Vagal nerve stimulation activates vagal afferent fibers that reduce cardiac efferent parasympathetic effects

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 309, Issue 9, 2015, Pages H1579-H1590

  Yamakawa, Kentaro ^a,b   Rajendran, Pradeep S ^a   Takamiya, Tatsuo ^a,b   Yagishita, Daigo ^a   So, Eileen L ^a   Mahajan, Aman ^a,b   Shivkumar, Kalyanam ^a   Vaseghi, Marmar ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Afferent cardiac neurotransmission; Electrophysiology; Parasympathetic; Vagotomy

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; FEMALE; HEART ELECTROPHYSIOLOGY; HEART HEMODYNAMICS; HEART MUSCLE POTENTIAL; HEART RATE; MALE; NEUROTRANSMISSION; NONHUMAN; PARASYMPATHETIC TONE; PR INTERVAL; PRIORITY JOURNAL; VAGUS NERVE; VAGUS NERVE STIMULATION; YORKSHIRE PIG; ACTION POTENTIAL; ANIMAL; CHOLINERGIC SYSTEM; DRUG EFFECTS; EFFERENT NERVE; HEART; HEART VENTRICLE; HEART VENTRICLE FUNCTION; HEMODYNAMICS; INNERVATION; PHYSIOLOGY; PIG; SENSORY NERVE; SURGERY; VAGOTOMY;

ATROPINE; CHOLINERGIC RECEPTOR BLOCKING AGENT;

ACTION POTENTIALS; AFFERENT PATHWAYS; ANIMALS; ATROPINE; EFFERENT PATHWAYS; FEMALE; HEART; HEART RATE; HEART VENTRICLES; HEMODYNAMICS; MALE; PARASYMPATHETIC NERVOUS SYSTEM; PARASYMPATHOLYTICS; SUS SCROFA; SWINE; VAGOTOMY; VAGUS NERVE; VAGUS NERVE STIMULATION; VENTRICULAR FUNCTION;

EID: 84946063708     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00558.2015     Document Type: Article

References (56)

1. Ajijola OA, Yagishita D, Patel KJ, Vaseghi M, Zhou W, Yamakawa K, So E, Lux RL, Mahajan A, Shivkumar K. Focal myocardial infarction induces global remodeling of cardiac sympathetic innervation: neural remodeling in a spatial context. Am J Physiol Heart Circ Physiol 305: H1031-H1040, 2013.
2. Ando M, Katare RG, Kakinuma Y, Zhang D, Yamasaki F, Muramoto K, Sato T. Efferent vagal nerve stimulation protects heart against ischemia- induced arrhythmias by preserving connexin43 protein. Circulation 112: 164-170, 2005.
3. Armour JA. The little brain on the heart. Cleve Clin J Med 74, Suppl 1: S48-S51, 2007.
4. Armour JA, Murphy DA, Yuan BX, Macdonald S, Hopkins DA. Gross and microscopic anatomy of the human intrinsic cardiac nervous system. Anat Rec 247: 289-298, 1997.
5. Barron KW, Bishop VS. The influence of vagal afferents on the left ventricular contractile response to intracoronary administration of catecholamines in the conscious dog. Circ Res 49: 159-169, 1981.
6. Brack KE, Coote JH, Ng GA. Vagus nerve stimulation protects against ventricular fibrillation independent of muscarinic receptor activation. Cardiovasc Res 91: 437-446, 2011.
7. Brack KE, Patel VH, Coote JH, Ng GA. 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, 2007.
8. Brooks WW, Verrier RL, Lown B. Influence of vagal tone on stellectomy- induced changes in ventricular electrical stability. Am J Physiol Heart Circ Physiol 234: H503-H507, 1978.
9. Chen LN, Zang WJ, Yu XJ, Liu J, Li DL, Kong SS, Lu J, Xu XL. Compensatory recovery of vagal control of hemodynamics after unilateral vagotomy. Physiol Res 57: 119-132, 2008.
10. Farrell TG, Paul V, Cripps TR, Malik M, Bennett ED, Ward D, Camm AJ. Baroreflex sensitivity and electrophysiological correlates in patients after acute myocardial infarction. Circulation 83: 945-952, 1991.
11. Haws CW, Lux RL. Correlation between in vivo transmembrane action potential durations and activation-recovery intervals from electrograms. Effects of interventions that alter repolarization time. Circulation 81: 281-288, 1990.
12. Herre JM, Thames MD. Responses of sympathetic nerves to programmed ventricular stimulation. J Am Coll Cardiol 9: 147-153, 1987.
13. Hirota K, Ishiko N. Influences of the sympathetic and parasympathetic nerve transection on cardiovascular reflexes induced by volleys in the IXth nerve fibers of rat. J Auton Nerv Syst 46: 237-249, 1994.
14. Hoover DB, Shepherd AV, Southerland EM, Armour JA, Ardell JL. Neurochemical diversity of afferent neurons that transduce sensory signals from dog ventricular myocardium. Auton Neurosci 141: 38-45, 2008.
15. Huang WA, Shivkumar K, Vaseghi M. Device-based autonomic modulation in arrhythmia patients: the role of vagal nerve stimulation. Curr Treat Options Cardiovasc Med 17: 379, 2015.
16. Hull SS Jr, Evans AR, Vanoli E, Adamson PB, Stramba-Badiale M, Albert DE, Foreman RD, Schwartz PJ. Heart rate variability before and after myocardial infarction in conscious dogs at high and low risk of sudden death. J Am Coll Cardiol 16: 978-985, 1990.
17. Imataka K, Yamaoki K, Seki A, Takayama Y, Fujii J. Peculiar mitral valve and papillary muscle lesions induced by vagus manipulations in rabbits. An experimental model for nonrheumatic mitral regurgitation. Jpn Heart J 27: 377-386, 1986.
18. James R, Arnold J, Allen JD, Pantridge JF, Shanks RG. The effects of heart rate, myocardial ischemia and vagal stimulation on the threshold for ventricular fibrillation. Circulation 55: 311-317, 1977.
19. Jellinek M, Kaye MP, Kaiser GC, Cooper T. Effect of cervical vagosympathectomy on myocardial catecholamine concentration. Am J Physiol 209: 951-954, 1965.
20. Kalia M, Sullivan JM. Brainstem projections of sensory and motor components of the vagus nerve in the rat. J Comp Neurol 211: 248-265, 1982.
21. Katare RG, Ando M, Kakinuma Y, Arikawa M, Handa T, Yamasaki F, Sato T. Vagal nerve stimulation prevents reperfusion injury through inhibition of opening of mitochondrial permeability transition pore independent of the bradycardiac effect. J Thorac Cardiovasc Surg 137: 223-231, 2009.
22. Kerzner J, Wolf M, Kosowsky BD, Lown B. Ventricular ectopic rhythms following vagal stimulation in dogs with acute myocardial infarction. Circulation 47: 44-50, 1973.
23. Kleiger RE, Miller JP, Bigger JT Jr, Moss AJ. Decreased heart rate variability and its association with increased mortality after acute myocardial infarction. Am J Cardiol 59: 256-262, 1987.
24. Kolman BS, Verrier RL, Lown B. The effect of vagus nerve stimulation upon vulnerability of the canine ventricle: role of sympathetic-parasympathetic interactions. Circulation 52: 578-585, 1975.
25. La Rovere MT, Bigger JT Jr, Marcus FI, Mortara A, Schwartz PJ. Baroreflex sensitivity and heart-rate variability in prediction of total cardiac mortality after myocardial infarction ATRAMI (Autonomic Tone and Reflexes After Myocardial Infarction) Investigators. Lancet 351: 478-484, 1998.
26. Maccanon DM, Horvath SM. Effect of bilateral cervical vagotomy in the dog. Am J Physiol 189: 569-572, 1957.
27. Matta RJ, Verrier RL, Lown B. Repetitive extrasystole as an index of vulnerability to ventricular fibrillation. Am J Physiol 230: 1469-1473, 1976.
28. Millar CK, Kralios FA, Lux RL. Correlation between refractory periods and activation-recovery intervals from electrograms: effects of rate and adrenergic interventions. Circulation 72: 1372-1379, 1985.
29. Ng GA, Brack KE, Coote JH. Effects of direct sympathetic and vagus nerve stimulation on the physiology of the whole heart-a novel model of isolated Langendorff perfused rabbit heart with intact dual autonomic innervation. Exp Physiol 86: 319-329, 2001.
30. Ng GA, Brack KE, Patel VH, Coote JH. Autonomic modulation of electrical restitution, alternans and ventricular fibrillation initiation in the isolated heart. Cardiovasc Res 73: 750-760, 2007.
31. Olgin JE, Takahashi T, Wilson E, Vereckei A, Steinberg H, Zipes DP. Effects of thoracic spinal cord stimulation on cardiac autonomic regulation of the sinus and atrioventricular nodes. J Cardiovasc Electrophysiol 13: 475-481, 2002.
32. Prechtl JC, Powley TL. The fiber composition of the abdominal vagus of the rat. Anat Embryol (Berl) 181: 101-115, 1990.
33. Randall WC, Armour JA. Complex cardiovascular responses to vagosympathetic stimulation. Proc Soc Exp Biol Med 145: 493-499, 1974.
34. Rosenshtraukh L, Danilo P, Anyukhovsky EP, Steinberg SF, Rybin V, Brittain-Valenti K, Molina-Viamonte V, Rosen MR. Mechanisms for vagal modulation of ventricular repolarization and of coronary occlusioninduced lethal arrhythmias in cats. Circ Res 75: 722-732, 1994.
35. Sabbah HN, Ilsar I, Zaretsky A, Rastogi S, Wang M, Gupta RC. Vagus nerve stimulation in experimental heart failure. Heart Fail Rev 16: 171-178, 2011.
36. Scherf D, Blumenfeld S, Yildiz M. Experimental study on ventricular extrasystoles provoked by vagal stimulation. Am Heart J 62: 670-675, 1961.
37. Scherlag BJ, Kabell G, Harrison L, Lazzara R. Mechanisms of bradycardia- induced ventricular arrhythmias in myocardial ischemia and infarction. Circulation 65: 1429-1434, 1982.
38. Schwartz PJ, Billman GE, Stone HL. Autonomic mechanisms in ventricular fibrillation induced by myocardial ischemia during exercise in dogs with healed myocardial infarction. An experimental preparation for sudden cardiac death. Circulation 69: 790-800, 1984.
39. Schwartz PJ, Pagani M, Lombardi F, Malliani A, Brown AM. A cardiocardiac sympathovagal reflex in the cat. Circ Res 32: 215-220, 1973.
40. Schwartz PJ, Verrier RL, Lown B. Effect of stellectomy and vagotomy on ventricular refractoriness in dogs. Circ Res 40: 536-540, 1977.
41. Shen MJ, Zipes DP. Role of the autonomic nervous system in modulating cardiac arrhythmias. Circ Res 114: 1004-1021, 2014.
42. Shinlapawittayatorn K, Chinda K, Palee S, Surinkaew S, Thunsiri K, Weerateerangkul P, Chattipakorn S, KenKnight BH, Chattipakorn N. Low-amplitude, left vagus nerve stimulation significantly attenuates ventricular dysfunction and infarct size through prevention of mitochondrial dysfunction during acute ischemia-reperfusion injury. Heart Rhythm 10: 1700-1707, 2013.
43. Standish A, Enquist LW, Schwaber JS. Innervation of the heart and its central medullary origin defined by viral tracing. Science 263: 232-234, 1994.
44. Takahashi N, Ito M, Ishida S, Fujino T, Saikawa T, Arita M. Effects of vagal stimulation on cesium-induced early afterdepolarizations and ventricular arrhythmias in rabbits. Circulation 86: 1987-1992, 1992.
45. Takahashi N, Ito M, Iwao T, Ohie T, Yonemochi H, Nakagawa M, Saikawa T, Sakata T. Vagal modulation of ventricular tachyarrhythmias induced by left ansae subclaviae stimulation in rabbits. Jpn Heart J 39: 503-511, 1998.
46. Takato T, Ashida T, Seko Y, Fujii J, Kawai S. Ventricular tachyarrhythmia- related basal cardiomyopathy in rabbits with vagal stimulation-a novel experimental model for inverted Takotsubo-like cardiomyopathy. J Cardiol 56: 85-90, 2010.
47. Vaseghi M, Shivkumar K. The role of the autonomic nervous system in sudden cardiac death. Prog Cardiovasc Dis 50: 404-419, 2008.
48. Vaseghi M, Yamakawa K, Sinha A, So EL, Zhou W, Ajijola OA, Lux RL, Laks M, Shivkumar K, Mahajan A. Modulation of regional dispersion of repolarization and T-peak to T-end interval by the right and left stellate ganglia. Am J Physiol Heart Circ Physiol 305: H1020-H1030, 2013.
49. WJ. Functional anatomy of the peripheral sympathetic and parasympathetic system. In: The Integrative Action of the Autonomic Nervous System: Neurobiology of Homeostasis. Cambridge, UK: Cambridge Univ Press, 2006, p. 13-34.
50. Waxman MB, Sharma AD, Asta J, Cameron DA, Wald RW. The protective effect of vagus nerve stimulation on catecholamine-halothaneinduced ventricular fibrillation in dogs. Can J Physiol Pharmacol 67: 801-809, 1989.
51. Weiss JL, Frederiksen JW, Weisfeldt ML. Hemodynamic determinants of the time-course of fall in canine left ventricular pressure. J Clin Invest 58: 751-760, 1976.
52. Yamakawa K, So EL, Rajendran PS, Hoang JD, Makkar N, Mahajan A, Shivkumar K, Vaseghi M. Electrophysiological effects of right and left vagal nerve stimulation on the ventricular myocardium. Am J Physiol Heart Circ Physiol 307: H722-H731, 2014.
53. Yoon MS, Han J, Tse WW, Rogers R. Effects of vagal stimulation, atropine, and propranolol on fibrillation threshold of normal and ischemic ventricles. Am Heart J 93: 60-65, 1977.
54. Zannad F, De Ferrari GM, Tuinenburg AE, Wright D, Brugada J, Butter C, Klein H, Stolen C, Meyer S, Stein KM, Ramuzat A, Schubert B, Daum D, Neuzil P, Botman C, Castel MA, D'Onofrio A, Solomon SD, Wold N, Ruble SB. Chronic vagal stimulation for the treatment of low ejection fraction heart failure: results of the NEural Cardiac TherApy foR Heart Failure (NECTAR-HF) randomized controlled trial. Eur Heart J 36: 425-433, 2015.
55. Zhao M, Sun L, Liu JJ, Wang H, Miao Y, Zang WJ. Vagal nerve modulation: a promising new therapeutic approach for cardiovascular diseases. Clin Exp Pharmacol Physiol 39: 701-705, 2012.
56. Zuanetti G, De Ferrari GM, Priori SG, Schwartz PJ. Protective effect of vagal stimulation on reperfusion arrhythmias in cats. Circ Res 61: 429-435, 1987.