Neurophysiologic Findings of Neuronal Migration Disorders: Intrinsic Epileptogenicity of Focal Cortical Dysplasia on Electroencephalography,Electrocorticography,and Magnetoencephalography

Abstract

We define specific neurophysiologic characteristics for focal cortical dysplasia, a neuronal migration disorder. We reviewed data from published reports and our patients with focal cortical dysplasia. Our patients underwent preoperative scalp video-electroencephalography (EEG), magnetic resonance imaging (MRI), magnetoencephalography, and intraoperative or extraoperative electrocorticography monitoring. Scalp EEG showed trains of rhythmic epileptiform spike or sharp waves. Positive spikes correlated with early seizure onset, MRI lesion around the rolandic fissure, hemiparesis, and a less favorable outcome. Interictal electrocorticography showed continuous epileptogenic discharges: repetitive electrographic seizures and bursting discharges or continuous or quasicontinuous rhythmic spiking. Ictal electrocorticography showed paroxysmal fast and/or repetitive spiking. Magnetoencephalography showed clustered spike sources within and extending from the lesion. Cortical stimulation gave more frequent, lower-threshold afterdischarges and higher-threshold primary motor function. Focal cortical dysplasias are highly and intrinsically epileptogenic. For surgical seizure control, EEG, electrocorticography, and magnetoencephalography must delineate the intrinsic epileptogenic zone within and extending from the focal cortical dysplasia identified by MRI. (J Child Neurol 2005;20:357—363).

Get full access to this article

View all access options for this article.

References

Woo C. , Chuang SH , Becker LE , et al: Radiological-pathological correlation in focal cortical dysplasia and hemimegalencephaly in 18 children. Pediatr Neurol 2001; 25: 295—303.

Palmini A. , Gambardella A. , Andermann F. , et al: Intrinsic epileptogenicity of human dysplastic cortex as suggested by corticography and surgical results. Ann Neurol 1995;37:476—487.

Gambardella A. , Palmini A. , Andermann F. , et al: Usefulness of focal rhythmic discharges on scalp EEG of patients with focal cortical dysplasia and intractable epilepsy . Electroencephalogr Clin Neurophysiol 1996 ;98:243—249.

Boonyapisit K. , Najm I. , Klem G. , et al: Epileptogenicity of focal malformations due to abnormal cortical development: Direct electrocorticographic-histopathologic correlations. Epilepsia 2003;44:69—76.

Franciones S. , Nobili L. , Cardinale F. , et al: Intra-lesional stereo-EEG activity in Taylor's focal cortical dysplasia. Epileptic Disord 2003;5(Suppl 2):105—114.

Abraham K. , Ajmone Marsan C : Patterns of cortical discharges and their relation to routine scalp electroencephalography . Electroencephalogr Clin Neurophysiol 1958 ; 10: 447—461.

Cooper R. , Winter AL , Crow HJ , Walter WG : Comparison of sub-cortical, cortical and scalp activity using chronically indwelling electrodes in man. Electroencephalogr Clin Neurophysiol 1965;18:217—228.

Zimmerman JE , Thiene P. , Harding JT : Design and operation of stable rf-biased superconducting quantum interference devices and a note on the properties of perfectly clean metal contacts. J Appl Physiol 1970;41:1572—1580.

Cohen D. : Magnetoencephalography: Detection of the brain's electrical activity with a superconducting magnetometer. Science 1972 ;175:664—666.

10.

Brodmann K. : Vergleichende Localisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig, JA Barth, 1909.

11.

Barth DS , Suthering WW , Engel J.Jr , Beatty J. : Neuromagnetic localization of epileptiform spike activity in the human brain . Science 1982;218:891—894.

12.

Gallen CC , Hirschkoff EC , Buchanan DS : Magnetoencephalography and magnetic source imaging. Neuroimaging Clin N Am 1995;5:227—249.

13.

Hari R. : The neuromagnetic method in the study of the human auditory cortex. Adv Audiol 1990;6:222—282.

14.

Hämäläinen MS : Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain. Rev Mod Physics 1993;65:413—497.

15.

Oishi M. , Otsubo H. , Kameyama S. , et al: Epileptic spikes: Magnetoencephalography versus simultaneous electrocorticography. Epilepsia 2002;43:1390—1395.

16.

Merlet I. , Paetau R. , Garcia-Larrea L. , et al: Apparent asynchrony between interictal electric and magnetic spikes. Neuroreport 1997;8:1071—1076.

17.

Sato S. , Balish M. , Muratore R. : Principles of magnetoencephalography. J Clin Neurophysiol 1991;8:144—156.

18.

Snead OC III: Surgical treatment of medically refractory epilepsy in childhood. Brain Dev 2001;23:199—207.

19.

Iida K. , Otsubo H. , Matsumoto Y. , et al: Characterizing magnetic spike sources with magnetoencephalogaphy-guided neuronavigation in pediatric epilepsy surgery. J Neurosurg: Pediatrics 2005, in press.

20.

Lesser RP , Luders H. , Klem G. , et al: Cortical afterdischarge and functional response thresholds: Results of extraoperative testing. Epilepsia 1984;25:615—621.

21.

Desbiens R. , Berkovic SF , Dubeau F. , et al: Life-threatening focal status epilepticus due to occult cortical dysplasia. Arch Neurol 1993;50:695—700.

22.

Gregory DL , Wong PK : The clinical significance of positive spike discharges in newborns and children . Am J EEG Technol 1992;32:103—117.

23.

Matsuo F. , Knott JR : Focal positive spikes in electroencephalography. Electroencephalogr Clin Neurophysiol 1977;42:15—25.

24.

Otsubo H. , Steinlin M. , Hwang PA , et al: Positive epileptiform discharges in children with neuronal migration disorders. Pediatr Neurol 1997;16:23—31.

25.

Otsubo H. , Ochi A. , Elliott I. , et al: MEG predicts epileptic zone in lesional extrahippocampal epilepsy: 12 pediatric epilepsy surgery cases. Epilepsia 2001;42:1523—1530.

26.

Header W. , Mackay M. , Otsubo H. , et al: Cortical dysplastic lesions in children with intractable epilepsy: Role of complete neurosurgical resection. J Neurosurg 2004;100:118—124.

27.

Knowlton RC , Laxer KD , Aminoff MJ , et al: Magnetoencephalography in partial epilepsy: Clinical yield and localization accuracy. Ann Neurol 1997;42:622—631.

28.

Minassian BA , Otsubo H. , Weiss S. , et al: Magnetoencephalographic localization in pediatric epilepsy surgery: Comparison with invasive intracranial electroencephalography . Ann Neurol 1999; 46:627—633.

29.

Morioka T. , Nishio S. , Ishibashi H. , et al: Intrinsic epileptogenicity of focal cortical dysplasia as revealed by magnetoencephalography and electrocorticography. Epilepsy Res 1999;33:177—187.

30.

Smith JR , Schwartz BJ , Gallen C. , et al: Utilization of multichannel magnetoencephalography in the guidance of ablative seizure surgery. J Epilepsy 1995 ;8:1191—1203.

31.

Bast T. , Oezkan O. , Rona S. , et al: EEG and MEG source analysis of single and averaged interictal spikes reveals intrinsic epileptogenicity in focal cortical dysplasia. Epilepsia 2004;45:621—631.

32.

Edwards JC , Wyllie E. , Ruggeri PM , et al: Seizure outcome after surgery for epilepsy due to malformation of cortical development. Neurology 2000;55:1110—1114.

33.

Otsubo H. , Chitoku S. , Ochi A. , et al: Diagnosis and treatment of malignant rolandic-sylvian epilepsy in children: Magnetoencephalography, intracranial invasive video-EEG and surgery . Neurology 2001;57:590—596.

34.

Otsubo H. , Hwang PA , Jay V. , et al: Focal cortical dysplasia in children with localization-related epilepsy: EEG, MRI, and SPECT findings. Pediatr Neurol 1993; 9: 101—107.

35.

Sheth RD , Guiterrez AR , Riggs JE : Rolandic epilepsy and cortical dysplasia: MRI correlation of epileptiform discharges. Pediatr Neurol 1997;17:177—179.

36.

Kuzniecky R. , Berkovic S. , Andermann F. , et al: Focal cortical myoclonus and rolandic cortical dysplasia: Clarification by magnetic resonance imaging. Ann Neurol 1988;23:317—325.

37.

Kuzniecky R. , Morawetz R. , Faught E. , Black L. : Frontal and central lobe focal dysplasia: Clinical, EEG and imaging features. Dev Med Child Neurol 1995;37:159—166.

38.

Wyllie E. , Luders H. , Morris HH , et al: Subdural electrodes in the evaluation for epilepsy surgery in children and adults. Neuropediatrics 1988; 19:80-86.

39.

Jayakar P. , Alvarez LA , Duchowny MS , Resnick TJ : A safe and effective paradigm to functionally map the cortex in childhood . J Clin Neurophysiol 1992;9:288—293.

40.

Chitoku S. , Otsubo H. , Harada Y. , et al: Extraoperative cortical stimulation of motor function in children . Pediatr Neurol 2001;24:344—350.

41.

Penfield WJ , Jasper HH : Epilepsy and the Functional Anatomy of the Human Brain. Boston, Little Brown, 1954.

42.

Jayakar P. : Invasive EEG monitoring in children. When, where, and what? J Clin Neurophysiol 1999;16:408—418.

43.

Walker AE : Electrocorticography in epilepsy. A surgeon's appraisal. Electroencephalogr Clin Neurophysiol 1951;1(Suppl):S2.

44.

Jacobs KM , Gutnick MJ , Prince DA : Hyperexcitability in a model of cortical maldevelopment. Cereb Cortex 1996;6:511—523.

45.

Holmes GL , Sarkisian M. , Ben-Ari Y. , et al: Consequences of cortical dysplasia during development in rats . Epilepsia 1999;40: 537—544.

46.

Chitoku S. , Otsubo H. , Hara Y. , et al: Characteristics of prolonged afterdischarge: Children with malformation of cortical development. J Child Neurol 2003 ;18:247—253.

47.

Duchowny M. , Jayakar P. , Levin B. : Aberrant neural circuits in malformations of cortical development and focal epilepsy. Neurology 2000;55:423—428.

48.

Tassi L. , Pasquier B. , Minotti L. , et al: Cortical dysplasia: Electro-clinical, imaging, and neuropathologic study of 13 patients. Epilepsia 2001;42:1112—1123.

49.

Marusic P. , Najm IM , Ying Z. , et al: Focal cortical dysplasias in eloquent cortex: Functional characteristics and correlation with MRI and histopathologic changes. Epilepsia 2002;43:27—32.

50.

Akai T. , Otsubo H. , Pang EW , et al: Complex central cortex in pediatric patients with malformations of cortical development. J Child Neurol 2002 ;17:347—352.

51.

Palmini A. , Najm I. , Avanzini G. , et al: Terminology and classification of the cortical dysplasias. Neurology 2004;62(Suppl 3):S2—S8.

52.

Rosenow F. , Luders HO , Dinner DS , et al: Histopathological correlates of epileptogenicity as expressed by electrocorticographic spiking and seizure frequency. Epilepsia 1998;39:850—856.

53.

Jones AC , Shyamsundar MM , Thomas MW , et al: Comprehensive mutation analysis of TSC1 and TSC2 and phenotypic correlations in 150 families with tuberous sclerosis. Am J Hum Genet 1999;64:5013—5015.

54.

Roach ES , Gomez MR , Northrup H. : Tuberous sclerosis complex consensus conference: Revised clinical diagnostic criteria. J Child Neurol 1998;13:624—628.

55.

Mackay MT , Becker LE , Chuang SH , et al: Malformation of cortical development with balloon cells; Clinical and radiological correlates in children. Neurology 2003;60:580—586.