pmc logo image
Logo of thijTHI JOURNAL WEBSITECurrent Issue.See also Cardiovascular Diseases Journal in PMC.SubscribeSubmissions

Formats:

Tex Heart Inst J. 1993; 20(3): 158–169.
PMCID: PMC325088
Brain-heart interactions. The neurocardiology of arrhythmia and sudden cardiac death.
A M Davis and B H Natelson
Department of Physical Medicine and Rehabilitation, UMDNJ-NJ Medical School, East Orange 07018.
Abstract
Neuroanatomic connections between the brain and the heart provide links that allow cardiac arrhythmias to occur in response to brain activation. Recognition and analysis of such links in the pathogenesis of malignant cardiac arrhythmia are emphasized in this review. Neurocardiac links have been shown to produce arrhythmia both experimentally and clinically; specific examples, including stroke, epilepsy, and environmental stress are presented. We hypothesize that the individual with a diseased heart has a greater likelihood of experiencing cardiac arrhythmia and sudden cardiac death when the neurocardiac axis is activated. Reviewing possible mechanisms of brain-related arrhythmias, we suggest that the nervous system directs the events leading to cardiac damage by raising catecholamine levels and potentially inducing arrhythmia.
Full text
Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (2.3M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
  • Natelson BH. Need for an integrative approach in medical diagnosis. Am J Med. 1986 Jun;80(6):1017–1018. [PubMed]
  • Natelson BH. Neurocardiology. An interdisciplinary area for the 80s. Arch Neurol. 1985 Feb;42(2):178–184. [PubMed]
  • Clark MB, Dwyer EM, Jr, Greenberg H. Sudden death during ambulatory monitoring. Analysis of six cases. Am J Med. 1983 Nov;75(5):801–806. [PubMed]
  • Savage HR, Kissane JQ, Becher EL, Maddocks WQ, Murtaugh JT, Dizadji H. Analysis of ambulatory electrocardiograms in 14 patients who experienced sudden cardiac death during monitoring. Clin Cardiol. 1987 Nov;10(11):621–632. [PubMed]
  • Greenberg HM. Bradycardia at onset of sudden death: potential mechanisms. Ann N Y Acad Sci. 1984;427:241–252. [PubMed]
  • Schmidinger H, Weber H. Sudden death during ambulatory Holter monitoring. Int J Cardiol. 1987 Aug;16(2):169–176. [PubMed]
  • Bayés de Luna A, Coumel P, Leclercq JF. Ambulatory sudden cardiac death: mechanisms of production of fatal arrhythmia on the basis of data from 157 cases. Am Heart J. 1989 Jan;117(1):151–159. [PubMed]
  • Olshausen KV, Witt T, Pop T, Treese N, Bethge KP, Meyer J. Sudden cardiac death while wearing a Holter monitor. Am J Cardiol. 1991 Feb 15;67(5):381–386. [PubMed]
  • Pepine CJ, Morganroth J, McDonald JT, Gottlieb SO. Sudden death during ambulatory electrocardiographic monitoring. Am J Cardiol. 1991 Sep 15;68(8):785–788. [PubMed]
  • Friedman M, Manwaring JH, Rosenman RH, Donlon G, Ortega P, Grube SM. Instantaneous and sudden deaths. Clinical and pathological differentiation in coronary artery disease. JAMA. 1973 Sep 10;225(11):1319–1328. [PubMed]
  • Spain DM, Bradess VA. Sudden death from coronary heart disease. Survival time, frequency of thrombi, and cigarette smoking. Chest. 1970 Aug;58(2):107–110. [PubMed]
  • Davies MJ, Thomas A. Thrombosis and acute coronary-artery lesions in sudden cardiac ischemic death. N Engl J Med. 1984 May 3;310(18):1137–1140. [PubMed]
  • James TN. Degenerative lesions of a coronary chemoreceptor and nearby neural elements in the hearts of victims of sudden death. J Am Coll Cardiol. 1986 Jul;8(1 Suppl A):12A–21A. [PubMed]
  • Shvalev VN, Vikhert AM, Stropus RA, Sosunov AA, Pavlovich ER, Kargina-Terentyeva RA, Zhuchkova NI, Anikin AYu, Maryan KL. Changes in neural and humoral mechanisms of the heart in sudden death due to myocardial abnormalities. J Am Coll Cardiol. 1986 Jul;8(1 Suppl A):55A–64A. [PubMed]
  • Stambler BS, Wood MA, Ellenbogen KA. Sudden death in patients with congestive heart failure: future directions. Pacing Clin Electrophysiol. 1992 Apr;15(4 Pt 1):451–470. [PubMed]
  • Abdalla IS, Prineas RJ, Neaton JD, Jacobs DR, Jr, Crow RS. Relation between ventricular premature complexes and sudden cardiac death in apparently healthy men. Am J Cardiol. 1987 Nov 1;60(13):1036–1042. [PubMed]
  • Lown B, DeSilva RA. Roles of psychologic stress and autonomic nervous system changes in provocation of ventricular premature complexes. Am J Cardiol. 1978 May 22;41(6):979–985. [PubMed]
  • Randall WC, Kaye MP, Hageman GR, Jacobs HK, Euler DE, Wehrmacher W. Cardiac dysrhythmias in the conscious dog after surgically induced autonomic imbalance. Am J Cardiol. 1976 Aug;38(2):178–183. [PubMed]
  • Wehrmacher WH, Talano JV, Kaye MP, Randall WC. The unbalanced heart. Animal models of cardiac dysrhythmias. Cardiology. 1979;64(2):65–74. [PubMed]
  • Lown B. Sudden cardiac death: the major challenge confronting contemporary cardiology. Am J Cardiol. 1979 Feb;43(2):313–328. [PubMed]
  • Lown B, Verrier RL, Rabinowitz SH. Neural and psychologic mechanisms and the problem of sudden cardiac death. Am J Cardiol. 1977 May 26;39(6):890–902. [PubMed]
  • Ruggiero DA, Mraovitch S, Granata AR, Anwar M, Reis DJ. A role of insular cortex in cardiovascular function. J Comp Neurol. 1987 Mar 8;257(2):189–207. [PubMed]
  • Oppenheimer SM, Cechetto DF. Cardiac chronotropic organization of the rat insular cortex. Brain Res. 1990 Nov 12;533(1):66–72. [PubMed]
  • Yasui Y, Breder CD, Saper CB, Cechetto DF. Autonomic responses and efferent pathways from the insular cortex in the rat. J Comp Neurol. 1991 Jan 15;303(3):355–374. [PubMed]
  • Cassell MD, Gray TS. The amygdala directly innervates adrenergic (C1) neurons in the ventrolateral medulla in the rat. Neurosci Lett. 1989 Feb 13;97(1-2):163–168. [PubMed]
  • Cechetto DF, Chen SJ. Subcortical sites mediating sympathetic responses from insular cortex in rats. Am J Physiol. 1990 Jan;258(1 Pt 2):R245–R255. [PubMed]
  • Allen GV, Cechetto DF. Functional and anatomical organization of cardiovascular pressor and depressor sites in the lateral hypothalamic area: I. Descending projections. J Comp Neurol. 1992 Jan 15;315(3):313–332. [PubMed]
  • Mastrianni JA, Palkovits M, Kunos G. Activation of brainstem endorphinergic neurons causes cardiovascular depression and facilitates baroreflex bradycardia. Neuroscience. 1989;33(3):559–566. [PubMed]
  • Sved AF, Felsten G. Stimulation of the locus coeruleus decreases arterial pressure. Brain Res. 1987 Jun 23;414(1):119–132. [PubMed]
  • Barraco RA, el-Ridi MR. Cardiorespiratory responses following electrical stimulation of caudal sites in the rat medulla. Brain Res Bull. 1989 Oct–Nov;23(4-5):299–310. [PubMed]
  • D'Agrosa LS. Cardiac arrhythmias of sympathetic origin in the dog. Am J Physiol. 1977 Nov;233(5):H535–H540. [PubMed]
  • Gillis RA, Pearle DL, Hoekman T. Failure of beta-adrenergic receptor blockade to prevent arrhythmias induced by sympathetic nerve stimulation. Science. 1974 Jul 5;185(4145):70–72. [PubMed]
  • Inoue H, Zipes DP. Results of sympathetic denervation in the canine heart: supersensitivity that may be arrhythmogenic. Circulation. 1987 Apr;75(4):877–887. [PubMed]
  • De Ferrari GM, Schwartz PJ. Autonomic nervous system and arrhythmias. Ann N Y Acad Sci. 1990;601:247–262. [PubMed]
  • Barber MJ, Mueller TM, Henry DP, Felten SY, Zipes DP. Transmural myocardial infarction in the dog produces sympathectomy in noninfarcted myocardium. Circulation. 1983 Apr;67(4):787–796. [PubMed]
  • Inoue H, Zipes DP. Time course of denervation of efferent sympathetic and vagal nerves after occlusion of the coronary artery in the canine heart. Circ Res. 1988 Jun;62(6):1111–1120. [PubMed]
  • Schwartz PJ, Vanoli E, Zaza A, Zuanetti G. The effect of antiarrhythmic drugs on life-threatening arrhythmias induced by the interaction between acute myocardial ischemia and sympathetic hyperactivity. Am Heart J. 1985 May;109(5 Pt 1):937–948. [PubMed]
  • Euler DE, Nattel S, Spear JF, Moore EN, Scanlon PJ. Effect of sympathetic tone on ventricular arrhythmias during circumflex coronary occlusion. Am J Physiol. 1985 Nov;249(5 Pt 2):H1045–H1050. [PubMed]
  • Vanoli E, De Ferrari GM, Stramba-Badiale M, Hull SS, Jr, Foreman RD, Schwartz PJ. Vagal stimulation and prevention of sudden death in conscious dogs with a healed myocardial infarction. Circ Res. 1991 May;68(5):1471–1481. [PubMed]
  • De Ferrari GM, Vanoli E, Stramba-Badiale M, Hull SS, Jr, Foreman RD, Schwartz PJ. Vagal reflexes and survival during acute myocardial ischemia in conscious dogs with healed myocardial infarction. Am J Physiol. 1991 Jul;261(1 Pt 2):H63–H69. [PubMed]
  • Amitzur G, Manoach M, Weinstock M. The influence of cardiac cholinergic activation on the induction and maintenance of ventricular fibrillation. Basic Res Cardiol. 1984 Nov–Dec;79(6):690–697. [PubMed]
  • Schwartz PJ, Vanoli E, Stramba-Badiale M, De Ferrari GM, Billman GE, Foreman RD. Autonomic mechanisms and sudden death. New insights from analysis of baroreceptor reflexes in conscious dogs with and without a myocardial infarction. Circulation. 1988 Oct;78(4):969–979. [PubMed]
  • Evans DE, Alter WA, 3rd, Shatsky SA, Gunby EN. Cardiac arrhythmias resulting from experimental head injury. J Neurosurg. 1976 Dec;45(6):609–616. [PubMed]
  • Evans DE, Kobrine AI, Rizzoli HV. Cardiac arrhythmias accompanying acute compression of the spinal cord. J Neurosurg. 1980 Jan;52(1):52–59. [PubMed]
  • McNair JL, Clower BR, Sanford RA. The effect of reserpine pretreatment on myocardial damage associated with simulated intracranial hemorrhage in mice. Eur J Pharmacol. 1970 Jan;9(1):1–6. [PubMed]
  • Hawkins WE, Clower BR. Myocardial damage after head trauma and simulated intracranial haemorrhage in mice: the role of the autonomic nervous system. Cardiovasc Res. 1971 Oct;5(4):524–529. [PubMed]
  • Shanlin RJ, Sole MJ, Rahimifar M, Tator CH, Factor SM. Increased intracranial pressure elicits hypertension, increased sympathetic activity, electrocardiographic abnormalities and myocardial damage in rats. J Am Coll Cardiol. 1988 Sep;12(3):727–736. [PubMed]
  • Uchida M, Saito K, Niitsu T, Okuda H. Model of electrocardiographic changes seen with subarachnoid hemorrhage in rabbits. Stroke. 1989 Jan;20(1):112–118. [PubMed]
  • Cechetto DF, Wilson JX, Smith KE, Wolski D, Silver MD, Hachinski VC. Autonomic and myocardial changes in middle cerebral artery occlusion: stroke models in the rat. Brain Res. 1989 Nov 20;502(2):296–305. [PubMed]
  • Smith KE, Hachinski VC, Gibson CJ, Ciriello J. Changes in plasma catecholamine levels after insula damage in experimental stroke. Brain Res. 1986 Jun 4;375(1):182–185. [PubMed]
  • Lathers CM, Schraeder PL, Weiner FL. Synchronization of cardiac autonomic neural discharge with epileptogenic activity: the lockstep phenomenon. Electroencephalogr Clin Neurophysiol. 1987 Sep;67(3):247–259. [PubMed]
  • Lathers CM, Schraeder PL. Autonomic dysfunction in epilepsy: characterization of autonomic cardiac neural discharge associated with pentylenetetrazol-induced epileptogenic activity. Epilepsia. 1982 Dec;23(6):633–647. [PubMed]
  • Goodman JH, Homan RW, Crawford IL. Kindled seizures elevate blood pressure and induce cardiac arrhythmias. Epilepsia. 1990 Sep–Oct;31(5):489–495. [PubMed]
  • Mameli P, Mameli O, Tolu E, Padua G, Giraudi D, Caria MA, Melis F. Neurogenic myocardial arrhythmias in experimental focal epilepsy. Epilepsia. 1988 Jan–Feb;29(1):74–82. [PubMed]
  • Hod M, Diamant YZ. The offspring of a diabetic mother--short- and long-range implications. Isr J Med Sci. 1992 Feb;28(2):81–86. [PubMed]
  • Evans DE, Gillis RA. Effect of diphenylhydantoin and lidocaine on cardiac arrhythmias induced by hypothalamic stimulation. J Pharmacol Exp Ther. 1974 Dec;191(3):506–517. [PubMed]
  • Oppenheimer SM, Wilson JX, Guiraudon C, Cechetto DF. Insular cortex stimulation produces lethal cardiac arrhythmias: a mechanism of sudden death? Brain Res. 1991 May 31;550(1):115–121. [PubMed]
  • Kujime K, Natelson BH. Effects of stellectomy on cardiac rhythm disturbances induced by ouabain in guinea pigs. J Pharmacol Exp Ther. 1984 Apr;229(1):113–117. [PubMed]
  • Markgraf CG, Kapp BS. Lesions of the amygdaloid central nucleus block conditioned cardiac arrhythmias in the rabbit receiving digitalis. J Auton Nerv Syst. 1991 Jun 1;34(1):37–45. [PubMed]
  • Natelson BH. Stress, predisposition and the onset of serious disease: implications about psychosomatic etiology. Neurosci Biobehav Rev. 1983 Winter;7(4):511–527. [PubMed]
  • Chinn C, Natelson BH. Termination of ouabain-induced cardiac arrhythmias by anterior hypothalamic stimulation. Res Commun Chem Pathol Pharmacol. 1984 Feb;43(2):203–208. [PubMed]
  • Somberg JC, Smith TW. Localization of the neurally mediated arrhythmogenic properties of digitalis. Science. 1979 Apr 20;204(4390):321–323. [PubMed]
  • Thron CD, Riancho JA, Borison HL. Lack of protection against ouabain cardiotoxicity after chronic ablation of the area postrema in cats. Exp Neurol. 1984 Sep;85(3):574–583. [PubMed]
  • Skinner JE, Reed JC. Blockade of frontocortical-brain stem pathway prevents ventricular fibrillation of ischemic heart. Am J Physiol. 1981 Feb;240(2):H156–H163. [PubMed]
  • Carpeggiani C, Landisman C, Montaron MF, Skinner JE. Cryoblockade in limbic brain (amygdala) prevents or delays ventricular fibrillation after coronary artery occlusion in psychologically stressed pigs. Circ Res. 1992 Mar;70(3):600–606. [PubMed]
  • Rabkin SW. Morphine and the endogenous opioid dynorphin in the brain attenuate digoxin-induced arrhythmias in guinea pigs. Pharmacol Toxicol. 1992 Nov;71(5):353–360. [PubMed]
  • Strawn WB, Bondjers G, Kaplan JR, Manuck SB, Schwenke DC, Hansson GK, Shively CA, Clarkson TB. Endothelial dysfunction in response to psychosocial stress in monkeys. Circ Res. 1991 May;68(5):1270–1279. [PubMed]
  • Johansson G, Jonsson L, Lannek N, Blomgren L, Lindberg P, Poupa O. Severe stress-cardiopathy in pigs. Am Heart J. 1974 Apr;87(4):451–457. [PubMed]
  • Natelson BH, Cagin NA. The role of shock predictability during aversive conditioning in producing psychosomatic digitalis toxicity. Psychosom Med. 1981 Jun;43(3):191–197. [PubMed]
  • Cagin NA, Natelson BH. Cholinergic activation produces psychosomatic digitalis toxicity. J Pharmacol Exp Ther. 1981 Sep;218(3):709–711. [PubMed]
  • Natelson BH, Grover E, Cagin NA, Ottenweller JE, Tapp WN. Learned fear: a cause of arrhythmia onset in the presence of digitalis. Pharmacol Biochem Behav. 1989 Jun;33(2):431–434. [PubMed]
  • Randall DC, Hasson DM. Cardiac arrhythmias in the monkey during classically conditioned fear and excitement. Pavlov J Biol Sci. 1981 Apr–Jun;16(2):97–107. [PubMed]
  • Corbalan R, Verrier R, Lown B. Psychological stress and ventricular arrhythmias during myocardial infarction in the conscious dog. Am J Cardiol. 1974 Nov;34(6):692–696. [PubMed]
  • Rosenfeld J, Rosen MR, Hoffman BF. Pharmacologic and behavioral effects on arrhythmias that immediately follow abrupt coronary occlusion: a canine model of sudden coronary death. Am J Cardiol. 1978 May 22;41(6):1075–1082. [PubMed]
  • Kirby DA, Pinto JM, Hottinger S, Johnson DA, Lown B. Behavioral arousal enhances inducibility and rate of ventricular tachycardia. Am J Physiol. 1991 Dec;261(6 Pt 2):H1734–H1739. [PubMed]
  • Pinto JM, Kirby DA, Maher TJ, Lown B. Decreases in repetitive extrasystole threshold in the conscious pig with myocardial infarct were reversed by tyrosine. Life Sci. 1991;49(6):419–426. [PubMed]
  • Tapp WN, Natelson BH, Creighton D, Khazam C, Ottenweller JE. Alprazolam reduces stress-induced mortality in cardiomyopathic hamsters. Pharmacol Biochem Behav. 1989 Jan;32(1):331–336. [PubMed]
  • Tapp WN, Natelson BH. Verapamil sensitizes cardiomyopathic hamsters to the effects of stress. Res Commun Chem Pathol Pharmacol. 1988 Dec;62(3):511–514. [PubMed]
  • Schwartz PJ. Idiopathic long QT syndrome: progress and questions. Am Heart J. 1985 Feb;109(2):399–411. [PubMed]
  • Tapp WN, Knox FS, 3rd, Natelson BH. The heart rate spectrum in simulated flight: reproducibility and effects of atropine. Aviat Space Environ Med. 1990 Oct;61(10):887–892. [PubMed]
  • 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. 1987 Feb 1;59(4):256–262. [PubMed]
  • Rich MW, Saini JS, Kleiger RE, Carney RM, teVelde A, Freedland KE. Correlation of heart rate variability with clinical and angiographic variables and late mortality after coronary angiography. Am J Cardiol. 1988 Oct 1;62(10 Pt 1):714–717. [PubMed]
  • Akselrod S, Gordon D, Ubel FA, Shannon DC, Berger AC, Cohen RJ. Power spectrum analysis of heart rate fluctuation: a quantitative probe of beat-to-beat cardiovascular control. Science. 1981 Jul 10;213(4504):220–222. [PubMed]
  • Cornélissen G, Bakken E, Delmore P, Orth-Gomér K, Akerstedt T, Carandente O, Carandente F, Halberg F. From various kinds of heart rate variability to chronocardiology. Am J Cardiol. 1990 Oct 1;66(10):863–868. [PubMed]
  • Aharon-Peretz J, Harel T, Revach M, Ben-Haim SA. Increased sympathetic and decreased parasympathetic cardiac innervation in patients with Alzheimer's disease. Arch Neurol. 1992 Sep;49(9):919–922. [PubMed]
  • Porges SW. Vagal tone: a physiologic marker of stress vulnerability. Pediatrics. 1992 Sep;90(3 Pt 2):498–504. [PubMed]
  • Dougherty CM, Burr RL. Comparison of heart rate variability in survivors and nonsurvivors of sudden cardiac arrest. Am J Cardiol. 1992 Aug 15;70(4):441–448. [PubMed]
  • Van Hoogenhuyze D, Weinstein N, Martin GJ, Weiss JS, Schaad JW, Sahyouni XN, Fintel D, Remme WJ, Singer DH. Reproducibility and relation to mean heart rate of heart rate variability in normal subjects and in patients with congestive heart failure secondary to coronary artery disease. Am J Cardiol. 1991 Dec 15;68(17):1668–1676. [PubMed]
  • Binder T, Frey B, Porenta G, Heinz G, Wutte M, Kreiner G, Gössinger H, Schmidinger H, Pacher R, Weber H. Prognostic value of heart rate variability in patients awaiting cardiac transplantation. Pacing Clin Electrophysiol. 1992 Nov;15(11 Pt 2):2215–2220. [PubMed]
  • Andreoli A, di Pasquale G, Pinelli G, Grazi P, Tognetti F, Testa C. Subarachnoid hemorrhage: frequency and severity of cardiac arrhythmias. A survey of 70 cases studied in the acute phase. Stroke. 1987 May–Jun;18(3):558–564. [PubMed]
  • Stober T, Sen S, Anstätt T, Bette L. Correlation of cardiac arrhythmias with brainstem compression in patients with intracerebral hemorrhage. Stroke. 1988 Jun;19(6):688–692. [PubMed]
  • Bashour TT, Cohen MS, Ryan C, Antonini C., Sr Sinus node suppression in acute strokes--case reports. Angiology. 1988 Dec;39(12):1048–1055. [PubMed]
  • Oppenheimer SM, Hachinski VC. The cardiac consequences of stroke. Neurol Clin. 1992 Feb;10(1):167–176. [PubMed]
  • Terrence CF, Jr, Wisotzkey HM, Perper JA. Unexpected, unexplained death in epileptic patients. Neurology. 1975 Jun;25(6):594–598. [PubMed]
  • Leestma JE, Walczak T, Hughes JR, Kalelkar MB, Teas SS. A prospective study on sudden unexpected death in epilepsy. Ann Neurol. 1989 Aug;26(2):195–203. [PubMed]
  • Lane RD, Wallace JD, Petrosky PP, Schwartz GE, Gradman AH. Supraventricular tachycardia in patients with right hemisphere strokes. Stroke. 1992 Mar;23(3):362–366. [PubMed]
  • Oppenheimer S. Cardiac dysfunction during seizures and the sudden epileptic death syndrome. J R Soc Med. 1990 Mar;83(3):134–136. [PubMed]
  • Marshall DW, Westmoreland BF, Sharbrough FW. Ictal tachycardia during temporal lobe seizures. Mayo Clin Proc. 1983 Jul;58(7):443–446. [PubMed]
  • Gilchrist JM. Arrhythmogenic seizures: diagnosis by simultaneous EEG/ECG recording. Neurology. 1985 Oct;35(10):1503–1506. [PubMed]
  • Keilson MJ, Hauser WA, Magrill JP, Goldman M. ECG abnormalities in patients with epilepsy. Neurology. 1987 Oct;37(10):1624–1626. [PubMed]
  • PHIZACKERLEY PJ, POOLE EW, WHITTY CW. Sino-auricular heart block as an epileptic manifestation; a case report. Epilepsia. 1954 Nov;3:89–91. [PubMed]
  • Haslam RH, Jameson HD. Cardiac standstill simulating repeated epileptic attacks. A case report. JAMA. 1973 May 7;224(6):887–889. [PubMed]
  • Stern S, Tzivoni D. Atrial and ventricular asystole for 19 seconds without syncope. Report of a case. Isr J Med Sci. 1976 Jan;12(1):28–33. [PubMed]
  • Kiok MC, Terrence CF, Fromm GH, Lavine S. Sinus arrest in epilepsy. Neurology. 1986 Jan;36(1):115–116. [PubMed]
  • Terrence CF, Rao GR, Perper JA. Neurogenic pulmonary edema in unexpected, unexplained death of epileptic patients. Ann Neurol. 1981 May;9(5):458–464. [PubMed]
  • Kaprio J, Koskenvuo M, Rita H. Mortality after bereavement: a prospective study of 95,647 widowed persons. Am J Public Health. 1987 Mar;77(3):283–287. [PubMed]
  • Lown B, Temte JV, Reich P, Gaughan C, Regestein Q, Hal H. Basis for recurring ventricular fibrillation in the absence of coronary heart disease and its management. N Engl J Med. 1976 Mar 18;294(12):623–629. [PubMed]
  • Katz C, Martin RD, Landa B, Chadda KD. Relationship of psychologic factors to frequent symptomatic ventricular arrhythmia. Am J Med. 1985 Apr;78(4):589–594. [PubMed]
  • Ruberman W, Weinblatt E, Goldberg JD, Chaudhary BS. Psychosocial influences on mortality after myocardial infarction. N Engl J Med. 1984 Aug 30;311(9):552–559. [PubMed]
  • Frasure-Smith N, Prince R. The ischemic heart disease life stress monitoring program: impact on mortality. Psychosom Med. 1985 Sep–Oct;47(5):431–445. [PubMed]
  • Tavazzi L, Zotti AM, Rondanelli R. The role of psychologic stress in the genesis of lethal arrhythmias in patients with coronary artery disease. Eur Heart J. 1986 May;7 Suppl A:99–106. [PubMed]
  • Eliot RS, Buell JC. Role of emotions and stress in the genesis of sudden death. J Am Coll Cardiol. 1985 Jun;5(6 Suppl):95B–98B. [PubMed]
  • Samuels MA. Neurogenic heart disease: a unifying hypothesis. Am J Cardiol. 1987 Dec 28;60(18):15J–19J. [PubMed]
  • Oppenheimer S. The insular cortex and the pathophysiology of stroke-induced cardiac changes. Can J Neurol Sci. 1992 May;19(2):208–211. [PubMed]