Folia Psychiatrica et Neurologica Japonica, Vol. 31, No. 3, 1977

Periodic EEG Patterns Observed in Two Cases With Partial Seizures Akira Terao, M.D., Satoru Tawara, M.D., Yoshinobu Takemoto, M.D., Nobuzugu Nomura, M.D., Shukuro Araki, M.D. and Teruo Shirabe, M.D.* Department of Internal Medicine, Division of Neurology, Kawasaki Medical School, Kurashiki

* Department

of Pathology, Division of Neuropathology, Kawasaki Medical School, Kurashiki

INTRODUCTlON EEG patterns in which burst of high voltage slow activity, sharp wave, or both, recur more or less regularly against a background of low amplitude slow activity are relatively uncommon. These periodic EEG patterns have been described as diagnostic findings in cases of subacute sclerosing panencephalitis, herpes simplex encephalitis and subacute spongiform encephalopathy. The similar periodic phenomena have also been reported in some cases of cerebral lipidosis, progressive myoclonus epilepsy, hepatic coma, severe anoxic encephalopathy, extremely deep anesthesia, and in some cases of premature infant physiologically. Periodicity therefore has no claim to The mechanism underlying periodic EEG phenomena is by no means clear but a number of suggestions have been made. Recently, we observed ictal or interictal periodic EEG patterns in two cases with partial seizures. In one case with metastatic brain tumor, the typical periodic lateralized epileptiform discharges (PLEDs, Chatrian et d 5 > were noted on the right hemisphere. From the findings of the postmortem examination and the clinical course, primary importance of cerebral cortex to produce Received for publication March 2, 1977.

PLEDs was suggested. In another case with idiopathic hypoparathyroidism, focal periodic discharges were observed. The EEG features in both cases were studied correlatively with their clinical pictures and clinicopathological findings. CASE REPORTS Case 1.

M.M., an elderly woman aged 74, was admitted to Kawasaki Medical School Hospital on September 15, 1975. She died two months later on November 16, 1975. At the beginning of December 1974, a tumor was noted on her left upper eyelid and it was surgically removed. The histological Snding of the tumor was adenocarcinoma and the patient was given a series of radiation therapy, a total of 5,700r. On September 10, 1975, she complained of epigastric pain and tumor was noted in the right hypochondriac region. Four days later, she developed left hemiplegia, followed by disturbance of consciousness, urinary incontinence, and convulsive seizure. Clinical Examination-On admission the patient was semicomatous, and jaundice was noted on the bulbar conjunctiva and on the skin. Her face was turned to the left and her eyeballs revealed conjugate deviation to the left side. The pupils were equally

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round and react to light, but sluggish in the right. Fundoscopic examination revealed normal disc bilaterally. Continuous clonic jerks in the left limbs subsided after intravenous administration of diazepam, and the left hemiparesis with mild hemisensory disturbance was noted. The deep reflexes were abolished and no pathologic reflexes were elicited in the four limbs. Plain roentogenograms of the skull and the chest revealed no abnormalities. Electrocardiogram was within normal limit. Echoencephalogram showed one cm midline shift to the left. Brain scanning with technetium 9 9 m pertechnetate revealed no abnormalities. Laboratory Data-Examination of the blood disclosed 12.6- per 1OOml hemoglobin, 4,020,000red blood cells, 12,700 white blood cells. Serum proteins were 6.3 gm per 100 ml, blood sugar was 192 mg per lOOml, total serum bilirubin was 9.9 mg per lOOml, direct one 67 percent. Choliiesterase was 225 IU, alkaline phosphatase 256 IU, GPT 187 IU, GOT 139 IU, ammonia 80 y per 100ml (Sept. 16, 1975), 85 y per 1OOml (Sept. 23, 1975).

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Upon admission, cerebrospinal fluid examination revealed an opening pressure of 220 mm of water. The fluid appeared slightly yellowish, and contained 55 mg of protein per lOOml, 109 mg of sugar per 100 ml and no cell increase. Clinical Course-The patient was treated with anticonvulsants, dexamethasone and glycerol, and the clonic jerks were abolished. Five days after admission, she was alert, normally oriented, and the left hemiparesis was mild. However, she gradually grew worse again and on October 10, 1975, she revealed completed left hemiplegia; the upper limb was spastic and the lower one was fluccid. A week before death, she became drowsy, doubly incontinent, and speechless. The day before death, clonic jerks of the left lower limb reappeared. The patient was in a profound coma and unresponsive to any form of stimulus. The clonic jerk ceased (Fig. 1). EEG Observations-On September 17, two days after admission, the first EEG recording was made (Fig. 2). It showed an unusual repetitive sharp waves at a fre-

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Fig. 2: Case 1. A 74-year-old woman with metastatic carcinoma in the right parieto-occipital region. The 1st EEG recording, two days after admission, showed PLED'S at a frequency of about 1.5 per second on the right hemisphere. PLED'S were followed by muscle action potentials recorded simultaneously on the left anterior tibial muscle.

quency of about 1.5 per second on irregular slow wave background domrnantly on the right. These sharp waves were followed by muscle action potentials recorded simultane ously on the left anterior tibial muscle. The

second EEG recording, on September 22, revealed periodic slow waves instead of sharp waves. On October 11, the third EEG recording was made (Fig. 3). It revealed no

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G -5 Fig. 3: Case 1. The 3rd EEG recording (Oct. 11, 1975) revealed no periodic EEG patterns, and delta wave bursts were noted dominantly on the right.

periodic EEG patterns, and delta wave bursts were noted dominantly on the right. The last EEG recording, on November 15, the day before death, showed high voltage periodic EEG complexes at a frequency of about 2 to 3 per second (Fig. 4). Somatosensory evoked responses (SER) were recorded, on September 17, from the scalp electrodesla (Fig. 5 ) , A-SER elicited from the median nerve stimulation revealed lowered secondary response on the right (upper trace), and GSER elicited from the posterior tibia1 nerve stimulation showed lowering of peaks on both sides. Pathological Findings in Case 1-At necropsy, pancreatic head carcinoma which

compressed common biliary tract was found. Multiple metastatic foci in heart, left lung, adrenals, uterus, Douglas’ pouch, small intestine, colon, and in subcutaneous tissues (neck, abdominal wall and iliac region) were also noted. The brain weighed 1,280 gm,but it appeared moderately edematous with broad, flat gyri in the right hemisphere. The dura mater, hypophysis and the basal arteries were icteric. Coronal sections of the brain revealed a main metastatic carcinoma ( 5 X 5 X 6 cm) in the right parieto-occipital region. The tumor invaded from cortex to subcortical white matter. The white matter of the right hemisphere including the fron-

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Fig. 4: Case 1. The last EEG recording, the day before death (Nov. 15, 1975) showed high voltage periodic EEG complex at a frequency of about 2 to 3 per second. tal lobe was extensively swollen and edematous and was stained yellowish (Fig. 6 ) . Demyelinating changes of the white matter corresponding with edematous and icteric area were observed diffusely by H.E. and Kluver-Barrera stain (Fig. 7). MicroscopicaUy, nerve cells of cerebral cortex around the metastatic mass showed ischemic changes with glial proliferation, although the cortical structures were fairly well preserved in the right hemisphere. The basal ganglia and the brain stem were intact. Case 2.

Z.H., an elderly woman, aged 61, was admitted to Kawasaki Medical School Hos-

pital on June 12, 1976. At the age of 31, the patient began to have tetanic carpal spasm corresponding with menstruation in every month, and the phenomena disappeared on menopause at the age of 43, when she had an operation for bilateral cataract. At the age of 56, the tetanic spasm reappeared and on March, 1976 at the age of 61, the patient began to have another seizure, which was often precipitated by diarrhea, hunger, fatigue, drowsiness, or siren of ambulance. She raised her left arm and left leg in a tonic attitude, and her eyes then turned to the left, head and trunk turned to the left. This was followed by a few coarse, clonic jerks of the left upper limb and hyperven-

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Fig. 5 : Case 1. Somatosensory evoked response (SER) recording: A-SER elicited from the median nerve stimulation revealed lowered secondary response on the right (upper trace), and C-SER elicited from the posterior tibia1 nerve stimulation showed lowering of peaks on both sides.

tilation. The seizure duration was 30 to 60 seconds and did not developed into generalized convulsion. She almost could not speak, but she replied “Yes” when she was called by her name. It seemed to the observer that she understood and she had recollection of the attack. Her attacks were ushered in by a change in the appearance of things or per-

sons. She explained, “The person seemed to be beautifully glittering as a queen or Gekko-Kamen, a fictional hero with moonlight mask”. At the same time, the patient sometimes smelled sulfur odor or heard muttering sound of a crowd. Clinical Examinationan admission the patient manifested repetitive seizures about every five minutes. The patient was well

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Fig. 6: Case 1. Coronal sections of the brain revealed a main metastatic carcinoma ( 5 X 5 X 6 cm) in the right parieto-occipital region. The tumor invaded from cortex to subcortical white matter. The white matter of the right hemisphere including the frontal lobe was extensively swollen and was stained yellowish.

nourished, well developed. Her blood pressure was 124/76mmHg, pulse was 96/min and regular, and there was no abnormal findings on physical examination. Neurological examination was unremarkable; prompt pupillary light responses, normal optic fundi and normal tendon reflexes without pathological ones. Chvostek’s sign and Trousseau’s phenomenon were not observed. Laboratory Data-Laboratory findings on admission are shown in Table 1. Examinations of urine, feces and CBC were within normal limit. The serum potassium and calcium levels were decreased, and serum phosphorous levels were increased. Renal functions were partially disturbed, but were not considered so severe as to cause serum electrolytes imbalance. Glucose

Fig. 7: Case 1. Demyelinating changes of the white matter corresponding with edematous and icteric area were observed diffusely by H. E. (left) and Kltiver-Barrera stain (right).

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Table 1: Laboratory Findings in Case 2 Blood chemistry Bil. 0.7 mg/dl I1 4 A1-P 30 IU/l Chol. 203 mg/dl 345 IUldl ChE 13 IU/l GPT GOT 22IU/l Crn. 1 . 3 mg/dl BUN 16mg/dl 2.2 mg/dl Ur. A. Serum protein fractions T. P. 6.8 g/dl A/G 1.27 Alb 56.7% 3.8% Ul-Gl Ut-Gl 13.9% 8-G1 13.4% r-Gl 12.8%

tolerance test, thyroid and adrenal functions were within normal limit. Parathyroid functions were examined; percent tubular reabsorption phosphate (% TRP) was 99.6%, phosphorous clearance was 4.7 ml/min, serum parathormone was 0.19 ng/ml (normal, below 0.5 nglml). Ellsworth-Howard test revealed 5.1 times increase of phosphorous diuresis following intravenous administration of 200 U of parathormone. The result in the patient was typical of the response in idiopathic hypoparathyroidism. The electrocardiogram showed a prolonged Q-T interval. Lumber puncture revealed normal findings. Right carotid angiogram, brain scanning, and echoencephaloRrem revealed no abnormalities. Roentogenograms of the skull demonstrated no intrncran;d calcification. Psychometrics revealed an intelligence quotient of 78 (WAIS). Clinical Course-The patient was treated with anticonvulsants, i.e. diphenylhydantoine, calbamazepine, diazepam, and the seizures were perfectly subsided four days after admission. The anticonvulsants were

Serum electrolytes (mEq/L.) Na 135 (134-144) K 2.7 (3.2-4.7) c1 96 (98-1 07) Ca 2.9 (4.0-5.5) P 2.9 (1.4-2.6) Mg 1.9 (1.6-2.1) Urine electrolytes (mEq/day) Ca 4.1 (2.5-1 5) 6.3 (20-40) P Serum enzymes CPK 168IU/1 (0-70) LDH 276IU/1 (29-92) Renal function PSP test 15 min. 10.8% 120min. 41.4% Concentration test Max. 1030 C. cm. 79.5ml/min

later withdrawn because of the appearance of drug eruption over the trunk and the extremities. The seizures were not reappeared with the successive administration of vitamin D and calcium compound. Electroencephalographic sharp waves and periodic discharges were disappeared. The serum electrolytes and serum enzyme (LDH, CPK) levels revealed normal values. EEG Observations-The basic EEG activities were diffuse and dominant fast waves intermingled with 9 to 10 Hz alpha waves. Corresponding with clinical seizure, small spike train in the right frontal and mid-temporal region was followed by continuous 4 to 5 Hz theta waves restricted on the right hemisphere. The seizure pattern of about one minute duration disappeared promptly with the termination of the clinical seizure. Periodic EEG pattern was observed interictally, and it appeared in the right anterior and mid-temporal region accompanied with phase reversal of sharp waves in the right anterior temporal region (Figs. 8, 9 ) . Some irregularity in the periodicity of the

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Case 2. A 61-year-old woman with idiopathic hypoparathyroidism. Periodic EEG pattern was observed interictally in the right anterior and mid-temporal region (F8-T4) with phase reversal of sharp waves in the right anterior temporal region (F8). Fig. 8:

discharges occurred, and the discharge interval shortened just before the clinical seizures. SERs were recorded chronologically and the prolonged peak latencies of A- and CSER were restored to normal range on August 17, 1976, when the patient had already been successfully treated. Relative-

ly low A-SER amplitude on the right was also noted (Fig. 10). DISCUSSION The occurrence of periodic EEG pattern with concomitant relatively localized cerebral lesion has been observed in intra-

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cranial tumors (esp. brain abscess, glioma or hematoma) ,9 i2 cerebrovascular lesions (esp. acute stage of cerebral infarction)? io lo or in artificial cerebral damage following prefrontal 10botomy.~ Chatrian et aL3 studied this pattern in detail and called it “periodic lateralized epileptiform discharges” (PLEDs). Markand and Daly10 studied patients who exhibited

periodic paroxysmal activity of focal or lateralized distribution in the EEG. They concluded that this pattern occurs exclusively in acute limited lesions of the cerebral hemispheres. Chatrian et d 3recorded PLEDs in 33 subjects. Twenty-nine of 33 patients experienced epileptic seizures consisting of epilepsia partialis continua in seven cases, reitera-

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Fig. 10: Case 2. SER’s were recorded chronologically: the prolonged peak latences of A- and C-SER were restored to normal range, when the patient had already been successfully treated. Relatively low A-SER amplitude on the right was noted. tive, sporadic or isolated focal motor seizures in 18 cases and continuous psychical seizures in four cases. The etiology of the lesion(s) of disorders was: cerebral infarct(s) in 13 cases, recent infarct or chronic focal seizure disorder in seven cases, chronic focal seizure disorder in three cases, space-occupying lesion (metastases and glioblastomas) in eight cases, pneumococcal meningitis in one case and postvaccinal encephalomyelitis in one case. Markand and Dalylo found some irregularity in the periodicity of the discharges in their cases. Therefore, they used the term “pseudoperiodic” lateralized paroxysmal discharges (PLPD’s) . However, both PLED’S and PLPD’s may be the essentially identical phenomena with a common pathophysiological basis. They reported sixteen

patients exhibited PLPD’s. Typically, PLPD’s repeated every one to two seconds and consisted of moderate- to high-amplitude, sharp, biphasic or triphasic discharges over a large area of one cerebral hemisphere. Except for one patient who was alert, all patients exhibited varing degrees of altered consciousness when their tracing revealed PLPD’s. Three patients were comatose, 10 patients were stuporous or lethargic, and two patients were confused and disoriented. All patients with PLPD’s had focal (partial) seizures of the motor type with or without secondary generalization. A few patients had continuous focal motor seizures, or epilepsia partialis continua. Most patients had abrupt onset of seizures and had no history of epileptic disorder. This strongly suggested that an acute cerebral

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lesion caused both the seizures and the PLPD’s. Twelve patients had acute thrombotic or embolic infarctions, and two had sickle cell disease with multiple cerebral infarctions due to intravascular sickling. One patient suffered from neurosyphilis and another had acute necrotizing encephalitis. A few cases with PLED’s or PLPD’s have been found in Japan. Miyazaki et uZ.I2 reported in each case with PLED’s suffering from acute disseminating encephalomyelitis and brain metastases of lung cancer. He suggested that liver damage in these two cases might play an important role to produce this EEG pattern. Ogura et aL1* reported two cases of syphilitic meningoencephalitis with PLED’s, and there are several reports about periodic EEG patterns simulating PLED’s.le The EEG pattern of PLED’s may superficially resemble EEG findings of subacute sclerosing panencephalitis (SSPE) . The PLED’S consist of unilateral, high-amplitude sharp waves or spikes that occur with a more or less regular periodicity, usually once in one to two seconds. The differentiation from SSPE is ease because the PLED’s are seen in the setting of a recent focal cerebral hemispheric insult, the EEG complexes are either focal or lateralized, and regardless of the course of the disease, they spontaneously disappear in a few days or weeksa6l 1 About the possible mechanism of origin of periodic EEG pattern, the following theories have been presented1‘ : 1) severe cortical damage in the presence of functioning subcortical structures (Lesse et al.) 2) cortical isolation secondary to histopathologic changes in cerebral hemispheric white matter (Bogacz et al.) 3) brain stem origin (Fenyo and Hasznos) 4) brain stem origin with fairly functional cortex (Ohya et d.).In Case 1, when autopsied, marked cerebral edema was noted in the right hemisphere. The white matter including the frontal lobe was extensively swollen

and edematous and was stained yellowish, suggesting destructed blood brain barrier in the region. Microscopically, demyelinating changes of the white matter corresponding with edematous and icteric area was observed diffusely, although the cortical structures were fairly well preserved in the right hemisphere. The deeper structures, basal ganglia and brain stem were also intact. From the findings, the appearance of PLED’s in Case 1 may correspond with the second cortical isolation theory abovementioned. Chronological observation of PLED’s in Case 1 suggested that there was certain correlation between the appearance of PLED’s and cerebral edema. The episodic or transient appearance of PLED’s might result from a reversible (functional) severance of the cerebral cortex from normal connections with deeper structures. The occurrence of PLED’s may correspond with the stage in which cerebral edema invades relatively white matter as to spare cerebral cortex. Then, PLED’s will disappear with alleviation of cerebral edema (refunctioning of white matter) or with severe progression of cerebral edema (ultimate dysfunction of cortex). Henry and Scoville*made direct electrical recording from the cortex of 34 patients before, throughout and following prefrontal lobotomy. All cases showed a marked decrease in electrical activity from the cortex rostra1 to the section, and all but one showed the development of burst-suppression activity confined to isolated cortex. Echlin et al.? reported that paroxysmal hypersynchronous discharges, or abnormal bursting had been shown to occur in humans, monkeys and cats from almost any area of neuronally isolated cerebral cortex, and that the burst phenomenon induced by partial isolation of nerve cells might be a factor in the mechanism undarlying focal cortical seizures. About the factor responsible for burst-suppression activity, Fischer-Williamse suggested that it

Periodic EEG Patterns was undercut cortex i.e. an anatomical or functional, complete or partial, cut-off from normal connection with deeper structures. In Case 1, as already mentioned, the primary importance of cerebral cortex to produce PLED’s was supported clinicopathologically. While uremia and electrolyte imbalance occurred in about one-half of the patients of Chatrian et d.,S the syndrome can clearly occur without such derangements, as was often the case with the patients of Markand and Da1y.l” The latters suggested that systematic metabolic alterations might play no more than a secondary role in pathogenesis. In Case 1, as shown in Fig. 1, no correlation was found between PLED’S and metabolic alterations. In Case 2 with idiopathic hypoparathyroidism, tetanic spasms were replaced by partial complex epileptic seizures 18 years after menopause. Disappearance of tetanic spasms at menopause and the later recurring may be explained by the effect of menopause on serum levels of calcium and inorganic phosphorous. Aoki’ reported that the serum calcium level was decreased with the advance of age in regularly menstruating women, and toward the menopause, the serum calcium level was rapidly increased, reached maximum in two to five years after menopause, and was slightly decreased thereafter. The inorganic phosphorous level also varied in a similar attitude. Convulsions frequently occur with hypoparathyroidism. Certain features regarding seizures and the EEG seem to be generally acceptedu: 1) Tetany occurs first and usually may precede the seizures by days to years. 2) The seizures are usually grand mal, although focal seizures have been described. 3) The EEG abnormalities are usually generalized, but focal abnormalities may also be found. 4) The EEG reverts to or toward normal in the vast majority of cases and seizures are controlled when the serum calcium is restored to normal. 5 ) Anticonvulsants alone are not

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effective in controlling the seizures. These features except the last one were observed suitably in Case 2. Focal epileptic seizures may form 20 percent of all hypocalcemic seizures, and may occur alone or in addition to generalized seizures in any one patient.16 They may be motor or sensory with or without associated adversive phenomena. There is evidence to suggest that patients liable to focal seizures have an increased seizure incidence when they became hypocalcemic. It has also stated that seizures may increase in frequency at the time of menstruation.16 The appearance of partial seizures in metabolic disorders as in Case 2 has been noted also in cases with hyperosmoiar nonketotic hyperglycemia as an initial symptom.? l7 Yamell et d.le observed partial seizures, esp. PLED’s in elderly patients who were receiving intravenous neophylline therapy. In these autopsied cases, focal central nervous system lesions were found histopathologically. In Case 2, firing from subclinical epileptogenic cerebral lesion, such as from a focal cerebral infarct might be precipitated with hypocalcemia due to idiopathic hypoparathyroidism. The remarkable therapeutic effect of anticonvulsants in this case might also support the speculation. From the findings that the interval of periodic discharge in Case 2 shortened with the initiation of clinical seizures, the periodic pattern may be regarded as subclinical and repetitive epileptic discharges from an irritative lesion deeply seated in the right anterior temporal lobe. SERs were also recorded in Case 2 and prolonged peak latencies were observed. The latencies r e vealed shortening when epileptic seizures were all abolished after administration of anticonvulsants. Buchsbaum et d 2 reported prolonged peak latencies of SER’s in cases with pseudohypoparathyroidism. The lowering of SER amplitude on the right hemisphere in Case 2 might suggest the lesioned side.

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SUMMARY Two cases with partial seizure and periodic EEG pattern were reported. Case l. A 74-year-old woman revealed typical periodic lateralized epileptiform discharges (PLED’S) on the right hemisphere. The patient was semicomatous with mild jaundice and epilepsia partialis continua in the left lower limb. Postmortem examination revealed a main metastatic carcinoma of pancreas head origin in the right parietooccipital region. In the right hemisphere, the cortical structures were relatively preserved, but the white matter including the frontal lobe was swollen and its demyelinating changes were observed diffusely. The PLEDs might result from an anatomical or functional severance of the cerebral cortex from normal connections with deeper structures. Case 2. A 61-year-old woman, with idiopathic hypoparathyroidism showed partial complex seizure. The EEG revealed an anterior temporal spike focus and slowing in the right hemisphere, corresponding with repetitive seizures of about one minute duration and with several minutes interval. An interictal periodic EEG pattern appeared in the right anterior and mid-temporal region. No cerebral abnormalities were found with other neurological examinations including brain scanning, carotisangiogram, and echoencephalogram. The periodic pattern was assumed as subclinical focal seizure discharges from the right anterior temporal deep structures. REFERENCES 1 Aoki, T.: The effect of menopause on

serum levels of calcium and inorganic phosphorous, Folia Endocrinol Jap, 51: 556-560, 1975. 2 Buchsbaum, M., King, C. and Henkin,

R. I.: Average evoked response and psychological performance in patients with pseudohypoparathyroidism,J Neurol Neurosurg Psychiat, 35: 270-276, 1972.

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al.

3 Chartrian, G. E., Shaw, C. M. and Leffman,

H.: The significance of periodic lateralized epileptiform discharges in the EEG: An electrographic, clinical and pathological study, Electroenceph Clin Neurophysiol, 17: 177-193, 1964. 4 Echlin, F. A,, Arett, V. and all, J.: Paroxysmal high voltage discharges from isolated and partially isolated human and animal cerebral cortex, Electroenceph Clin Neurophysiol, 4: 147-164, 1952. 5 Erkulvawatr, S., Hines, K., Evans, C. and Rhinehart, W.: Events, evolution and prognosis of pseudoperiodic lateralized epileptiform discharges (PLEDs) , Electroenceph Clin Neurophysiol, 40: 3 13-3 14, 1976. 6 Fischer-Williams, M. : Burst-suppression

activity as an indication of undercut cortex, Electroenceph Clin Neurophysiol, 15: 723-724, 1963. 7 Flugel, K.A. and Druschky, K. F.: EEG

in hyperosmolar non-ketotic diabetic coma, Electroenceph Clin Neurophysiol, 41: 663, 1976. 8 Henry, C. E. and Scoville, W. B.: Suppres-

sion-burst activity from isolated cerebral cortex in man, Electroenceph Clin Neurophysiol, 4: 1-22, 1952. 9 Kiloh, L. G., McComas, A. J. and Osselton, J. W.: Clinical Electroencephalography 3rd Ed.: 147-148, 1972, Butterworths, London. 10 Markand, 0. N. and Daly, D. D.: Pseudoperiodic lateralized paroxysmal discharges in electroencephalogram, Neurology, 21: 975-981, 1971. 11 Markand, 0. N. and Panszi, J. G.: The

electroencephalogram in subacute sclerosing panencephalitis, Arch Neurol, 32: 719726, 1975. 12 Miyazaki, M.,Aki, M. and Ebe, M.: Re-

port of two cases with periodic sharp wave, Clin EEG, 4: 152-157, 1962 (in Japanese). 13 ODoherty, D. S. and Canary, J. F.: Neurologic aspects of endocrine disturbances, In: Baker, A. B. and Baker, L. H. (eds.) : Clinical Neurology, 3(43 1: 4-5, 1975, Harper & Row, N Y & London. 14 Ogura, M., Yuzawa, C., Miyashita, S., Saito, M., Matsuzawa, T. and Tanaka, T.: Two cases of dementia paralytica with periodic EEG complex, Clin EEG, 12: 184-1 89, 1970 (in Japanese). 15 Rose, G. A. and Vas, C. J.: Neurological complications and electroencephalographic changes in hypoparathyroidism, Acta Neu-

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rol Scandinav, 42: 537-550, 1966. 16 Sato, T., Kutsuzawa, T. and Ikeda, K.:

187-190, 1973. 18 Terao, A. and Araki, S.: Clinical applica-

Periodically recurring discharge (PRD) observed in two cases with cerebrovascular stroke, Clin EEG, 14: 609-613, 1972 (in Japanese). 17 Singh, B. M., Gupta, D. R. and Strobos, R. J. : Nonketotic hyperglycemia and epilepsia partialis continua, Arch Neurol, 29:

tion of somatosensory cerebral evoked response for the localization and the level diagnosis of neuronal lesions, Folia Psychiat Neurol Jap, 29: 341-354, 1975. 19 Yamell, P. R. and Chu, N.S.: Focal seizures and aminophylline, Neurology, 25: 819-822, 1975.