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Ictal and peri-ictal changes in cervical vagus nerve activity associated with cardiac effects

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Abstract

The vagus nerves convey both afferent and efferent information about autonomic activity related to cardiovascular functions. Those functions have been shown to change due to epileptic seizures, which suggests that ictal events might be detected via the vagus electroneurogram (VENG). In this study, we characterize the association of ictal and peri-ictal VENG with cardiac parameters. The electrocorticogram (ECoG), electrocardiogram, and the VENG were recorded in anesthetized rats, which were intravenously infused with either a pentylenetetrazole (PTZ) solution (PTZ-lot, n = 11) or saline (control-lot, n = 6). Control animals were subsequently vagotomized and also infused with a PTZ solution (n = 5, V-PTZ-lot). Cardiac and VENG parameters were assessed during different ECoG stages of ictal activity. None of the parameters changed in the control-lot. PTZ infusion induced seizures in all rats. Cardiac-related VENG showed distinctive firing patterns for the left and right vagus nerves. Significant ictal and post-ictal changes were seen in both the left and the right VENG in association with cardiac changes and increased parasympathetic influence on the heart. Changes in VENG parameters might provide a new way to assess the ictal state of patients, which could be suitable for triggering on-demand vagus nerve stimulation.

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References

  1. Ardell JL, Randall WC (1986) Selective vagal innervation of sinoatrial and atrioventricular nodes in canine heart. Am J Physiol 251(4):764–773

    Google Scholar 

  2. Asala SA, Bower AJ (1986) An electron microscope study of vagus nerve composition in the ferret. Anat Embryol 175(2):247–253

    Article  PubMed  CAS  Google Scholar 

  3. Boon P, Vonck K, Van Walleghem P, D’Have M, Goossens L, Vandekerckhove T et al (2001) Programmed and magnet-induced vagus nerve stimulation for refractory epilepsy. J Clin Neurophysiol 18(5):402–407

    Article  PubMed  CAS  Google Scholar 

  4. Cerati D, Schwartz PJ (1991) Single cardiac vagal fiber activity, acute myocardial ischemia, and risk for sudden death. Circ Res 69(5):1389–1401

    PubMed  CAS  Google Scholar 

  5. Coleridge HM, Coleridge JC, Kaufman MP, Dangel A (1981) Operational sensitivity and acute resetting of aortic baroreceptors in dogs. Circ Res 48(5):676–684

    PubMed  CAS  Google Scholar 

  6. De Herdt V, Boon P, Ceulemans B, Hauman H, Lagae L, Legros B et al (2007) Vagus nerve stimulation for refractory epilepsy: a Belgian multicenter study. Eur J Paediatr Neurol 11(5):261–269

    Article  PubMed  Google Scholar 

  7. Einthoven W, Flohil A, Battaerd PJTA (1908) On vagus currents examined with the string galvanometer. Exp Physiol 1(3):243–245

    Google Scholar 

  8. Evans DHL, Murray JG (1954) Histological and functional studies on the fibre composition of the vagus nerve of the rabbit. J Anat 88(3):320–337

    PubMed  CAS  Google Scholar 

  9. Hamilton RM (2004) Can cardiac vagal tone be estimated from the 10-second ECG? Int J Cardiol 95(1):109–115

    Article  PubMed  Google Scholar 

  10. Hamlin RL, Smith CR (1968) Effects of vagal stimulation on S-A and A-V nodes. Am J Physiol 215(3):560–568

    PubMed  CAS  Google Scholar 

  11. Harreby KR, Sevcencu C, Struijk JJ (2011) Early seizure detection in rats based on vagus nerve activity. Med Biol Eng Comput 49(2):143–151

    Article  PubMed  Google Scholar 

  12. Adkins RA, O’Donovan CA, Terry RS Jr (1999) Assignee: Cyberonic. Automatic activation of a neurostimulator device using a detection algorithm based on cardiac activity. US Patent 5,928,272

  13. Giftakis JE, Torgerson NA (2010) Assignee: Medtronic. Seizure detection algorithm adjustment. US2010/0121215 A1

  14. Kerem DH, Geva AB (2005) Forecasting epilepsy from the heart rate signal. Med Biol Eng Comput 43(2):230–239

    Article  PubMed  CAS  Google Scholar 

  15. Lathers CM, Schraeder PL (1982) Autonomic dysfunction in epilepsy: characterization of autonomic cardiac neural discharge associated with pentylenetetrazol-induced epileptogenic activity. Epilepsia 23(6):633–647

    Article  PubMed  CAS  Google Scholar 

  16. 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(2):227–240

    Article  PubMed  CAS  Google Scholar 

  17. McAllen RM, Spyer KM (1978) The baroreceptor input to cardiac vagal motoneurones. J Physiol 282:365–374

    PubMed  CAS  Google Scholar 

  18. McLachlan RS (1993) Suppression of interictal spikes and seizures by stimulation of the vagus nerve. Epilepsia 34(5):918–923

    Article  PubMed  CAS  Google Scholar 

  19. Mormann F, Andrzejak RG, Elger CE, Lehnertz K (2007) Seizure prediction: the long and winding road. Brain 130(2):314–333

    Article  PubMed  Google Scholar 

  20. Morris GL III (2003) A retrospective analysis of the effects of magnet-activated stimulation in conjunction with vagus nerve stimulation therapy. Epilepsy Behav 4(6):740–745

    Article  PubMed  Google Scholar 

  21. Morris GL III, Mueller WM (1999) Long-term treatment with vagus nerve stimulation in patients with refractory epilepsy. The Vagus Nerve Stimulation Study Group E01–E05. Neurology 53(8):1731–1735

    PubMed  Google Scholar 

  22. Novak V, Reeves AL, Novak P, Low PA, Sharbrough FW (1999) Time-frequency mapping of R-R interval during complex partial seizures of temporal lobe origin. J Auton Nerv Syst 77(2–3):195–202

    Article  CAS  Google Scholar 

  23. Paintal AS (1953) A study of right and left atrial receptors. J Physiol 120(4):596–610

    PubMed  CAS  Google Scholar 

  24. Paintal AS (1973) Vagal sensory receptors and their reflex effects. Physiol Rev 53(1):159–227

    PubMed  CAS  Google Scholar 

  25. Ramzan IM, Levy G (1985) Kinetics of drug action in disease states. XIV. Effect of infusion rate on pentylenetetrazol concentrations in serum, brain and cerebrospinal fluid of rats at onset of convulsions. J Pharmacol Exp Ther 234(3):624–628

    PubMed  CAS  Google Scholar 

  26. Schuele SU, Lüders HO (2008) Intractable epilepsy: management and therapeutic alternatives. Lancet Neurol 7(6):514–524

    Article  PubMed  Google Scholar 

  27. Sevcencu C, Struijk JJ (2010) Autonomic alterations and cardiac changes in epilepsy. Epilepsia 51(5):725–737

    PubMed  Google Scholar 

  28. Spyer KM, Brooks PA, Izzo PN (1994) Vagal preganglionic neurons supplying the heart. In: Schwartz PJ, Levy MN (eds) Vagal control of the heart: experimental basis and clinical implications. Futura Publishing Company ed., Armonk, pp 45–64

  29. Task Force of The European Society of Cardiology and The North American Society of Pacing and Electrophysiology (1996) Heart rate variability: standards of measurement, physiological interpretation, and clinical use. Eur Heart J 17(3):354–381

    Google Scholar 

  30. Terndrup TE, Darnall R, Knuth SL, Bartlett D Jr (1999) Effects of experimental cortical seizures on respiratory motor nerve activities in piglets. J Appl Physiol 86(6):2052–2058

    PubMed  CAS  Google Scholar 

  31. Uthman BM, Wilder BJ, Penry JK, Dean C, Ramsay RE, Reid SA et al (1993) Treatment of epilepsy by stimulation of the vagus nerve. Neurology 43(7):1338–1345

    PubMed  CAS  Google Scholar 

  32. Woodbury DM, Woodbury JW (1990) Effects of vagal stimulation on experimentally induced seizures in rats. Epilepsia 31:7–19

    Article  Google Scholar 

  33. World Health Organization (2005) Atlas—epilepsy care in the world 2005. World Health Organization, Geneva

Download references

Acknowledgments

This study was supported by the Danish National Advanced Technology Foundation. We thank the staff at Aalborg Biomedical Laboratory for their generous help during the experiments. The authors have filed a patent application on seizure prediction using VN activity.

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Authors and Affiliations

  1. Department of Health Science and Technology, Center for Sensory-Motor Interaction, Aalborg University, Aalborg, Denmark

    Kristian R. Harreby & Cristian Sevcencu

  2. Department of Health Science and Technology, Medical Informatics Group, Aalborg University, Aalborg, Denmark

    Johannes J. Struijk

Authors
  1. Kristian R. Harreby
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  2. Cristian Sevcencu
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  3. Johannes J. Struijk
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Correspondence to Kristian R. Harreby.

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Harreby, K.R., Sevcencu, C. & Struijk, J.J. Ictal and peri-ictal changes in cervical vagus nerve activity associated with cardiac effects. Med Biol Eng Comput 49, 1025–1033 (2011). https://doi.org/10.1007/s11517-011-0782-7

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  • DOI: https://doi.org/10.1007/s11517-011-0782-7

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