The anticonvulsant effect of electrical fields

Current Neurology and Neuroscience Reports

Volumn 1, Issue 2, 2001, Pages 155-161

  Weinstein, Steven ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Epileptic Seizure; Seizure Onset; Status Epilepticus; Transcranial Magnetic Stimulation; Vagus Nerve Stimulator

Indexed keywords

ANIMAL; ANIMAL MODEL; BIOLOGICAL MODEL; CLINICAL TRIAL; ELECTROCONVULSIVE THERAPY; ELECTROSTIMULATION; ELECTROSTIMULATION THERAPY; EPILEPSY; HIPPOCAMPUS; HUMAN; KINDLING; MAGNETISM; MOUSE; PATHOPHYSIOLOGY; PRIMATE; RAT; REVIEW; SEIZURE; VAGUS NERVE;

ANIMALS; CLINICAL TRIALS; ELECTRIC STIMULATION; ELECTRIC STIMULATION THERAPY; ELECTROCONVULSIVE THERAPY; EPILEPSY; HIPPOCAMPUS; HUMANS; KINDLING, NEUROLOGIC; MAGNETICS; MICE; MODELS, ANIMAL; MODELS, NEUROLOGICAL; PRIMATES; RATS; SEIZURES; VAGUS NERVE;

EID: 0035295977     PISSN: 15284042     EISSN: 15346293     Source Type: Journal    
DOI: 10.1007/s11910-001-0011-0     Document Type: Article

References (70)

1. Colder BW, Wilson CL, Frysinger RC, et al.: Neuronal synchrony in relation to burst discharge in epileptic human temporal lobes. J Neurophysiol 1996, 75:2496–2508.
2. Timofeeva OA, Swanson TA: Neurophysiology of epileptic seizures. Experimental neurophysiology. In Epileptic Seizures. Pathophysiology and Clinical Semiology. Edited by Lüders HO, Noachtar S. New York: Churchill Livingstone; 2000:23–31.
3. Risinger MW: Noninvasive ictal electroencephalography in humans. In Epileptic Seizures. Pathophysiology and Clinical Semiology. Edited by Lüders HO, Noachtar S. New York: Churchill Livingstone; 2000:32–48.
4. Dudek EF, Snow RW, Taylor CP: Role of electrical interactions in synchronization of epileptiform bursts. In Advances in Neurology, vol 44. Edited by Delgado-Escueta AV, Ward AA Jr, Woodbury DM, Porter RJ. New York: Raven Press; 1986:593–617.
5. Faber DS, Korn H: Electrical field effects: their relevance in central neural networks. Physiologic Rev 1989, 69:821–862.
6. Jefferys JG: Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiologic Rev 1995, 74:689–723.
7. Velasco M, Velasco F, Velasco AL, et al.: Subacute electrical stimulation of the hippocampus blocks intractable temporal lobe seizures and paroxysmal EEG activities. Epilepsia 2000, 41:158–169. An initial attempt at moving a theoretical possibility into the clinical realm. Details of patients, implantation, stimulation paradigms, electroencephalogram examples, statistics, and pathology. Everything present except chronic utilization. DOI: 10.1111/j.1528-1157.2000.tb00135.x
8. Borck C, Jefferys JG: Seizure-like events in disinhibited ventral slices of adult rat hippocampus. J Neurophysiol 1999, 82:2130–2142. This paper provides details sufficient for the neurologist, rather than the neurobiologist, to understand cell slices. Intriguing that potassium levels are higher at the onset of a seizure event compared with just a burst. Synaptic activity increased during, rather than prior, to the seizure, and CA3 clearly appears to be in the driver seat.
9. Feucht M, Möller U, Witte H, et al.: Application of correlation dimension and pointwise dimensionfor non-linear topographical analysis of focal onset seizures. Med Biol Engineering & Computing 1999, 37:208–217. Extracranial recordings, but makes the error of ignoring the initial attenuation at seizure onset. Demonstrates some of the methods of nondynamic mathematics. DOI: 10.1007/BF02513289
10. Jerger K, Netoff TI, Francis J, et al.: Earliest dynamical changes preceding seizures: a comparison of detection methods. Presented at Computational Neurosciences, Belgium, 2000. This was presented in Belgium and was submitted for publication. Detailed analysis using many dynamic and nondynamic methods of three different seizures recorded intracranially in four children with differing focal epilepsies. No clear advantage to the latter methods, although both beat the neurologist in identifying seizure onsets.
11. Lange HH, Lieb JP, Engel J Jr, Crandall PH: Tempero-spatial patterns of pre-ictal spike activity in human temporal lobe epilepsy. Electroencephalograph Clin Neurophysiol 1983, 56:543–555. DOI: 10.1016/0013-4694(83)90022-6
12. Martinerie J, Adam C, LeVan Quyen M, et al.: Epileptic seizures can be anticipated by non-linear analysis. Nat Med, 1998, 4:1173–1176. These investigators study signals from depth electrodes implanted in the hippocampus. Minimal details of seizure types and electroencephalogram, but they anticipate onset by minutes using nonlinear analysis. DOI: 10.1038/2667
13. Moser HR, Weber B, Wieser HG, Meier PF: Electroencephalograms in epilepsy: analysis and seizure prediction with the framework of Lyapunov theory. Physica D, 1999, 130:291–305. DOI: 10.1016/S0167-2789(99)00043-3
14. Rogowski Z, Gath I, Bental E: On the prediction of epileptic seizures. Biol Cybernet, 1981, 42:9–15. DOI: 10.1007/BF00335153
15. Salant Y, Gath I, Henriksen O: Prediction of epileptic seizures from two-channel EEG. Med Biol Engineering & Computing 1998, 36:549–556. DOI: 10.1007/BF02524422
16. Widman G, Bingmann D, Lehnertz K, Elger CE: Reduced signal complexity of intracellular recordings: a precursor for epileptiform activity? Brain Res 1999, 836:156–163. DOI: 10.1016/S0006-8993(99)01647-9
17. Gluckman BJ, Neel EJ, Nethoff TI, et al.: Electric field suppression of epileptiform activity in hippocampal slices. J Neurophysiol 1996, 76:4202–4205.
18. Gluckman BJ, Nguyen H, Weinstein S, Schiff SJ: Adaptive electric field control of epileptic seizures. Submitted for publication. This paper uses the high-potassium hippocampal slice and electric fields to extinguish bursts and seizure events. Comparison of feedback mechanisms and direct current to control state. Full-wave better than half-wave rectified feedback.
19. Jefferys JG: Influence of electrical fields on the excitability of granule cells in guinea-pig hippocampal slices. J Physiol 1981, 319:143–152.
20. Warren RJ, Durand DM: Effects of applied currents on spontaneous epileptiform activity induced by low calcium in the rat hippocampus. Brain Res 1998, 806:186–195. This paper uses a sensor and stimulator in CA1 to inhibit bursts and seizure-like events. This is the demonstration that increasing the tissue resistance in the low-calcium model contributes to the need for only small amounts of current. DOI: 10.1016/S0006-8993(98)00723-9
21. Lesser RP, Kim SH, Beyderman L, et al.: Brief bursts of pulse stimulation terminate after discharges caused by cortical stimulation. Neurology 1999, 53:2073–2081. This paper uses the novel approach of “fighting fire with fire.” Will need to be tried on spontaneously occurring seizures when monitoring patients and after the hardware is modified. Safety needs to be demonstrated because of the large amount of current provided.
22. Durman RS, Vaidya VA: Molecular and cellular actions of chronic electroconvulsive seizures. J Electro Convuls Ther 1998, 14:181–193. This is a good review of the story that electrical fields alter gene expression, leading to changes in morphology of the hippocampus.
23. Jennum P: Transcranial magnetic stimulation and epilepsy. In Transcranial Magnetic Stimulation (EEG suppl 51). Edited by Paulus W, Hallett M, Rossini PM, Rothwell JC. Amesterdam: Elsevier; 1999:212–220.
24. Sackeim HA, The anticonvulsant hypothesis of the mechanisms of action of ECT: current status. J Electro Convuls Ther 1999, 15:5–26.
25. Ziemann U, Streinoff BJ, Tergau F, Paulus W: Transcranial magnetic stimulation: its current role in epilepsy research. Epilepsy Res 1998, 30:11–30. DOI: 10.1016/S0920-1211(97)00079-X
26. Fisher RS, Mirski M, Krauss GL: Brain stimulation. In Epilepsy: A Comprehensive Textbook. Edited by Engel J Jr, Pedley TA. Philadelphia: Lippincott-Raven; 1997:1867–1875.
27. Schachter SC, Saper CB: Vagus nerve stimulation. Epilepsia, 1998, 39:677–686. DOI: 10.1111/j.1528-1157.1998.tb01151.x
28. Boylan LS, Haskett RF, Mulsant BH, et al.: Determinants of seizure threshold in ECT: benzodiazepine use, anesthetic dosage, and other factors. J Electro Convuls Ther 2000, 16:3–18.
29. Blackwood DH, Cull RE, Freeman CP, et al.: A study of the incidence of epilepsy following ECT. J Neurol Neurosurg Psychiatr 1980, 43:1098–1102. DOI: 10.1136/jnnp.43.12.1098
30. Devinsky O, Duchowny MS: Seizures after convulsive therapy: a retrospective case survey. Neurology, 1983, 33:921–925.
31. Meldrum BS: Neuropathological consequences of chemically and electrically induced seizures. Ann NY Acad Sci 1986, 462:186–193. DOI: 10.1111/j.1749-6632.1986.tb51253.x
32. Small JG, Milstein V, Small IF, Sharpley PH: Does ECT produce kindling? Biol Psychiatr 1981, 16:773–778.
33. Lippmann S, Manshadi M, Wehry M, et al.: 1,250 electroconvulsive treatments without evidence of brain injury. Br J Psychiatr 1985, 147:203–204. DOI: 10.1192/bjp.147.2.203
34. Burnham WM, Gombos Z, Nobrega J, Cottrell GA: Kindlinglike effects of electroconvulsive shock seizures. In Kindling 5. Edited by Corcoran ME, Moshé SL. New York: Plenum Press; 1998:121–129. This paper has a paucity of original science, but it is a good review to read before starting trials using electroconvulsive therapy to treat seizures.
35. González MD, Palomar M, Rovira R: Electroconvulsive therapy for status epilepticus. Ann Intern Med 1997, 127:247–248.
36. Post RM, Putman F, Contel NR, Goldman B: Electroconvulsive seizures inhibit amygdala kindling: implications for mechanisms of action in affective illness. Epilepsia 1984, 25:234–239.
37. Tomasson K, Winokur G, Pfohl B: Failed and short seizures associated with prior electroconvulsive therapy. Eur Arch Psychiatr Clin Neurosci 1992, 241:307–313. DOI: 10.1007/BF02195981
38. Krueger RB, Fama JM, Devanand DP, et al.: Does ECT permanently alter seizure threshold? Biol Psychiatr 1993, 33:272–276. DOI: 10.1016/0006-3223(93)90294-N
39. Coffey CE, Lucke J, Weiner RD, et al.: Seizure threshold in electroconvulsive therapy (ECT) II. The anticonvulsant effect of ECT. Biol Psychiatr 1995, 37:777–788. DOI: 10.1016/0006-3223(95)00053-J
40. Jayakar P: Physiological principles of electrical stimulation. In Electrical and Magnetic Stimulation of the Brain and Spinal Cord Edited by Devinsky O, Beric A, Dogali M. New York: Raven Press; 1993.
41. Bezard E, Boraud T, Nguyen JP, et al.: Cortical stimulation and epileptic seizure: a study of the potential risk in primates. Neurosurgery 1999, 45:346–350. This paper presents data from three monkeys implanted for 40 days, and demonstrates that daily administration of current to the motor cortex does not produce gross changes to the electroencephalogram or behavior. Needs more details of what was done and how analyzed. DOI: 10.1097/00006123-199908000-00030
42. Weiss SR, Li XL, Noguera EC, et al.: Quenching: persistent alterations in seizure and after discharge threshold following low-frequency stimulation. In Kindling 5. Edited by Corcoran ME, Moshé SL. New York: Plenum Press; 1998. This was a well-done study and the design worth replicating. The paper clearly demonstrates how what one is measuring may actually be caused by what one is not (see Weiss et al. [43]).
43. Weiss SR, Eisdath A, Li XL, et al.: Quenching revisited: Low level direct current inhibits amygdala-kindled seizures. Exper Neurol 1998, 154:185–192. The authors realized their error and went on to examine how the unanticipated direct current leak around a bad stimulating electrode may be responsible for quenching. The concept is good, with increasing seizure thresholds and seizure inhibition, but probably at the cost of neuronal integrity. DOI: 10.1006/exnr.1998.6932
44. Clark S, Wilson WA: Mechanisms of epileptogenesis. In Jasper’s Basic Mechanisms of the Epilepsies, edn 3, Advances in Neurology. Edited by Delagado-Escueta AV, Wilson WA, Olsen RW, Porter RJ. Philadelphia: Lippincott; 1999:607–630.
45. Nakagawa M, Durand D: Suppression of spontaneous epileptiform activity with applied currents. Brain Res, 1991, 567:241–247. DOI: 10.1016/0006-8993(91)90801-2
46. Durand D: Electrical stimulation can inhibit synchronized neuronal activity. Brain Res 1986, 382:139–144. DOI: 10.1016/0006-8993(86)90121-6
47. Kayyali H, Durand D: Effects of applied currents on epileptiform bursts in vitro. Exper Neurol 1991, 113:249–254. DOI: 10.1016/0014-4886(91)90181-B
48. Hammond EJ, Uthman BM, Reid SA, Wilder BJ: Electrophysiological studies of cervical vagus nerve stimulation in humans: I. EEG effects. Epilepsia, 1992, 33:1013–1020. DOI: 10.1111/j.1528-1157.1992.tb01752.x
49. Uthman BM, Wilder BJ, Hammond EJ, Reid SA: Efficacy and safety of vagus nerve stimulation in patients with complex partial seizures. Epilepsia 1990, 31(suppl 2):S44-S50.
50. Handforth A, DeGiorgio CM, Schachter SC, et al.: Vagus nerve stimulation therapy for partial-onset seizures. Neurology 1998, 51:48–55. DOI: 10.1159/000006529
51. Zabara J: Inhibition of experimental seizures in canines by repetitive vagal stimulation. Epilepsia 1992, 33:1005–1012. DOI: 10.1111/j.1528-1157.1992.tb01751.x
52. Woodbury DM, Woodbury JW: Effects of vagal stimulation on experimentally induced seizures in rats. Epilepsia 1990, 31(suppl 2):S7-S19.
53. McLachlan RS: Suppression of interictal spikes and seizures by stimulation of the vagus nerve. Epilepsia 1993, 34:918–923. DOI: 10.1111/j.1528-1157.1993.tb02112.x
54. Lockard JS, Congdon WC, DuCharme LL: Feasibility and safety of vagal stimulation in monkey model. Epilepsia 1990, 31(suppl 2):S20-S26.
55. Fisher RS, Uematsu S, Krauss GL, et al.: Placebo-controlled pilot study of centromedian thalamic stimulation in treatment of intractable seizures. Epilepsia 1992, 33:841–851. DOI: 10.1111/j.1528-1157.1992.tb02192.x
56. Mirski MA, Rossell LA, Terry JB, Fisher RS: Anticonvulsant effect of anterior thalamic high frequency electrical stimulation in the rat. Epilepsy Res 1997, 28:89–100. DOI: 10.1016/S0920-1211(97)00034-X
57. Velasco F, Velasco M, Velasco AL, et al.: Electrical stimulation of the centromedian thalamic nuclei on various intractable seizure patterns: I. Clinical seizures and paroxysmal EEG activity. Epilepsia 1993, 34:1052–1064. DOI: 10.1111/j.1528-1157.1993.tb02134.x
58. Velasco M, Velasco F, Velasco AL, et al.: Effect if chronic electrical stimulation of the centromedian thalamic nuclei on various intractable seizure patterns: II. Psychological performance and background EEG activity. Epilepsia 1993, 34:1065–1074. DOI: 10.1111/j.1528-1157.1993.tb02135.x
59. Velasco F, Velasco M, Velasco AL, et al.: Electrical stimulation of the centromedian thalamic nucleus in control of seizures: long-term studies. Epilepsia 1995, 36:63–71. DOI: 10.1111/j.1528-1157.1995.tb01667.x
60. Velasco M, Velasco F, Velasco AL, et al.: Electrocortical and behavioral responses produced by acute electrical stimulation of the human centromedian thalamic nucleus. Electroencephalograph Clin Neurophysiol 1996, 102:461–471. DOI: 10.1016/S0013-4694(96)95203-0
61. Vercueil L, Benazzouz A, Bressand K, et al.: High-frequency stimulation of the sub-thalamic nucleus suppresses absence seizures in the rat: comparison with neurotoxic lesions. Epilepsy Res 1998, 31:39–46. Rats with spontaneous generalized absence (GAERS) have their subthalamic nuclei implanted and stimulated and compared with animals with kainate-induced excitotoxic lesions. The high-frequency stimulation does a better job, suggesting that at least for this model the basal ganglia be involved in seizures. DOI: 10.1016/S0920-1211(98)00011-4
62. Barker AT: The history and basic principles of magnetic nerve stimulation. In Transcranial Magnetic Stimulation (EEG Suppl 51). Edited by Paulus W, Hallett M, Rossini PM, Rothwell JC. Amsterdam: Elsevier; 1999:3–21. This is a good review of the science of transcranial magnetic stimulation. The coils, their fields, and their ability to penetrate the skull are discussed. The figure of 8 coil does not have its effect at its center (field strength 0). Uncertain if the hippocampus can be stimulated.
63. Wassermann EM: Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Magnetic Stimulation, June 5–7, 1996. Electroencephalograph Clin Neurophysiol 1998, 108:1–16. This is a great review of repetitive transcranial magnetic stimulation. Pertinent to this paper is a literature review of all known induced seizures at that time. Other side effects reviewed are medical and psychologic. DOI: 10.1016/S0168-5597(97)00096-8
64. Potschka H, Thun-Battersby S, Löscher W: Effect of low-intensity 50-Hz magnetic fields on kindling acquisition and fully kindled seizures in rats. Brain Res 1998, 809:269–276. DOI: 10.1016/S0006-8993(98)00919-6
65. Tassinari CA, Michelucci R, Forti A, et al.: Transcranial magnetic stimulation in epileptic patients: usefulness and safety. Neurology 1990, 40:1132–1133.
66. Tergau F, Naumann U, Paulus W, Steinhoff BJ: Low-frequency repetitive transcranial magnetic stimulation improves intractable epilepsy. Lancet 1999, 353:2209. Pilot study of nine patients receiving repetitive transcranial magnetic stimulation. All tolerated the procedure well and there was no increase in seizures; they decreased by self-report. DOI: 10.1016/S0140-6736(99)01301-X
67. Menkes DL, Gruenthal M: Slow-frequency repetitive transcranial magnetic stimulation in a patient with focal cortical dysplasia. Epilepsia 2000, 41:240–242. This is a case report that provides encouragement to those seeking a noninvasive way to deliver a field and inhibit seizures in an intractable patient. Would be better without self-reported improvement or given sham stimulation. DOI: 10.1111/j.1528-1157.2000.tb00146.x
68. Fleischmann A, Hirschman S, Dolberg OT, et al.: Chronic treatment with repetitive transcranial magnetic stimulation inhibits seizure induction by electroconvulsive shock in rats. Biol Psychiatr 1999, 45:750–758. DOI: 10.1016/S0006-3223(98)00211-X
69. Ebert U, Ziemann U: Altered seizure susceptibility after high-frequency transcranial stimulation in rats. Neurosci Let 1999, 273:155–158. DOI: 10.1016/S0304-3940(99)00636-9
70. Jennum P, Klitgaard H: Repetitive transcranial magnetic stimulations of the rat. Effect of acute and chronic stimulations on pentylenetetrazole-induced clonic seizures. Epilepsy Res 1996, 23:115–122. DOI: 10.1016/0920-1211(95)00088-7