Suppression and control of epileptiform activity by electrical stimulation: a review

Epilepsy is a devastating disease affecting /spl sim/1% of the world's population. Although drug therapy is effective in many patients, 25% are not responsive to anticonvulsants. In addition, up to 50% of those receiving regular mediation suffer major side effects. Surgical resection is another treatment also associated with serious complications. An alternative method to control seizure activity is electrical stimulation. Several electrical stimulation protocols have been developed in animal models of epilepsy that can reduce or completely suppress seizures. Moreover, in over 5000 patients worldwide, electrical stimulation has been used to control seizures. The mechanisms underlying some of the techniques of seizure control are not understood. Some stimulation protocols, such as DC stimulation, rely on the effects of fields and currents on the membrane polarization. Other methods using single pulses, such as phase-resetting, desynchronization, and chaos control rely on the modulation of the dynamic properties of the neuronal networks. Both low- and high-frequency periodic stimulation can suppress seizures not only during stimulation, but also by inducing long-term changes in brain function. The purpose of this review is to present these approaches and to discuss their underlying mechanisms and potential for clinical implementation.

[1]  L. Kalinowsky,et al.  OBSERVATIONS IN ELECTRIC SHOCK THERAPY APPLIED TO PROBLEMS OF EPILEPSY , 1943 .

[2]  O. Pompeiano,et al.  Synchronization of the EEG produced by low-frequncy electrical stimulation of the region of the solitary tract , 1961 .

[3]  J. M. Brookhart,et al.  The effects of applied polarization on evoked electro-cortical waves in the cat. , 1962, Electroencephalography and clinical neurophysiology.

[4]  E. Furshpan,et al.  Intracellular and extracellular responses of the several regions of the Mauthner cell of the goldfish. , 1962, Journal of neurophysiology.

[5]  E. Furshpan,et al.  Two inhibitory mechanisms in the Mauthner neurons of goldfish. , 1963, Journal of neurophysiology.

[6]  A Malliani,et al.  Spike generation and propagation initiated in dendrites by transhippocampal polarization. , 1966, Brain research.

[7]  M. Sterman,et al.  Afferent vagal stimulation: neurographic correlates of induced EEG synchronization and desynchronization. , 1967, Brain research.

[8]  R. Guttman,et al.  Oscillation and Repetitive Firing in Squid Axons Comparison of experiments with computations , 1970 .

[9]  H. Lux.  Fast recording ion specific microelectrodes: their use in pharmacological studies in the CNS. , 1974, Neuropharmacology.

[10]  J. B. Ranck,et al.  Which elements are excited in electrical stimulation of mammalian central nervous system: A review , 1975, Brain Research.

[11]  C. Nicholson,et al.  Calcium and potassium changes in extracellular microenvironment of cat cerebellar cortex. , 1978, Journal of neurophysiology.

[12]  D. Prince,et al.  Cellular and field potential properties of epileptogenic hippocampal slices , 1978, Brain Research.

[13]  E. N. Best,et al.  Null space in the Hodgkin-Huxley Equations. A critical test. , 1979, Biophysical journal.

[14]  C. Antzelevitch,et al.  Phase resetting and annihilation of pacemaker activity in cardiac tissue. , 1979, Science.

[15]  D. Blackwood,et al.  A study of the incidence of epilepsy following ECT , 1980, Journal of neurology, neurosurgery, and psychiatry.

[16]  J. Rinzel,et al.  Control of repetitive firing in squid axon membrane as a model for a neuroneoscillator. , 1980, The Journal of physiology.

[17]  A. Winfree.  The geometry of biological time , 1991 .

[18]  J. Jefferys,et al.  Influence of electric fields on the excitability of granule cells in guinea‐pig hippocampal slices. , 1981, The Journal of physiology.

[19]  P. Kellaway,et al.  Proposal for Revised Clinical and Electroencephalographic Classification of Epileptic Seizures , 1981, Epilepsia.

[20]  D. Stegeman,et al.  Solution Methods of Electrical Field Problems in Physiology , 1982, IEEE Transactions on Biomedical Engineering.

[21]  K. Krnjević,et al.  Stimulation-evoked changes in extracellular K+ and Ca2+ in pyramidal layers of the rat's hippocampus. , 1982, Canadian journal of physiology and pharmacology.

[22]  H. Haas,et al.  Synchronized bursting of CA1 hippocampal pyramidal cells in the absence of synaptic transmission , 1982, Nature.

[23]  F. Dudek,et al.  Synchronous neural afterdischarges in rat hippocampal slices without active chemical synapses. , 1982, Science.

[24]  K. Krnjević,et al.  Depth distribution and mechanism of changes in extracellular K+ and Ca2+ concentrations in the hippocampus. , 1982, Canadian journal of physiology and pharmacology.

[25]  J. Fermaglich.  Electric Fields of the Brain: The Neurophysics of EEG , 1982 .

[26]  B. Lerer,et al.  Effect of Electroconvulsive Shock on Muscarinic Cholinergic Receptors in Rat Cerebral Cortex and Hippocampus , 1983, Journal of neurochemistry.

[27]  F. Dudek,et al.  Synchronous epileptiform bursts without chemical transmission in CA2, CA3 and dentate areas of the hippocampus , 1984, Brain Research.

[28]  W. R. Adey,et al.  Influences of sinusoidal electric fields on excitability in the rat hippocampal slice , 1984, Brain Research.

[29]  R. W. Turner,et al.  Extracellular fields influence transmembrane potentials and synchronization of hippocampal neuronal activity , 1984, Brain Research.

[30]  F. Dudek,et al.  Synchronization without active chemical synapses during hippocampal afterdischarges. , 1984, Journal of neurophysiology.

[31]  J. Jefferys,et al.  Low‐calcium field burst discharges of CA1 pyramidal neurones in rat hippocampal slices. , 1984, The Journal of physiology.

[32]  F. Dudek,et al.  Excitation of hippocampal pyramidal cells by an electrical field effect. , 1984, Journal of neurophysiology.

[33]  F. Edward Dudek,et al.  Electrical fields directly contribute to action potential synchronization during convulsant-induced epileptiform bursts , 1984, Brain Research.

[34]  U. Heinemann,et al.  Chemical synaptic transmission is not necessary for epileptic seizures to persist in the baboon Papio papio , 1985, Experimental Neurology.

[35]  G. Somjen,et al.  Potassium and calcium concentrations in interstitial fluid of hippocampal formation during paroxysmal responses. , 1985, Journal of neurophysiology.

[36]  C. Nicholson,et al.  A model for the polarization of neurons by extrinsically applied electric fields. , 1986, Biophysical journal.

[37]  W. R. Adey,et al.  Long-term effects of sinusoidal extracellular electric fields in penicillin-treated rat hippocampal slices , 1986, Brain Research.

[38]  W. R. Adey,et al.  Comparison between the effects of extracellular direct and sinusoidal currents on excitability in hippocampal slices , 1986, Brain Research.

[39]  F. Dudek,et al.  Evidence for neuronal interactions by electrical field effects in the CA3 and dentate regions of rat hippocampal slices , 1986, Brain Research.

[40]  R K Wong,et al.  Cellular basis of neuronal synchrony in epilepsy. , 1986, Advances in neurology.

[41]  D. Durand,et al.  Electrical stimulation can inhibit synchronized neuronal activity , 1986, Brain Research.

[42]  C. Nicholson,et al.  Modulation by applied electric fields of Purkinje and stellate cell activity in the isolated turtle cerebellum. , 1986, The Journal of physiology.

[43]  F. Rattay.  Analysis of Models for External Stimulation of Axons , 1986, IEEE Transactions on Biomedical Engineering.

[44]  A. Winfree.  When time breaks down , 1987 .

[45]  S J Korn,et al.  Epileptiform burst activity induced by potassium in the hippocampus and its regulation by GABA-mediated inhibition. , 1987, Journal of neurophysiology.

[46]  R. Dingledine,et al.  Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. , 1988, Journal of neurophysiology.

[47]  C. Nicholson,et al.  Effects of electric fields on transmembrane potential and excitability of turtle cerebellar Purkinje cells in vitro. , 1988, The Journal of physiology.

[48]  H Korn,et al.  Electrical field effects: their relevance in central neural networks. , 1989, Physiological reviews.

[49]  J. Lockard,et al.  Feasibility and Safety of Vagal Stimulation In Monkey Model , 1990, Epilepsia.

[50]  D. Woodbury,et al.  Effects of Vagal Stimulation on Experimentally Induced Seizures in Rats , 1990, Epilepsia.

[51]  D. Durand,et al.  Suppression of spontaneous epileptiform activity with applied currents , 1991, Brain Research.

[52]  M. Avoli,et al.  Epileptiform activity induced by low extracellular magnesium in the human cortex maintained in vitro , 1991, Annals of neurology.

[53]  D. Durand,et al.  Effects of applied currents on epileptiform bursts in vitro , 1991, Experimental Neurology.

[54]  J. Zabara.  Inhibition of Experimental Seizures in Canines by Repetitive Vagal Stimulation , 1992, Epilepsia.

[55]  H. Jongsma,et al.  Three ways of abolishing automaticity in sinoatrial node: ionic modeling and nonlinear dynamics. , 1992, The American journal of physiology.

[56]  F. Dudek,et al.  Prolonged field bursts in the dentate gyrus: dependence on low calcium, high potassium, and nonsynaptic mechanisms. , 1992, Journal of neurophysiology.

[57]  D. Durand,et al.  Effects of induced electric fields on finite neuronal structures: a simulation study , 1993, IEEE Transactions on Biomedical Engineering.

[58]  D. Durand.  Ictal Patterns in Experimental Models of Epilepsy , 1993, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[59]  H. Sackeim,et al.  Does ECT permanently alter seizure threshold? , 1993, Biological Psychiatry.

[60]  M Velasco,et al.  Effect of Chronic Electrical Stimulation of the Centromedian Thalamic Nuclei on Various Intractable Seizure Patterns: I. Clinical Seizures and Paroxysmal EEG Activity , 1993, Epilepsia.

[61]  Steven H. Strogatz,et al.  Nonlinear Dynamics and Chaos , 2024 .

[62]  W. Ditto,et al.  Controlling chaos in the brain , 1994, Nature.

[63]  A. Winfree,et al.  Electrical turbulence in three-dimensional heart muscle. , 1994, Science.

[64]  D M Durand,et al.  Desynchronization of epileptiform activity by extracellular current pulses in rat hippocampal slices. , 1994, The Journal of physiology.

[65]  R S Fisher,et al.  Electrical Stimulation of the Mammillary Nuclei Increases Seizure Threshold to Pentylenetetrazol in Rats , 1994, Epilepsia.

[66]  W. Abraham,et al.  Flip side of synaptic plasticity: Long‐term depression mechanisms in the hippocampus , 1994, Hippocampus.

[67]  Abdelhamid Benazzouz,et al.  Responses of substantia nigra pars reticulata and globus pallidus complex to high frequency stimulation of the subthalamic nucleus in rats: electrophysiological data , 1995, Neuroscience Letters.

[68]  T. L. Richardson,et al.  Epileptiform activity in the dentate gyrus during low-calcium perfusion and exposure to transient electric fields. , 1995, Journal of neurophysiology.

[69]  J. Jefferys,et al.  Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. , 1995, Physiological reviews.

[70]  S. Schiff,et al.  Periodic pacing an in vitro epileptic focus. , 1995, Journal of neurophysiology.

[71]  C. Coffey,et al.  Seizure threshold in electroconvulsive therapy (ECT) II. The anticonvulsant effect of ECT , 1995, Biological Psychiatry.

[72]  F. Dudek,et al.  MULTIPLE-UNIT RECORDINGS DURING SLOW FIELD-POTENTIAL SHIFTS IN LOW-[Ca2+]o SOLUTIONS IN RAT HIPPOCAMPAL AND CORTICAL SLICES , 1996, Neuroscience.

[73]  W. Ditto,et al.  Electric field suppression of epileptiform activity in hippocampal slices. , 1996, Journal of neurophysiology.

[74]  D. Durand,et al.  A generalized cable equation for magnetic stimulation of axons , 1996, IEEE Transactions on Biomedical Engineering.

[75]  W. Grill,et al.  Quantification of recruitment properties of multiple contact cuff electrodes. , 1996, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[76]  M Velasco,et al.  Electrocortical and behavioral responses produced by acute electrical stimulation of the human centromedian thalamic nucleus. , 1997, Electroencephalography and clinical neurophysiology.

[77]  R. Racine,et al.  Long-term enhancement of entorhinal-dentate evoked potentials following `modified' ECS in the rat , 1997, Brain Research.

[78]  C. Kellner,et al.  Electroconvulsive therapy for treatment of intractable seizures , 1997, Neurology.

[79]  P. Burnet,et al.  Differential effects of acute and chronic electroconvulsive shock on the abundance of messenger RNAs for voltage-dependent potassium channel subunits in the rat brain , 1997, Neuroscience.

[80]  SINGULAR STIMULUS PARAMETERS TO ANNIHILATE SPONTANEOUS POTASSIUM , 1997 .

[81]  Alec Eidsath,et al.  Quenching Revisited: Low Level Direct Current Inhibits Amygdala-Kindled Seizures , 1998, Experimental Neurology.

[82]  Samuel F. Berkovic,et al.  Febrile seizures and generalized epilepsy associated with a mutation in the Na+-channel ß1 subunit gene SCN1B , 1998, Nature Genetics.

[83]  P. Burnet,et al.  Changes in mRNA abundance of microtubule‐associated proteins in the rat brain following electroconvulsive shock , 1998, Neuroreport.

[84]  N. Newberry,et al.  Differential effects of electroconvulsive shock on the glutamate receptor mRNAs for NR2A, NR2B and mGluR5b. , 1998, Brain research. Molecular brain research.

[85]  Douglas C. Wallace,et al.  Radicals r'aging , 1998, Nature Genetics.

[86]  T Chang,et al.  The influence of electric fields on the epileptiform bursts induced by high potassium in CA3 region of rat hippocampal slice. , 1998, Neurological research.

[87]  Dominique M Durand,et al.  Effects of applied currents on spontaneous epileptiform activity induced by low calcium in the rat hippocampus , 1998, Brain Research.

[88]  A Benazzouz,et al.  High-frequency stimulation of the sub-thalamic nucleus suppresses absence seizures in the rat: comparison with neurotoxic lesions , 1998, Epilepsy Research.

[89]  Walter Paulus,et al.  Low-frequency repetitive transcranial magnetic stimulation improves intractable epilepsy , 1999, The Lancet.

[90]  Ulf Ziemann,et al.  Altered seizure susceptibility after high-frequency transcranial magnetic stimulation in rats , 1999, Neuroscience Letters.

[91]  M. Apuzzo,et al.  Long-Term Multicenter Experience with Vagus Nerve Stimulation for Intractable Partial Seizures , 2000, Stereotactic and Functional Neurosurgery.

[92]  Effect of high frequency stimulation on epileptiform activity in the hippocampus , 1999 .

[93]  M. Apuzzo,et al.  Vagus Nerve Stimulation for Intractable Partial Seizures: Results of the XE5 Trial , 1999 .

[94]  Enrico Gobbetti,et al.  Encyclopedia of Electrical and Electronics Engineering , 1999 .

[95]  D. Durand,et al.  Modulation of burst frequency, duration, and amplitude in the zero-Ca(2+) model of epileptiform activity. , 1999, Journal of neurophysiology.

[96]  D. Durand,et al.  Electric Stimulation of Excitable Tissue , 1999 .

[97]  R. Lesser,et al.  Brief bursts of pulse stimulation terminate afterdischarges caused by cortical stimulation , 1999, Neurology.

[98]  M Velasco,et al.  Subacute Electrical Stimulation of the Hippocampus Blocks Intractable Temporal Lobe Seizures and Paroxysmal EEG Activities , 2000, Epilepsia.

[99]  D M Durand,et al.  Effects of applied electric fields on low-calcium epileptiform activity in the CA1 region of rat hippocampal slices. , 2000, Journal of neurophysiology.

[100]  W. Grill,et al.  Neuroprosthetic Applications of Electrical Stimulation , 2000, Assistive technology : the official journal of RESNA.

[101]  R. Davis,et al.  Cerebellar stimulation for cerebral palsy spasticity, function, and seizures. , 2000, Archives of medical research.

[102]  B. Uthman.  Vagus nerve stimulation for seizures. , 2000, Archives of medical research.

[103]  Christopher R. Johnson.  Numerical Methods for Bioelectric Field Problems , 2000 .

[104]  Erika E. Fanselow,et al.  Reduction of Pentylenetetrazole-Induced Seizure Activity in Awake Rats by Seizure-Triggered Trigeminal Nerve Stimulation , 2000, The Journal of Neuroscience.

[105]  O. Steinlein,et al.  Ion channels and epilepsy in man and mouse. , 2000, Current opinion in genetics & development.

[106]  M Velasco,et al.  Acute and chronic electrical stimulation of the centromedian thalamic nucleus: modulation of reticulo-cortical systems and predictor factors for generalized seizure control. , 2000, Archives of medical research.

[107]  B. Erwin,et al.  Mechanisms of deep brain stimulation and future technical developments , 2000, Neurological research.

[108]  Dominique M. Durand,et al.  A 3D differential coil design for localized magnetic stimulation , 2000, Proceedings of the 22nd Annual International Conference of the IEEE Engineering in Medicine and Biology Society (Cat. No.00CH37143).

[109]  N. O. Dalby.  GABA-level increasing and anticonvulsant effects of three different GABA uptake inhibitors , 2000, Neuropharmacology.

[110]  Robert Plonsey,et al.  Electrical Stimulation of Excitable Tissue , 2000 .

[111]  D M Durand,et al.  Suppression of epileptiform activity by high frequency sinusoidal fields in rat hippocampal slices , 2001, The Journal of physiology.

[112]  Dominique M. Durand,et al.  A 3-D differential coil design for localized magnetic stimulation , 2001, IEEE Transactions on Biomedical Engineering.