Cortical lateralization and cardiac autonomic control. Insights from insular stroke and epilepsy

Victor Constantinescu, Olivier Detante, Daniela Matei, Irina Constantinescu, Catalina Arsenescu-Georgescu, Pascal Defaye, Cristian Dinu Popescu, Dan Cuciureanu

Abstract


Autonomic nervous system dysfunction is a common complication of stroke. Human studies and experimental data showed a hemispheric lateralization of autonomic activity concerning the forebrain and particularly the insular cortex. Insular cortex involvement is associated with more pronounced autonomic imbalance leading to life threatening arrhythmias and sudden death. We present two case reports of insular infarction in young patients without any cardiac comorbidity, illustrating a specific lateralized function of insula and its influence on the sympatho-vagal balance that implied differentiated therapeutic management after stroke. The right insular stroke was associated to sympathetic activation and left insular stroke was associated to parasympathetic predominance. The same lateralization of autonomic function with opposite effects on sympatho-vagal balance was also reported in two insular epilepsy cases, illustrating the fact that, beyond the controlling network, the cortical modulation of the autonomic nervous system is asymmetric. Identifying high risk patients prone to develop neurogenic cardiac complications, by better understanding of dysautonomia pathophysiology and consequent implementation of prophylactic and therapeutic interventions may significantly reduce mortality rate in stroke and epilepsy.

Keywords


insular cortex, ischemic stroke, epilepsy, cardiac dysautonomia

Full Text:

PDF

References


Dampney RA, Horiuchi J, Tagawa T, Fontes MA, Potts PD, Polson JW. Medullary and supramedullary mechanisms regulating sympathetic vasomotor tone. Acta Physiol Scand 2003; 177(3):209-218.

Feldman JL, Mitchell GS, Nattie EE. Breathing: rhythmicity, plasticity, chemosensitivity. Annu Rev Neurosci 2003; 26: 239-266.

Benarroch EE. Periaqueductal gray: an interface for behavioral control. Neurology 2012; 78(3):210-217.

Critchley HD, Elliott R, Mathias CJ, Dolan RJ. Neural activity relating to generation and representation of galvanic skin conductance responses: a functional magnetic resonance imaging study. J Neurosci 2000; 20(8):3033-3040.

Mesulam MM, Mufson EJ. Insula of the old world monkey. I. Architectonicsin the insulo-orbito-temporal component of the paralimbic brain. J Comp Neurol 1982; 212:1–22.

Ture U, Yasargil MG, Al-Mefty O, Yasargil DC. Arteries of the insula. J Neurosurg 2000; 92:676–687.

Hakan Ay, Murat Arsava E, Koroshetz WJ, Sorensen AG. Middle Cerebral Artery Infarcts Encompassing the Insula Are More Prone to Growth. Stroke 2008; 39:373-378.

Sander D, Klingelhofer J. Changes of circadian blood pressure patterns afterhemodynamic and thromboembolic brain infarction. Stroke 1994; 25:1730–1737.

Nagai M, Hoshide S, KarioK, The insular cortex and cardiovascular system: a new insight into the brain-heart axis. J Am Soc Hypertens 2010; 4(4):174–182.

Scheitz JF, Erdur H, Haeusler KG, et al. Insular cortex lesions, cardiac troponin, and detection of previously unknown atrial fibrillation in acute ischemic stroke: insights from the troponin elevation in acute ischemic stroke study. Stroke 2015; 46(5):1196-1201.

Nei M, Ho RT, Abou-Khalil BW, et al. EEG and ECG in sudden unexplained death in epilepsy. Epilepsia 2004; 45(4):338-345.

Ozdemir O, Hachinski V. Brain lateralization and sudden death: its role in the neurogenic heart syndrome. J Neurol Sci 2008; 268(1-2):6-11.

Jansen K, Varon C, Van Huffel S, Lagae L. Peri-ictal ECG changes in childhood epilepsy: implications for detection systems. Epilepsy Behav 2013; 29(1):72-76.

Blumhardt LD, Smith PE, Owen L. Electrocardiographic accompaniments of temporal lobe epileptic seizures. Lancet 1986; 1(8489):1051-1056.

Yancy CW, Jessup M, Bozkurt B, et al. 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol 2013; 62:e147–239.

Shahani BT, Day TJ, Cros D, Khalil N, Kneebone CS. RR interval variation and the sympathetic skin response in the assessment of autonomic function in peripheral neuropathy. Arch Neurol 1990; 47:659–664.

Task Force of the European Society of Cardiology and the North American Society of Pacing Electrophysiology. Heart rate variability. Standards of Measurement, Physiological Interpretation and Clinical Use. Circulation 1996; 93:1043-1065.

Ewing DJ, Clarke BF. Autonomic neuropathy: its diagnosis and prognosis. Clin Endocrinol Metab 1986; 15:855– 888.

Hilz MJ, Dütsch M. Quantitative studies of autonomic function. Muscle Nerve 2006; 33:6–20.

Stein PK, Fauchier L, Babuty D. Sudden death, arrhythmic events and measurements of heart rate variability. J Am Coll Cardiol 1999; 34(7):2148–2149.

Naver HK, Blomstrand C, Wallin BG. Reduced heart rate variability after right-sided stroke. Stroke 1996; 27:247–251.

Korpelainen JT, Sotaniemi KA, Huikuri HV, Myllyä VV. Abnormal heart rate variability as a manifestation of autonomic dysfunction in hemispheric brain infarction. Stroke 1996; 27:2059–2063.

Mäkikallio AM, Mäkikallio TH, Korpelainen JT, Sotaniemi KA, Huikuri HV, Myllylä VV. Heart rate dynamics predict poststroke mortality. Neurology 2004; 62:1822–1826.

Klingelhoefer J, Sander D. Cardiovascular consequences of clinical stroke. Ballieres Clin Neurol 1997; 6:309-335.

Oppenheimer SM, Cechetto DF. Cardiac chronotropic organization of the rat insular cortex. Brain Res 1990; 533:66-72.

Zhang ZH, Rashba S, Oppenheimer SM. Insular cortex lesions after baroreceptor sensitivity in the urethane-anesthetized rat. Brain Res 1998; 813(1):73-81.

Saad MA, Huerta F, Trancard J, Elghozi JL. Effects of middle cerebral artery occlusion on baroreceptor reflex control of heart rate in the rat. J Auton Nerv Syst 1989; 27:165-172.

Hilz MJ, Dutsch M, Perrine K, Nelson PK, Devinsky O. Hemisheric influence on autonomic modulation and baroreflex sensitivity. Ann Neurol 2001; 49:575-584.

Oppenheimer SM, Gelb AW, Girvin JP, Hachinski VC. Cardiovascular effects of human insular stimulation. Neurology 1992; 42:1727-1732.

King AB, Menon RS, Hachinski V, Cechetto DF. Human forebrain activation by visceral stimuli. J Comp Neurol 1999; 413:572-582.

Colivicchi F, Bassi A, Santini M, Caltagirone C. Cardiac autonomic derangement and arrhythmias in right-sided stroke with insular involvement. Stroke 2004; 35:2094-2098.

Al-Qudah Z, Yacoub HA, Souayah N. Serial heart rate variability testing for the evaluation of autonomic dysfunction after stroke. J Vasc Interv Neurol 2014; 7(5):12-17.

Rincon F, Dhamoon M, Moon Y, et al. Stroke location and association with fatal cardiac outcomes: Northern Manhattan Study (NOMAS). Stroke 2008; 39:2425–2431.

Strittmatter M, Meyer S, Fischer C, Georg T, Schmitz B. Location-dependent patterns in cardio-autonomic dysfunction in ischaemic stroke. Eur Neurol 2003; 50(1):30-38.

Meyer S, Strittmatter M, Fischer C, Georg T, Schmitz B. Lateralization in autonomic dysfunction in ischemic stroke involving the insular cortex. Neuroreport 2004; 15(2):357-361.

Hilz MJ, Schwab S. Stroke-induced sudden-autonomic death: areas of fatality beyond the insula. Comment on Stroke 2008; 39(9):2425-2431.

Bennaroch EE. Central Autonomic Network: Functional Organization and Clinical Correlations. Armonk, NY: Futura Publishing Company, Inc., 1997.

Lytton W, Williams S, Sober S. Unmasking unmasked: neural dynamics following stroke. Elsevier (Ed.). Progress in Brain Research, Volume 121, Chapter 12; 1999:203-218.

Penfield W, Jasper H. Epilepsy and the Functional Anatomy of the Human Brain. Boston: Little Brown 1954; 183–238.

Schiff SJ, Sauer T, Kumar R, Weinstein SL. Neuronal spatiotemporal pattern discrimination: the dynamical evolution of seizures. NeuroImage 2005; 28:1043–1055.

Mullen T, Worrell G, Makeig S. Multivariate principal oscillation pattern analysis of ICA sources during seizure. Conf Proc IEEE Eng Med Biol Soc 2012; 2012:2921-2924.

Jiruska P, de Curtis M, Jefferys JG, Schevon CA, Schiff SJ, Schindler K. Synchronization and desynchronization in epilepsy: controversies and hypotheses. J Physiol 2013; 591(4):787-797.

Rabiller G, He J-W, Nishijima Y, Wong A, Liu J. Perturbation of brain oscillations after ischemic stroke: a potential biomarker for post-stroke function and therapy. Int J Mol Sci 2015; 16(10):25605-25640.

Ding L, Hua W, Niu H, Chen K, Zhang S. Primary prevention of sudden cardiac death using implantable cardioverter defibrillators. Europace. 2008; 10(9):1034-1041.

Russo AM, Stainback RF, Bailey SR, et al. ACCF/HRS/AHA/ASE/HFSA/SCAI/SCCT/SCMR 2013 appropriate use criteria for implantable cardioverter-defibrillators and cardiac resynchronization therapy: a report of the American College of Cardiology Foundation Appropriate Use Criteria Task Force, Heart Rhythm Society, American Heart Association, American Society of Echocardiography, Heart Failure Society of America, Society for Cardiovascular Angiography and Interventions, Society of Cardiovascular Computed Tomography, and Society for Cardiovascular Magnetic Resonance. Heart Rhythm 2013; 10.

Yoshida T, Yoshino A, Kobayashi Y, Inoue M, Kamakura K, Nomura S. Effects of slow repetitive transcranial magnetic stimulation on heart rate variability according to power spectrum analysis. J Neurol Sci 2001; 184:77-80.

Clarke BM, Upton ARM, Kamath MV, Al-Harbi T, Castellanos CM. Transcranial magnetic stimulation for migraine: clinical effects. J Headache Pain 2006: 7:341-346.

Hays SA, Ruiz A, Bethea T, et al. Vagus nerve stimulation during rehabilitative training enhances recovery of forelimb function after ischemic stroke in aged rats. Neurobiol Aging 2016; 43:111-118.

Velagapudi P, Turagam M, Laurence T, Kocheril A. Cardiac arrhythmias and sudden unexpected death in epilepsy (SUDEP). Pacing Clin Electrophysiol 2012, 35:363–370.

Britton JW, Ghearing GR, Benarroch EE, Cascino GD. The ictal bradycardia syndrome: localization and lateralization. Epilepsia 2006; 47(4):737-744.

Garcia M, D'Giano C, Estellés S, Leiguarda R, Rabinowicz A. Ictal tachycardia: its discriminating potential between temporal and extratemporal seizure foci. Seizure 2001; 10(6):415-419.

Opherk C, Hirsch LJ. Ictal heart rate differentiates epileptic from non-epileptic seizures. Neurology 2002; 58(4):636-638.

Rugg-Gunn FJ, Simister RJ, Squirrell M, Holdright DR, Duncan JS. Cardiac arrhythmias in focal epilepsy: a prospective long-term study. Lancet 2004; 364(9452):2212-2219.

Schernthaner C, Lindinger G, Pötzelberger K, Zeiler K, Baumgartner C. Autonomic epilepsy-the influence of epileptic discharges on heart rate and rhythm. Wien Klin Wochenschr 1999; 111(10):392-401.

Leutmezer F, Schernthaner C, Lurger S, Pötzelberger K, Baumgartner C. Electrocardiographic changes at the onset of epileptic seizures. Epilepsia 2003; 44(3):348-354.

Abela E, Rummel C, Hauf M, Weisstanner C, Schindler K, Wiest R. Neuroimaging of epilepsy: lesions, networks, oscillations. Clin Neuroradiol 2014; 24(1):5-15.

Swartz CM, Abrams R, Lane RD, DuBois MA, Srinivasaraghavan J. Heart rate differences between right and left unilateral electroconvulsive therapy. J Neurol Neurosurg Psychiatry 1994; 57(1):97-99.

Evrengul H, Tanriverdi H, Dursunoglu D, et al. Time and frequency domain analyses of heart rate variability in patients with epilepsy. Epilepsy Res 2005; 63(2-3):131-139.

Hilz MJ, Devinsky O, Doyle W, Mauerer A, Dutsch M. Decrease of sympathetic cardiovascular modulation after temporal lobe epilepsy surgery. Brain 2002; 125:985-995.

Oppenheimer S. Cerebrogenic cardiac arrhythmias: Cortical lateralization and clinical significance. Clin Auton Res 2006; 16(1):6-11.

Eggleston KS, Olin BD, Fisher RS. Ictal tachycardia: the head–heart connection. Seizure 2014; 23(7):496-505.

Adjei P, Surges R, Scott CA, Kallis C, Shorvon S, Walker MC. Do subclinical electrographic seizure patterns affect heart rate and its variability? Epilepsy Res 2009; 87(2-3):281-285.

Di Gennaro G, Quarato PP, Sebastiano F, et al. Ictal heart rate increase precedes EEG discharge in drug-resistant mesial temporal lobe seizures. Clin Neurophysiol 2004; 115(5):1169-1177.

Massetani R, Strata G, Galli R, et al. Alteration of cardiac function in patients with temporal lobe epilepsy: different roles of EEG-ECG monitoring and spectral analysis of RR variability. Epilepsia 1997; 38(3):363-369.

Mayer H, Benninger F, Urak L, Plattner B, Geldner J, Feucht M. EKG abnormalities in children and adolescents with symptomatic temporal lobe epilepsy. Neurology 2004; 63(2):324-328.

Schwartz PJ. Vagal stimulation for heart diseases: from animals to men. An example of translational cardiology. Neth Heart J 2013; 21(2):82-84.

Piepoli MF. Exercise training in chronic heart failure: mechanisms and therapies. Neth Heart J 2013; 21(2):85-90.

De Decker K, Beese U, Staal MJ, Dejongste MJ. Electrical neuromodulation for patients with cardiac diseases. Neth Heart J 2013; 21(2):91-94.

Voskuil M, Verloop WL, Blankestijn PJ, Agostoni P, Stella PR, Doevendans PA. Percutaneous renal denervation for the treatment of resistant essential hypertension; the first Dutch experience. Neth Heart J 2011; 19:319–323.

Verloop WL, Voskuil M, Doevendans PA. Renal denervation: a new treatment option in resistant arterial hypertension. Neth Heart J 2013; 21(2):95-98.

Stemper B, Devinsky O, Haendl T, Welsch G, Hilz MJ. Effects of vagus nerve stimulation on cardiovascular regulation in patients with epilepsy. Acta Neurol Scand 2008; 117(4):231-236.

Ogbonnaya S, Kaliaperumal C. Vagal nerve stimulator: evolving trends. J Nat Sci Biol Med 2013; 4(1):8-13.

Pelleg A, Hurt CM, Soler-Baillo JM, Polansky M. Electrophysiological-anatomic correlates of ATP-triggered vagal reflex in dogs. Am J Physiol 1993; 265:H681–690.

Krahl SE. Vagus nerve stimulation for epilepsy: A review of the peripheral mechanisms. Surg Neurol Int 2012; 3:S47-S52.

Ben-Menachem E, Mañon-Espaillat R, Ristanovic R, Wilder BJ, Stefan H, Mirza W, Tarver WB, Wernicke JF. Vagus nerve stimulation for treatment of partial seizures: A controlled study of effect on seizures. First International Vagus Nerve Stimulation Study Group. Epilepsia 1994; 35(3):616-626.




DOI: http://dx.doi.org/10.22551/2017.16.0403.10108

Copyright (c) 2017 Victor Constantinescu, Olivier Detante, Daniela Matei, Irina Constantinescu, Catalina Arsenescu-Georgescu, Pascal Defaye, Cristian Dinu Popescu, Dan Cuciureanu

Creative Commons License
Archive of Clinical Cases is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

 

ISSN: 2360-6975