Epilepsy Res., 5 (1990) 146-154
146
Elsevier EPIRES 00286
Multidisciplinary analysis of patients with extratemporal complex partial seizures. II. Predictive value of semiology B.E. Swartz 1'2'4, E. Halgr~n 3'4, A . V . D e l g a d o - E s c u e t a 1,2,4, P. Feldstein 3,4, H. M a l d o n a d o 1'2'4 and G . O . Walsh 1'2 1Comprehensive Epilepsy Program, 2Department of Neurology, and 3Brain Research Institute, University of California at Los Angeles, Los Angeles, CA (U.S.A.), and VA Southwest Regional Epilepsy Cente/, Neurology and Research Services, Los Angeles, CA (U.S.A.) (Received 29 September 1988; revision received 21 April 1989; accepted 23 April 1989)
Key words: Complex partial seizures; Extratemporal semiology
Eight patients were diagnosed as having extratemporai seizures based on their ictai electroclinical manifestations. The correlation between the focus based on semiology and that based on intracranial electrographic ,~ecordingand surgical excision was excellent in five. good in three, The electroclinical manifestations of seizures are important data to consider in the diagnosis and treatment of extratemporal seizure loci.
INTRODUCTION We had the opportunity to classify a small group of patients according to their ictai and interictal electroclinical characteristics before we could be biased by other non-invasive tests. In part I we described the relative sensitivities of a diagnostic battery that included neurological exam, interictal EEG, CCTV-EEG (ictal), CAT, MRI and FDGPET scans and a neuropsychological test battery~. In this paper we describe the semiologic classification in more detail and present the results of intracranial monitoring and surgical excision. Correspondence to: Dr. B.E. Swartz, M.D., Comphrehensire Epilepsy Program, Dept. of Neurology, West Los Angeles VA Medical Center, Wilshire & Sawtelle Boulevards, West Los Angeles, CA 90073, U.S.A.
The first criteria that Walker stated 4s, which must be met prior to surgical resection for seizure control, are that the clinical manifestations of seizures must originate from a localized brain area. What constitutes a 'localizing clinical sign' is not universally agreed upon even for temporal lobe epilepsy 12'~6. Although good results in 75-90% of patients are widely reported following anterior temporal Iobectomy, recent multidisciplinary analyses of patients with putative temporal lobe epilepsy have shown that the classification of ictal behavior provides additional localizing information t5'~7. In Dodrill's series, surgical success improved from 81% to 100% when ictal characteristics not typical of temporal lobe seizures were recognized and surgical excision could be extended outside the temporal lobe. Because diagnosis based on seizure characteris-
0920-1211/90/$03.50 © 1990 Elsevier S~ience Publishers B.V. (Biomedical Division)
147 tics is even more difficult with extratemporal foci, we initially reviewed which characteristics were proven to be associated with a given brain region41. The proof was based on stereo-EEG, subdural recordings or electrocorticography followed by excision and freedom from seizures. We then applied the principles of neuroanatomical clas~,ification of complex partial seizures as developed by Penfield and collaborators 34-37, Rasmussen 3s-4°, Bancaud g-6, Bancaud et al. 7-1°, Geier et al) s-2~, Ajmone Marsan and colleagues ~-3, Ludwig et al. 2s, Wieser and colleagues 5°-52, Delgado-Escueta et al. t4-16 and Walsh and Delgado-Escueta 49 to this patient group. Some of the proven behaviors are as follows: seizures from frontal-polar cortex have been shown to produce initial loss of consciousness followed by contraversive head and eye movement with rapid generalization 34. The superior, mid and inferior frontal gyri anterior to Brodmann's area 6 (dorsolateral frontal cortex) can produce pseudoabsence attacks 4°'42, tonic forward extension of the head, neck and trunk followed by contraversive movements, loss of consciousness, and clonic face and arm movements s'22'49 or even contraversive rotation ~. The precentral region, area 6, has been shown to produce auras of pain or odd sensations in the arm followed by forced tonic posturing s'43. In addition, this region produces seizures indistinguishable from area 4 due to rapid spread. The central region, area 4, is known for epilepsia partialis continua s] and for a somatotopic march of clonic movements 4'27. Rapid generalization can occur from any of these regions a'as'4°. Supplementary motor area (SMA) seizures may show slow postural changes with contraversion of the head and eyes toward an uplifted hand, tonic extension of the opposite arm and/or legs, and synergistic postures of the side ipsilateral to the focus. They can also cause inhibition of movements, gestural activities, or speech. Palilallic vocalization, hissing or true expressive aphasia can exist. Consciousness may be preserved early in the seizure. Sensory phenomena of tingling or burning that is not somatotopic may occur; autonomic changes such as mydriasis and flushing can also be seen 2,s' I0,23,34,37,47
Autonomic phenomena are much more substan-
tial in cingulate seizures and include: mydriasis, pallor, tachycardia, urination, conjunctival injection, hyperpnea or apnea which is associated with auras of suffocation 19-2],34. Motor effects of cingular seizures include head nodding or extension (with or without loss of consciousness), arm elevation is followed by contra- or ipsiversive posturing as spread to the SMA occurs. Sudden falls without loss of consciousness, sudden tonic arm movements and bilateral asymmetric facial twitching can occur. The patient may cry, laugh or moan; consciousness may be partially ('dreamy state') or completely lost and pseudoabsences have been noted. Repetitive, reactive, bilateral complex automatisms, genital manipulation and fetal posturing may also occur 9'21'29'a3'45, although these are often late in the seizures. The manifestations of parietal lobe seizures depend on the specific region. The inferior lobule, especially opercular seizures, may produce gustatory auras or light-headedness proceeding to swallowing and lip and tongue movements. They can be reflexic, precipitated by food or sounds 34. Others report auras of 'bad tastes,' arm pain, loss of control of movements proceeding to tonic posturing of both hands or gestural automatisms TM. Post-central gyrus discharges produce contralateral tingling, numbness (sometimes in a Jacksonian march), pain, sensations of heat, coldness, or swelling. Epilepsia partialis continua, tonic leg seizures, nausea and vomiting followed by adversive seizures 34 can occur. Rotation, metamorphopsia, and right-left confusion have been described from superior iobule 2aa'43. The parieto-occipital junction is associated with unformed visual hallucinations leading to vertigo and tinnitus or contralaterai numbness a. Finally, junctional seizures (parieto-temporo-occipital) produce speech arrest, Wernicke's dysphasia, gestural, verbal and dyspraxic automatisms a. Others report bilateral stiffening of upper then lower extremities 3 and illusions of an emotional type 34. METHODS Five to 12 seizures per patient were recorded using scalp and sphenoi~al biotelemetry and videotaping of ictal behaviors. The patients were
148 tested for level of consciousness during at least one of the seizures. All authors viewed each seizure several times to come to a consensus classification. Awake and sleep interictal EEGs were also recorded. The recording sites and selection of montages are described in part 144. After all non-invasive tests were completed, 8 patients underwent various surgical explorations individually determined on a case by case basis. An excellent correlation is said to exist if the resuits of intracranial monitoring match the ictal focus as hypothesized by the semiologic classification. A good correlation meant that the ictal zone included but was larger or smaller than the hypothesized zone. RESULTS Eight patients underwent surgical procedures. Three had 'medial frontal' type electroclinical manifestation. One of these, patient no. 2, was in
the group with a discrete PET lesion and excellent concordance among all tests. A second-for-second diagram of his seizures is shown in Fig. 1A and appears at first glance to 'defy meaningful classification 's4. On closer inspection, an initial arrest with darting eye movements and/or grimace is rapidly followed by head, eye and somtimes trunk deviation to the left and bilateral tonic limb posturing. The head and eye deviations with bilateral limb postures were consistent with an SMA focus. Loss of consciousness occurred early with the change in expression. The mid-portion of the seizure consisted of a variety of complex automatisms with oral and trunkal movements (sometimes preceded by a loss of tone), while the end of the seizure shows reactive, semipurposeful automatisms and disorientation postictally. The fifth through seventh seizures all occurred within 1 h, which may have compressed the normal sequence and duration of the seizures. The interictal and ictal EEGs were non-localizing, although lateralized to the
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TABLE I
Results of intracranial electrographicmonitoring with or without surgical excision of the focus Patient (hypothesized Recordings and seizurefocus) surgery
Correlation between hypothesis Pathology and flnal results
1a Medial frontal
Correlation with surgical results- excellent
Non-specific gliosis.
Correlation with intracranial recording and surgical results - good
Biopsy: non-specific gliosis of meninges and cortex with neuronal sclerosis, deep cut and rare lymphocytes. Surgery: calcified AVM with gliosis,
Good
Subpial giiosis with neuronal loss in layer 2-3. Superficial white matter gliosis particularly perivascular. Normal by routine stains and electron microscopy.
2 Medial frontal
15 Deep medial frontal
4b Dorsolateral frontal
6a Dorsolateral frontal
8a Parieto-occipital
9 Precentral frontal (area 6)
13 Temporo-parietal
Surface electrocorticography showed spike and wave discharges over the left SMAc with slowing of the dorsolateral cortex adjacent. L SMA removal provided only temporary decrease of seizures for one month. He underwent a second wider excision which extended to the pericallosal gyrus medially, onto the dorsolateral convexity 3.5 cm from midline and anterior to the primary motor area 7.5 cm. He is now seizure free for 5 months. Ictal recordings with subdural grid on the m~.diai surface over the lesions and with strips on the dorsolateral convexity overlying the lesions showed simultaneous ictal onsets at the medial frontal electrodes which were on the anterior edge of the lesion and from three sites contiguous to this extending 3 cm over the dorsolateral surface. Surgical excision of the lesion resulted in 80% decrease in seizures. Interictal EEG showed bilateral frontocingulate and supra-cingulate epileptiform activity, but most ictal recordings showed onsets in the right fronto-cingulate region. Electrocorticography revealed focal spikes, and spike and wave and slowing superior to the posterior edge of the third frontal gyms. Excision was deferred due to the proximity to Broca's region. Electrocorticography and gross inspection revealed widespread damage of the left dorsolateral cortex. The pole had been previously removed for a suspected cerebral abscess. A wide excision of the dorsolateral cortex sparing the primary motor strip was done. He is seizure free with minimal additional deficit for 1 year, 3 months. Electrocorticography revealed focal spikes in the parietal lobe anterior to the parietooccipital junction. A mass was discovered at the parieto-occipital junction. Resection of the tuber and area of focal spiking resulted in control of seizures, on medications for 2 years. Eiectrocorticography revealed a slow wave focus overlying a neoplasm of the white matter beneath area 6. The patient was seizure free on medications for 2 years following excision and radiation therapy. Subdural strip recordings revealed widespread right temporal onset of seizures with prolonged afterdischarge (2-3 rain) over the parietal opercular cortex. She is seizure free with one aura 6 months after right temporal lobectomy.
a Previously illustrated in Swartz and Delgado-Escueta 41. b Previously illustrated in Delgado-Escueta et al) 4. ¢ Supplementary motor area.
Correlation with electrocorticographyexcellent
Correlation with surgical results- excellent
Non-specific giiosis.
Correlation with surgical results- excellent
Tuberous sclerosis.
Correlation with surgical results- excellent
Grade II astrocytoma,
Correlation with intracranial monitoring and surgical results- good
Extensive gliosis and cell loss of cortical (lateral) and hippocampal tissue.
150
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Fig, 1B, CAT, MRI and PETimages in the same patient.
left. The MRI, CAT and PET scans show a discrete lesion of the medial posterior frontal cortex (SMA; Fig. 1B). Neuropsychological assessment was also consistent with frontal dysfunction, including low primary memory, poor verbal fluency and strategy formation, and response rigidity. He had a dorsolateral subdural plate and two medial subdural strips placed. A typical seizure onset seen during intracranial recording is shown in Fig. 2. The intracranial recordings were interpreted as showing a good correlation with the proposed ictal origin (Table I) because the ictal region recorded intracranially included the medial frontal lobe surface but extended byond it to the dorsolateral surface. He underwent a focal resection of his lesion in the SMA and has had an 80% reduction of seizure frequency. Two patients had dorsolateral electroclinical
characteristics. One underwent electrocorticography which showed an actively spiking zone on the lateral frontal surface as hypothesized. Wide excision was not attempted because of the proximity of Broca's speech area. The other had widespread dorsolateral spiking and a wide frontal Iobectomy sparing the motor strip. He has been seizure free for 32 months. These two were classified as having an excellent correlation to the presurgically predicted locus. Patient no. 9 had a precentral semiology. Electrocorticography revealed focal slowing and sharp waves above an astrocytoma of the white matter. This was removed, radiation therapy was given and the patient was seizure free for 2 years before being lost to follow-up. One patient with hypothesized temporo-parietal origins (no. 13) had subdural strips placed in both
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these areas. A diffuse temporal lobe onset of her seizures was followed by a prolonged afterdischarge in the parietal region. She is seizure free with one aura in 28 months of postoperative follow-up. This case is called a 'good correlation' beTABLE II
Correlation of intracranial electrographic recording with or without subsequent surgical excision excellent = complete agreement; good = in agreement but showing a greater or less extensive area of dysfunction; poor = a normal test result.
Patient
CA T
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Neuropsych.
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poor excellent poor good excellent excellent poor poor
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cause the hypothesized focus included but was larger than the actual one. Another patient with parietal lobe seizure semiology underwent electrocorticography which showed an active spiking zone just anterior to a parieto-occipital tuber. Both the tuber and spiking zone were excised with complete control of seizures for 3.5 years. Thus, this patient is considered to have excellent correlation of preand postsurgical ictal focus identification. In total, 5/8 (62.5%) of the patients had an excellent correlation between intracranial electrographic studies and the electroclinical classification. The remaining 37.5% had a good correlation (Table I). The other neurodiagnostic test correlations are shown in Table II. FDG-PET scans had an excellent correlation in 50%, good in 25% and poor in 25%. Neuropsychological tests were slightly more accurate than PET with an excellent correlation in 25% and good in 62.5%. MRI had an excellent correlation in 62.5% and a poor correlation in 37.5%. CAT scanning had an excellent
152 correlation in 37.5%, good in 12.5% and poor in 50%. Six of 8 patients became seizure free after resective surgery. One of these had 1 immediate postoperative seizure, and 1 patient had a single aura. The follow-up period is 21 months-4.5 years. Of the two with continued seizures, one developed a progressive syndrome consistent with Rasmussen's encephalitis and later underwent hemispherectomy with control of seizures, the other had an 80% reduction in the seizure frequency after a focal lesional resection. DISCUSSION Traditionally, many authors have considered the clinical manifestations of complex partial seizures to be of value in the discrimination of temporal, frontal and other extratemporal seizure locii~'3°'32'46. Subvarieties of partial complex seizures based on localization and behaviors were appended to the recent Classification of the Epilepsies and Epileptic Syndromes 13. Other investigators are unconvinced of this view n'26 and do not specifically mention semiology in lists of criteria for surgery 17a. Complex partial seizures of extratemporai origin have characteristics which distinguish them from those of temporal lobe origin. When careful juxtaposition of behaviors and of ictal EEG patterns is made with modern techniques of neuroimaging and neuropsychological assessment, good concordance between tests of lesion localization can be obtained. Furthermore, good agreement with results of intracranial monitoring and surgical excision is also possible. In spite of improved neurodiagnostics there always remains a group of patients who have complex partial seizures but no other sign of cerebral
REFERENCES 1 Ajmone Marsan, C. and Abraham, K., A Seizure Atlas. E[ectroenceph. Clin. Neurophysiol., Suppl. 15, Elsevier, Amsterdam, 1960, pp. 1-215. 2 Ajmone Marsan, C. and Goldhammer, L., Clinical ictal patterns and electrographic data in cases of partial seizures of frontal, central, and parietal origin. In: M.A.B. Brazier
dysfunction. In this study, neuroimaging was normal in 25% (PET) to 50% (CAT). As more patients undergo surgery without structural lesions these numbers will increase. To approach these patients surgically one can use very widespread sampling of multiple brain regions with stereoEEG and/or subdural plates. This will often require several implantations prior to surgery, causing increased risk to the patient. Even then the results are not guaranteed. Holmes et al. 24 reported that of 8 patients with both frontal and temporal hypometabolism on ISFDG-PET scans, only 4 had temporal lobe seizure onsets recorded by subdural strip electrodes. Those 4 underwent temporal lobectomy but only 2 improved. If attention to ictal behaviors can improve surgical outcome from 75% to greater than 90% in temporal lobe epilepsy16'17, it should also improve outcome in extratemporal seizures, None of our 8 patients would have undergone surgical exploration without information that corroborated the electroclinical picture. Nevertheless, considered alone, the location of the ictal focus based on electroclinical characteristics had an excellent correlation with the results of intracranial electrographic recordings and surgical excision in 62.5% and had a good correlation in 37.5%. CONCLUSION Resective surgery for seizure control requires careful use of all pertinent non-invasive test data. Careful classification of electroclinical features is an important source of data in the planning of intracranial monitoring or surgical excision. The ability to classify seizures based on electroclinical manifestation remains an important adjunct in the armamentarium of the epileptologist, as it has been since the time of Penfield,
(Ed.), Epilepsy: its Phenomena in Man, Academic Press, New York, 1973, pp. 235-258. 3 Ajmone Marsan, C. and Ralston, B.L., The Epileptic Seizure: its Functional Morphology and Diagnostic Significance, Thomas, Springfield, IL, 1957. 4 Bancaud, J., Les crises 6pileptiques d'origine occipitale (~tude strrro.61ectroencrphalographique), Rev. d'OtoNeuro-Ophtalmoi., 41 (1969) 299-315.
153 5 Bancaud, J., Topographic relationship between cerebral lesions and seizure discharges. In: R. Canger, F. Angeleri and J.K. Penry (Eds.), Advances in Epileptology. Xith Epilepsy Int. Syrup., Raven Press, New York, 1980, pp. 103-109. 6 Bancaud, J., Srmiologie clinique des crises ~pileptiques d'origine temporale, Rev. NeuroL, 143 (1986) 392-400. 7 Bancaud, J., Bonis, A., Munari, C., Szikla, G., Chodkiewicz, J.P. and Talairach, J., Localizing value of the clinical manifestations of the partial seizures, Acta Neurochir. (Wien), Suppl. 33 (1984) 7-15. 8 Bancaud, J., Talairach, J., Bonis, A., Schaub, A., Szikla, G., Morel, P. et Bordas.Ferrer, M., La St~r~o-dlectroenc~phalographie clansl'Epilepsie, Masson, Paris, 1965. 9 Bancaud, J., Talairach, 3, Geier, S., Bonis, A., Trottier, S. et Manrique, M., Manifestations comportementales induites par la stimulation 61ectrique du gyrus cingulaire antrrieur chez rhomme, Rev. Neurol., 132 (1976) 705-724. 10 Bancaud, J., Talairach, 3., Schauh, C., Bonis, A., Szikla, G. and Colomb, D., Stereotaxic functional exploration of the epilepsies of the supplementary areas of the mesial surface of the hemisphere, Eleetroenceph. Clin. Neurophysiol., 14 (1962) 788. 11 Bossi, L., Munari, C., Stoffels, C. et al., Somatomotor manifestations in temporal lobe epilepsy, Epilepsia, 25 (1984) 70-76. 12 Brey, R. and Laxer, K.D., Type I/II complex partial seizures: no correlation with surgical outcome, Epilepsia, 26 (1986) 657-660. 13 Commission on Classification and Terminology of the International League Against Epilepsy, Proposal for the classification of the epilepsies and epileptic syndrome, Epilep. sia, 26 (1985) 268-278. 14 Delgado-Escueta, A.V., Swartz, B.E., Maldonado, H.M., Walsh, G.O., Rand, R.W. and Halgren, E., Complex partial seizures of frontal lobe origin. In: H.G. Wieser and C.E. Elger (Eds.), Presurgical Evaluation of Epileptics, Sprin~er, Berlin. 1986, pp. 267-299. 15 Delgado-Escueta, A.V. and Walsh, G.O., The selection process for surgery of intractable complex partial seizures; surface EEG and depth electrography. In: J.K. Penry and D.P. Purpura (Eds.), Epilepsy, Raven Press, New York, 1983, pp. 296-325. 16 Delgado-Escueta, A.V. and Walsh, G.O., Type I complex partial seizures of hippocampal origin: excellent results of anterior temporal lobectomy, Neurology, 35 (1985) 143-154. 17 Dodrill, C.B., Wilkins, R.J., Ojemann, G.A., Ward, A.A., Wyler, A.R., Van Belle, G. and Tamas, L., Multidisciplinary prediction of seizure relief from cortical resection surgery, Ann. Neurol., 20 (1986) 2-12. 17a Engel, Jr., J., Rausch, R., Lieb, J.B., Kuhl, D.E. and Crandall, P.H., Correlation of criteria used for localizing epileptic foci in patients considered for surgical therapy of epilepsy, Ann. NeuroL, 9 (1981)215-224. 18 Geier, S., Bancaud, J., Bonis, A. and Enjelvin, M., Nonmotor frontal epilepsy: study of EEG and clinical features using ~ele-EEG and tele-stereo.EEG~ Electro~nceph, C!i.n..
Neurophysiol., 34 (1973) 699. 19 Geier, S., Bancaud, 3., Talairach, J., Bonis, A., Enjelvin, M. and Hossard-Bouchard, H., Automatisms during frontal lobe seizures, Brain, 99 (1976) 447-458. 20 Geier, S., Bancaud, J., Talairach, J., Bonis, A., HossardBouchard, H. and Enjelvin, M., Ictal tonic postural changes and automatisms of the upper limb during epileptic parietal lobe discharges, Epilepsia, 18 (1977) 517-524. 21 Geier, S., Bancaud, J., Talairach, J., Bonis, A., Szikla, G. and Enjelvin, M., The seizures of frontal lobe epilepsy: a study of clinical manifestations, Neurology, 27 (1977) 951-958. 22 Goldring, S., The role of the prefrontal cortex in grand mal convulsion, Arch. Neurol., 26 (1972) 109-119. 23 Greene, J.R., Angevine, J.B., White, J.C., Edes, A.O. and Smith, R.D., Significance of the supplementary motor area in partial seizures and in cerebral localization, Neuro. surgery, 6 (1980) 64-75. 24 Holmes, M., Kelly, K. and Theodore, W., Complex partial seizures: correlation of clinical and metabolic features, Arch. Neurol., 45 (1988) 1191-1193. 2-~ Hochman, S.M., Rotary seizures associated with frontal lobe malignant neoplasm: a case report, Epilepsia, 1 (1983) 11-14. 26 Ives, J.R., Video recording during long-term EEG monitoring of epileptic patients. In: R.J. Gumnit (Ed.), 1nten. sire Neurodiagnostic Monitoring. Advances in Neurology, Vol. 46, Raven Press, New York, 1986, pp. 1-117. 27 Jackson, J.H., A study of convulsions. In: Selected Writings of John Hughlings Jackson, Vol. 1, Hodder and Stoughton, London, 1870. 28 Ludwig, B.I., Ajmone Marsan, C. and Van Buren, J., Depth and direct cortical recording in seizure disorders of extratemporal origin, Neurology, 26 (1976) 1085-1099. 29 Mazars, G., Cingulate gyrus epileptogenic foci as an origin for generalized seizures. In: 3. Gastaut, H. Jasper, J. Bancaud and A. Waltregny (Eds.), The Physiopathogenesis of the Epilepsies, Thomas, Springfield, IL, 1969, pp. 186-189. 29a Munari, C. and Bancaud, J., The role of stereo-encepha. iography in the evaluation of partial epileptic seizures. In: R.J. Porter and P.L. Morseili (Eds.), The Epilepsies, But. terworth, London, 1985, pp. 267-306. 30 Munari, C., Bonis, A. and Kochen, S., Eye movements and occipital seizures in man, Acta Neurochir. (Wien), Suppl. 33 (1984) 47-52. 31 Munari, C., Stoffels, C., Bossi, L. et al., Automatic activities in frontal lobe seizures without involvement of temporal lobe structures. In: M. Dam, L. Gram and 3.K. Penry (Eds.), Advances in Epileptology. Xllth Epilepsy Int. Symp., Raven Press, New York, 1981,pp. 63-64. 32 Munari, C., Stoffels, C., Bossi, L., Bonis, A., Talairach, J. and Bancaud, J., Automatic activities during frontal and temporal seizures: are they the same? In: M. Dam, L. Gram and 3.K. Penry (Eds,), Advances in Epileptology. Xllth Epilepsy Int. Symp., Raven Press, New York, 1981, pp. 287-291. 33 Niedermeyer, E. and Walker, A.E., Mesio-frontal epilepsy, E!ectroenceph, C!in. Neurophysiol., 3! (!971) !e4-105.
154 34 Peafield, W and Jasper, H., Epilepsy and the Functional Anatomy of the Human Brain, Little, Brown and Co., Boston, MA, 19S4. 35 Penfield, W. and Kristiansen, K., Epileptic Seizure Patterns, Thomas, Springfield, IL, 1951. 36 Penfield, W. and Rasmussen, T., The Cerebral Cortex of Man, MacmillanPress, New York, 1950, pp. 1-238. 37 Penfield, W. and Welch, K., The supplementary motor area of the cerebral cortex, a clinical and experimental study, Arch. Neurol. Psychiat., 66 (1951) 289-317. 38 Rasmussen, T.B., Cortical resection for medically refractory focal epilepsy: results, lessonsand questions. In: T. Rasmussen and R. Marinok (Eds.), Functional Neurosurgery, Raven Press, New York, 1979, pp. 253-269. 39 Rasmussen, T.B,, Localization aspects of epileptic seizure phenomena. In: R.A. Thompson and J.R. Green (Eds.), New Perspectives it: Cerebral Localization, Raven Press, New York, 1979, pp, 253-269. 40 Rasmussen, T.B., Characteristics of a pure culture of frontal lobe epilepsy, Epilepsia, 29 (1983) 482-493. 41 Swartz, B,E. and Delgado-Escueta, A.V., Complex partial seizures of extratemporal origin: 'the evidence for.' In: H. Wieser, E.J. Speckmann and J. Engel (Eds.), The Epileptic Focus. Current Problems in Epilepsy, Vol. 3, John Libbey, London, 1987, pp. 137-174. 42 Swartz, B.E., Delgado-Escueta, A.V., Maldonado, H,M. and Walsh, G.O., Pseudo-absence seizures: a frontal lobe phenomenon? Presented at the XIII Int. Congress of Epilepsy, Hamburg, 1985. 43 Swartz, B.E., Halgren, E., Delgado-Escueta, A.V,, Blahd, W., Mandelkern, M., Feldstein, P., Rand, R.W,, Maldonado, H.M. and Khonsary, A., Seizure semiology, neuropsychometrics and neuroimaging eorrelaries in frontal lobe epilepsies, Epilepsia, 27 (1986) 597-598, 44 Swartz, B.E., Halgren, E., Delgado-Escueta, A.V., Mandelkern, M., Fcldstein, P., Maldonado, H., Ropchan, J.,
Blahd, W., Walsh, G.O., Quinones, N. and McGee, M., Multidisciplinary analysis of patients with extratemporal complex partial seizures. I. Interest agreement, Epilepsy Res., 5 (1990) 61-73. 45 Talairach, J., Bancaud, J., G¢ier, S., Bordas-Ferrer, M., Bonis, A., Szikla, G. and Rusu, M., The cingulate gyms and human behavior, Eleetroenceph. Clin. Neurphysiol., 34 (1973) 45-52. 46 Tharp, B., Orbital frontal seizures, a unique e!ectroencephalographic and clinical syndrome, Epilepsia, 13 (1972) 627-642. 47 Van Buren, J.M. and Fedio, P., Functional representation on the medial aspect of the frontal lobes in man, Neurosurgery, 44 (1976) 275-289, 48 Walker, A.E., Temporal Iobectomy, J. Neurosurg., 6 (1967) 641-649. 49 Waish, G.O. and Delgado-Escueta, A.V., Type II complex partial seizures: poor results of anterior temporal lobectomy, Neurology, 34 (1984) 1-13. 50 Wieser, H.G., Electroclinical Features of the Psychomotor Seizure, Fischer, Stuttgart, 1983, pp. 177-220. 5i Wieser, H.G., Stereoelectroencephalic correlates of focal motor seizures. In: E.J. Spackmann and C.E. EIger (Eds.), Epilepsy and the Motor System, Urban and Schwarzenberg, Munich, 1983, pp. 287-309. 52 Wieser) H.G,, Graf, H.P., Bernoullie, C. and Siegfried, J., Quantitative analysis of intracerebral recordings in epilepsin partialis continua, Electroenceph. Clin, Neurophysiol., 44 (1978) 14-22. 53 Williamson, P.D. and Spencer, S.S., Clinical and EEG features of complex partial seizures of extratemporal origin, Epilepsia, 27, Suppl. 2 (1986) $46-$63. 54 Wflliamson, P,D., Wieser, H.G. and Delgado-Escueta, A.V., Clinical characteristics of partial seizures. In: J. Engel (Ed.), Surgical Treatment of Epilepsies, Raven Press, New York, 1986, pp. 101-120.
146
Elsevier EPIRES 00286
Multidisciplinary analysis of patients with extratemporal complex partial seizures. II. Predictive value of semiology B.E. Swartz 1'2'4, E. Halgr~n 3'4, A . V . D e l g a d o - E s c u e t a 1,2,4, P. Feldstein 3,4, H. M a l d o n a d o 1'2'4 and G . O . Walsh 1'2 1Comprehensive Epilepsy Program, 2Department of Neurology, and 3Brain Research Institute, University of California at Los Angeles, Los Angeles, CA (U.S.A.), and VA Southwest Regional Epilepsy Cente/, Neurology and Research Services, Los Angeles, CA (U.S.A.) (Received 29 September 1988; revision received 21 April 1989; accepted 23 April 1989)
Key words: Complex partial seizures; Extratemporal semiology
Eight patients were diagnosed as having extratemporai seizures based on their ictai electroclinical manifestations. The correlation between the focus based on semiology and that based on intracranial electrographic ,~ecordingand surgical excision was excellent in five. good in three, The electroclinical manifestations of seizures are important data to consider in the diagnosis and treatment of extratemporal seizure loci.
INTRODUCTION We had the opportunity to classify a small group of patients according to their ictai and interictal electroclinical characteristics before we could be biased by other non-invasive tests. In part I we described the relative sensitivities of a diagnostic battery that included neurological exam, interictal EEG, CCTV-EEG (ictal), CAT, MRI and FDGPET scans and a neuropsychological test battery~. In this paper we describe the semiologic classification in more detail and present the results of intracranial monitoring and surgical excision. Correspondence to: Dr. B.E. Swartz, M.D., Comphrehensire Epilepsy Program, Dept. of Neurology, West Los Angeles VA Medical Center, Wilshire & Sawtelle Boulevards, West Los Angeles, CA 90073, U.S.A.
The first criteria that Walker stated 4s, which must be met prior to surgical resection for seizure control, are that the clinical manifestations of seizures must originate from a localized brain area. What constitutes a 'localizing clinical sign' is not universally agreed upon even for temporal lobe epilepsy 12'~6. Although good results in 75-90% of patients are widely reported following anterior temporal Iobectomy, recent multidisciplinary analyses of patients with putative temporal lobe epilepsy have shown that the classification of ictal behavior provides additional localizing information t5'~7. In Dodrill's series, surgical success improved from 81% to 100% when ictal characteristics not typical of temporal lobe seizures were recognized and surgical excision could be extended outside the temporal lobe. Because diagnosis based on seizure characteris-
0920-1211/90/$03.50 © 1990 Elsevier S~ience Publishers B.V. (Biomedical Division)
147 tics is even more difficult with extratemporal foci, we initially reviewed which characteristics were proven to be associated with a given brain region41. The proof was based on stereo-EEG, subdural recordings or electrocorticography followed by excision and freedom from seizures. We then applied the principles of neuroanatomical clas~,ification of complex partial seizures as developed by Penfield and collaborators 34-37, Rasmussen 3s-4°, Bancaud g-6, Bancaud et al. 7-1°, Geier et al) s-2~, Ajmone Marsan and colleagues ~-3, Ludwig et al. 2s, Wieser and colleagues 5°-52, Delgado-Escueta et al. t4-16 and Walsh and Delgado-Escueta 49 to this patient group. Some of the proven behaviors are as follows: seizures from frontal-polar cortex have been shown to produce initial loss of consciousness followed by contraversive head and eye movement with rapid generalization 34. The superior, mid and inferior frontal gyri anterior to Brodmann's area 6 (dorsolateral frontal cortex) can produce pseudoabsence attacks 4°'42, tonic forward extension of the head, neck and trunk followed by contraversive movements, loss of consciousness, and clonic face and arm movements s'22'49 or even contraversive rotation ~. The precentral region, area 6, has been shown to produce auras of pain or odd sensations in the arm followed by forced tonic posturing s'43. In addition, this region produces seizures indistinguishable from area 4 due to rapid spread. The central region, area 4, is known for epilepsia partialis continua s] and for a somatotopic march of clonic movements 4'27. Rapid generalization can occur from any of these regions a'as'4°. Supplementary motor area (SMA) seizures may show slow postural changes with contraversion of the head and eyes toward an uplifted hand, tonic extension of the opposite arm and/or legs, and synergistic postures of the side ipsilateral to the focus. They can also cause inhibition of movements, gestural activities, or speech. Palilallic vocalization, hissing or true expressive aphasia can exist. Consciousness may be preserved early in the seizure. Sensory phenomena of tingling or burning that is not somatotopic may occur; autonomic changes such as mydriasis and flushing can also be seen 2,s' I0,23,34,37,47
Autonomic phenomena are much more substan-
tial in cingulate seizures and include: mydriasis, pallor, tachycardia, urination, conjunctival injection, hyperpnea or apnea which is associated with auras of suffocation 19-2],34. Motor effects of cingular seizures include head nodding or extension (with or without loss of consciousness), arm elevation is followed by contra- or ipsiversive posturing as spread to the SMA occurs. Sudden falls without loss of consciousness, sudden tonic arm movements and bilateral asymmetric facial twitching can occur. The patient may cry, laugh or moan; consciousness may be partially ('dreamy state') or completely lost and pseudoabsences have been noted. Repetitive, reactive, bilateral complex automatisms, genital manipulation and fetal posturing may also occur 9'21'29'a3'45, although these are often late in the seizures. The manifestations of parietal lobe seizures depend on the specific region. The inferior lobule, especially opercular seizures, may produce gustatory auras or light-headedness proceeding to swallowing and lip and tongue movements. They can be reflexic, precipitated by food or sounds 34. Others report auras of 'bad tastes,' arm pain, loss of control of movements proceeding to tonic posturing of both hands or gestural automatisms TM. Post-central gyrus discharges produce contralateral tingling, numbness (sometimes in a Jacksonian march), pain, sensations of heat, coldness, or swelling. Epilepsia partialis continua, tonic leg seizures, nausea and vomiting followed by adversive seizures 34 can occur. Rotation, metamorphopsia, and right-left confusion have been described from superior iobule 2aa'43. The parieto-occipital junction is associated with unformed visual hallucinations leading to vertigo and tinnitus or contralaterai numbness a. Finally, junctional seizures (parieto-temporo-occipital) produce speech arrest, Wernicke's dysphasia, gestural, verbal and dyspraxic automatisms a. Others report bilateral stiffening of upper then lower extremities 3 and illusions of an emotional type 34. METHODS Five to 12 seizures per patient were recorded using scalp and sphenoi~al biotelemetry and videotaping of ictal behaviors. The patients were
148 tested for level of consciousness during at least one of the seizures. All authors viewed each seizure several times to come to a consensus classification. Awake and sleep interictal EEGs were also recorded. The recording sites and selection of montages are described in part 144. After all non-invasive tests were completed, 8 patients underwent various surgical explorations individually determined on a case by case basis. An excellent correlation is said to exist if the resuits of intracranial monitoring match the ictal focus as hypothesized by the semiologic classification. A good correlation meant that the ictal zone included but was larger or smaller than the hypothesized zone. RESULTS Eight patients underwent surgical procedures. Three had 'medial frontal' type electroclinical manifestation. One of these, patient no. 2, was in
the group with a discrete PET lesion and excellent concordance among all tests. A second-for-second diagram of his seizures is shown in Fig. 1A and appears at first glance to 'defy meaningful classification 's4. On closer inspection, an initial arrest with darting eye movements and/or grimace is rapidly followed by head, eye and somtimes trunk deviation to the left and bilateral tonic limb posturing. The head and eye deviations with bilateral limb postures were consistent with an SMA focus. Loss of consciousness occurred early with the change in expression. The mid-portion of the seizure consisted of a variety of complex automatisms with oral and trunkal movements (sometimes preceded by a loss of tone), while the end of the seizure shows reactive, semipurposeful automatisms and disorientation postictally. The fifth through seventh seizures all occurred within 1 h, which may have compressed the normal sequence and duration of the seizures. The interictal and ictal EEGs were non-localizing, although lateralized to the
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TABLE I
Results of intracranial electrographicmonitoring with or without surgical excision of the focus Patient (hypothesized Recordings and seizurefocus) surgery
Correlation between hypothesis Pathology and flnal results
1a Medial frontal
Correlation with surgical results- excellent
Non-specific gliosis.
Correlation with intracranial recording and surgical results - good
Biopsy: non-specific gliosis of meninges and cortex with neuronal sclerosis, deep cut and rare lymphocytes. Surgery: calcified AVM with gliosis,
Good
Subpial giiosis with neuronal loss in layer 2-3. Superficial white matter gliosis particularly perivascular. Normal by routine stains and electron microscopy.
2 Medial frontal
15 Deep medial frontal
4b Dorsolateral frontal
6a Dorsolateral frontal
8a Parieto-occipital
9 Precentral frontal (area 6)
13 Temporo-parietal
Surface electrocorticography showed spike and wave discharges over the left SMAc with slowing of the dorsolateral cortex adjacent. L SMA removal provided only temporary decrease of seizures for one month. He underwent a second wider excision which extended to the pericallosal gyrus medially, onto the dorsolateral convexity 3.5 cm from midline and anterior to the primary motor area 7.5 cm. He is now seizure free for 5 months. Ictal recordings with subdural grid on the m~.diai surface over the lesions and with strips on the dorsolateral convexity overlying the lesions showed simultaneous ictal onsets at the medial frontal electrodes which were on the anterior edge of the lesion and from three sites contiguous to this extending 3 cm over the dorsolateral surface. Surgical excision of the lesion resulted in 80% decrease in seizures. Interictal EEG showed bilateral frontocingulate and supra-cingulate epileptiform activity, but most ictal recordings showed onsets in the right fronto-cingulate region. Electrocorticography revealed focal spikes, and spike and wave and slowing superior to the posterior edge of the third frontal gyms. Excision was deferred due to the proximity to Broca's region. Electrocorticography and gross inspection revealed widespread damage of the left dorsolateral cortex. The pole had been previously removed for a suspected cerebral abscess. A wide excision of the dorsolateral cortex sparing the primary motor strip was done. He is seizure free with minimal additional deficit for 1 year, 3 months. Electrocorticography revealed focal spikes in the parietal lobe anterior to the parietooccipital junction. A mass was discovered at the parieto-occipital junction. Resection of the tuber and area of focal spiking resulted in control of seizures, on medications for 2 years. Eiectrocorticography revealed a slow wave focus overlying a neoplasm of the white matter beneath area 6. The patient was seizure free on medications for 2 years following excision and radiation therapy. Subdural strip recordings revealed widespread right temporal onset of seizures with prolonged afterdischarge (2-3 rain) over the parietal opercular cortex. She is seizure free with one aura 6 months after right temporal lobectomy.
a Previously illustrated in Swartz and Delgado-Escueta 41. b Previously illustrated in Delgado-Escueta et al) 4. ¢ Supplementary motor area.
Correlation with electrocorticographyexcellent
Correlation with surgical results- excellent
Non-specific giiosis.
Correlation with surgical results- excellent
Tuberous sclerosis.
Correlation with surgical results- excellent
Grade II astrocytoma,
Correlation with intracranial monitoring and surgical results- good
Extensive gliosis and cell loss of cortical (lateral) and hippocampal tissue.
150
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Fig, 1B, CAT, MRI and PETimages in the same patient.
left. The MRI, CAT and PET scans show a discrete lesion of the medial posterior frontal cortex (SMA; Fig. 1B). Neuropsychological assessment was also consistent with frontal dysfunction, including low primary memory, poor verbal fluency and strategy formation, and response rigidity. He had a dorsolateral subdural plate and two medial subdural strips placed. A typical seizure onset seen during intracranial recording is shown in Fig. 2. The intracranial recordings were interpreted as showing a good correlation with the proposed ictal origin (Table I) because the ictal region recorded intracranially included the medial frontal lobe surface but extended byond it to the dorsolateral surface. He underwent a focal resection of his lesion in the SMA and has had an 80% reduction of seizure frequency. Two patients had dorsolateral electroclinical
characteristics. One underwent electrocorticography which showed an actively spiking zone on the lateral frontal surface as hypothesized. Wide excision was not attempted because of the proximity of Broca's speech area. The other had widespread dorsolateral spiking and a wide frontal Iobectomy sparing the motor strip. He has been seizure free for 32 months. These two were classified as having an excellent correlation to the presurgically predicted locus. Patient no. 9 had a precentral semiology. Electrocorticography revealed focal slowing and sharp waves above an astrocytoma of the white matter. This was removed, radiation therapy was given and the patient was seizure free for 2 years before being lost to follow-up. One patient with hypothesized temporo-parietal origins (no. 13) had subdural strips placed in both
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these areas. A diffuse temporal lobe onset of her seizures was followed by a prolonged afterdischarge in the parietal region. She is seizure free with one aura in 28 months of postoperative follow-up. This case is called a 'good correlation' beTABLE II
Correlation of intracranial electrographic recording with or without subsequent surgical excision excellent = complete agreement; good = in agreement but showing a greater or less extensive area of dysfunction; poor = a normal test result.
Patient
CA T
MRI
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Neuropsych.
1 2 4 6 8 9 13 15
poor excellent poor good excellent excellent poor poor
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cause the hypothesized focus included but was larger than the actual one. Another patient with parietal lobe seizure semiology underwent electrocorticography which showed an active spiking zone just anterior to a parieto-occipital tuber. Both the tuber and spiking zone were excised with complete control of seizures for 3.5 years. Thus, this patient is considered to have excellent correlation of preand postsurgical ictal focus identification. In total, 5/8 (62.5%) of the patients had an excellent correlation between intracranial electrographic studies and the electroclinical classification. The remaining 37.5% had a good correlation (Table I). The other neurodiagnostic test correlations are shown in Table II. FDG-PET scans had an excellent correlation in 50%, good in 25% and poor in 25%. Neuropsychological tests were slightly more accurate than PET with an excellent correlation in 25% and good in 62.5%. MRI had an excellent correlation in 62.5% and a poor correlation in 37.5%. CAT scanning had an excellent
152 correlation in 37.5%, good in 12.5% and poor in 50%. Six of 8 patients became seizure free after resective surgery. One of these had 1 immediate postoperative seizure, and 1 patient had a single aura. The follow-up period is 21 months-4.5 years. Of the two with continued seizures, one developed a progressive syndrome consistent with Rasmussen's encephalitis and later underwent hemispherectomy with control of seizures, the other had an 80% reduction in the seizure frequency after a focal lesional resection. DISCUSSION Traditionally, many authors have considered the clinical manifestations of complex partial seizures to be of value in the discrimination of temporal, frontal and other extratemporal seizure locii~'3°'32'46. Subvarieties of partial complex seizures based on localization and behaviors were appended to the recent Classification of the Epilepsies and Epileptic Syndromes 13. Other investigators are unconvinced of this view n'26 and do not specifically mention semiology in lists of criteria for surgery 17a. Complex partial seizures of extratemporai origin have characteristics which distinguish them from those of temporal lobe origin. When careful juxtaposition of behaviors and of ictal EEG patterns is made with modern techniques of neuroimaging and neuropsychological assessment, good concordance between tests of lesion localization can be obtained. Furthermore, good agreement with results of intracranial monitoring and surgical excision is also possible. In spite of improved neurodiagnostics there always remains a group of patients who have complex partial seizures but no other sign of cerebral
REFERENCES 1 Ajmone Marsan, C. and Abraham, K., A Seizure Atlas. E[ectroenceph. Clin. Neurophysiol., Suppl. 15, Elsevier, Amsterdam, 1960, pp. 1-215. 2 Ajmone Marsan, C. and Goldhammer, L., Clinical ictal patterns and electrographic data in cases of partial seizures of frontal, central, and parietal origin. In: M.A.B. Brazier
dysfunction. In this study, neuroimaging was normal in 25% (PET) to 50% (CAT). As more patients undergo surgery without structural lesions these numbers will increase. To approach these patients surgically one can use very widespread sampling of multiple brain regions with stereoEEG and/or subdural plates. This will often require several implantations prior to surgery, causing increased risk to the patient. Even then the results are not guaranteed. Holmes et al. 24 reported that of 8 patients with both frontal and temporal hypometabolism on ISFDG-PET scans, only 4 had temporal lobe seizure onsets recorded by subdural strip electrodes. Those 4 underwent temporal lobectomy but only 2 improved. If attention to ictal behaviors can improve surgical outcome from 75% to greater than 90% in temporal lobe epilepsy16'17, it should also improve outcome in extratemporal seizures, None of our 8 patients would have undergone surgical exploration without information that corroborated the electroclinical picture. Nevertheless, considered alone, the location of the ictal focus based on electroclinical characteristics had an excellent correlation with the results of intracranial electrographic recordings and surgical excision in 62.5% and had a good correlation in 37.5%. CONCLUSION Resective surgery for seizure control requires careful use of all pertinent non-invasive test data. Careful classification of electroclinical features is an important source of data in the planning of intracranial monitoring or surgical excision. The ability to classify seizures based on electroclinical manifestation remains an important adjunct in the armamentarium of the epileptologist, as it has been since the time of Penfield,
(Ed.), Epilepsy: its Phenomena in Man, Academic Press, New York, 1973, pp. 235-258. 3 Ajmone Marsan, C. and Ralston, B.L., The Epileptic Seizure: its Functional Morphology and Diagnostic Significance, Thomas, Springfield, IL, 1957. 4 Bancaud, J., Les crises 6pileptiques d'origine occipitale (~tude strrro.61ectroencrphalographique), Rev. d'OtoNeuro-Ophtalmoi., 41 (1969) 299-315.
153 5 Bancaud, J., Topographic relationship between cerebral lesions and seizure discharges. In: R. Canger, F. Angeleri and J.K. Penry (Eds.), Advances in Epileptology. Xith Epilepsy Int. Syrup., Raven Press, New York, 1980, pp. 103-109. 6 Bancaud, J., Srmiologie clinique des crises ~pileptiques d'origine temporale, Rev. NeuroL, 143 (1986) 392-400. 7 Bancaud, J., Bonis, A., Munari, C., Szikla, G., Chodkiewicz, J.P. and Talairach, J., Localizing value of the clinical manifestations of the partial seizures, Acta Neurochir. (Wien), Suppl. 33 (1984) 7-15. 8 Bancaud, J., Talairach, J., Bonis, A., Schaub, A., Szikla, G., Morel, P. et Bordas.Ferrer, M., La St~r~o-dlectroenc~phalographie clansl'Epilepsie, Masson, Paris, 1965. 9 Bancaud, J., Talairach, 3, Geier, S., Bonis, A., Trottier, S. et Manrique, M., Manifestations comportementales induites par la stimulation 61ectrique du gyrus cingulaire antrrieur chez rhomme, Rev. Neurol., 132 (1976) 705-724. 10 Bancaud, J., Talairach, 3., Schauh, C., Bonis, A., Szikla, G. and Colomb, D., Stereotaxic functional exploration of the epilepsies of the supplementary areas of the mesial surface of the hemisphere, Eleetroenceph. Clin. Neurophysiol., 14 (1962) 788. 11 Bossi, L., Munari, C., Stoffels, C. et al., Somatomotor manifestations in temporal lobe epilepsy, Epilepsia, 25 (1984) 70-76. 12 Brey, R. and Laxer, K.D., Type I/II complex partial seizures: no correlation with surgical outcome, Epilepsia, 26 (1986) 657-660. 13 Commission on Classification and Terminology of the International League Against Epilepsy, Proposal for the classification of the epilepsies and epileptic syndrome, Epilep. sia, 26 (1985) 268-278. 14 Delgado-Escueta, A.V., Swartz, B.E., Maldonado, H.M., Walsh, G.O., Rand, R.W. and Halgren, E., Complex partial seizures of frontal lobe origin. In: H.G. Wieser and C.E. Elger (Eds.), Presurgical Evaluation of Epileptics, Sprin~er, Berlin. 1986, pp. 267-299. 15 Delgado-Escueta, A.V. and Walsh, G.O., The selection process for surgery of intractable complex partial seizures; surface EEG and depth electrography. In: J.K. Penry and D.P. Purpura (Eds.), Epilepsy, Raven Press, New York, 1983, pp. 296-325. 16 Delgado-Escueta, A.V. and Walsh, G.O., Type I complex partial seizures of hippocampal origin: excellent results of anterior temporal lobectomy, Neurology, 35 (1985) 143-154. 17 Dodrill, C.B., Wilkins, R.J., Ojemann, G.A., Ward, A.A., Wyler, A.R., Van Belle, G. and Tamas, L., Multidisciplinary prediction of seizure relief from cortical resection surgery, Ann. Neurol., 20 (1986) 2-12. 17a Engel, Jr., J., Rausch, R., Lieb, J.B., Kuhl, D.E. and Crandall, P.H., Correlation of criteria used for localizing epileptic foci in patients considered for surgical therapy of epilepsy, Ann. NeuroL, 9 (1981)215-224. 18 Geier, S., Bancaud, J., Bonis, A. and Enjelvin, M., Nonmotor frontal epilepsy: study of EEG and clinical features using ~ele-EEG and tele-stereo.EEG~ Electro~nceph, C!i.n..
Neurophysiol., 34 (1973) 699. 19 Geier, S., Bancaud, 3., Talairach, J., Bonis, A., Enjelvin, M. and Hossard-Bouchard, H., Automatisms during frontal lobe seizures, Brain, 99 (1976) 447-458. 20 Geier, S., Bancaud, J., Talairach, J., Bonis, A., HossardBouchard, H. and Enjelvin, M., Ictal tonic postural changes and automatisms of the upper limb during epileptic parietal lobe discharges, Epilepsia, 18 (1977) 517-524. 21 Geier, S., Bancaud, J., Talairach, J., Bonis, A., Szikla, G. and Enjelvin, M., The seizures of frontal lobe epilepsy: a study of clinical manifestations, Neurology, 27 (1977) 951-958. 22 Goldring, S., The role of the prefrontal cortex in grand mal convulsion, Arch. Neurol., 26 (1972) 109-119. 23 Greene, J.R., Angevine, J.B., White, J.C., Edes, A.O. and Smith, R.D., Significance of the supplementary motor area in partial seizures and in cerebral localization, Neuro. surgery, 6 (1980) 64-75. 24 Holmes, M., Kelly, K. and Theodore, W., Complex partial seizures: correlation of clinical and metabolic features, Arch. Neurol., 45 (1988) 1191-1193. 2-~ Hochman, S.M., Rotary seizures associated with frontal lobe malignant neoplasm: a case report, Epilepsia, 1 (1983) 11-14. 26 Ives, J.R., Video recording during long-term EEG monitoring of epileptic patients. In: R.J. Gumnit (Ed.), 1nten. sire Neurodiagnostic Monitoring. Advances in Neurology, Vol. 46, Raven Press, New York, 1986, pp. 1-117. 27 Jackson, J.H., A study of convulsions. In: Selected Writings of John Hughlings Jackson, Vol. 1, Hodder and Stoughton, London, 1870. 28 Ludwig, B.I., Ajmone Marsan, C. and Van Buren, J., Depth and direct cortical recording in seizure disorders of extratemporal origin, Neurology, 26 (1976) 1085-1099. 29 Mazars, G., Cingulate gyrus epileptogenic foci as an origin for generalized seizures. In: 3. Gastaut, H. Jasper, J. Bancaud and A. Waltregny (Eds.), The Physiopathogenesis of the Epilepsies, Thomas, Springfield, IL, 1969, pp. 186-189. 29a Munari, C. and Bancaud, J., The role of stereo-encepha. iography in the evaluation of partial epileptic seizures. In: R.J. Porter and P.L. Morseili (Eds.), The Epilepsies, But. terworth, London, 1985, pp. 267-306. 30 Munari, C., Bonis, A. and Kochen, S., Eye movements and occipital seizures in man, Acta Neurochir. (Wien), Suppl. 33 (1984) 47-52. 31 Munari, C., Stoffels, C., Bossi, L. et al., Automatic activities in frontal lobe seizures without involvement of temporal lobe structures. In: M. Dam, L. Gram and 3.K. Penry (Eds.), Advances in Epileptology. Xllth Epilepsy Int. Symp., Raven Press, New York, 1981,pp. 63-64. 32 Munari, C., Stoffels, C., Bossi, L., Bonis, A., Talairach, J. and Bancaud, J., Automatic activities during frontal and temporal seizures: are they the same? In: M. Dam, L. Gram and 3.K. Penry (Eds,), Advances in Epileptology. Xllth Epilepsy Int. Symp., Raven Press, New York, 1981, pp. 287-291. 33 Niedermeyer, E. and Walker, A.E., Mesio-frontal epilepsy, E!ectroenceph, C!in. Neurophysiol., 3! (!971) !e4-105.
154 34 Peafield, W and Jasper, H., Epilepsy and the Functional Anatomy of the Human Brain, Little, Brown and Co., Boston, MA, 19S4. 35 Penfield, W. and Kristiansen, K., Epileptic Seizure Patterns, Thomas, Springfield, IL, 1951. 36 Penfield, W. and Rasmussen, T., The Cerebral Cortex of Man, MacmillanPress, New York, 1950, pp. 1-238. 37 Penfield, W. and Welch, K., The supplementary motor area of the cerebral cortex, a clinical and experimental study, Arch. Neurol. Psychiat., 66 (1951) 289-317. 38 Rasmussen, T.B., Cortical resection for medically refractory focal epilepsy: results, lessonsand questions. In: T. Rasmussen and R. Marinok (Eds.), Functional Neurosurgery, Raven Press, New York, 1979, pp. 253-269. 39 Rasmussen, T.B,, Localization aspects of epileptic seizure phenomena. In: R.A. Thompson and J.R. Green (Eds.), New Perspectives it: Cerebral Localization, Raven Press, New York, 1979, pp, 253-269. 40 Rasmussen, T.B., Characteristics of a pure culture of frontal lobe epilepsy, Epilepsia, 29 (1983) 482-493. 41 Swartz, B,E. and Delgado-Escueta, A.V., Complex partial seizures of extratemporal origin: 'the evidence for.' In: H. Wieser, E.J. Speckmann and J. Engel (Eds.), The Epileptic Focus. Current Problems in Epilepsy, Vol. 3, John Libbey, London, 1987, pp. 137-174. 42 Swartz, B.E., Delgado-Escueta, A.V., Maldonado, H,M. and Walsh, G.O., Pseudo-absence seizures: a frontal lobe phenomenon? Presented at the XIII Int. Congress of Epilepsy, Hamburg, 1985. 43 Swartz, B.E., Halgren, E., Delgado-Escueta, A.V,, Blahd, W., Mandelkern, M., Feldstein, P., Rand, R.W,, Maldonado, H.M. and Khonsary, A., Seizure semiology, neuropsychometrics and neuroimaging eorrelaries in frontal lobe epilepsies, Epilepsia, 27 (1986) 597-598, 44 Swartz, B.E., Halgren, E., Delgado-Escueta, A.V., Mandelkern, M., Fcldstein, P., Maldonado, H., Ropchan, J.,
Blahd, W., Walsh, G.O., Quinones, N. and McGee, M., Multidisciplinary analysis of patients with extratemporal complex partial seizures. I. Interest agreement, Epilepsy Res., 5 (1990) 61-73. 45 Talairach, J., Bancaud, J., G¢ier, S., Bordas-Ferrer, M., Bonis, A., Szikla, G. and Rusu, M., The cingulate gyms and human behavior, Eleetroenceph. Clin. Neurphysiol., 34 (1973) 45-52. 46 Tharp, B., Orbital frontal seizures, a unique e!ectroencephalographic and clinical syndrome, Epilepsia, 13 (1972) 627-642. 47 Van Buren, J.M. and Fedio, P., Functional representation on the medial aspect of the frontal lobes in man, Neurosurgery, 44 (1976) 275-289, 48 Walker, A.E., Temporal Iobectomy, J. Neurosurg., 6 (1967) 641-649. 49 Waish, G.O. and Delgado-Escueta, A.V., Type II complex partial seizures: poor results of anterior temporal lobectomy, Neurology, 34 (1984) 1-13. 50 Wieser, H.G., Electroclinical Features of the Psychomotor Seizure, Fischer, Stuttgart, 1983, pp. 177-220. 5i Wieser, H.G., Stereoelectroencephalic correlates of focal motor seizures. In: E.J. Spackmann and C.E. EIger (Eds.), Epilepsy and the Motor System, Urban and Schwarzenberg, Munich, 1983, pp. 287-309. 52 Wieser) H.G,, Graf, H.P., Bernoullie, C. and Siegfried, J., Quantitative analysis of intracerebral recordings in epilepsin partialis continua, Electroenceph. Clin, Neurophysiol., 44 (1978) 14-22. 53 Williamson, P.D. and Spencer, S.S., Clinical and EEG features of complex partial seizures of extratemporal origin, Epilepsia, 27, Suppl. 2 (1986) $46-$63. 54 Wflliamson, P,D., Wieser, H.G. and Delgado-Escueta, A.V., Clinical characteristics of partial seizures. In: J. Engel (Ed.), Surgical Treatment of Epilepsies, Raven Press, New York, 1986, pp. 101-120.
