motomera S, Borquez D, Zerkowski HR, Doetsch N & Brodde OE (1990). Muscarinic cholinoreceptors in the human heart: Demonstration, subclassification and distribution. Naunyn Schmiedebergs Arch Pharmacol 341, 14-21.
38. Dhein S, van Koppen CJ & Brodde OE (2001). Muscarinic receptors in the mammalian heart. Pharmacol Res 44, 161-182.
39. Dickerson LW, Rodak DJ, Fleming TJ, Gatti PJ, Massari VJ, McKenzie JC & Gillis RA (1998). Parasympathetic neurons in the cranial medial ventricular fat pad on the dog heart selectively decrease ventricular contractility. J Auton Nerv Syst 70, 129-141.
40. Dunlap ME, Bibevsky S, Rosenberry TL & Ernsberger P (2002). Mechanisms of altered vagal control in heart failure: influence of muscarinic receptors and acetylcholinesterase activity. Am J Physiol Heart Circ Physiol 285, H1362-H1640.
41. Edwards FR, Hirst GD, Klemm MF & Steele PA (1995). Different types of ganglion cell in the cardiac plexus of guinea-pigs. J Physiol 486, 453-471.
42. Eliakim M, Bellet S, Tawil E & Muller O (1961). Effect of vagal stimulation and acetylcholine on the ventricle. Circ Res 9, 1372-1379.
43. Evans DHL & Murray JG (1954). Histological and functional studies on the fibre composition of the vagus nerve of the rabbit. J Anat 88, 320-337.
44. Fields JZ, Roeske WR, Morkin E & Yamamura HI (1978). Cardiac muscarinic cholinergic receptors: biochemical identification and characterization. J Biol Chem 253, 3251-3258.
45. Ford TW, Bennett JA, Kidd C & McWilliam PN (1990). Neurones in the dorsal vagal motor nucleus of the cat with non-myelinated axons projecting to the heart and lungs. Exp Physiol 75, 459-473.
46. Ford TW & McWilliam PN (1986). The effects of electrical stimulation of myelinated and non-myelinated vagal fibres on heart rate in the rabbit. J Physiol 380, 341-347.
47. Fry CH, Meng E & Young JS (2010). The physiological function of lower urinary tract smooth muscle. Auton Neurosci 154, 3-13.
48. Garcia-Perez M & Jordan D (2001). Effect of stimulating non-myelinated vagal axons on atrio-ventricular conduction and left ventricular function in anaesthetized rabbits. Auton Neurosci 86, 183-191.
49. Gatti PJ, Johnson TA, McKenzie JC, Lauenstein JM, Gray A & Massari VJ (1997). Vagal control of left ventricular contractility is selectively mediated by a cranioventricular intracardiac ganglion in the cat. J Auton Nerv Syst 66, 138-144.
50. Gatti PJ, Johnson TA & Massari VJ (1996). Can neurons in the nucleus ambiguus selectively regulate cardiac rate and atrio-ventricular conduction J Auton Nerv Syst 57, 123-127.
51. Gatti PJ, Johnson TA, Phan P, Jordan IK, Coleman W & Massari VJ (1995). The physiological and anatomical demonstration of functionally selective parasympathetic ganglia located in discrete fat pads on the feline heart. J Auton Nerv Syst 51, 255-259.
52. Gill DS, Lintern MC, Wetherell J, Coote JH & Smith ME (2003). Guinea pig heart acetylcholinesterase after continuous physostigmine administration. Hum Exp Toxicol 22, 373-381.
53. Hancock SC, Hoover DB & Houghland MW (1987). Distribution of muscarinic receptors and acetylcholinesterase in rat heart. J Auton Nerv Syst 19, 59-66.
54. Harman MA & Reeves TJ (1968). Effects of efferent vagal stimulation on atrial and ventricular function. Am J Physiol 215, 1210-1217.
55. Harvey RD & Belevych AE (2003). Muscarinic regulation of cardiac ion channels. Br J Pharmacol 139, 1074-1084.
56. Heinbecker P & O'Leary J (1933a). Nature and function of certain fibres of the vagus-a new concept in peripheral nerve organization. Proc Soc Exp Biol Med 30, 506-508.
57. Heinbecker P & O'Leary J (1933b). The mammalian vagus nerve-a functional and histological study. Am J Physiol 106, 623-646.
58. Henning RJ & Levy MN (1991). Effects of autonomic nerve stimulation, asynchrony, and load on dP/dtmax and on dP/dtmin. Am J Physiol Heart Circ Physiol 260, H1290-H1298.
59. Herring N, Golding S & Paterson DJ (2000). Pre-synaptic NO-cGMP pathway modulates vagal control in isolated adult guinea pig atria. J Mol Cell Cardiol 32, 1795-1804.
60. Herring N & Paterson DJ (2001). Nitric oxide-cGMP pathway facilitates acetylcholine release and bradycardia during vagal nerve stimulation in the guinea-pig in vitro. J Physiol 535, 507-518.
61. Herring N & Paterson DJ (2009). Neuromodulators of peripheral cardiac sympatho-vagal balance. Exp Physiol 94, 46-53.
62. Higgins CB, Vatner SF & Braunwald E (1973). Parasympathetic control of the heart. Pharmacol Rev 25, 119-155.
63. Hirsch EF ( 1971). The Innervation of the Vertebrate Heart, pp. 80-101. Charles C Thomas Publisher, Springfield, IL, USA.
64. Hoover DB, Ganote CE, Ferguson SM, Blakely RD & Parsons RL (2004). Localization of cholinergic innervation in guinea-pig heart by immunohistochemistry for high-affinity choline transporters. Cardiovasc Res 62, 112-121.
65. Hoover DB, Isaacs ER, Jacques F, Hoard JL, Page P & Armour JA (2009). Localization of multiple neurotransmitters in surgically derived specimens of human atrial ganglia. Neuroscience 164, 1170-1179.
66. Hsieh JH, Chen RF, Wu JJ, Yen CT & Chai CY (1998). Vagal innervation of the gastrointestinal tract arises from dorsal motor nucleus while that of the heart largely from nucleus ambiguus. J Auton Nerv Syst 70, 38-50.
67. Itto M & Zipes DP (1994). Efferent sympathetic and vagal innervation of the canine right ventricle. Circulation 90, 1459-1468.
68. Izzo PN, Deuchars J & Spyer KM (1993). Localization of cardiac vagal preganglionic motoneurones in the rat: immunocytochemical evidence of synaptic inputs containing 5-hydroxytryptamine. J Comp Neurol 327, 572-583.
69. Jacobowitz DM, Cooper T & Barner HB (1967). Histochemical and chemical studies of the localization of adrenergic and cholinergic nerves in the normal and denervated cat hearts. Circ Res 20, 289-298.
70. Johnson TA, Gray AL, Lauestein JM, Newton SS & Massari VJ (2004). Parasympathetic control of the heart 1. An interventriculo-septal ganglion is the major source of the vagal intracardiac innervation of the ventricles. J Appl Physiol 96, 2265-2272.
71. Jones JFX (2001). Vagal control of the heart. Exp Physiol 86, 791-801.
72. Jones JFX, Wang Y & Jordan D (1995). Heart rate responses to selective stimulation of cardiac vagal C-fibres in anaesthetized cats and rabbits. J Physiol 489, 203-214.
73. Jones JFX, Wang Y & Jordan D (1998). Activity of C-fibre cardiac vagal efferents in anaesthetized cats and rats. J Physiol 507, 869-880.
74. Jordan D (2011). Parasympathetic preganglionic neurones. In Central Regulation of Autonomic Functions, ed. Llewellyn-Smith IJ & Verberne AJM, pp. 120-139. OUP, New York.
75. Jordan D, Khalid MEM, Schneiderman N & Spyer KM (1982). The location and properties of preganglionic vagal cardiomotor neurones in the rabbit. Pflugers Arch 395, 244-250.
76. Karnovsky MJ & Roots L (1964). A "direct colouring" thiocholine method for cholinesterases. J Histochem Cytochem 12, 219-221.
77. Kawano H, Okada R & Yano K (2003). Histological study on the distribution of autonomic nerves in human heart. Heart Vessels 18, 32-39.
78. Kaye MP, Geesbreght JM & Randall WC (1970). Distribution of autonomic nerves to the canine heart. Am J Physiol 218, 1025-1029.
79. Kent KM, Epstein SE, Cooper T & Jacobowitz DM (1974). Cholinergic innervation of the canine and human ventricular conducting system: Anatomic and electrophysiological correlations. Circulation 50, 948-955.
80. Kent KM, Smith ER, Redwood DR & Epstein SE (1973). Electrical stability of acutely ischemic myocardium. Influences of heart rate and vagal stimulation. Circulation 47, 291-298.
81. Klimaschewski L, Kummer W, Mayer B, Courand JY, Preissler U, Phillipin B & Heyin C (1992). Nitric oxide synthase in cardiac nerve fibers of rat and guinea-pig heart. Circ Res 71, 1533-1537.
82. Kolman BS, Verrier RL & Lown B (1975). The effect of vagus nerve stimulation upon vulnerability of the canine ventricle: Role of the sympathetic-parasympathetic interactions. Circulation 52, 578-585.
83. Kong S, Liu J-H, Ramage AG & Wang Y (2007). Cardiac vagal preganglionic neurones in the intermediate zone of the brainstem in anaesthetized cats. Exp Physiol 92, 1023-1028.
84. Levy MN (1977). Parasympathetric control of the heart. In Neural Regulation of the Heart, ed. Randall WC, pp. 97-129. OUP, New York.
85. Levy MN & Martin PJ (1996). Autonomic control of cardiac conduction and automaticity. In Nervous Control of the Heart, ed. Shepherd JT & Vatner SF, pp. 201-225. HAP, Amsterdam.
86. Levy MN & Schwartz PJ (2004). Vagal Control of the Heart: Experimental Basis and Clinical Implications. Futura, New York.
87. Levy MN & Zieske H (1969). Effect of enhanced contractility on the left ventricular response to vagus nerve stimulation in dogs. Circ Res 24, 303-311.
88. Lewis ME, Al-Khalidi AH, Bonser RS, Clutton-Brock T, Morton D, Paterson DJ & Coote JH (2001). Vagus nerve stimulation decreases left ventricular contractility in vivo in the human and pig heart. J Physiol 534, 547-552.
89. Li D, Wang L, Chee-Wan L, Dawson TA & Paterson DJ (2007). Noradrenergic cell specific gene transfer with neuronal nitric oxide synthase reduces cardiac sympathetic neurotransmission in hypertensive rats. Hypertension 50, 69-74.
90. Liu L & Nattel S (1997). Differing sympathetic and vagal effects on atrial fibrillation in dogs: role of refractoriness heterogeneity. Am J Physiol Heart Circ Physiol 273, H805-H816.
91. Luiten PGM, Ter Horst GJ, Karst H & Steffins AB (1985). The course of paraventricular hypothalamic efferents to autonomic structures in medulla and spinal cord. Brain Res 329, 374-378.
92. McAllen RM, Salo LM, Paton JFR & Pickering AE (2011). Processing of central and reflex drives by rat cardiac ganglion neurones: an intracellular analysis. J Physiol 589, 5801-5818.
93. McAllen RM & Spyer KM (1976). The location of cardiac vagal preganglionic motoneurones in the medulla of the cat. J Physiol 258, 187-204.
94. McSwiney BA & Spurrel WR (1933). The gastric fibres of the vagus nerve. J Physiol 77, 447-458.
95. McWilliam PN & Woolley DC (1988). The actions of myelinated and non-myelinated vagal fibres on atrial contraction in the rabbit. J Auton Nerv Syst 22, 67-73.
96. Martins JB & Zipes DP (1980a). Epicardial phenol interrupts refractory period responses to sympathetic but not vagal stimulation in canine left ventricular epicardium and endocardium. Circ Res 47, 33-40.
97. Martins JB & Zipes DP (1980b). Effects of sympathetic and vagal nerves on recovery properties of the endocardium and epicardium of the canine left ventricle. Circ Res 46, 100-110.
98. Martins JB & Zipes JB (1983). Distribution of local repolarization changes produced by efferent vagal stimulation in the canine ventricles. J Am Coll Cardiol 2, 1191-1199.
99. Massari VJ, Dickerson LW, Gray AL, Lauenstein J-M, Blinder KJ, Newsome JT, Rodak DJ, Fleming TJ, Gatti PJ & Gillis RA (1998). Neural control of left ventricular contractility in the dog heart: synaptic interactions of negative inotropic vagal preganglionic neurons in the nucleus ambiguus with tyrosine hydroxylase immunoreactive terminals. Brain Res 802, 205-220.
100. Massari VJ, Johnson TA & Gatti PJ (1995). Cardiotopic organization of the nucleus ambiguus? An anatomical and physiological analysis of neurons regulating atrioventricular conduction. Brain Res 679, 227-240.
101. Mittmann C, Pinkepank G, Stamatelopoulou S, Wieland T, Nürnberg B, Hirt S & Eschenhagen T (2003). Differential coupling of m-cholinoceptors to Gi/Go-proteins in failing human myocardium. J Mol Cell Cardiol 35, 1241-1249.
102. Mohan RM, Heaton DA, Danson EJF, Krishnan SPR, Cai S, Channon KM & Paterson DJ (2002). Neuronal nitric oxide synthase gene transfer promotes cardiac vagal gain of function. Circ Res 91, 1089-1091.
103. Myers RW, Pearlman AS, Hyman RM, Goldstein RA, Kent KM, Goldstein RE & Epstein SE (1974). Beneficial effects of vagal stimulation and bradycardia during experimental acute myocardial ischemia. Circulation 49, 943-947.
104. Nakano H, Furukawa Y, Inoue Y, Sawaki S, Oguchi T & Chiba S (1998). Right ventricular responses to vagal stimulation of fibers to discrete cardiac regions in dog hearts. J Auton Nerv Syst 74, 179-188.
105. Nalivaiko E, Antunes VR & Paton JFR (2009). Control of cardiac contractility in rat working heart-brain preparation. Exp Physiol 95, 107-119.
106. Ng GA, Brack KE & Coote JH (2001). Effect of direct sympathetic and vagus nerve stimulation on the physiology of the whole heart - a novel Langendorff perfused rabbit heart with intact dual autonomic innervation. Exp Physiol 86, 319-329.
107. Nonidez JF (1939). Studies on the innervation of the heart 1. Distribution of the cardiac nerves with special reference to the identification of sympathetic and parasympathetic postganglionics. Am J Anat 65, 361-413.
108. Nonidez JF (1943). The structure and innervation of the conductive system of the heart of the dog and Rhesus monkey, as seen with a silver impregnation technique. Am Heart J 26, 577-597.
109. Onkka P, Maskoun W, Rhee K-S, Hellyer J, Patel J, Tan J, Chen LS, Vinters HV, Fishbein MC & Chen P-S (2013). Sympathetic nerve fibers and ganglia in canine vagus nerves: Localization and quantitation. Heart Rhythm 10, 585-591.
110. Oppenheimer SM ( 2006). Cerebrogenic cardiac arrhythmias: cortical lateralization and clinical significance. Clin Auton Res 16, 6-11.
111. Oppenheimer SM & Cechetto DF (1990). Cardiac chronotropic organization of the rat insular cortex. Brain Res 533, 66-72.
112. Oppenheimer SM, Gebb AW, Girvan JP & Hachinski VC (1992). Cardiovascular effects of human insular stimulation. Neurology 42, 1727-1732.
113. Oppenheimer SM & Lima J (1998). Neurology and the heart. J Neurol Neurosurg Psychiatry 64, 289-297.
114. O'Shea JE & Evans BK (1985). Innervation of bat heart: cholinergic and adrenergic nerves innervate all chambers. Am J Physiol Heart Circ Physiol 249, H876-H882.
115. Pardini BJ, Patel KP, Schmid PG & Lund DD (1987). Location, distribution and projections of intracardiac ganglion cells in the rat. J Auton Nerv Syst 20, 91-101.
116. Patel VH, Brack KE, Coote JH & Ng GA (2008). A novel method of measuring the nitric oxide-dependent fluorescence using 4, 5-diaminofluorescein (DAF2) in the isolated Langendorff-perfused rabbit heart. Pflugers Arch 456, 635-645.
117. Paterson DJ ( 2001). Nitric oxide and the autonomic regulation of cardiac excitability. Exp Physiol 86, 1-12.
118. Paton JRF, Kasparov S & Paterson DJ (2002). Nitric oxide and autonomic control of heart rate: a question of specificity. Trends Neurosci 25, 626-631.
119. Pauza DH, Saburkina I, Rysevaite K, Inokaitis H, Jokubauskas M, Jalife J & Pauziene N (2013). Neuroanatomy of the murine cardiac conduction system. A combined stereomicroscopic and fluorescence immunohistochemical study. Auton Neurosci 176, 32-47.
120. Pauza DH, Skripka V & Pauziene N (2002). Morphology of the intrinsic cardiac nervous system in the dog: a whole-mount study employing histochemical staining with acetylcholinesterase. Cells Tissues Organs 172, 297-320.
121. Pauza DH, Skripka V, Pauziene N & Stropus R (2000). Morphology, distribution and variability of the epicardial neural ganglionated subplexuses in the human heart. Anat Rec 259, 353-382.
122. Persson K, Johansson K, Alm P, Larsson B & Andersson KE (1997). Morphological and functional evidence against a sensory and sympathetic origin of nitric oxide synthase-containing nerves in the rat lower urinary tract. Neuroscience 77, 271-281.
123. Priola DV, Spurgeon WA & Geis WP (1977). The intrinsic innervation of the canine heart. A functional study. Circ Res 40, 50-56.
124. Rabinowitz SH, Verrier RL & Lown B (1976). Muscarinic effects of vagosympathetic trunk stimulation on the repetitive extrasystole (RE) threshold. Circulation 53, 622-627.
125. Randall WC (1984). Nervous Control of Cardiovascular Function. OUP, New York.
126. Randall WC, Ardell JL, Calderwood D, Milosavljevic M & Goyal SC (1986a). Parasympathetic ganglia innervating the canine atrioventricular nodal region. J Auton Nerv Syst 16, 311-323.
127. Randall WC, Ardell JL, Wurster RD & Milosavljevic M (1987). Vagal postganglionic innervation of the canine sinoatrial node. J Auton Nerv Syst 20, 13-23.
128. Randall WC & Armour JA (1977). Gross and microscopic anatomy of the cardiac innervation. In Neural Regulation of the Heart, ed. Randall WC, pp. 15-41. OUP, New York.
129. Randall WC, Brown DR, McGuirt AS, Thompson GW, Armour JA & Ardell JL (2003). Interactions within the intrinsic cardiac nervous system contribute to chronotropic regulation. Am J Physiol Regul Integr Comp Physiol 285, R1066-R1075.
130. Randall WC, Milosavljevic M, Wurster RD, Geis GS & Ardell (1986b). Selective vagal innervation of the heart. Ann Clin Lab Sci 16, 198-208.
131. Randall WC, Wurster RD, Randall DC & Xi-Moy SX (1996). From cardioaccelerator and inhibitory nerves to a "heart brain": an evolution of concepts. In Nervous Control of the Heart, ed. Shepherd JT & Vatner SF, pp. 173-199. HAP, Amsterdam.
132. Richardson AP & Hinsey JC (1933). A functional study of the nodose ganglion of the vagus with various degeneration methods. Proc Soc Exp Biol Med 30, 1141-1143.
133. Rogers RC & Hermann GE (1986). Hypothalamic paraventricular nucleus stimulation-induced gastric acid secretion and bradycardia suppressed by oxytocin antagonist. Peptides 7, 695-700.
134. Rubino A, Hasall JS & Burnstock G (1996). Autonomic control of the myocardium: Non-adrenergic non-cholinergic (NANC) mechanisms. In Nervous Control of the Heart, ed. Shepherd JT & Vatner SF, pp. 139-171. HAP, Amsterdam.
135. Rysevaite K, Saburkina I, Pauziene N, Vaitkevicius R, Noujaim SF, Jalife J & Pauza DH (2011). Immunohistochemical characterization of the intrinsic cardiac neural plexus in whole-mount mouse heart preparations. Heart Rhythm 8, 732-739.
136. Saburkina I, Rysevaite K, Pauziene N, Mischke K, Schauerte P, Jalife J & Pauza DH (2010). Epicardial neural ganglionated plexus of ovine heart: anatomical basis for experimental cardiac electrophysiology and nerve protective cardiac surgery. Heart Rhythm 7, 942-950.
137. Sampaio KN, Mauad H, Spyer KM & Ford TW (2003). Differential chronotropic and dromotropic responses to focal stimulation of cardiac vagal ganglia in the rat. Exp Physiol 88, 315-327.
138. Samuels MA (2007). The brain-heart connection. Circulation 116, 77-84.
139. Sarnoff SJ, Brockman SK, Gilmore JP, Linden RJ & Mitchell JH (1960). Regulation of ventricular contraction: Influence of cardiac sympathetic and vagal nerve stimulation on atrial and ventricular dynamics. Circ Res 8, 1108-1122.
140. Sawchenko PE & Swanson LW (1982). Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat. J Comp Neurol 205, 260-272.
141. Schwartz PJ ( 1996). The autonomic nervous system and life-threatening arrhythmias. In Nervous Control of the Heart, ed. Shepherd JT & Vatner SF, pp. 329-356. HAP, Amsterdam.
142. Shimizu S, Akiyama T, Kawada T, Shishido T, Yamazaki T, Kamiya A, Mizuno M, Sano S & Sugimachi M (2009). In vivo direct monitoring of vagal acetylcholine release to the sinoatrial node. Auton Neurosci 148, 44-49.
143. Singh S, Johnson PI, Javed A, Gray TS, Lonchyna VA & Wurster RD (1999). Monoamine and histamine-synthesizing enzymes and neurotransmitters within neurons of adult human cardiac ganglia. Circulation 99, 411-419.
144. Singh S, Johnson PI, Lee RE, Orfei E, Lonchyna VA, Sullivan HJ, Montoya A, Tran H, Wehrmacher WH & Wurster RD (1996). Topography of cardiac ganglia in the adult human heart. J Thorac Cardiovasc Surg 112, 943-953.
145. Standish A, Enquist LW, Escardo JA & Schwaber JS (1995). Central neural circuit innervating the rat heart defined by neuronal transport of pseudorabies virus. J Neurosci 15, 1998-2012.
146. Syrota A, Comar D, Paillotin G, Davy J-M, Ammont M-C, Stulzaft O & Maziere B (1985). Muscarinic cholinergic receptor in the human heart evidenced under physiological conditions by positron emission tomography. Proc Natl Acad Sci U S A 82, 584-588.
147. Taggart P, Critchley H & Lambiase PD (2011). Heart-brain interactions in cardiac arrhythmia. Heart 97, 698-708.
148. Takanaga A, Hayakawa T, Tanaka K, Kawabata K, Maeda S & Seki M (2003). Immunohistochemical characterization of cardiac vagal preganglionic neurons in the rat. Auton Neurosci 106, 132-137.
149. Tanaka K, Hassal CJS & Burnstock G (1993). The distribution of intracardiac neurones and nerve terminals that contain a marker for nitric oxide, NADPH-diaphorase, in the guinea-pig heart. Cell Tissue Res 73, 293-300.
150. Tcheng KT (1951). Innervation of the dog's heart. Am Heart J 41, 512-524.
151. Ter Horst GJ, Hautvast RW, De Jongile MJ & Korf J (1996). Neuroanatomy of cardiac activity regulating circuitry: a transneuronal retrograde viral labeling study in the rat. Eur J Neurosci 8, 2029-2041.
152. Ulphani JS, Cain JH, Inderyas F, Gordan D, Gikas PV, Shade G, Mayor D, Arora R, Kadish AH & Goldberger JJ (2010). Quantitative analysis of parasympathetic innervation of the porcine heart. Heart Rhythm 7, 1113-1119.
153. Ventura S, Bavetta S, Milner P, Ralevic V & Burnstock G (1998). Nitric oxide synthase is co-located with vasoactive intestinal polypeptide in postganglionic parasympathetic nerves innervating the rat vas deferens. Neuroscience 83, 607-616.
154. Verrier RL & Lown B (1984). Behavioural stress and cardiac arrhythmias. Ann Rev Physiol 46, 155-176.
155. 2+]i in cardiac sympathetic neurons. J Mol Cell Cardiol 43, 717-725.
156. Wang Y, Jones JFX, Jeggo RD, Daly MB, Jordan D & Ramage AG (2000). Effect of pulmonary C-fibre activation on cardiac vagal neurones in the nucleus ambiguus in anaesthetized cats. J Physiol 526, 157-165.
157. Woolley DC, McWilliam PN, Ford TW & Clarke RW (1987). The effect of selective electrical stimulation of non-myelinated vagal fibres on heart rate in the rabbit. J Auton Nerv Syst 21, 215-221.
158. Xenopoulos NP & Applegate RJ (1994). The effect of vagal stimulation on left ventricular systolic and diastolic performance. Am J Physiol Heart Circ Physiol 266, H2167-H2173.
159. Yamada S, Yamamura HI & Roeske WR (1980). Alterations in cardiac autonomic receptors following 6-hydroxydopamine treatment in rats. Mol Pharmacol 18, 185-192.
160. Yang CM, Yeh HM, Sung TC, Chen FF & Wang YY (1992). Characterisation of muscarinic receptor subtypes in canine left ventricular membranes. J Recept Res 12, 427-449.
161. Yasahura O, Matsuo A, Bellier JP & Aimi Y (2007). Demonstration of choline acetyltransferase of a peripheral type in the rat heart. J Histochem Cytochem 55, 287-299.
162. Yuan B-X, Ardell JL, Hopkins DA & Armour JA (1994). Gross and microscopic anatomy of canine intrinsic cardiac neurons. Anat Rec 239, 75-87.
163. Zang W-J, Chen L-N & Yu X-J (2005). Progress in the study of vagal control of cardiac ventricles. Acta Physiol Sinica 57, 659-672.
164. Zhang ZH, Rashba S & Oppenheimer SM (1998). Insular cortex lesions alter baroreceptor sensitivity in the urethane anaesthetized rat. Brain Res 813, 73-81.
165. Zuanetti G, De Ferrari GM, Priori SG & Schwartz PJ (1987). Protective effect of vagal stimulation on reperfusion arrhythmias in cats. Circ Res 61, 429-435.