Single-pulse electrical stimulation identifies epileptogenic frontal cortex in the human brain

Objective: To assess the value of single-pulse electrical stimulation (SPES) to identify frontal epileptogenic cortex during presurgical assessment. Methods: SPES (1-millisecond pulses, 4 to 8 mA, 0.1 Hz) has been used during chronic recordings in 30 patients with intracranial electrodes in the frontal lobes. As a result of presurgical assessment, 17 patients were considered to have frontal epilepsy and 13 extrafrontal epilepsy. Results: Two types of responses to SPES were seen: 1) early responses: starting immediately after the stimulus and considered as normal responses; 2) late responses: two types of responses seen in some areas after the initial early response: a) delayed responses: spikes or sharp waves occurring between 100 milliseconds and 1 second after stimulation. Frontal delayed responses were seen in 11 frontal patients and 1 extrafrontal patient, whereas extrafrontal delayed responses were seen in 1 frontal and 10 extrafrontal patients. b) Repetitive responses: two or more consecutive sharp-and-slow-wave complexes, each resembling the initial early response. Repetitive responses were seen only when stimulating the frontal lobes of 10 frontal patients. Among the 17 frontal patients, 13 had late responses exclusively in the epileptogenic frontal lobe, whereas only 3 showed them in both frontal lobes. Frontal late responses were associated with neuropathologic abnormalities, and complete resection of abnormal SPES areas was associated with good postsurgical seizure outcome. Conclusions: Single-pulse electrical stimulation (SPES) could be an important additional investigation during presurgical assessment to identify frontal epileptogenicity. SPES can be useful in patients who have widespread or multiple epileptogenic areas, normal neuroimaging, or few seizures during telemetry.

[1]  L F Quesney,et al.  Presurgical EEG investigation in frontal lobe epilepsy. , 1992, Epilepsy research. Supplement.

[2]  M. Cortez,et al.  Brain Sterols in the AY‐9944 Rat Model of Atypical Absence Seizures , 2002, Epilepsia.

[3]  G. Alarcón,et al.  Power spectrum and intracranial EEG patterns at seizure onset in partial epilepsy. , 1995, Electroencephalography and clinical neurophysiology.

[4]  M. Brazier,et al.  EVOKED RESPONSES RECORDED FROM THE DEPTHS OF THE HUMAN BRAIN , 1964, Annals of the New York Academy of Sciences.

[5]  C D Binnie,et al.  Prognostic factors in presurgical assessment of frontal lobe epilepsy , 1999, Journal of neurology, neurosurgery, and psychiatry.

[6]  R G Grossman,et al.  Electrophysiological connections between the hippocampus and entorhinal cortex in patients with complex partial seizures. , 1989, Journal of neurosurgery.

[7]  B W Connors,et al.  Synchronized excitation and inhibition driven by intrinsically bursting neurons in neocortex. , 1989, Journal of neurophysiology.

[8]  J. Jefferys,et al.  Ictal Epileptiform Activity Is Facilitated by Hippocampal GABAA Receptor-Mediated Oscillations , 2000, The Journal of Neuroscience.

[9]  J G Jefferys,et al.  Chronic epileptic foci in vitro in hippocampal slices from rats with the tetanus toxin epileptic syndrome. , 1989, Journal of neurophysiology.

[10]  Jerome Engel,et al.  Outcome with respect to epileptic seizures. , 1993 .

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

[12]  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.

[13]  P. Williamson Frontal lobe seizures. Problems of diagnosis and classification. , 1992, Advances in neurology.

[14]  M. Gutnick,et al.  Injection of tetanus toxin into the neocortex elicits persistent epileptiform activity but only transient impairment of GABA release , 1993, Neuroscience.

[15]  S. Schachter,et al.  A Workshop on Antiepileptic Drug Monotherapy Indications , 2002, Epilepsia.

[16]  P. Chauvel,et al.  Callosal transfer between mesial frontal areas in frontal lobe epilepsies. , 1992, Advances in neurology.

[17]  T L Babb,et al.  Functional connections in the human temporal lobe , 2004, Experimental Brain Research.

[18]  J Bancaud,et al.  Unilateral connections between amygdala and hippocampus in man. A study of epileptic patients with depth electrodes. , 1983, Electroencephalography and clinical neurophysiology.

[19]  C D Binnie,et al.  Responses to single pulse electrical stimulation identify epileptogenesis in the human brain in vivo. , 2002, Brain : a journal of neurology.

[20]  C. Jack,et al.  Factors Predictive of the Outcome of Frontal Lobe Epilepsy Surgery , 2000, Epilepsia.

[21]  T. Rasmussen Tailoring of Cortical Excisions for Frontal Lobe Epilepsy , 1991, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.