Neural control of the heart: Recent concepts and clinical correlations

Neurology

Volumn 83, Issue 3, 2014, Pages 261-271

  Palma, Jose Alberto ^a   Benarroch, Eduardo E ^b  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTONOMIC NERVOUS SYSTEM; BRAIN; HEART; HEART DISEASES; HUMANS; NERVOUS SYSTEM DISEASES;

EID: 84905859324     PISSN: 00283878     EISSN: 1526632X     Source Type: Journal    
DOI: 10.1212/WNL.0000000000000605     Document Type: Article

References (128)

1. Mangoni ME, Nargeot J. Genesis and regulation of the heart automaticity. Physiol Rev 2008;88:919-982.
2. Bucchi A, Barbuti A, Difrancesco D, Baruscotti M. Funny current, and cardiac rhythm: insights from HCN knockout and transgenic mouse models. Front Physiol 2012;3:240.
3. Joung B, Tang L, Maruyama M, et al. Intracellular calcium dynamics and acceleration of sinus rhythm by betaadrenergic stimulation. Circulation 2009;119:788-796.
4. Gao Z, Rasmussen TP, Li Y, et al. Genetic inhibition of Na1-Ca21 exchanger current disables fight or flight sinoatrial node activity without affecting resting heart rate. Circ Res 2013;112:309-317.
5. Mudd JO, Kass DA. Tackling heart failure in the twentyfirst century. Nature 2008;451:919-928.
6. Armour JA. Cardiac neuronal hierarchy in health and disease. Am J Physiol Regul Integr Comp Physiol 2004;287:R262-R271.
7. Kapa S, Venkatachalam KL, Asirvatham SJ. The autonomic nervous system in cardiac electrophysiology: an elegant interaction and emerging concepts. Cardiol Rev 2010;18:275-284.
8. Armour JA, Murphy DA, Yuan BX, Macdonald S, Hopkins DA. Gross and microscopic anatomy of the human intrinsic cardiac nervous system. Anat Rec 1997;247:289-298.
9. Hou Y, Scherlag BJ, Lin J, et al. Ganglionated plexi modulate extrinsic cardiac autonomic nerve input: effects on sinus rate, atrioventricular conduction, refractoriness, and inducibility of atrial fibrillation. J Am Coll Cardiol 2007;50:61-68.
10. Kawashima T. The autonomic nervous system of the human heart with special reference to its origin, course, and peripheral distribution. Anat Embryol 2005;209:425-438.
11. McAllen RM, Spyer KM. The location of cardiac vagal preganglionic motoneurones in the medulla of the cat. J Physiol 1976;258:187-204.
12. Ciriello J, Calaresu FR. Medullary origin of vagal preganglionic axons to the heart of the cat. J Auton Nerv Syst 1982;5:9-22.
13. Chiou CW, Eble JN, Zipes DP. Efferent vagal innervation of the canine atria and sinus and atrioventricular nodes: the third fat pad. Circulation 1997;95:2573-2584.
14. Coote JH. Myths and realities of the cardiac vagus. J Physiol 2013;591:4073-4085.
15. Stoebner R, Bellin DA, Haigney MC. Cardiac electrophysiology and the athlete: a primer for the sports clinician. Curr Sports Med Rep 2012;11:70-77.
16. Mighiu AS, Heximer SP. Controlling parasympathetic regulation of heart rate: a gatekeeper role for RGS proteins in the sinoatrial node. Front Physiol 2012;3:204.
17. Olshansky B, Sullivan RM. Inappropriate sinus tachycardia. J Am Coll Cardiol 2013;61:793-801.
18. Verrier RL, Josephson ME. Impact of sleep on arrhythmogenesis. Circ Arrhythm Electrophysiol 2009;2:450-459.
19. Eckberg DL. Point:counterpoint: respiratory sinus arrhythmia is due to a central mechanism vs. respiratory sinus arrhythmia is due to the baroreflex mechanism. J Appl Physiol 2009;106:1740-1742.
20. Berntson GG, Bigger JT Jr, Eckberg DL, et al. Heart rate variability: origins, methods, and interpretive caveats. Psychophysiology 1997;34:623-648.
21. Campos LA, Pereira VL Jr, Muralikrishna A, Albarwani S, Bras S, Gouveia S. Mathematical biomarkers for the autonomic regulation of cardiovascular system. Front Physiol 2013;4:279.
22. Guyenet PG. The sympathetic control of blood pressure. Nat Rev Neurosci 2006;7:335-346.
23. Sampaio KN, Mauad H, Michael Spyer K, Ford TW. Chronotropic and dromotropic responses to localized glutamate microinjections in the rat nucleus ambiguus. Brain Res 2014;1542:93-103.
24. Jean A. The nucleus tractus solitarius: neuroanatomic, neurochemical and functional aspects [in French]. Arch Int Physiol Biochim Biophys 1991;99:A3-A52.
25. Dampney RA, Horiuchi J. Functional organisation of central cardiovascular pathways: studies using c-fos gene expression. Prog Neurobiol 2003;71:359-384.
26. Hainsworth R. Cardiovascular control from cardiac and pulmonary vascular receptors. Exp Physiol 2014;99:312-319.
27. Saper CB. The central autonomic nervous system: conscious visceral perception and autonomic pattern generation. Annu Rev Neurosci 2002;25:433-469.
28. Cechetto DF. Central representation of visceral function. Fed Proc 1987;46:17-23.
29. Barbas H. Flow of information for emotions through temporal and orbitofrontal pathways. J Anat 2007;211: 237-249.
30. Ter Horst GJ, Postema F. Forebrain parasympathetic control of heart activity: retrograde transneuronal viral labeling in rats. Am J Physiol 1997;273:H2926-H2930.
31. Spyer KM. Annual Review Prize Lecture: central nervous mechanisms contributing to cardiovascular control. J Physiol 1994;474:1-19.
32. Barbas H, Saha S, Rempel-Clower N, Ghashghaei T. Serial pathways from primate prefrontal cortex to autonomic areas may influence emotional expression. BMC Neurosci 2003;4:25.
33. Verberne AJ, Owens NC. Cortical modulation of the cardiovascular system. Prog Neurobiol 1998;54:149-168.
34. Craig AD. How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 2009;10:59-70.
35. Critchley HD, Mathias CJ, Josephs O, et al. Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. Brain 2003;126:2139-2152.
36. Napadow V, Dhond R, Conti G, Makris N, Brown EN, Barbieri R. Brain correlates of autonomic modulation: combining heart rate variability with fMRI. Neuroimage 2008;42:169-177.
37. Gianaros PJ, Van Der Veen FM, Jennings JR. Regional cerebral blood flow correlates with heart period and highfrequency heart period variability during working-memory tasks: Implications for the cortical and subcortical regulation of cardiac autonomic activity. Psychophysiology 2004; 41:521-530.
38. Lane RD, McRae K, Reiman EM, Chen K, Ahern GL, Thayer JF. Neural correlates of heart rate variability during emotion. Neuroimage 2009;44:213-222.
39. Thayer JF, Ahs F, Fredrikson M, Sollers JJ III, Wager TD. A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neurosci Biobehav Rev 2012;36:747-756.
40. Penfield W, Faulk ME Jr. The insula: further observations on its function. Brain 1955;78:445-470.
41. Oppenheimer SM, Gelb A, Girvin JP, Hachinski VC. Cardiovascular effects of human insular cortex stimulation. Neurology 1992;42:1727-1732.
42. Macefield VG, James C, Henderson LA. Identification of sites of sympathetic outflow at rest and during emotional arousal: concurrent recordings of sympathetic nerve activity and fMRI of the brain. Int J Psychophysiol 2013;89:451-459.
43. Nieuwenhuys R. The insular cortex: a review. Prog Brain Res 2012;195:123-163.
44. Craig AD. The sentient self. Brain Struct Funct 2010; 214:563-577.
45. Craig AD. Significance of the insula for the evolution of human awareness of feelings from the body. Ann NY Acad Sci 2011;1225:72-82.
46. Zaki J, Davis JI, Ochsner KN. Overlapping activity in anterior insula during interoception and emotional experience. Neuroimage 2012;62:493-499.
47. Oppenheimer S. Cerebrogenic cardiac arrhythmias: cortical lateralization and clinical significance. Clin Auton Res 2006;16:6-11.
48. Nagai M, Hoshide S, Kario K. The insular cortex and cardiovascular system: a new insight into the brain-heart axis. J Am Soc Hypertens 2010;4:174-182.
49. Macey PM, Wu P, Kumar R, et al. Differential responses of the insular cortex gyri to autonomic challenges. Auton Neurosci 2012;168:72-81.
50. Vogt BA, Vogt L, Farber NB, Bush G. Architecture and neurocytology of monkey cingulate gyrus. J Comp Neurol 2005;485:218-239.
51. Seeley WW, Menon V, Schatzberg AF, et al. Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 2007;27:2349-2356.
52. Critchley HD. Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants. Int J Psychophysiol 2009;73:88-94.
53. Terreberry RR, Neafsey EJ. The rat medial frontal cortex projects directly to autonomic regions of the brainstem. Brain Res Bull 1987;19:639-649.
54. Hurley KM, Herbert H, Moga MM, Saper CB. Efferent projections of the infralimbic cortex of the rat. J Comp Neurol 1991;308:249-276.
55. Ahern GL, Sollers JJ, Lane RD, et al. Heart rate and heart rate variability changes in the intracarotid sodium amobarbital test. Epilepsia 2001;42:912-921.
56. LeDoux J. The amygdala. Curr Biol 2007;17:R868-R874.
57. Ulrich-Lai YM, Herman JP. Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 2009;10:397-409.
58. van der Kooy D, Koda LY, McGinty JF, Gerfen CR, Bloom FE. The organization of projections from the cortex, amygdala, and hypothalamus to the nucleus of the solitary tract in rat. J Comp Neurol 1984;224:1-24.
59. Kim MJ, Loucks RA, Palmer AL, et al. The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behav Brain Res 2011;223:403-410.
60. Saper CB, Loewy AD, Swanson LW, Cowan WM. Direct hypothalamo-autonomic connections. Brain Res 1976;117:305-312.
61. Coote JH. A role for the paraventricular nucleus of the hypothalamus in the autonomic control of heart and kidney. Exp Physiol 2005;90:169-173.
62. Stocker SD, Simmons JR, Stornetta RL, Toney GM, Guyenet PG. Water deprivation activates a glutamatergic projection from the hypothalamic paraventricular nucleus to the rostral ventrolateral medulla. J Comp Neurol 2006;494:673-685.
63. Dampney RA. Functional organization of central pathways regulating the cardiovascular system. Physiol Rev 1994;74:323-364.
64. Grimaldi D, Silvani A, Benarroch EE, Cortelli P. Orexin/ hypocretin system and autonomic control: new insights and clinical correlations. Neurology 2014;82: 271-278.
65. Ciriello J, de Oliveira CV. Cardiac effects of hypocretin-1 in nucleus ambiguus. Am J Physiol Regul Integr Comp Physiol 2003;284:R1611-R1620.
66. Dergacheva O, Philbin K, Bateman R, Mendelowitz D. Hypocretin-1 (orexin A) prevents the effects of hypoxia/hypercapnia and enhances the GABAergic pathway from the lateral paragigantocellular nucleus to cardiac vagal neurons in the nucleus ambiguus. Neuroscience 2011;175:18-23.
67. Sevoz-Couche C, Brouillard C, Camus F, et al. Involvement of the dorsomedial hypothalamus and the nucleus tractus solitarii in chronic cardiovascular changes associated with anxiety in rats. J Physiol 2013;591:1871-1887.
68. Kleiger RE, Stein PK, Bigger JT Jr. Heart rate variability: measurement and clinical utility. Ann Noninvasive Electrocardiol 2005;10:88-101.
69. Lahiri MK, Kannankeril PJ, Goldberger JJ. Assessment of autonomic function in cardiovascular disease: physiological basis and prognostic implications. J Am Coll Cardiol 2008;51:1725-1733.
70. Barron SA, Rogovski Z, Hemli J. Autonomic consequences of cerebral hemisphere infarction. Stroke 1994;25: 113-116.
71. Korpelainen JT, Sotaniemi KA, Makikallio A, Huikuri HV, Myllyla VV. Dynamic behavior of heart rate in ischemic stroke. Stroke 1999;30:1008-1013.
72. He L, Li C, Luo Y, Dong W, Yang H. Clinical prognostic significance of heart abnormality and heart rate variability in patients with stroke. Neurol Res 2010;32: 530-534.
73. Lakusic N, Mahovic D, Babic T. Gradual recovery of impaired cardiac autonomic balance within first six months after ischemic cerebral stroke. Acta Neurol Belg 2005;105:39-42.
74. Lotufo PA, Valiengo L, Bensenor IM, Brunoni AR. A systematic review and meta-analysis of heart rate variability in epilepsy and antiepileptic drugs. Epilepsia 2012;53: 272-282.
75. Tombul T, Anlar O, Tuncer M, Huseyinoglu N, Eryonucu B. Impaired heart rate variability as a marker of cardiovascular autonomic dysfunction in multiple sclerosis. Acta Neurol Belg 2011;111:116-120.
76. van Dijk JG, Haan J, Zwinderman K, Kremer B, van Hilten BJ, Roos RA. Autonomic nervous system dysfunction in Parkinson's disease: relationships with age, medication, duration, and severity. J Neurol Neurosurg Psychiatry 1993;56:1090-1095.
77. Kallio M, Haapaniemi T, Turkka J, et al. Heart rate variability in patients with untreated Parkinson's disease. Eur J Neurol 2000;7:667-672.
78. Verrier RL, Antzelevitch C. Autonomic aspects of arrhythmogenesis: the enduring and the new. Curr Opin Cardiol 2004;19:2-11.
79. Olshansky B. Interrelationships between the autonomic nervous system and atrial fibrillation. Prog Cardiovasc Dis 2005;48:57-78.
80. Lyon AR, Rees PS, Prasad S, Poole-Wilson PA, Harding SE. Stress (Takotsubo) cardiomyopathy: a novel pathophysiological hypothesis to explain catecholamineinduced acute myocardial stunning. Nat Clin Pract Cardiovasc Med 2008;5:22-29.
81. Wittstein IS, Thiemann DR, Lima JA, et al. Neurohumoral features of myocardial stunning due to sudden emotional stress. N Engl J Med 2005;352:539-548.
82. Yoshimura S, Toyoda K, Ohara T, et al. Takotsubo cardiomyopathy in acute ischemic stroke. Ann Neurol 2008;64:547-554.
83. Gelow J, Kruer M, Yadav V, Kaul S. Apical ballooning resulting from limbic encephalitis. Am J Med 2009;122: 583-586.
84. Lee VH, Connolly HM, Fulgham JR, Manno EM, Brown RD Jr, Wijdicks EF. Tako-tsubo cardiomyopathy in aneurysmal subarachnoid hemorrhage: an underappreciated ventricular dysfunction. J Neurosurg 2006;105: 264-270.
85. Stollberger C, Wegner C, Finsterer J. Seizure-associated Takotsubo cardiomyopathy. Epilepsia 2011;52:e160-e167.
86. Berganzo K, Ciordia R, Gomez-Esteban JC, et al. Takotsubo cardiomyopathy in a patient with bilateral lesions in the dorsal medulla. Clin Auton Res 2011;21:65-67.
87. Freeman R. Cardiovascular manifestations of autonomic epilepsy. Clin Auton Res 2006;16:12-17.
88. Moseley BD, Wirrell EC, Nickels K, Johnson JN, Ackerman MJ, Britton J. Electrocardiographic and oximetric changes during partial complex and generalized seizures. Epilepsy Res 2011;95:237-245.
89. Rugg-Gunn FJ, Simister RJ, Squirrell M, Holdright DR, Duncan JS. Cardiac arrhythmias in focal epilepsy: a prospective long-term study. Lancet 2004;364:2212-2219.
90. Blumhardt LD, Smith PE, Owen L. Electrocardiographic accompaniments of temporal lobe epileptic seizures. Lancet 1986;1:1051-1056.
91. Keilson MJ, Hauser WA, Magrill JP. Electrocardiographic changes during electrographic seizures. Arch Neurol 1989;46:1169-1170.
92. Leutmezer F, Schernthaner C, Lurger S, Potzelberger K, Baumgartner C. Electrocardiographic changes at the onset of epileptic seizures. Epilepsia 2003;44:348-354.
93. Marshall DW, Westmoreland BF, Sharbrough FW. Ictal tachycardia during temporal lobe seizures. Mayo Clinic Proc 1983;58:443-446.
94. Opherk C, Coromilas J, Hirsch LJ. Heart rate and EKG changes in 102 seizures: analysis of influencing factors. Epilepsy Res 2002;52:117-127.
95. Britton JW, Ghearing GR, Benarroch EE, Cascino GD. The ictal bradycardia syndrome: localization and lateralization. Epilepsia 2006;47:737-744.
96. Kerling F, Dutsch M, Linke R, Kuwert T, Stefan H, Hilz MJ. Relation between ictal asystole and cardiac sympathetic dysfunction shown by MIBG-SPECT. Acta Neurol Scand 2009;120:123-129.
97. Surges R, Scott CA, Walker MC. Enhanced QT shortening and persistent tachycardia after generalized seizures. Neurology 2010;74:421-426.
98. Seyal M, Pascual F, Lee CY, Li CS, Bateman LM. Seizure-related cardiac repolarization abnormalities are associated with ictal hypoxemia. Epilepsia 2011;52: 2105-2111.
99. Surges R, Jordan A, Elger CE. Ictal modulation of cardiac repolarization, but not of heart rate, is lateralized in mesial temporal lobe epilepsy. PLoS One 2013;8:e64765.
100. Parisi P, Oliva A, Coll Vidal M, et al. Coexistence of epilepsy and Brugada syndrome in a family with SCN5A mutation. Epilepsy Res 2013;105:415-418.
101. Partemi S, Cestele S, Pezzella M, et al. Loss-of-function KCNH2 mutation in a family with long QT syndrome, epilepsy, and sudden death. Epilepsia 2013;54:e112-e116.
102. Tomson T, Nashef L, Ryvlin P. Sudden unexpected death in epilepsy: current knowledge and future directions. Lancet Neurol 2008;7:1021-1031.
103. Ozdemir O, Hachinski V. Brain lateralization and sudden death: its role in the neurogenic heart syndrome. J Neurol Sci 2008;268:6-11.
104. Abboud H, Berroir S, Labreuche J, Orjuela K, Amarenco P. Insular involvement in brain infarction increases risk for cardiac arrhythmia and death. Ann Neurol 2006;59: 691-699.
105. Christensen H, Boysen G, Christensen AF, Johannesen HH. Insular lesions, ECG abnormalities, and outcome in acute stroke. J Neurol Neurosurg Psychiatry 2005;76: 269-271.
106. Colivicchi F, Bassi A, Santini M, Caltagirone C. Prognostic implications of right-sided insular damage, cardiac autonomic derangement, and arrhythmias after acute ischemic stroke. Stroke 2005;36:1710-1715.
107. Daniele O, Caravaglios G, Fierro B, Natale E. Stroke and cardiac arrhythmias. J Stroke Cerebrovasc Dis 2002;11: 28-33.
108. Gunther A, Salzmann I, Nowack S, et al. Heart rate variability: a potential early marker of sub-acute poststroke infections. Acta Neurol Scand 2012;126:189-196.
109. Bassi A, Colivicchi F, Santini M, Caltagirone C. Cardiac autonomic dysfunction and functional outcome after ischaemic stroke. Eur J Neurol 2007;14:917-922.
110. Ay H, Koroshetz WJ, Benner T, et al. Neuroanatomic correlates of stroke-related myocardial injury. Neurology 2006;66:1325-1329.
111. Laowattana S, Zeger SL, Lima JA, Goodman SN, Wittstein IS, Oppenheimer SM. Left insular stroke is associated with adverse cardiac outcome. Neurology 2006;66:477-483.
112. Goldstein DS. The electrocardiogram in stroke: relationship to pathophysiological type and comparison with prior tracings. Stroke 1979;10:253-259.
113. Hays A, Diringer MN. Elevated troponin levels are associated with higher mortality following intracerebral hemorrhage. Neurology 2006;66:1330-1334.
114. Maramattom BV, Manno EM, Fulgham JR, Jaffe AS, Wijdicks EF. Clinical importance of cardiac troponin release and cardiac abnormalities in patients with supratentorial cerebral hemorrhages. Mayo Clin Proc 2006;81: 192-196.
115. van Bree MD, Roos YB, van der Bilt IA, et al. Prevalence and characterization of ECG abnormalities after intracerebral hemorrhage. Neurocrit Care 2010;12:50-55.
116. Di Pasquale G, Andreoli A, Lusa AM, et al. Cardiologic complications of subarachnoid hemorrhage. J Neurosurg Sci 1998;42:33-36.
117. Di Pasquale G, Pinelli G, Andreoli A, Manini G, Grazi P, Tognetti F. Holter detection of cardiac arrhythmias in intracranial subarachnoid hemorrhage. Am J Cardiol 1987;59:596-600.
118. Kawahara E, Ikeda S, Miyahara Y, Kohno S. Role of autonomic nervous dysfunction in electrocardio-graphic abnormalities and cardiac injury in patients with acute subarachnoid hemorrhage. Circ J 2003;67:753-756.
119. van der Bilt IA, Hasan D, Vandertop WP, et al. Impact of cardiac complications on outcome after aneurismal subarachnoid hemorrhage: a meta-analysis. Neurology 2009;72:635-642.
120. Richard C. Stress-related cardiomyopathies. Ann Intensive Care 2011;1:39.
121. Kothavale A, Banki NM, Kopelnik A, et al. Predictors of left ventricular regional wall motion abnormalities after subarachnoid hemorrhage. Neurocrit Care 2006;4:199-205.
122. Chatterjee S. ECG changes in subarachnoid haemorrhage: a synopsis. Neth Heart J 2011;19:31-34.
123. van der Bilt I, Hasan D, van den Brink R, et al. Cardiac dysfunction after aneurysmal subarachnoid hemorrhage: relationship with outcome. Neurology 2014;82: 351-358.
124. Palma JA, Carmona-Abellan MM, Barriobero N, et al. Is cardiac function impaired in premotor Parkinson's disease? A retrospective cohort study. Mov Disord 2013;28:591-596.
125. Velseboer DC, de Haan RJ, Wieling W, Goldstein DS, de Bie RM. Prevalence of orthostatic hypotension in Parkinson's disease: a systematic review and meta-analysis. Parkinsonism Relat Disord 2011;17:724-729.
126. Palma JA, Urrestarazu E, Alegre M, et al. Cardiac autonomic impairment during sleep is linked with disease severity in Parkinson's disease. Clin Neurophysiol 2013;124:1163-1168.
127. Deguchi K, Sasaki I, Tsukaguchi M, et al. Abnormalities of rate-corrected QT intervals in Parkinson's disease: a comparison with multiple system atrophy and progressive supranuclear palsy. J Neurol Sci 2002;199:31-37.
128. Palma JA, Iriarte J, Alegre M, Valencia M, Artieda J, Urrestarazu E. Cardiac autonomic impairment during sleep as a marker of human prion diseases: a preliminary report. Clin Neurophysiol 2014;125:208-210..