Deep Brain Stimulation in Epilepsy

Summary Since the pioneering studies of Cooper et al. to influence epilepsy by cerebellar stimulation, numerous attempts have been made to reduce seizure frequency by stimulation of deep brain structures. Evidence from experimental animal studies suggests the existence of a nigral control of the epilepsy system. It is hypothesized that the dorsal midbrain anticonvulsant zone in the superior colliculi is under inhibitory control of efferents from the substantia nigra pars reticulata. Inhibition of the subthalamic nucleus (STN) could release the inhibitory effect of the substantia nigra pars reticulata on the dorsal midbrain anticonvulsant zone and thus activate the latter, raising the seizure threshold. Modulation of the seizure threshold by stimulation of deep brain structures—in particular, of the STN—is a promising future treatment option for patients with pharmacologically intractable epilepsy. Experimental studies supporting the existence of the nigral control of epilepsy system and preliminary results of STN stimulation in animals and humans are reviewed, and alternative mechanisms of seizure suppression by STN stimulation are discussed.

[1]  A. A. Leão,et al.  SPREADING DEPRESSION OF ACTIVITY IN THE CEREBRAL CORTEX , 1944 .

[2]  M. Meyer A study of efferent connexions of the frontal lobe in the human brain after leucotomy. , 1949, Brain : a journal of neurology.

[3]  R.N.Dej.,et al.  Epilepsy and the Functional Anatomy of the Human Brain , 1954, Neurology.

[4]  R. Heath ELECTRICAL SELF-STIMULATION OF THE BRAIN IN MAN. , 1963, The American journal of psychiatry.

[5]  J Bancaud,et al.  [Ammon's horn and amygdaline nucleus: clinical and electric effects of their stimulation in man]. , 1966, Revue neurologique.

[6]  [Epileptic attacks induced by stimulation of the amygdaloid nucleus and horn of Ammon (value of stimulation in the determination of temporal epilepsy in humans)]. , 1968, Revue neurologique.

[7]  S Gilman,et al.  The effect of chronic cerebellar stimulation upon epilepsy in man. , 1973, Transactions of the American Neurological Association.

[8]  H. Fields,et al.  Stimulation of internal capsule for relief of chronic pain. , 1974, Journal of neurosurgery.

[9]  I. Cooper,et al.  Chronic cerebellar stimulation in epilepsy. Clinical and anatomical studies. , 1976, Archives of neurology.

[10]  I S Cooper,et al.  Safety and efficacy of chronic cerebellar stimulation. , 1977, Applied neurophysiology.

[11]  K. Akert,et al.  Efferent connections of cortical, area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique , 1977, The Journal of comparative neurology.

[12]  J. V. Van Buren,et al.  Preliminary evaluation of cerebellar stimulation by double-blind stimulation and biological criteria in the treatment of epilepsy. , 1978, Journal of neurosurgery.

[13]  W. Schultz,et al.  Proximal limb movements in response to microstimulation of primate dentate and interpositus nuclei mediated by brain-stem structures. , 1979, Brain : a journal of neurology.

[14]  K. Usunoff,et al.  Corticosubthalamic projection in the cat: an electron microscopic study , 1979, Brain Research.

[15]  A. Upton,et al.  Reversibility of chronic neurologic deficits. Some effects of electrical stimulation of the thalamus and internal capsule in man. , 1980, Applied neurophysiology.

[16]  M. Iadarola,et al.  Seizure protection and increased nerve-terminal GABA: delayed effects of GABA transaminase inhibition. , 1980, Science.

[17]  H. Morton,et al.  Stimulation of the cerebral cortex in the intact human subject , 1980, Nature.

[18]  Jeffrey T. Keller,et al.  Connections of the subthalamic nucleus in the monkey , 1981, Brain Research.

[19]  M. Iadarola,et al.  Substantia nigra: site of anticonvulsant activity mediated by gamma-aminobutyric acid. , 1982, Science.

[20]  J. McNamara,et al.  Evidence that Substantia Nigra is crucial to neural network of kindled seizures. , 1983, European journal of pharmacology.

[21]  K. Gale,et al.  Lesions of substantia nigra protect against experimentally induced seizures , 1983, Brain Research.

[22]  M. Kaijima,et al.  Abortive amygdaloid kindled seizures following micro-injection of γ-vinyl-GABA in the vicinity of substantia nigra in rats , 1983, Neuroscience Letters.

[23]  L. P. Gonzalez,et al.  Intranigral muscimol suppresses ethanol withdrawal seizures , 1984, Brain Research.

[24]  R. Lesser,et al.  Transient neuropsychological abnormalities (including Gerstmann's Symdrome) during cortical stimulation , 1984, Neurology.

[25]  H. Kornhuber,et al.  The cortico-nigral projection: reduced glutamate content in the substantia nigra following frontal cortex ablation in the rat , 1984, Brain Research.

[26]  D. Mclellan,et al.  A double-blind trial of chronic cerebellar stimulation in twelve patients with severe epilepsy. , 1984, Journal of neurology, neurosurgery, and psychiatry.

[27]  J. McNamara,et al.  Evidence implicating substantia nigra in regulation of kindled seizure threshold , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  K. Gale,et al.  Infusion of opiates into substantia nigra protects against maximal electroshock seizures in rats. , 1985, The Journal of pharmacology and experimental therapeutics.

[29]  W. Löscher,et al.  Evidence for impaired GABAergic activity in the substantia nigra of amygdaloid kindled rats , 1985, Brain Research.

[30]  R. Browning,et al.  Effect of Midbrain and Pontine Tegmental Lesions on Audiogenic Seizures in Genetically Epilepsy‐Prone Rats , 1985, Epilepsia.

[31]  I. S. Cooper,et al.  Therapeutic implications of modulation of metabolism and functional activity of cerebral cortex by chronic stimulation of cerebellum and thalamus , 1985, Biological Psychiatry.

[32]  J. Deniau,et al.  Disinhibition as a basic process in the expression of striatal functions. I. The striato-nigral influence on tecto-spinal/tecto-diencephalic neurons , 1985, Brain Research.

[33]  S Afsharpour,et al.  Topographical projections of the cerebral cortex to the subthalamic nucleus , 1985, The Journal of comparative neurology.

[34]  A R Upton,et al.  Suppression of seizures and psychosis of limbic system origin by chronic stimulation of anterior nucleus of the thalamus. , 1985, International journal of neurology.

[35]  Browning Ra,et al.  Role of the brain-stem reticular formation in tonic-clonic seizures: lesion and pharmacological studies. , 1985 .

[36]  M. Iadarola,et al.  Substance P antagonists in substantia nigra are anticonvulsant , 1986, Brain Research.

[37]  B. Meldrum,et al.  Excitatory neurotransmission within substantia nigra pars reticulata regulates threshold for seizures produced by pilocarpine in rats: Effects of intranigral 2-amino-7-phosphonoheptanoate and n-methyl-d-aspartate , 1986, Neuroscience.

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

[39]  Y. Hosobuchi Subcortical electrical stimulation for control of intractable pain in humans. Report of 122 cases (1970-1984). , 1986, Journal of neurosurgery.

[40]  Marek A. Mirski,et al.  Anterior thalamus and substantia nigra: two distinct structures mediating experimental generalized seizures , 1986, Brain Research.

[41]  B. Meldrum,et al.  Anticonvulsant action of a kainate antagonist gamma-D-glutamyl aminomethylsulphonic acid injected focally into the substantia nigra and entopeduncular nucleus. , 1986, European journal of pharmacology.

[42]  T. Klockgether,et al.  Susceptibility to seizures produced by pilocarpine in rats after microinjection of isonnazid or γ-vinyl-GABA into the substantia nigra , 1986, Brain Research.

[43]  E. Cavalheiro,et al.  Intrastriatal N-methyl-d-aspartate prevents amygdala kindled seizures in rats , 1986, Brain Research.

[44]  K. Gale,et al.  Role of the substantia nigra in GABA-mediated anticonvulsant actions. , 1986, Advances in neurology.

[45]  J. McNamara,et al.  Microinjection of a benzodiazepine into substantia nigra elevates kindled seizure threshold , 1987, Brain Research.

[46]  J. McNamara,et al.  Evidence implicating alpha-2 adrenergic receptors in the anticonvulsant action of intranigral muscimol. , 1987, The Journal of pharmacology and experimental therapeutics.

[47]  M. Kudo,et al.  Ultrastructural analyses of afferent terminals in the subthalamic nucleus of the cat with a combined degeneration and horseradish peroxidase tracing method , 1987, The Journal of comparative neurology.

[48]  K. Gale,et al.  Substantia nigra-mediated anticonvulsant actions: Role of nigral output pathways , 1987, Experimental Neurology.

[49]  J. McNamara,et al.  The role of substantia nigra in the development of kindling: pharmacologic and lesion studies , 1987, Brain Research.

[50]  W. Löscher,et al.  Further evidence for abnormal GABAergic circuits in amygdala-kindled rats , 1987, Brain Research.

[51]  M Velasco,et al.  Electrical Stimulation of the Centromedian Thalamic Nucleus in the Treatment of Convulsive Seizures: A Preliminary Report , 1987, Epilepsia.

[52]  Hamid R. Toussi,et al.  Suppression of methionine sulfoximine seizures by intranigral γ-vinyl GABA injection , 1987 .

[53]  Suppression of methionine sulfoximine seizures by intranigral gamma-vinyl GABA injection. , 1987, European journal of pharmacology.

[54]  Z. Bortolotto,et al.  Microinjections of the γ-aminobutyrate antagonist, bicuculline methiodide, into the caudate-putamen prevent amygdala-kindled seizures in rats , 1987, Brain Research.

[55]  John W. Miller,et al.  Functional anatomy of pentylenetetrazol and electroshock seizures in the rat brainstem , 1987, Annals of neurology.

[56]  Z. Bortolotto,et al.  Paradoxical anticonvulsant activity of the excitatory amino acid N-methyl-D-aspartate in the rat caudate-putamen. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[57]  A. Depaulis,et al.  Evidence that activation of GABA receptors in the substantia nigra suppresses spontaneous spike-and-wave discharges in the rat , 1988, Brain Research.

[58]  H. Nagaya,et al.  The role of the nigrotegmental GABAergic pathway in the propagation of pentylenetetrazol-induced seizures , 1989, Brain Research.

[59]  A. Depaulis,et al.  Suppressive effects of intranigral injection of muscimol in three models of generalized non-convulsive epilepsy induced by chemical agents , 1989, Brain Research.

[60]  R. Maggio,et al.  Seizures evoked from area tempestas are subject to control by GABA and glutamate receptors in substantia nigra , 1989, Experimental Neurology.

[61]  Hong Zhang,et al.  Injection of benzodiazepines but not GABA or muscimol into pars reticulata of substantia nigra suppresses pentylenetetrazol seizures , 1989, Brain Research.

[62]  J. Deniau,et al.  Disinhibition as a basic process in the expression of striatal functions , 1990, Trends in Neurosciences.

[63]  M. Vergnes,et al.  Involvement of the nigral output pathways in the inhibitory control of the substantia nigra over generalized non-convulsive seizures in the rat , 1990, Neuroscience.

[64]  N. Canteras,et al.  Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat , 1990, Brain Research.

[65]  M Sramka,et al.  Clinical experience in intraoperational determination of brain inhibitory structures and application of implanted neurostimulators in epilepsy. , 1990, Stereotactic and functional neurosurgery.

[66]  The GABAergic nigro-collicular pathway is not involved in the inhibitory control of audiogenic seizures in the rat , 1990, Neuroscience Letters.

[67]  S. Moshé,et al.  Effects of substantia nigra γ-vinyl-GABA infusions on flurothyl seizures in adult rats , 1991, Brain Research.

[68]  Effects of substantia nigra gamma-vinyl-GABA infusions on flurothyl seizures in adult rats. , 1991, Brain research.

[69]  Hong Zhang,et al.  Anticonvulsant actions and interaction of GABA agonists and a benzodiazepine in pars reticulata of substantia nigra , 1991, Epilepsy Research.

[70]  B. Meldrum,et al.  Anticonvulsant action of 2-chloroadenosine injected focally into the inferior colliculus and substantia nigra. , 1991, European journal of pharmacology.

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

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

[73]  A. Depaulis The inhibitory control of the substantia nigra over generalized non-convulsive seizures in the rat. , 1992, Journal of neural transmission. Supplementum.

[74]  P. Dean,et al.  Anticonvulsant role of nigrotectal projection in the maximal electroshock model of epilepsy—II. Pathways from substantia nigra pars lateralis and adjacent peripeduncular area to the dorsal midbrain , 1992, Neuroscience.

[75]  P. Dean,et al.  Anticonvulsant role of nigrotectal projection in the maximal electroshock model of epilepsy—I. Mapping of dorsal midbrain with bicuculline , 1992, Neuroscience.

[76]  S. Moshé,et al.  Age‐Dependent Differences in the Anticonvulsant Effects of 2–Amino‐7‐Phosphono‐Heptanoic Acid or Ketamine Infusions Into the Substantia Nigra of Rats , 1992, Epilepsia.

[77]  R P Lesser,et al.  Placebo‐Controlled Pilot Study of Centromedian Thalamic Stimulation in Treatment of Intractable Seizures , 1992, Epilepsia.

[78]  H. Kita,et al.  Response characteristics of subthalamic neurons to the stimulation of the sensorimotor cortex in the rat , 1993, Brain Research.

[79]  L. Ryan,et al.  Subthalamic nucleus lesion regularizes firing patterns in globus pallidus and substantia nigra pars reticulata neurons in rats , 1993, Brain Research.

[80]  L. Ryan,et al.  Subthalamic nucleus and globus pallidus lesions alter activity in nigrothalamic neurons in rats , 1994, Brain Research Bulletin.

[81]  Harold Morris,et al.  Mirror Focus: Function of Seizure Frequency and Influence on Outcome After Surgery , 1994, Epilepsia.

[82]  Su Vui Lo,et al.  Mortality in epilepsy , 1994, The Lancet.

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

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

[85]  H. Savaki,et al.  Functional Metabolic Mapping of the Rat Brain during Unilateral Electrical Stimulation of the Subthalamic Nucleus , 1994, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[86]  J. Velíšková,et al.  Further evidence of involvement of substantia nigra GABAB receptors in seizure suppression in developing rats. , 1994, Brain research. Developmental brain research.

[87]  Antoine Depaulis,et al.  Endogenous control of epilepsy: The nigral inhibitory system , 1994, Progress in Neurobiology.

[88]  A. Benabid,et al.  Acute and long-term effects of subthalamic nucleus stimulation in Parkinson's disease. , 1994, Stereotactic and functional neurosurgery.

[89]  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.

[90]  Lippincott Williams Wilkins,et al.  A randomized controlled trial of chronic vagus nerve stimulation for treatment of medically intractable seizures , 1995, Neurology.

[91]  A. Parent,et al.  Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop , 1995, Brain Research Reviews.

[92]  F. Fazio,et al.  Increased interictal cerebral glucose metabolism in a cortical-subcortical network in drug naive patients with cryptogenic temporal lobe epilepsy. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[93]  R. Post,et al.  Quenching: inhibition of development and expression of amygdala kindled seizures with low frequency stimulation. , 1995, Neuroreport.

[94]  A. Parent,et al.  Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidium in basal ganglia circuitry , 1995, Brain Research Reviews.

[95]  Cockerell Oc,et al.  The mortality of epilepsy. , 1996 .

[96]  C. Deransart,et al.  Involvement of nigral glutamatergic inputs in the control of seizures in a genetic model of absence epilepsy in the rat , 1996, Neuroscience.

[97]  A L Benabid,et al.  Abnormal involuntary movements induced by subthalamic nucleus stimulation in parkinsonian patients , 1996, Movement disorders : official journal of the Movement Disorder Society.

[98]  E. Bézard,et al.  High frequency stimulation of the internal Globus Pallidus (GPi) simultaneously improves parkinsonian symptoms and reduces the firing frequency of GPi neurons in the MPTP-treated monkey , 1996, Neuroscience Letters.

[99]  M. Rodrigues,et al.  Combined study of99mTc-HMPAO SPECT and computerized electroencephalographic topography (CET) in patients with medically refractory complex partial epilepsy , 1996, Annals of nuclear medicine.

[100]  J. Degos,et al.  Improvement of severe postural cerebellar tremor in multiple sclerosis by chronic thalamic stimulation , 1996, Movement disorders : official journal of the Movement Disorder Society.

[101]  A. Benabid,et al.  Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. , 1996, Journal of neurosurgery.

[102]  S L Moshé,et al.  Subthalamic nucleus: a new anticonvulsant site in the brain. , 1996, Neuroreport.

[103]  S Noachtar,et al.  Localization of Epileptic Auras Induced on Stimulation by Subdural Electrodes , 1997, Epilepsia.

[104]  Robert S Fisher,et al.  Anticonvulsant effect of anterior thalamic high frequency electrical stimulation in the rat , 1997, Epilepsy Research.

[105]  A. Benabid,et al.  Roles of GABA, glutamate, acetylcholine and STN stimulation on thalamic VM in rats , 1997, Neuroreport.

[106]  S A Chkhenkeli,et al.  Effects of therapeutic stimulation of nucleus caudatus on epileptic electrical activity of brain in patients with intractable epilepsy. , 1997, Stereotactic and functional neurosurgery.

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

[108]  D. R. Smith,et al.  Behavioural assessment of mice lacking D1A dopamine receptors , 1998, Neuroscience.

[109]  J. Deniau,et al.  Relationships between the Prefrontal Cortex and the Basal Ganglia in the Rat: Physiology of the Corticosubthalamic Circuits , 1998, The Journal of Neuroscience.

[110]  A. Benabid,et al.  Long‐Term Electrical Inhibition of Deep Brain Targets in Movement Disorders , 2008, Movement disorders : official journal of the Movement Disorder Society.

[111]  Colin Deransart,et al.  Role of the subthalamo-nigral input in the control of amygdala-kindled seizures in the rat , 1998, Brain Research.

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

[113]  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.

[114]  R. J. Allan,et al.  Neurophysiological identification of the subthalamic nucleus in surgery for Parkinson's disease , 1998, Annals of neurology.

[115]  Y. Smith,et al.  Microcircuitry of the direct and indirect pathways of the basal ganglia. , 1998, Neuroscience.

[116]  R. Browning,et al.  Effect of Precollicular Transection on Audiogenic Seizures in Genetically Epilepsy-Prone Rats , 1999, Experimental Neurology.

[117]  E. Montgomery,et al.  Chronic thalamic stimulation for the tremor of multiple sclerosis , 1999, Neurology.

[118]  J. Tepper,et al.  Subthalamic stimulation-induced synaptic responses in substantia nigra pars compacta dopaminergic neurons in vitro. , 1999, Journal of neurophysiology.

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

[120]  C. Deransart,et al.  Evidence for the involvement of the pallidum in the modulation of seizures in a genetic model of absence epilepsy in the rat , 1999, Neuroscience Letters.

[121]  C. L. Kwan,et al.  Thalamic stimulation and functional magnetic resonance imaging: localization of cortical and subcortical activation with implanted electrodes. Technical note. , 1999 .

[122]  A. Lozano,et al.  Comparative effects of unilateral and bilateral subthalamic nucleus deep brain stimulation , 1999, Neurology.

[123]  A L Benabid,et al.  Bilateral subthalamic or pallidal stimulation for Parkinson's disease affects neither memory nor executive functions: A consecutive series of 62 patients , 1999, Annals of neurology.

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

[125]  P. Pollak,et al.  Transient acute depression induced by high-frequency deep-brain stimulation. , 1999, The New England journal of medicine.

[126]  J. Rothwell,et al.  The impact of deep brain stimulation on executive function in Parkinson's disease. , 2000, Brain : a journal of neurology.

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

[128]  M. Kitagawa,et al.  Deep brain stimulation of subthalamic area for severe proximal tremor , 2000, Neurology.

[129]  A. Benabid,et al.  Effect of high-frequency stimulation of the subthalamic nucleus on the neuronal activities of the substantia nigra pars reticulata and ventrolateral nucleus of the thalamus in the rat , 2000, Neuroscience.

[130]  J. Bolam,et al.  Relationship of Activity in the Subthalamic Nucleus–Globus Pallidus Network to Cortical Electroencephalogram , 2000, The Journal of Neuroscience.

[131]  A. Benabid,et al.  Future prospects of brain stimlation , 2000, Neurological research.

[132]  A L Benabid,et al.  Neuropsychological changes between “off” and “on” STN or GPi stimulation in Parkinson’s disease , 2000, Neurology.

[133]  K. Nakano Neural circuits and topographic organization of the basal ganglia and related regions , 2000, Brain and Development.

[134]  Y. Katayama,et al.  Thalamotomy Caused by Cardioversion in a Patient Treated with Deep Brain Stimulation , 2001, Stereotactic and Functional Neurosurgery.

[135]  W C Koller,et al.  Deep brain stimulation of the Vim nucleus of the thalamus for the treatment of tremor. , 2000, Neurology.

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

[137]  K. Gale,et al.  Postural and Anticonvulsant Effects of Inhibition of the Rat Subthalamic Nucleus , 2000, The Journal of Neuroscience.

[138]  P J Kelly,et al.  Comparison of anatomic and neurophysiological methods for subthalamic nucleus targeting. , 2000, Neurosurgery.

[139]  A L Benabid,et al.  Deep brain stimulation of the subthalamic nucleus for Parkinson's disease: methodologic aspects and clinical criteria. , 2000, Neurology.

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

[141]  M Velasco,et al.  Centromedian–Thalamic and Hippocampal Electrical Stimulation for the Control of Intractable Epileptic Seizures , 2001, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[142]  W. Hacke,et al.  Deep brain stimulation for the treatment of Parkinson's disease: subthalamic nucleus versus globus pallidus internus , 2001, Journal of neurology, neurosurgery, and psychiatry.

[143]  H. Lüders Clinical evidence for secondary epileptogenesis. , 2001, International review of neurobiology.

[144]  C. Hammond,et al.  High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. , 2001, Journal of neurophysiology.

[145]  Tamer S. Issa,et al.  DBS and diathermy interaction induces severe CNS damage , 2001, Neurology.

[146]  Philippe Kahane,et al.  Deep brain stimulation in epilepsy with particular reference to the subthalamic nucleus. , 2002, Epileptic disorders : international epilepsy journal with videotape.

[147]  Mojgan Hodaie,et al.  Chronic Anterior Thalamus Stimulation for Intractable Epilepsy , 2002, Epilepsia.

[148]  C. Deransart,et al.  The control of seizures by the basal ganglia? A review of experimental data. , 2002, Epileptic disorders : international epilepsy journal with videotape.