Pathophysiology and functional consequences of human partial epilepsy: Lessons from positron emission tomography studies

Acta Physiologica Hungarica

Volumn 90, Issue 4, 2003, Pages 281-303

  Juhász, Csaba ^a,b   Chugani, Diane C ^a   Chugani, H T ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CHILDREN'S HOSPITAL OF MICHIGAN   (United States)

Author keywords

Cognitive and behavioral abnormalities; Cortical and subcortical brain dysfunction; Epilepsy; Neuroimaging; Positron emission tomography

Indexed keywords

TRACER;

BEHAVIOR DISORDER; BRAIN CORTEX; BRAIN METABOLISM; COGNITIVE DEFECT; CORRELATION ANALYSIS; DISEASE ASSOCIATION; ELECTROPHYSIOLOGY; EPILEPTOGENESIS; FOCAL EPILEPSY; HUMAN; NERVE CELL NETWORK; NEUROIMAGING; NEUROPATHOLOGY; POSITRON EMISSION TOMOGRAPHY; PREOPERATIVE EVALUATION; REVIEW; SEIZURE;

EPILEPSIES, PARTIAL; HUMANS; TOMOGRAPHY, EMISSION-COMPUTED;

EID: 0348048557     PISSN: 0231424X     EISSN: None     Source Type: Journal    
DOI: 10.1556/APhysiol.90.2003.4.2     Document Type: Review

References (98)

1. Azmitia EC, Whitaker-Azmitia PM: Awakening the sleeping giant: anatomy and plasticity of the brain serotonergic system. J. Clin. Psychiatry 52 (Suppl), 4-16 (1991)
2. Bentourkia M, Michel C, Ferriere G, Bol A, Coppens A, Sibomana M, Bausart R, Labar D, De Volder AG: Evolution of brain glucose metabolism with age in epileptic infants, children and adolescents. Brain Dev. 20, 524-529 (1998)
3. Bernasconi A, Antel SB, Collins DL et al.: Texture analysis and morphological processing of magnetic resonance imaging assist detection of focal cortical dysplasia in extra-temporal partial epilepsy. Ann. Neurol. 49, 770-775 (2001)
4. Bittar RG, Andermann F, Olivier A et al.: Interictal spikes increase cerebral glucose metabolism and blood flow: a PET study. Epilepsia 40, 170-178 (1999)
5. Bruehl C, Witte OW: Cellular activity underlying altered brain metabolism during focal epileptic activity. Ann. Neurol. 38, 414-420 (1995)
6. Cavazos JE, Das I, Sutula TP: Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J. Neurosci. 14, 3106-3121 (1994)
7. Cendes F, Andermann F, Gloor P et al.: MRI volumetric measurement of amygdala and hippocampus in temporal lobe epilepsy. Neurology 43, 719-725 (1993)
8. Cendes F, Caramanos Z, Andermann F, Dubeau F, Arnold DL: Proton magnetic resonance spectroscopic imaging and magnetic resonance imaging volumetry in the lateralization of temporal lobe epilepsy: a series of 100 patients. Ann. Neurol. 42, 737-746 (1997)
9. Chan S, Chin SS, Nordli DR, Goodman RR, DeLaPaz RL, Pedley TA: Prospective magnetic resonance imaging identification of focal cortical dysplasia, including the noll-balloon cell subtype. Ann. Neurol. 44, 749-757 (1998)
10. 11C]methyl-L-tryptophan positron emission tomography. Ann. Neurol. 44, 858-866 (1998)
11. 11C]-methyl-L-tryptophan metabolism via the kynurenine pathway in tuberous sclerosis complex. Neuroscience 24, 692 [Abstract] (1998)
12. 18FDG positron emission tomography. Science 231, 840-843 (1986)
13. Chugani HT, Phelps ME, Mazziotta JC: Positron emission tomography study of human brain functional development. Ann. Neurol. 22, 487-97 (1987)
14. Chugani HT, Shields WD, Shewmon DA et al.: Infantile spasms: I. PET identifies focal cortical dysgenesis in cryptogenic cases for surgical treatment. Ann. Neurol. 27, 406-413 (1990)
15. Chugani HT, Shewmon DA, Sankar R et al.: Infantile spasms: II. Lenticular nuclei and brain stem activation on positron emission tomography. Ann. Neurol. 31, 212-219 (1992)
16. Chugani HT, Shewmon DA, Shields WD et al.: Surgery for intractable infantile spasms: neuroimaging perspectives. Epilepsia 34, 764-771 (1993)
17. Chugani HT, Jacobs B: Metabolic recovery in caudate nucleus of children following cerebral hemispherectomy. Ann. Neurol. 36, 794-797 (1994)
18. Chugani HT, Rintahaka PJ, Shewmon DA: Ictal patterns of cerebral glucose utilization in children with epilepsy. Epilepsia 35, 813-822 (1994)
19. Chugani HT, da Silva E, Chugani DC: Infantile spasms: III. Prognostic implications of bitemporal hypometabolism on positron emission tomography. Ann. Neurol. 39, 643-649 (1996)
20. 14C] deoxyglucose. Brain Res. 150, 487-501 (1978)
21. Crino PB, Eberwine J: Cellular and molecular basis of cerebral dysgenesis. J. Neurosci. Res. 50, 907-916 (1997)
22. DeCarli C, Hatta J, Fazilat S, Fazilat S, Gaillard WD, Theodore WH: Extratemporal atrophy in patients with complex partial seizures of left temporal origin. Ann. Neurol. 43, 41-45 (1998)
23. DeLong GR, Heinz ER: The clinical syndrome of early-life bilateral hippocampal sclerosis. Ann. Neurol. 42, 11-17 (1997)
24. 1A receptors in malformations of cortical development. Epilepsia (in press) [Abstract] (2002)
25. Dupont S, Semah F, Baulac M, Samson Y: The undelying pathophysiology of ictal dystonia in temporal lobe epilepsy: an FDG-PET study. Neurology 51, 1289-1292 (1998)
26. Engel J Jr, Kuhl DE, Phelps ME: Patterns of human local cerebral glucose metabolism during epileptic seizures. Science 218, 64-66 (1982)
27. Engel J Jr, Kuhl DE, Phelps ME, Mazziotta JC: Interictal cerebral glucose metabolism in partial epilepsy and its relation to EEG changes. Ann. Neurol. 12, 510-517 (1982)
28. Engel J Jr: Intracerebral recordings: organization of the human epileptogenic region. J. Clin. Neurophysiol. 10, 90-98 (1993)
29. Fuerst D, Shah J, Shah A, Watson C: Hippocampal sclerosis is a progressive disorder: a longitudinal volumetric MRI study. Ann. Neurol. 53, 413-416 (2003)
30. Gaillard WD, Bhalia S, Bookheimer SY, Fazilat S, Sato S, Theodore WH: FDG-PET and volumetric MRI in the evaluation of patients with partial epilepsy. Neurology 45, 123-126 (1995)
31. 15O water positron emission tomography study. Epilepsia 37, 515-521 (1996)
32. Gaillard WD, Kopylev L, Weinstein S, Conry J, Pearl PL, Spanaki MV, Fazilat S, Fazilat S, Venzina LG, Dubovsky E, Theodore WH: Low incidence of abnormal (18)FDG-PET in children with new-onset partial epilepsy: a prospective study. Neurology 58, 717-722 (2002)
33. Gale K: Subcortical structures and pathways involved in convulsive seizure generation. J. Clin. Neurophysiol. 9, 264-277 (1992)
34. Haginoya K, Kon K, Yokoyama H: The perfusion defect seen with SPECT in West syndrome is not correlated with seizure prognosis or developmental outcome. Brain Dev. 22, 16-23 (2000)
35. Haglund MM, Ojemalm GA, Hochman DW: Optical imaging of epileptiform and functional activity in human cerebral cortex. Nature 358, 668-671 (1992)
36. Hajek M, Wieser HG, Khan N, Antonini A, Schrott PR, Maguire P, Beer HF, Leenders KL: Preoperative and postoperative glucose consumption in mesiobasal and lateral temporal lobe epilepsy. Neurology 44, 2125-2132 (1994)
37. 14C-2-deoxyglucose method. Brain Res. Brain Res. Rev. 20, 1-23 (1995)
38. Hashizume K, Tanaka T: Multiple subpial transection in kainic acid-induced focal cortical seizure. Epilepsy Res. 32, 389-399 (1998)
39. Henry TR, Mazziotta JC, Engel J Jr: Interictal metabolic anatomy of mesial temporal lobe epilepsy. Arch. Neurol. 50, 582-589 (1993)
40. Holmes O: The intracortical neuronal connectivity subserving focal epileptiform activity in rat cortex. Exp. Physiol. 79, 705-721 (1994)
41. Huttenlocher PR: Synaptic density in human frontal cortex - developmental changes and effects of aging. Brain Res. 163, 195-205 (1979)
42. Huttenlocher PR, de Courten C: The development of synapses in striate cortex of man. Hum. Neurobiol. 6, 1-9 (1987)
43. Jokeit H, Seitz RJ, Markowitsch HJ, Neumann N, Witte OW, Ebner A: Prefrontal asymmetric interictal glucose hypometabolism and cognitive impairment in patients with temporal lobe epilepsy. Brain 120, 2283-2294 (1997)
44. 11C]flumazenil positron emission tomography abnormalities of thalamic nuclei in temporal lobe epilepsy. Neurology 53, 2037-2045 (1999)
45. Juhász C, Chugani DC, Muzik O, Watson C, Shah J, Shah A, Chugani HT: Relationship between EEG and PET abnormalities in clinical epilepsy. J. Clin. Neurophysiol. 17, 29-42 (2000)
46. Juhász C, Chugani DC, Muzik O, Watson C, Shah J, Shah A, Chugani HT: Electroclinical correlates of flumazenil and fluorodeoxyglucose PET abnormalities in lesional epilepsy. Neurology 55, 825-834 (2000)
47. Juhász C, Chugani DC, Muzik O et al.: Is epileptogenic cortex truly hypometabolic on interictal positron emission tomography? Ann. Neurol. 48, 88-96 (2000)
48. Juhász C, Chugani DC, Muzik O, Shah A, Shah J, Watson C, Canady A, Chugani HT: Relationship of flumazenil and glucose PET abnormalities to neocortical epilepsy surgery outcome. Neurology 56, 1650-1658 (2001)
49. Juhász C, Chugani HT, Muzik O, Chugani DC: Neuroradiological assessment of brain structure and function and its implication in the pathogenesis of West syndrome. Brain Dev. 23, 488-95 (2001)
50. A-receptor binding in young children with epilepsy. Epilepsia 42, 1320-1326 (2001)
51. Juhász C, Behen ME, Muzik O, Chugani DC, Chugani HT: Bilateral prefrontal and temporal neocortical hypometabolism in children with epilepsy and aggression. Epilepsia 42, 991-1001 (2001)
52. Juhász C, Chugani HT, Muzik O, Chugani DC: Hypotheses from functional neuroimaging studies. Int. Rev. Neurobiol. 49, 37-55 (2002)
53. Juhász C, Chugani DC, Muzik O, Shah A, Asano E, Mangner T, Chakraborty PK, Sood S, Chugani HT: Alpha-methyl-L-tryptophan PET detects epileptogenic cortex in children with intractable epilepsy. Neurology 60, 960-968 (2003)
54. Kalviainen R, Salmenpera T, Partanen K, Vainio P, Riekkinen P, Pitkanen A: Reccurent seizures may cause hippocampal damage in temporal lobe epilepsy. Neurology 50, 1377-1382 (1998)
55. Kornblum HI, Chugani HT, Tatsukawa K, Gall CM: Cerebral hemidecortication alters expression of transforming growth factor alpha mRNA in the neostriatum of developing rats. Brain Res. Mol. Brain Res. 21, 107-114 (1994)
56. Koutroumanidis M, Hennessy MJ, Seed PT, Elwes RD, Jarosz J, Morris RG et al: Significance of interictal bilateral temporal hypometabolism in temporal lobe epilepsy. Neurology 54, 1811-1821 (2000)
57. Kosofsky BE, Molliver ME: The serotoninergic innervation of cerebral cortex: different classes of axon terminals arise from dorsal and median raphe nuclei. Synapse 1, 153-168 (1987)
58. Kovacs DA, Zoll JG: Seizure inhibition by median raphe nucleus stimulation in rat. Brain Res. 70, 165-169 (1974)
59. Krynauw RA: Infantile hemiplegia treated by removing one cerebral hemisphere. J. Neurol. Neurosurg. Psychiatry 13, 243-267 (1950)
60. 3. Ann. Neurol. 8, 348-360 (1980)
61. Lee JS, Asano E, Muzik O, Chugani DC, Juhász C, Pfund Z, Philip S, Behen ME, Chugani HT: Sturge-Weber syndrome: correlation between clinical course and FDG PET findings. Neurology 57, 189-195 (2001)
62. Liang F, Jones EG: Zif268 and FOS-like immunoreactivity in tetanus toxin-induced epilepsy: reciprocal changes in the epileptic focus and the surround. Brain Res. 778, 281-292 (1997)
63. Liang F, Le LD, Jones EG: Reciprocal up- and down-regulation of BDNF mRNA in tetanus toxin-induced epileptic focus and inhibitory surround in cerebral cortex. Cereb. Cortex 8, 481-491 (1998)
64. Marcinkiewicz M, Morcos R, Chretien M: CNS connections with the median raphe nucleus: retrograde tracing with WGA-apoHRP-Gold complex in the rat. J. Comp. Neurol. 289, 11-35 (1989)
65. Mathern GW, Babb TL, Vickrey BG, Melendez M, Pretorius JK: The clinical-pathogenic mechanisms of hippocampal neuron loss and surgical outcomes in temporal lobe epilepsy. Brain 118, 105-118 (1995)
66. Michael AE, Garey LJ: The development of dendritic spines in the human visual cortex. Hum. Neurobiol. 3, 223-227 (1984)
67. Moore GJ, Slovis TL, Chugani HT: Proton magnetic resonance spectroscopy in children with Sturge-Weber syndrome. J. Child. Neurol. 13, 332-335 (1998)
68. Morrell F: Secondary epileptogenesis in man. Arch. Neurol. 42, 318-335 (1985)
69. Morrell F, Whisler WW, Bleck TP: Multiple subpial transection: a new approach to the surgical treatment of focal epilepsy. J. Neurosurg. 70, 231-239 (1989)
70. Muller RA, Rothermel RD, Behen ME, Muzik O, Chakraborty PK, Chugani HT: Plasticity of motor organization in children and adults. Neuroreport 83, 103-108 (1997)
71. Muller RA, Rothermel RD, Behen ME, Muzik O, Chakraborty PK, Chugani HT: Language organization in patients with early and late left-hemisphere lesion: a PET study. Neuropsychologia 37, 545-557 (1999)
72. Muzik O, da Silva E, Juhász C, Chugani DC, Shah J, Nagy F, Canady A, von Stockhausen HM, Herholz K, Gates J, Frost M, Ritter F, Watson C, Chugani HT: Intracranial EEG vs. flumazenil and glucose PET in children with extratemporal lobe epilepsy. Neurology 54, 171-179 (2000)
73. Natsume J, Bernasconi N, Andermann F, Bernasconi A: MRI volumetry of the thalamus in temporal, extratemporal, and idiopathic generalized epilepsy. Neurology 60, 1296-1300 (2003)
74. Newberg AB, Alavi A, Berlin J, Mozley PD, O'Connor M, Sperling M: Ipsilateral and contralateral thalamic hypometabolism as a predictor of outcome after temporal lobectomy for seizures. J. Nucl. Med. 41, 1964-1968 (2000)
75. Nohria V, Lee N, Tien RD, Heinz ER, Smith JS, DeLong GR, Skeen MB, Resnick TJ, Crain B, Lewis DV: Magnetic resonance imaging evidence of hippocampal sclerosis in progression: a case report. Epilepsia 35, 1332-1336 (1994)
76. O'Brien TJ, So EL, Meyer FB, Parisi JE, Jack CR: Progressive hippocampal atrophy in chronic intractable temporal lobe epilepsy. Ann. Neurol. 45, 526-529 (1999)
77. Pintor M, Mefford IN, Hutter I, Pocotte SL, Wyler AR, Nadi NS et al.: The levels of biogenic amines, their metabolites and tyrosine hydroxylase in the human epileptic temporal cortex. Synapse 5, 152-156 (1990)
78. Prince DA, Wilder BJ: Control mechanisms in cortical epileptogenic foci. "Surround" inhibition. Arch. Neurol. 16, 194-202 (1967)
79. Salgado D, Alkadhi KA: Inhibition of epileptiform activity by serotonin in rat CA1 neurons. Brain Res. 669, 176-182 (1995)
80. Samanin R: Inhibitory effect of midbrain raphe stimulation on cortical evoked potentials in rats. Psychopharmacology 24, 375-378 (1971)
81. Sherwin A, Quesney F, Gauthier S et al.: Enzyme changes in actively spiking areas of human epileptic cerebral cortex. Neurology 34, 927-933 (1984)
82. Sloviter RS: The functional organization of the hippocampal dentate gyrus and its relevance to the pathogenesis of temporal lobe epilepsy. Ann. Neurol. 35, 640-654 (1994)
83. Smith MC: Multiple subpial transection in patients with extratemporal epilepsy. Epilepsia 39(suppl 4), S81-S89 (1998)
84. Spanaki MV, Siegel H, Kopylev L, Fazilat S, Dean A, Liow K, Ben-Menachem E, Gaillard WD, Theodore WH: The effect of vigabatrin (gamma-vinyl GABA) on cerebral blood flow and metabolism. Neurology 53, 1518-1522 (1999)
85. Spanaki MV, Kopylev L, DeCarli C, Gaillard WD, Liow K, Fazilat S, Reeves P, Sato S, Kufta C, Theodore WH: Postoperative changes in cerebral metabolism in temporal lobe epilepsy. Arch. Neurol. 57, 1447-1452 (2000)
86. Sperling MR, Gur RC, Alavi A et al.: Subcortical metabolic alterations in partial epilepsy. Epilepsia 31, 145-155 (1990)
87. Swartz BE, Tomiyasu U, Delgado-Escueta AV, Mandelkern M, Khonsari A: Neuroimaging in temporal lobe epilepsy: test sensitivity and relationships to pathology and postoperative outcome. Epilepsia 33, 624-634 (1992)
88. Szabó J: Organization of the ascending striatal afferents in monkeys. J. Comp. Neurol. 189, 307-321 (1980)
89. Szapiel SV: Optical imaging and its role in clinical neurology. Arch. Neurol. 58, 1061-1065 (2001)
90. Theodore WH, Bairamian D, Newmark ME, DiChiro G, Porter RJ, Larson S, Fishbein D: Effect of phenytoin on human cerebral glucose metabolism. J. Cereb. Blood Flow Metab. 6, 315-320 (1986)
91. Theodore WH, Bhatia S, Hatta J, Fazilat S, DeCarli C, Bookheimer SY, Gaillard WD: Hippocampal atrophy, epilepsy duration, and febrile seizures in patients with partial seizures. Neurology 52, 132-136 (1999)
92. 1A receptor binding in patients with temporal lobe epilepsy. Neurology 60, 749-756 (2003)
93. Trottier S, Evrard B, Vignal JP, Scarabin JM, Chauvel P: The serotonergic innervation of the cerebral cortex in man and its changes in focal cortical dysplasia. Epilepsy Res. 25, 79-106 (1996)
94. Van Bogaert P, Wikler D, Damhaut P, Szliwowski HB, Goldman S: Regional changes in glucose metabolism during brain development from the age of 6 years. Neuroimage 8, 62-68 (1998)
95. Van Bogaert P, Massager N, Tugendhaft P, Wikler D, Damhaut P, Levivier M, Brotchi J, Goldman S: Statistical parametric mapping of regional glucose metabolism in mesial temporal lobe epilepsy. Neuroimage 12, 129-138 (2000)
96. Vercueil L, Kahane P, Francois-Joubert A, Hirsch E, Hoffmann D, Depaulis A, Marescaux C: Basal ganglia involvement in rotational seizures. Epileptic. Disord. 1, 107-112 (1999)
97. Wieshmann UC, Woermann FG, Lemieux L, Free SL, Bartlett PA, Smith SJ, Duncan JS, Stevens JM, Shorvon SD: Development of hippocampal atrophy: a serial magnetic resonance imaging study in a patient who developed epilepsy after generalized status epilepticus. Epilepsia 38, 1238-1241 (1997)
98. Witte OW, Bruehl C, Schlaug G et al.: Dynamic changes of focal hypometabolism in relation to epileptic activity. J. Neurol. Sci. 124, 188-197 (1994)