Article abstract
Seizure patterns and other clinical features were analyzed in 55 epileptic patients with electrographic evidence of exclusive or predominant occipital involvement. Few statistically significant differences in clinical or ictal patterns were found between subjects with purely focal occipital involvement and those with temporal and temporo-parietalspread or minor additional independent foci. On the other hand, cases with bilateral synchronous occipital spike activity appeared to reflect a different type of epileptic disorder. Clinical pleomorphism was more apparent than is commonly conceived; thus, although the incidence of visual auras was relatively high (47 percent), epigastric, psychic, somatic, and other sensory phenomena were not infrequently encountered. lctal motor patterns were most commonly (53 percent) nonfocal or absent, but partial or focal motor attacks and psychomotor seizures were amply represented. lctal features with their localizing and lateralizing reliability were also analyzed and discussed in relation to those found in a companion study of seizures of fronto-centro-parietal origin.
Clinical ictal patterns in epileptic patients with occipital electroencephalographic foci BARRY 1. LUDWIQ, M.D., and COSIMO AJMONE MARSAN, M.D.
his study is complementary to a similar one T carried out recently by Ajmone Marsan and Goldhammer' on a group of patients with electroencephalographic (EEG) evidence of frontal, central, and parietal epileptiform activity. In the present work, pertinent clinical, radiographic, and etiopathologic data and all possible ictal sensory and motor phenomena are correlated in patients with EEG discharges localized to or propagated from the occipital lobe. The purpose of this study is to gain a better understanding of the functional pathology of the involved region(s), while contributing to the diagnostic identification and correct localization of the underlying epileptogenic process.
Patient material, method, and generalities. Patients were selected from among recent referrals and from the From the Branch of Electroencephalographyand Clinical Neurophysiology, National Institute of Neurological Diseases and Stroke, Bethesda, Maryland. Received for puMication November 4, 1974. Dr. Ajmone Marsan's address is Building 10, Room 4N262, National Institutes of Health, Bethesda, MD 20014.
files of our EEG Laboratory on the basis of unequivocal evidence of epileptiform activity involving primarily the occipital regions. All cases with unilateral or bilateral occipital maximal involvement were included despite possible spread of paroxysmal activity to adjacent areas or evidence of additional minor independent epileptiform foci. Cases with paroxysmal abnormalities over more anterior regions, with only secondary involvement of occipital areas, were excluded. Fifty-nine cases fulfilling these criteria were ascertained, of which four had no history of a clinical seizure disorder (see Zivin and Ajmone Marsan2) and were discarded. The remaining 55 cases had definite clinical evidence of seizures and form the basis of this investigation. Electroencephalographic evaluation. Multiple EEGs (range 2 to 29) were obtained on the majority (86 percent) of our patients, with the follow-up period varying between several weeks and more than 15 years. Single examinations were done on only eight subjects. At least 21 electrodes, placed in accordance with the International 10-20 ~ y s t e m were , ~ used in both referential and bipolar linkages. Recording was done under varying conditions,
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including wakefulness, drowsiness, sleep, hyperventilation, and photic stimulation. In some patients, tracings were performed both while the patients were on and off anticonvulsant medications, and in a few, pentylenetetrazol (Metrazol@) activation was utilized. Because a significant number of our epileptic patients were referred for possible neurosurgical therapy, intracranial electrodes were implanted in four patients, and direct cortical recording was performed in 13 with electrographic monitoring of the occipital and neighboring regions prior to cortical resection (for methods, see Ajmone Marsan and Van Buren4 and Ajmone Marsan and O’Connors). In certain patients, discrete occipital epileptogenic foci were clearly established on the basis of interictal and/or ictal findings. In a greater number of cases, however, and especially in those with a large number of tracings obtained over a protracted period, maximal epileptiform activity tended to vary somewhat in extent and in exact localization. Therefore, each patient was originally categorized according to his most constant and prominent EEG feature, while taking into consideration the existence of possible additional o r secondary localizations. Since the total number of cases was relatively small, their subdivision into an excessive number of groups would have been impractical, if not statistically reprehensible. Therefore, for purposes of correlating different seizure types with the largest number of EEG patterns, as well as analyzing these varying patterns with respect to divergent etiopathologic factors, patients were subdivided into four main groups: Group 1 consisted of 18 patients with epileptiform discharges involving the occipital areas only, either unilaterally or bilaterally independent, generally with one side clearly predominating. Group 2 consisted of eight patients with bilateral, synchronous involvement of both occipital areas, excluding cases of rhythmic 2 ?hto 3 ?hper second spike and wave activity (formerly entitled “pyknolepsy” and generally considered to be of centrencephalic origin). It was unclear at the outset whether these cases, which consisted predominantly of synchronous sharp slow complexes at 1 to 2 per second or rapid spike and waves interspersed with polyspikes, could be ascribed to a focal epileptogenic lesion located occipitally in proximity to the midline, or whether these bilateral synchronous discharges were the expression of a somewhat atypical centrencephalic disorder. Therefore, these few cases are considered separately from group I. Group 3 consisted of 17 patients with paroxysmal activity maximal over the occipital area with either prominent spread to, or independent involvement of, the ipsilateral temporal region. Group 4 consisted of 12 patients with epileptiform activity over the occipital area and its contiguous temporal region, with involvement of the adjacent parietal region and/or other minor independent foci. Six patients from the preceding groups who, in addition to their focal abnormalities, showed diffuse spike and 464
NEUROLOGY May 1975
wave discharges in all or some of their records also have been considered under a separate fifth group (group 5). Clinicul evaluation. All germane historic data as well as information on physical, neurologic, radiographic, and laboratory examinations were gathered from each patient’s chart. Seizure descriptions were obviously of great importance, in spite of the unavoidably uneven extent, quality, and reliability of these descriptions. Details obtained from the patient and relatives were considered and compared to direct observations of spontaneous ictal episodes by nursing staff, physicians, and EEG technicians (these data were available in a majority of patients). Where discrepancies existed, only the accounts derived from the most experienced medical observers were taken into consideration. All types of ictal episodes experienced by each subject, as well as descriptions and associations of each type, were tabulated and related to EEG findings as corroborated, whenever possible, by neurologic signs and radiologic and pathologic data.
Results. Age. The median age at which the first seizure occurred in our patient population (excluding febrile seizures) was 9 years, with arange of 5 weeks to 6 1 years. The median age at the time patients were first seen in our EEG department was 17 years, with a range of I to 61 years. The mean and median ages of seizure onset by EEG grouping is as follows: Group
1. Occipital only 2. Occipital bilateral synchronous 3 . Occipital plus temporal 4. Occipital plus temporal and other 5. Occipital plus bilateral spike and wave
Mean age
Median age
24
16
12
11-15
10
8
9
7-8
9
3-5
The age of onset in the “occipital only” group is higher than in the other groups. Neurologic and radiologic findings. Neurologic examination was negative or without evidence of a clearly lateralized or localized cerebral lesion in 27 patients, while radiologic studies (including pneumoencephalography and cerebral angiography in a considerable number of patients) were uninformative in establishing a cerebral abnormality in 37 patients. The type and incidence of either neurologic or radiologic abnormalities bespeaking cerebral pathology are separated into the five EEG groups, as shown in table 1. Of interest is the relatively high incidence (66 percent) of mental retardation and absence of herniparesis or visual field deficit in the focal occipital and spike and wave group, as well as the absence of visual disorders in group 2, but none of these figures proved to be statistically significant. However, the relatively low incidence of
Table 1. Type and incidence of clinical (and radiographic) findings in the total patient population and in the various EEG groups (percentages in parentheses)
Table 2. Probable etiopathologic factors and their distribution in the total patient population and in the various EEG groups (percentages in parentheses)
mental retardation in group 1, in comparison with the overall series, was significant (p < 0.01). Etiopathology. The underlying process was unknown in 14 patients (25 percent). Probable causal factors in the remaining 41 patients are outlined in table 2 , where they are separated into the various EEG groups. The table
shows that the incidence of vascular processes tends to be higher (p < 0.05) in groups 1 and 3 , a finding that achieves greater statistical significance (p < 0.01) if the more focal occipital-only group 1 is compared with group 4. Neither vascular nor expanding lesions seem to be involved in group 2, in which the most likely pathogenetic
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Occipital seizures
Table 3. Seizure patterns: Incidence in total population and in the various EEG localization groups (percentages in parentheses)
Table 4. Seizure patterns; comparison of their incidence between EEG localization groups
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Table 3. (Cont.)
mechanism (38 percent) is metabolic (hypocalcemia, porphyria, and hypoglycemia). Photic stimulation. Intermittent photic stimulation was performed on 54 patients at frequencies varying from 1 to 25 f/sec. No effect on background activity was noted during this procedure in 14 cases ( 2 6 percent). A symmetrical cerebral response, maximal in the occipital regions, was observed in 18 patients (33 percent), whereas consistently asymmetrical responses were seen in 14 subjects (26 percent); these were distributed among all EEG groups with predominantly lateralized abnormalities. The photic “driving” in 13 of these patients was better developed over the occipital area least involved in the epileptogenic process (for experimental data, see Dimov and Lanoir6). A significant photic activation of interictal occipital discharges was noted in seven patients (13 percent), resulting in widespread propagation of the evoked paroxysmal activity and clinical seizure production in three. This activation did not appear to occur preferentially in any of the four EEG groups.
Seizure patterns. Aura. No sensory aura was present in 18 patients (33 percent); two other subjects were either too young or too retarded to report any subjective sensations. The remaining 35 patients experienced one or more of the following auras. 1. Somatosensory. Sensations involving limbs, face, or other body part unilaterally were reported by four patients
and described generally as “numbness” or “tingling.” 2 . General body sensations, described as coldness, warmth, and generalized numbness, were experienced by three patients. 3 . Specific sensory. This constituted the vast majority of sensations, occurring in 33 patients, as follows: visual in 26, vertiginous in five, and olfactory in three. 4. Visceral sensations, all of an epigastric nature, were reported by seven patients. 5. Psychic auras were experienced by eight subjects and consisted of visual hallucinations in four and illusions (including perseveration, depersonalization and dija vu) in four. 6 . Feelings of fright and anxiety were reported by two patients. A closer analysis of ictal visual symptoms (both simple and complex) disclosed the following data: The more common type of visual aberration, the simple visual aura, included reports of elementary sensations of light and color in simple or gross form. These descriptions were quite variable among patients with respect to color, morphology, position in space, and type of movement; however, in any one particular patient, only one or at the most two visual patterns predominated, remaining constant through the years as aprelude to a seizure with no change in their own inherent qualities. A panoply of colors were reported: green, red-orange, white, yellow, p u r p l e - b l a c k , s i l v e r , r e d , and polychromatic. Morphologies or contours perceived included: a line or NEUROLOGY May 1975
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Occipital seizures
streak, a square, flashing light, zigzag lines of light, a spot, stars, a circle, ball of lights, dust-like particles, spark, nonspecific design or pattern, and a disk with star-like projection. Movement of the image was present rather often and was described either as rotatory, horizontal, peripheral, random, or in a direction away from or toward the patient. Simple visual phenomena had lateralizing features at their onset in two-thirds of patients (see below). In the remaining one-third, images were diffuse or described as directly in front of the patient. Visual hallucinations consisted of nonlateralized formed objects, figures, or scenes generally of a familiar nature, although unfamil-iar or grotesque scenes also were reported. Illusions comprised diffuse distortions of the size or shape of objects or, in the case of one subject, the changing color of printed matter to a scarlet red or kelly green shade. Perseverations (palinopsia) included cases in which an object or scene was persistently perceived in a lateralized field of vision despite actual disappearance of that image from either visual field. In table 3 the relative frequency of various auras and their relationship to the EEG groups is presented. Simple visual a u r a s o c c u r r e d q u i t e c o m m o n l y in t h e occipital-only and occipital-plus-temporal groups, whereas they were totally absent from the group manifesting bilaterally synchronous occipital discharges, a statistically significant disparity (p < 0.01) (table 4). Olfactory auras were present in three cases, all without evidence of temporal involvement. Similarly, of the four cases with visual hallucinations, three were found in the occipital-only group, whereas the other case, as well as all four cases with illusions and perseverations, had EEG evidence of occipital and temporal involvement. The incidence of somatosensory, general body, and visceral sensations was, in general, rather low. Autornatisms. Automatic behavior, either as the sole seizure manifestation or in association with other ictal phenomena, was described in 16 patients (29 percent) with occipital epileptiform activity. Furthermore, the incidence of ictal automatisms was essentially the same in patients with discrete occipital foci (40 percent) as in those with both occipital and temporal involvement (41 percent) (table 3). No automatisms were present in the occipital bilateral synchronous group, nor in those with diffuse spike and wave activity. Types of automatic behavior displayed were: alimentary in eight, ambulatory in four, gestural in two, mimetic in two, and complex and organized activities in five, with some patients showing more than one type of automatism. Motorputterns. Of our 55 patients, five (9 percent) had no tonic or clonic motor phenomena in the course of their seizures, 24 (44 percent) had only generalized grand ma1 or generalized tonic seizures, and 27 (49 percent) had partial o r f o c a l m o t o r p h e n o m e n a ( e x c l u d i n g automatisms) with or without secondary generalization. These phenomena have been subdivided into three major types of motor patterns: clonic, tonic, and head and eye adversive movements, and their occurrence in the various groups of patients also is indicated in table 3 , together with the other seizure patterns.
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This table reveals that seizures characterized by primary generalization or absence of motor features (short lapses of consciousness) occur quite commonly in all groups; however, they attain their highest percentage (87.5 percent) in group 2. Furthermore, no case of adversive head and eye movements or tonic posturing, and only one case of unilateral clonic seizure activity, occurred in either group 2 or 5. However, the small number of cases, especially in these latter two groups, weakens the significance of these observations. Definite ictal nystagmus was described in five patients during spontaneous seizures directly observed either by neurologic consultants or by EEG technicians who had additional electrographic documentation of both the ictal activation and the nystagmoid movements. Lateralizing ,features in the ictul patterns. There were 37 cases in which the seizure patterns had consistent lateralizing features (10 patients with lateralized auras only, 17 with lateralized motor patterns, and 10 with both). An attempt was made to assess the lateralizing reliability of these various ictal phenomena. For this purpose the side of the epileptogenic process first was established independently on the basis of electrographic, clinical, radiographic, and pathologic criteria. Dominant unilateral features were exhibited by the EEG data in 49 patients (24 strictly unilateral, 25 with bilateral involvement but definite unilateral predominance), by clinical examination (exclusive of the seizure patterns) in 17, by x-ray in 12, and by pathologic data in eight. Cerebral lateralization was considered definite on the basis of a strictly unilateral EEG focus, in the absence of conflicting data from other criteria, or of a predominant EEG lateralization, if corroborated by at least one of the above-mentioned parameters. By this method, 30 patients with a reasonably definite lateralization of the occipital epileptogenic process, as well as lateralized motor and/or sensory ictd patterns, were ascertained. Motor activity was contralateral to, or adversive from, the cerebral focus in all but one case (in which head deviation was contraversive but tonic posturing of the upper extremity was ipsilateral to the epileptogenic lesion). Thus head and eye movement and clonic activity was a correct lateralizing sign in all cases. Auras were contralateral to the cerebral focus in the two cases in which the aura consisted of a somatosensory sensation and in all 13 cases of stationary or nonhorizontally moving visual images. In the three cases in which the visual image moved laterally, the occipital epileptogenic focus was ipsilateral to the side of origin of the image and contralateral to its terminus. Comparison with foci in other regions. In order to contrast the ictal motor and sensory patterns of occipital origin with those patterns arising from focal epileptiform discharges initiated in other areas of the brain, our data can be compared with statistics drawn from a similar studyTof frontal, fronto-central, central, centro-parietal, and fronto-central plus temporal foci (tables 3 and 4). Noteworthy is the much higher incidence (p < 0.01) of all types of focal motor phenomena, clonic, tonic, and adversive head movements, in the comparison group.
Partial seizures with complex symptomatology (automatisms) are relatively frequent in both groups, although their likelihood of occurrence is also higher with seizures of frontal or fronto-temporal origin than with those of occipital derivation (p < 0.05). Conversely the incidence of primary generalized (or “no motor”) seizures is considerably higher in the study group (p < 0.01). The regional propensity for varying aura types is also readily appreciated in table 3. That visual auras should have a statistically higher frequency (p < 0.01) in cases of occipital involvement is not unexpected; however, it should be appreciated that visual auras did occur in all categories of the comparison group except in those cases with frontal foci. Furthermore, the visual phenomena described by these patients did not qualitatively differ significantly from those reported by our group of patients.
Discussion. Paroxysmal electrographic abnormalities localized in the occipital region are commonly observed in children, especially those younger than age 3. Such cases, both with or without clinical evidence of a seizure disorder, have been investigated e x t e n s i ~ e l y ~and - ’ ~tend to show electrographic and clinical ictal resolution with advancing age (48 percent by age 9 in Gibbs, Gillen, and Gibbs9). The majority (95 percent) of the subjects in the present series had seizure onset after age 8 and were followed for at least 10 years after seizure onset or beyond age 20, and yet clinical and EEG abnormalities persisted. It is probable, therefore, that few if any of these cases exemplify the more benign ‘‘occipital epilepsy” of infancy and childhood. In adults or mixed age populations, epileptic seizures arising from the occipital region are not nearly so prevalent, accounting for 8 percent of focal seizures in a series of 11,612 epileptic patient^,^ and their varying clinical and electrographic concomitants have not been so exhaustively examined. Presentations of individual or small numbers of cases are available in the literature,’ 1-13 but detailed investigations of relatively large series of such patients are rare.l4,l5 Ajmone Marsan and R a l ~ t o n ’have ~ discussed the potentiality for multiple and complex seizure patterns arising from an occipital focus, due to the anatomic propinquity and thus probable easy spread of discharges from that lobe to both suprasylvian and infrasylvian structures. Employing Metrazol@to induce seizures in patients with proven occipital epileptogenic lesions, these authors demonstrated clinical and electrographic evidence of spread of epileptiform activity far anteriorly into the temporal regions, producing automatisms, psychic hallucinations, illusions, and auditory and vertiginous phenomena, and into the suprasylvian areas, with clinical signs of somatic sensory, somatic motor, or supplementary motor activation. These data have been further documented by Bancaud17 and Takeda, Bancaud, and Talairach,ls who, utilizing stereotactically placed intracerebral electrodes, demonstrated propagation of epileptiform activity from occipital foci to temporal or parietal lobes; the site of
origin generally was below the calcarine fissure with temporal spread and above the fissure yith parietal spread. These authors further reported that the initial features of ictal episodes originating in the occipital area would consist of tonic adversion of the head and eyes and clonic movements of the eyes and eyelids (see also GastautI9). Contralateral eye movement and/or eye closure also have been induced with unilateral occipital stimulation. Contraversive movements of the head and eyes were found in only 29 percent of our cases and documented ictal nystagmus occurred in only 9 percent, an incidence substantially lower than would be anticipated from the data reported above. The reason for this discrepancy is unclear; however, Penfield’s“ and Bancaud’sI7 studies were performed in a controlled environment with continuous observation of all pertinent neurologic parameters by experienced personnel, whereas few of our cases were able to be so circumspectly monitored. The high incidence of automatisms in our series (29 percent), especially those seen in cases with no electrographic evidence of concurrent interictal temporal involvement, is of interest. Automatisms of extratemporal origin (i . e . , frontal convexity, fronto-polar, orbital, and supplementary motor) are well-described; however, automatic actions associated with occipital epileptiform activity are fairly rare, accounting for less than 1 percent of clinical ictal types in the Gibbs’ ~ e r i e sSuch . ~ automatisms in our series were indistinguishable from those that are part of typical psychomotor attacks except for the fact that they were preceded by visual auras in 13 of the 15 patients (87 percent) capable of expressing their subjective visual experiences. Presumably, deep temporal structures are activated in the course of an occipitally initiated psychomotor seizure, as demonstrated also by BancaudI7 and Takeda and associates.’* Subjective sensory experiences presaging overt signs of ictal activity were multiple and varied in our series, the most common being a simple visual aura (47 percent). The incidence of this type of aura in seizures of occipital origin varies markedly in different studies, reflecting the method by which patients are selected (i.e., on the basis of EEG alone or of both clinical and EEG criteria). Thus, in the series of Penfield and Kristiansen,20259 patients were evaluated, in 11 of whom (each with an occipital seizure focus) visual sensations constituted the initial symptom. On the other hand, visual auras totaled only 10 percent in the Gibbs’ s e r i e ~It. ~should not be construed, however, that visual auras, albeit commonly encountered with occipital lesions, are pathognomonic of primary occipital disease, for - as is shown in table 3 - visual auras are occasionally experienced by patients with central or parietal epileptiform lesions without neurologic or interictal electrographic evidence of more posterior involvement, and can be qualitatively indistinguishable from the visual phenomena initiated occipitally. Descriptions of the simple visual sensations occurring spontaneously in our cases (as well as in those of fronto-centro-parietal origin) were, in general, in accord NEUROLOGY May 1975
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with those elicited by Penfield and Rasmussen” with electrical stimulation of the occipital cortex. Unformed, simple photopsias or phosphenes were not the only visual concomitants of occipital activation, for more complex psychic phenomena also occurred, occasionally even in those cases with no obvious EEG evidence of temporal epileptiform involvement. These comprised visual hallucinations and illusions, including palinopsia. The latter is a rather rare type of visual after-image or perseveration occasionally reported in epileptic patients and occumng usually in a defective, although not amaurotic, field of vision; the etiologic lesion frequently lies in the right occipital parietal area.24 Othertypes of auras may accompany occipital seizures, either by themselves or following an initial visual sensation; those most commonly noted in our series were of the epigastric type, with a few instances of somatosensory and olfactory phenomena. This, again, presumably is indicative of the potentially extensive anterior spread of paroxysmal activity. One of the objectives of this study was to relate clinical ictal patterns (and other neurologic findings) to electrographic data. This was not totally accomplished, in part because of the relatively small number of cases with similar combinations of EEG topographic localizations, thus not lending themselves to facile characterization and classification. The fact remains, however, that scalp electroencephalography is not an absolutely reliable method for precisely localizing an epileptogenic process. Furthermore, even when the investigation is carried out by means of implanted electrodes or direct cortical recording, these processes seldom appear solitary or circumscribed, so that any attempt at categorization becomes somewhat specious. In fact, few statistical differences were found among groups 1 , 3 , and 4 with respect to the clinical data. On the other hand (see table 4) the bilateral synchronous occipital group appeared to be clearly distinct from the others in that none of its patients had a clinically detectable disturbance of visual function or visual aura. This group possessed the lowest incidence of auras in general, the highest percentage of nonfocal seizures (primarily generalized or “no motor”), and the highest incidence of metabolic abnormalities acting as probable causative epileptogenic agents. These data are more easily explained by imputing a subcortical or a diffuse (i.e., metabolic) process than by implicating a single mesial or bilateral cortical epileptogenic lesions (see also Marcus and Watsonz5).However, the reason for the preferential occipital expression of such hypothetical processes remains unexplained. This study, along with that of Ajmone Marsan and Goldhammer, has further attempted to delineate certain features that statistically differentiate seizures of an occipital origin from those of fronto-centro-parietal derivation (see table 4). These include the much greater incidence of visual auras and primary generalized seizures in the occipital group (even with group 2 excluded), and the greater frequency in the fronto-centro-parietal group of somatosensory, cephalic and general body auras, as well as all types of partial seizures with elementary ,22723
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syniptomatology (i.e., clonic movements, tonic postures, and contraversive turning of head and eyes). Lateralization of a presumptively localized epileptogenic focus, on the basis of unilateral ictal correlates, appears to be more reliable in the occipital series than with the latter series of cases. In the occipital group, head and eye deviation and clonic movements were contralateral to the involved region in all cases, and tonic posturing was a falsely localizing sign on only one occasion. T h i s stands i n contrast to the fronto-centro-parietal group, in which tonic phenomena and especially head and eye contraversion had been proven to be of substantially less Iateralizing value. Furthermore, i n the occipital group, stationary or nonhorizontally moving visual sensations were 100 percent accurate in lateralizing the responsible focus. In no case was ipsilateral localization found, although this has been described during cortical stimulation.2’ Of some interest were the three cases in which the visual phenomena moved laterally from one field to another (or from one eye to another), for in these cases the occipital focus was ipsilateral to the side of image origin and contralateral to its side of termination. Penfield and Rasmussenzl observed similar ipsilateral to contralateral movement of visual images following occipital cortical stimulation in two patients (Cases KW and KH); and several other of these authors’ subjects described visually perceived movement toward the contralateral side, usually from the midline, lending further credence to the hypothesis that moving visual auras are no: falsely localizing, but rather their incipient location is not so useful in lateralizing the side of cerebral involvement as is their direction of movement. Finally, despite the attempt to define clinical aids for localizing and/or lateralizing occipital epilepsy, it should be further emphasized that seizures of occipital lobe origin constitute more than mere “visual fits.” Rather they represent a pleomorphic process that, either through capriciousness or an inherent program, may spread to any one of a number of cortical or subcortical structures, with the potential to engender any one of a large combination of sensory or motor patterns simulating ictal events initiated elsewhere. Acknowledgments The authors wish to thank Dr. J. M. Van Buren, Chief of the Surgical Neurology Branch, National Institute of Neurological Diseases and Stroke, for permittingthe use of his patient files. They also gratefully acknowledge the assistance of Mrs. Doris Sadowsky, Office of Biometry,NationalInstitute of Neurological Diseases and Stroke, in the statistical analysis of the data. REFERENCES 1 . Ajmone Marsan C, Goldhammer L: Clinical ictal patterns and electrographic data in cases of partial seizuresof fronto-central-parietal origin. In Brazier MAB (Editor): Epilepsy:Its Phenomena in Man. New York, Academic Press, 1973, pp 236-260 2.Zivin L, Ajmone Marsan C: Incidence and prognostic significance of epileptiform activity in the EEG of nonepileptic subjects. Brain 91:751-778, 1968 3. Jasper H: The ten-twenty electrode system of the International Federation. Electroencephalogr Clin Neurophysiol 10:371-375, 1958 4. Ajmone Marsan C, Van Buren JM: Epileptiform activity in cortical and subcorticalstructures in the temporal lobe of man. In Baldwin M, Bailey
P (Editors): Temporal Lobe Epilepsy. Springfield, IL, Charles C Thomas, Publisher, 1958, pp 78-108 5.Ajmone Marsan C, OConnor M: Electrocorticography. In Remond A (Editor): Direct, Cortical and Depth Evaluation of the Brain. Handbookof Electroencephalography and Clinical Neurophysiology. Amsterdam, Elsevier Publishing Company, 1973. vol 10, pp 1-46 6. Dimov S, Lanoir J: Effets des lesions epileptogenes chroniques occipitales (cobalt alumine), chez le Papio paplo. Rev Neurol (Paris) 120:480-481, 1969 7. Gibbs FA, Gibbs EL: Atlas of Electroencephalography. Volume 2:Epilepsy. Cambridge, MA, Addison-Wesley Press, 1952,pp 222-224 8. Gibbs FA, Gibbs EL: Changes in epileptic foci with age. ElectroencephalogrClin Neurophysiol, Suppl 4,233, 1953 9. Gibbs EL, Gillen HW. Gibbs FA: Disappearance and migration of epileptic foci in childhood. Am J Dis Child 88596-603, 1954 10. Smith JMB, Kellaway P: The natural history and clinical correlates of occipital foci in children. In Kellaway P, Petersen I (Editors): Neurological and Electroencephalographic Correlative Studies in Infancy. New York, Grune & Stratton, Inc., 1964, pp 230-249 11. Penfield W, Jasper H: Epilepsy and the Functional Anatomy of the Human Brain. Boston, Little, Brown and Company, 1954. pp 116-126 12. Paillas JE, Vigouroux R, Darcourt G, et al: Considdrationssur I'dpilepsie occipitale: (A propos de 12 observations de ldsions occipitales operdes). Neurochirurgie 5:3-16, 1959 13. Huott AD, Madison DS, Niedermeyer E: Occipital lobe epilepsy: A clinical and electroencephalographic study. Eur Neurol 11 :325-339, 1974 14. Russel WR, Whkty CWM: Studies in traumatic epilepsy: 3. Visual fits. J Neurol Psychiatry 18:79-96, 1955
15.Marques Assis L, LivramentoJA, Cury M: Estudio clinico de 68casosde epilepsia occipital. Arch Neurol Psiquiat (S Paulo) 29:49-54, 1971 16. Ajmone Marsan C, Ralston B: The Epileptic Seizure: Its Functional Morphology and Diagnostic Significance. Springfidd, IL, Charles C Thomas, Publisher, 1957, pp 21 1-215 17. Bancaud J: Les crises dpileptiques d'origine occipitale (dtude st6rdo-dlectroencdphalographique). Rev Oto-Neuro-Ophthalmol 41 :299-311, 1969 18. Takeda A, Bancaud J, Talairach J: Concerning epileptic attacks of occipital origin. Electroencephalogr Clin Neurophysiol 28:647-648, 1970 19. Gastaut H: Un aspect mdconnu des ddcharges neuroniques occipitales: La crise oculo-clonique ou "nystagmus dpileptique," In Alajouanine PT (Editor): Activities of the Occipital Lobe. Paris, Masson, 1960, pp 169-185 20. Penfield W, Kristiansen K: Epileptic Seizure Patterns. Springfield, IL, Charles C Thomas, Publisher, 1951, pp 46-47 21. PenfieldW, RasmussenT: The Cerebral Cortexof Man:AClinical Study of Localizationof Function. New York, The Macmillan Company, 1950, pp 135-147 22. Critchley M: Types of visual perseveration: "Palinopsia" and "lllusoly Visual Spread." Brain 74:267-299, 1951 23. Bender MB: Neuro-ophthalmology. In Baker AB, Baker LH (Editors): Clinical Neurology. Volume I. Hagerstown, Harper & Row, Publishers, 1974, pp 38-39 24. Bender MB, Feldman M, Sobin AJ: Palinopsia. Brain 91:321, 1968 25. Marcus EM, Watson CW: Symmetrical epileptogenic foci in monkey cerebral cortex: Mechanisms of interaction and regional variations in capacity for synchronous discharge. Arch Neurol 19:99-116, 1968
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Clinical ictal patterns in epileptic patients with occipital electroencephalographic foci BARRY I. LUDWIG and COSIMO AJMONE MARSAN Neurology 1975;25;463 DOI 10.1212/WNL.25.5.463 This information is current as of May 1, 1975 Updated Information & Services
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Neurology ® is the official journal of the American Academy of Neurology. Published continuously since 1951, it is now a weekly with 48 issues per year. Copyright © 1975 by the American Academy of Neurology. All rights reserved. Print ISSN: 0028-3878. Online ISSN: 1526-632X.
Seizure patterns and other clinical features were analyzed in 55 epileptic patients with electrographic evidence of exclusive or predominant occipital involvement. Few statistically significant differences in clinical or ictal patterns were found between subjects with purely focal occipital involvement and those with temporal and temporo-parietalspread or minor additional independent foci. On the other hand, cases with bilateral synchronous occipital spike activity appeared to reflect a different type of epileptic disorder. Clinical pleomorphism was more apparent than is commonly conceived; thus, although the incidence of visual auras was relatively high (47 percent), epigastric, psychic, somatic, and other sensory phenomena were not infrequently encountered. lctal motor patterns were most commonly (53 percent) nonfocal or absent, but partial or focal motor attacks and psychomotor seizures were amply represented. lctal features with their localizing and lateralizing reliability were also analyzed and discussed in relation to those found in a companion study of seizures of fronto-centro-parietal origin.
Clinical ictal patterns in epileptic patients with occipital electroencephalographic foci BARRY 1. LUDWIQ, M.D., and COSIMO AJMONE MARSAN, M.D.
his study is complementary to a similar one T carried out recently by Ajmone Marsan and Goldhammer' on a group of patients with electroencephalographic (EEG) evidence of frontal, central, and parietal epileptiform activity. In the present work, pertinent clinical, radiographic, and etiopathologic data and all possible ictal sensory and motor phenomena are correlated in patients with EEG discharges localized to or propagated from the occipital lobe. The purpose of this study is to gain a better understanding of the functional pathology of the involved region(s), while contributing to the diagnostic identification and correct localization of the underlying epileptogenic process.
Patient material, method, and generalities. Patients were selected from among recent referrals and from the From the Branch of Electroencephalographyand Clinical Neurophysiology, National Institute of Neurological Diseases and Stroke, Bethesda, Maryland. Received for puMication November 4, 1974. Dr. Ajmone Marsan's address is Building 10, Room 4N262, National Institutes of Health, Bethesda, MD 20014.
files of our EEG Laboratory on the basis of unequivocal evidence of epileptiform activity involving primarily the occipital regions. All cases with unilateral or bilateral occipital maximal involvement were included despite possible spread of paroxysmal activity to adjacent areas or evidence of additional minor independent epileptiform foci. Cases with paroxysmal abnormalities over more anterior regions, with only secondary involvement of occipital areas, were excluded. Fifty-nine cases fulfilling these criteria were ascertained, of which four had no history of a clinical seizure disorder (see Zivin and Ajmone Marsan2) and were discarded. The remaining 55 cases had definite clinical evidence of seizures and form the basis of this investigation. Electroencephalographic evaluation. Multiple EEGs (range 2 to 29) were obtained on the majority (86 percent) of our patients, with the follow-up period varying between several weeks and more than 15 years. Single examinations were done on only eight subjects. At least 21 electrodes, placed in accordance with the International 10-20 ~ y s t e m were , ~ used in both referential and bipolar linkages. Recording was done under varying conditions,
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Occipital seizures
including wakefulness, drowsiness, sleep, hyperventilation, and photic stimulation. In some patients, tracings were performed both while the patients were on and off anticonvulsant medications, and in a few, pentylenetetrazol (Metrazol@) activation was utilized. Because a significant number of our epileptic patients were referred for possible neurosurgical therapy, intracranial electrodes were implanted in four patients, and direct cortical recording was performed in 13 with electrographic monitoring of the occipital and neighboring regions prior to cortical resection (for methods, see Ajmone Marsan and Van Buren4 and Ajmone Marsan and O’Connors). In certain patients, discrete occipital epileptogenic foci were clearly established on the basis of interictal and/or ictal findings. In a greater number of cases, however, and especially in those with a large number of tracings obtained over a protracted period, maximal epileptiform activity tended to vary somewhat in extent and in exact localization. Therefore, each patient was originally categorized according to his most constant and prominent EEG feature, while taking into consideration the existence of possible additional o r secondary localizations. Since the total number of cases was relatively small, their subdivision into an excessive number of groups would have been impractical, if not statistically reprehensible. Therefore, for purposes of correlating different seizure types with the largest number of EEG patterns, as well as analyzing these varying patterns with respect to divergent etiopathologic factors, patients were subdivided into four main groups: Group 1 consisted of 18 patients with epileptiform discharges involving the occipital areas only, either unilaterally or bilaterally independent, generally with one side clearly predominating. Group 2 consisted of eight patients with bilateral, synchronous involvement of both occipital areas, excluding cases of rhythmic 2 ?hto 3 ?hper second spike and wave activity (formerly entitled “pyknolepsy” and generally considered to be of centrencephalic origin). It was unclear at the outset whether these cases, which consisted predominantly of synchronous sharp slow complexes at 1 to 2 per second or rapid spike and waves interspersed with polyspikes, could be ascribed to a focal epileptogenic lesion located occipitally in proximity to the midline, or whether these bilateral synchronous discharges were the expression of a somewhat atypical centrencephalic disorder. Therefore, these few cases are considered separately from group I. Group 3 consisted of 17 patients with paroxysmal activity maximal over the occipital area with either prominent spread to, or independent involvement of, the ipsilateral temporal region. Group 4 consisted of 12 patients with epileptiform activity over the occipital area and its contiguous temporal region, with involvement of the adjacent parietal region and/or other minor independent foci. Six patients from the preceding groups who, in addition to their focal abnormalities, showed diffuse spike and 464
NEUROLOGY May 1975
wave discharges in all or some of their records also have been considered under a separate fifth group (group 5). Clinicul evaluation. All germane historic data as well as information on physical, neurologic, radiographic, and laboratory examinations were gathered from each patient’s chart. Seizure descriptions were obviously of great importance, in spite of the unavoidably uneven extent, quality, and reliability of these descriptions. Details obtained from the patient and relatives were considered and compared to direct observations of spontaneous ictal episodes by nursing staff, physicians, and EEG technicians (these data were available in a majority of patients). Where discrepancies existed, only the accounts derived from the most experienced medical observers were taken into consideration. All types of ictal episodes experienced by each subject, as well as descriptions and associations of each type, were tabulated and related to EEG findings as corroborated, whenever possible, by neurologic signs and radiologic and pathologic data.
Results. Age. The median age at which the first seizure occurred in our patient population (excluding febrile seizures) was 9 years, with arange of 5 weeks to 6 1 years. The median age at the time patients were first seen in our EEG department was 17 years, with a range of I to 61 years. The mean and median ages of seizure onset by EEG grouping is as follows: Group
1. Occipital only 2. Occipital bilateral synchronous 3 . Occipital plus temporal 4. Occipital plus temporal and other 5. Occipital plus bilateral spike and wave
Mean age
Median age
24
16
12
11-15
10
8
9
7-8
9
3-5
The age of onset in the “occipital only” group is higher than in the other groups. Neurologic and radiologic findings. Neurologic examination was negative or without evidence of a clearly lateralized or localized cerebral lesion in 27 patients, while radiologic studies (including pneumoencephalography and cerebral angiography in a considerable number of patients) were uninformative in establishing a cerebral abnormality in 37 patients. The type and incidence of either neurologic or radiologic abnormalities bespeaking cerebral pathology are separated into the five EEG groups, as shown in table 1. Of interest is the relatively high incidence (66 percent) of mental retardation and absence of herniparesis or visual field deficit in the focal occipital and spike and wave group, as well as the absence of visual disorders in group 2, but none of these figures proved to be statistically significant. However, the relatively low incidence of
Table 1. Type and incidence of clinical (and radiographic) findings in the total patient population and in the various EEG groups (percentages in parentheses)
Table 2. Probable etiopathologic factors and their distribution in the total patient population and in the various EEG groups (percentages in parentheses)
mental retardation in group 1, in comparison with the overall series, was significant (p < 0.01). Etiopathology. The underlying process was unknown in 14 patients (25 percent). Probable causal factors in the remaining 41 patients are outlined in table 2 , where they are separated into the various EEG groups. The table
shows that the incidence of vascular processes tends to be higher (p < 0.05) in groups 1 and 3 , a finding that achieves greater statistical significance (p < 0.01) if the more focal occipital-only group 1 is compared with group 4. Neither vascular nor expanding lesions seem to be involved in group 2, in which the most likely pathogenetic
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465
Occipital seizures
Table 3. Seizure patterns: Incidence in total population and in the various EEG localization groups (percentages in parentheses)
Table 4. Seizure patterns; comparison of their incidence between EEG localization groups
466
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Table 3. (Cont.)
mechanism (38 percent) is metabolic (hypocalcemia, porphyria, and hypoglycemia). Photic stimulation. Intermittent photic stimulation was performed on 54 patients at frequencies varying from 1 to 25 f/sec. No effect on background activity was noted during this procedure in 14 cases ( 2 6 percent). A symmetrical cerebral response, maximal in the occipital regions, was observed in 18 patients (33 percent), whereas consistently asymmetrical responses were seen in 14 subjects (26 percent); these were distributed among all EEG groups with predominantly lateralized abnormalities. The photic “driving” in 13 of these patients was better developed over the occipital area least involved in the epileptogenic process (for experimental data, see Dimov and Lanoir6). A significant photic activation of interictal occipital discharges was noted in seven patients (13 percent), resulting in widespread propagation of the evoked paroxysmal activity and clinical seizure production in three. This activation did not appear to occur preferentially in any of the four EEG groups.
Seizure patterns. Aura. No sensory aura was present in 18 patients (33 percent); two other subjects were either too young or too retarded to report any subjective sensations. The remaining 35 patients experienced one or more of the following auras. 1. Somatosensory. Sensations involving limbs, face, or other body part unilaterally were reported by four patients
and described generally as “numbness” or “tingling.” 2 . General body sensations, described as coldness, warmth, and generalized numbness, were experienced by three patients. 3 . Specific sensory. This constituted the vast majority of sensations, occurring in 33 patients, as follows: visual in 26, vertiginous in five, and olfactory in three. 4. Visceral sensations, all of an epigastric nature, were reported by seven patients. 5. Psychic auras were experienced by eight subjects and consisted of visual hallucinations in four and illusions (including perseveration, depersonalization and dija vu) in four. 6 . Feelings of fright and anxiety were reported by two patients. A closer analysis of ictal visual symptoms (both simple and complex) disclosed the following data: The more common type of visual aberration, the simple visual aura, included reports of elementary sensations of light and color in simple or gross form. These descriptions were quite variable among patients with respect to color, morphology, position in space, and type of movement; however, in any one particular patient, only one or at the most two visual patterns predominated, remaining constant through the years as aprelude to a seizure with no change in their own inherent qualities. A panoply of colors were reported: green, red-orange, white, yellow, p u r p l e - b l a c k , s i l v e r , r e d , and polychromatic. Morphologies or contours perceived included: a line or NEUROLOGY May 1975
467
Occipital seizures
streak, a square, flashing light, zigzag lines of light, a spot, stars, a circle, ball of lights, dust-like particles, spark, nonspecific design or pattern, and a disk with star-like projection. Movement of the image was present rather often and was described either as rotatory, horizontal, peripheral, random, or in a direction away from or toward the patient. Simple visual phenomena had lateralizing features at their onset in two-thirds of patients (see below). In the remaining one-third, images were diffuse or described as directly in front of the patient. Visual hallucinations consisted of nonlateralized formed objects, figures, or scenes generally of a familiar nature, although unfamil-iar or grotesque scenes also were reported. Illusions comprised diffuse distortions of the size or shape of objects or, in the case of one subject, the changing color of printed matter to a scarlet red or kelly green shade. Perseverations (palinopsia) included cases in which an object or scene was persistently perceived in a lateralized field of vision despite actual disappearance of that image from either visual field. In table 3 the relative frequency of various auras and their relationship to the EEG groups is presented. Simple visual a u r a s o c c u r r e d q u i t e c o m m o n l y in t h e occipital-only and occipital-plus-temporal groups, whereas they were totally absent from the group manifesting bilaterally synchronous occipital discharges, a statistically significant disparity (p < 0.01) (table 4). Olfactory auras were present in three cases, all without evidence of temporal involvement. Similarly, of the four cases with visual hallucinations, three were found in the occipital-only group, whereas the other case, as well as all four cases with illusions and perseverations, had EEG evidence of occipital and temporal involvement. The incidence of somatosensory, general body, and visceral sensations was, in general, rather low. Autornatisms. Automatic behavior, either as the sole seizure manifestation or in association with other ictal phenomena, was described in 16 patients (29 percent) with occipital epileptiform activity. Furthermore, the incidence of ictal automatisms was essentially the same in patients with discrete occipital foci (40 percent) as in those with both occipital and temporal involvement (41 percent) (table 3). No automatisms were present in the occipital bilateral synchronous group, nor in those with diffuse spike and wave activity. Types of automatic behavior displayed were: alimentary in eight, ambulatory in four, gestural in two, mimetic in two, and complex and organized activities in five, with some patients showing more than one type of automatism. Motorputterns. Of our 55 patients, five (9 percent) had no tonic or clonic motor phenomena in the course of their seizures, 24 (44 percent) had only generalized grand ma1 or generalized tonic seizures, and 27 (49 percent) had partial o r f o c a l m o t o r p h e n o m e n a ( e x c l u d i n g automatisms) with or without secondary generalization. These phenomena have been subdivided into three major types of motor patterns: clonic, tonic, and head and eye adversive movements, and their occurrence in the various groups of patients also is indicated in table 3 , together with the other seizure patterns.
468
NEUROLOGY May 1975
This table reveals that seizures characterized by primary generalization or absence of motor features (short lapses of consciousness) occur quite commonly in all groups; however, they attain their highest percentage (87.5 percent) in group 2. Furthermore, no case of adversive head and eye movements or tonic posturing, and only one case of unilateral clonic seizure activity, occurred in either group 2 or 5. However, the small number of cases, especially in these latter two groups, weakens the significance of these observations. Definite ictal nystagmus was described in five patients during spontaneous seizures directly observed either by neurologic consultants or by EEG technicians who had additional electrographic documentation of both the ictal activation and the nystagmoid movements. Lateralizing ,features in the ictul patterns. There were 37 cases in which the seizure patterns had consistent lateralizing features (10 patients with lateralized auras only, 17 with lateralized motor patterns, and 10 with both). An attempt was made to assess the lateralizing reliability of these various ictal phenomena. For this purpose the side of the epileptogenic process first was established independently on the basis of electrographic, clinical, radiographic, and pathologic criteria. Dominant unilateral features were exhibited by the EEG data in 49 patients (24 strictly unilateral, 25 with bilateral involvement but definite unilateral predominance), by clinical examination (exclusive of the seizure patterns) in 17, by x-ray in 12, and by pathologic data in eight. Cerebral lateralization was considered definite on the basis of a strictly unilateral EEG focus, in the absence of conflicting data from other criteria, or of a predominant EEG lateralization, if corroborated by at least one of the above-mentioned parameters. By this method, 30 patients with a reasonably definite lateralization of the occipital epileptogenic process, as well as lateralized motor and/or sensory ictd patterns, were ascertained. Motor activity was contralateral to, or adversive from, the cerebral focus in all but one case (in which head deviation was contraversive but tonic posturing of the upper extremity was ipsilateral to the epileptogenic lesion). Thus head and eye movement and clonic activity was a correct lateralizing sign in all cases. Auras were contralateral to the cerebral focus in the two cases in which the aura consisted of a somatosensory sensation and in all 13 cases of stationary or nonhorizontally moving visual images. In the three cases in which the visual image moved laterally, the occipital epileptogenic focus was ipsilateral to the side of origin of the image and contralateral to its terminus. Comparison with foci in other regions. In order to contrast the ictal motor and sensory patterns of occipital origin with those patterns arising from focal epileptiform discharges initiated in other areas of the brain, our data can be compared with statistics drawn from a similar studyTof frontal, fronto-central, central, centro-parietal, and fronto-central plus temporal foci (tables 3 and 4). Noteworthy is the much higher incidence (p < 0.01) of all types of focal motor phenomena, clonic, tonic, and adversive head movements, in the comparison group.
Partial seizures with complex symptomatology (automatisms) are relatively frequent in both groups, although their likelihood of occurrence is also higher with seizures of frontal or fronto-temporal origin than with those of occipital derivation (p < 0.05). Conversely the incidence of primary generalized (or “no motor”) seizures is considerably higher in the study group (p < 0.01). The regional propensity for varying aura types is also readily appreciated in table 3. That visual auras should have a statistically higher frequency (p < 0.01) in cases of occipital involvement is not unexpected; however, it should be appreciated that visual auras did occur in all categories of the comparison group except in those cases with frontal foci. Furthermore, the visual phenomena described by these patients did not qualitatively differ significantly from those reported by our group of patients.
Discussion. Paroxysmal electrographic abnormalities localized in the occipital region are commonly observed in children, especially those younger than age 3. Such cases, both with or without clinical evidence of a seizure disorder, have been investigated e x t e n s i ~ e l y ~and - ’ ~tend to show electrographic and clinical ictal resolution with advancing age (48 percent by age 9 in Gibbs, Gillen, and Gibbs9). The majority (95 percent) of the subjects in the present series had seizure onset after age 8 and were followed for at least 10 years after seizure onset or beyond age 20, and yet clinical and EEG abnormalities persisted. It is probable, therefore, that few if any of these cases exemplify the more benign ‘‘occipital epilepsy” of infancy and childhood. In adults or mixed age populations, epileptic seizures arising from the occipital region are not nearly so prevalent, accounting for 8 percent of focal seizures in a series of 11,612 epileptic patient^,^ and their varying clinical and electrographic concomitants have not been so exhaustively examined. Presentations of individual or small numbers of cases are available in the literature,’ 1-13 but detailed investigations of relatively large series of such patients are rare.l4,l5 Ajmone Marsan and R a l ~ t o n ’have ~ discussed the potentiality for multiple and complex seizure patterns arising from an occipital focus, due to the anatomic propinquity and thus probable easy spread of discharges from that lobe to both suprasylvian and infrasylvian structures. Employing Metrazol@to induce seizures in patients with proven occipital epileptogenic lesions, these authors demonstrated clinical and electrographic evidence of spread of epileptiform activity far anteriorly into the temporal regions, producing automatisms, psychic hallucinations, illusions, and auditory and vertiginous phenomena, and into the suprasylvian areas, with clinical signs of somatic sensory, somatic motor, or supplementary motor activation. These data have been further documented by Bancaud17 and Takeda, Bancaud, and Talairach,ls who, utilizing stereotactically placed intracerebral electrodes, demonstrated propagation of epileptiform activity from occipital foci to temporal or parietal lobes; the site of
origin generally was below the calcarine fissure with temporal spread and above the fissure yith parietal spread. These authors further reported that the initial features of ictal episodes originating in the occipital area would consist of tonic adversion of the head and eyes and clonic movements of the eyes and eyelids (see also GastautI9). Contralateral eye movement and/or eye closure also have been induced with unilateral occipital stimulation. Contraversive movements of the head and eyes were found in only 29 percent of our cases and documented ictal nystagmus occurred in only 9 percent, an incidence substantially lower than would be anticipated from the data reported above. The reason for this discrepancy is unclear; however, Penfield’s“ and Bancaud’sI7 studies were performed in a controlled environment with continuous observation of all pertinent neurologic parameters by experienced personnel, whereas few of our cases were able to be so circumspectly monitored. The high incidence of automatisms in our series (29 percent), especially those seen in cases with no electrographic evidence of concurrent interictal temporal involvement, is of interest. Automatisms of extratemporal origin (i . e . , frontal convexity, fronto-polar, orbital, and supplementary motor) are well-described; however, automatic actions associated with occipital epileptiform activity are fairly rare, accounting for less than 1 percent of clinical ictal types in the Gibbs’ ~ e r i e sSuch . ~ automatisms in our series were indistinguishable from those that are part of typical psychomotor attacks except for the fact that they were preceded by visual auras in 13 of the 15 patients (87 percent) capable of expressing their subjective visual experiences. Presumably, deep temporal structures are activated in the course of an occipitally initiated psychomotor seizure, as demonstrated also by BancaudI7 and Takeda and associates.’* Subjective sensory experiences presaging overt signs of ictal activity were multiple and varied in our series, the most common being a simple visual aura (47 percent). The incidence of this type of aura in seizures of occipital origin varies markedly in different studies, reflecting the method by which patients are selected (i.e., on the basis of EEG alone or of both clinical and EEG criteria). Thus, in the series of Penfield and Kristiansen,20259 patients were evaluated, in 11 of whom (each with an occipital seizure focus) visual sensations constituted the initial symptom. On the other hand, visual auras totaled only 10 percent in the Gibbs’ s e r i e ~It. ~should not be construed, however, that visual auras, albeit commonly encountered with occipital lesions, are pathognomonic of primary occipital disease, for - as is shown in table 3 - visual auras are occasionally experienced by patients with central or parietal epileptiform lesions without neurologic or interictal electrographic evidence of more posterior involvement, and can be qualitatively indistinguishable from the visual phenomena initiated occipitally. Descriptions of the simple visual sensations occurring spontaneously in our cases (as well as in those of fronto-centro-parietal origin) were, in general, in accord NEUROLOGY May 1975
469
Occipital seizures
with those elicited by Penfield and Rasmussen” with electrical stimulation of the occipital cortex. Unformed, simple photopsias or phosphenes were not the only visual concomitants of occipital activation, for more complex psychic phenomena also occurred, occasionally even in those cases with no obvious EEG evidence of temporal epileptiform involvement. These comprised visual hallucinations and illusions, including palinopsia. The latter is a rather rare type of visual after-image or perseveration occasionally reported in epileptic patients and occumng usually in a defective, although not amaurotic, field of vision; the etiologic lesion frequently lies in the right occipital parietal area.24 Othertypes of auras may accompany occipital seizures, either by themselves or following an initial visual sensation; those most commonly noted in our series were of the epigastric type, with a few instances of somatosensory and olfactory phenomena. This, again, presumably is indicative of the potentially extensive anterior spread of paroxysmal activity. One of the objectives of this study was to relate clinical ictal patterns (and other neurologic findings) to electrographic data. This was not totally accomplished, in part because of the relatively small number of cases with similar combinations of EEG topographic localizations, thus not lending themselves to facile characterization and classification. The fact remains, however, that scalp electroencephalography is not an absolutely reliable method for precisely localizing an epileptogenic process. Furthermore, even when the investigation is carried out by means of implanted electrodes or direct cortical recording, these processes seldom appear solitary or circumscribed, so that any attempt at categorization becomes somewhat specious. In fact, few statistical differences were found among groups 1 , 3 , and 4 with respect to the clinical data. On the other hand (see table 4) the bilateral synchronous occipital group appeared to be clearly distinct from the others in that none of its patients had a clinically detectable disturbance of visual function or visual aura. This group possessed the lowest incidence of auras in general, the highest percentage of nonfocal seizures (primarily generalized or “no motor”), and the highest incidence of metabolic abnormalities acting as probable causative epileptogenic agents. These data are more easily explained by imputing a subcortical or a diffuse (i.e., metabolic) process than by implicating a single mesial or bilateral cortical epileptogenic lesions (see also Marcus and Watsonz5).However, the reason for the preferential occipital expression of such hypothetical processes remains unexplained. This study, along with that of Ajmone Marsan and Goldhammer, has further attempted to delineate certain features that statistically differentiate seizures of an occipital origin from those of fronto-centro-parietal derivation (see table 4). These include the much greater incidence of visual auras and primary generalized seizures in the occipital group (even with group 2 excluded), and the greater frequency in the fronto-centro-parietal group of somatosensory, cephalic and general body auras, as well as all types of partial seizures with elementary ,22723
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NEUROLOGY May 1975
syniptomatology (i.e., clonic movements, tonic postures, and contraversive turning of head and eyes). Lateralization of a presumptively localized epileptogenic focus, on the basis of unilateral ictal correlates, appears to be more reliable in the occipital series than with the latter series of cases. In the occipital group, head and eye deviation and clonic movements were contralateral to the involved region in all cases, and tonic posturing was a falsely localizing sign on only one occasion. T h i s stands i n contrast to the fronto-centro-parietal group, in which tonic phenomena and especially head and eye contraversion had been proven to be of substantially less Iateralizing value. Furthermore, i n the occipital group, stationary or nonhorizontally moving visual sensations were 100 percent accurate in lateralizing the responsible focus. In no case was ipsilateral localization found, although this has been described during cortical stimulation.2’ Of some interest were the three cases in which the visual phenomena moved laterally from one field to another (or from one eye to another), for in these cases the occipital focus was ipsilateral to the side of image origin and contralateral to its side of termination. Penfield and Rasmussenzl observed similar ipsilateral to contralateral movement of visual images following occipital cortical stimulation in two patients (Cases KW and KH); and several other of these authors’ subjects described visually perceived movement toward the contralateral side, usually from the midline, lending further credence to the hypothesis that moving visual auras are no: falsely localizing, but rather their incipient location is not so useful in lateralizing the side of cerebral involvement as is their direction of movement. Finally, despite the attempt to define clinical aids for localizing and/or lateralizing occipital epilepsy, it should be further emphasized that seizures of occipital lobe origin constitute more than mere “visual fits.” Rather they represent a pleomorphic process that, either through capriciousness or an inherent program, may spread to any one of a number of cortical or subcortical structures, with the potential to engender any one of a large combination of sensory or motor patterns simulating ictal events initiated elsewhere. Acknowledgments The authors wish to thank Dr. J. M. Van Buren, Chief of the Surgical Neurology Branch, National Institute of Neurological Diseases and Stroke, for permittingthe use of his patient files. They also gratefully acknowledge the assistance of Mrs. Doris Sadowsky, Office of Biometry,NationalInstitute of Neurological Diseases and Stroke, in the statistical analysis of the data. REFERENCES 1 . Ajmone Marsan C, Goldhammer L: Clinical ictal patterns and electrographic data in cases of partial seizuresof fronto-central-parietal origin. In Brazier MAB (Editor): Epilepsy:Its Phenomena in Man. New York, Academic Press, 1973, pp 236-260 2.Zivin L, Ajmone Marsan C: Incidence and prognostic significance of epileptiform activity in the EEG of nonepileptic subjects. Brain 91:751-778, 1968 3. Jasper H: The ten-twenty electrode system of the International Federation. Electroencephalogr Clin Neurophysiol 10:371-375, 1958 4. Ajmone Marsan C, Van Buren JM: Epileptiform activity in cortical and subcorticalstructures in the temporal lobe of man. In Baldwin M, Bailey
P (Editors): Temporal Lobe Epilepsy. Springfield, IL, Charles C Thomas, Publisher, 1958, pp 78-108 5.Ajmone Marsan C, OConnor M: Electrocorticography. In Remond A (Editor): Direct, Cortical and Depth Evaluation of the Brain. Handbookof Electroencephalography and Clinical Neurophysiology. Amsterdam, Elsevier Publishing Company, 1973. vol 10, pp 1-46 6. Dimov S, Lanoir J: Effets des lesions epileptogenes chroniques occipitales (cobalt alumine), chez le Papio paplo. Rev Neurol (Paris) 120:480-481, 1969 7. Gibbs FA, Gibbs EL: Atlas of Electroencephalography. Volume 2:Epilepsy. Cambridge, MA, Addison-Wesley Press, 1952,pp 222-224 8. Gibbs FA, Gibbs EL: Changes in epileptic foci with age. ElectroencephalogrClin Neurophysiol, Suppl 4,233, 1953 9. Gibbs EL, Gillen HW. Gibbs FA: Disappearance and migration of epileptic foci in childhood. Am J Dis Child 88596-603, 1954 10. Smith JMB, Kellaway P: The natural history and clinical correlates of occipital foci in children. In Kellaway P, Petersen I (Editors): Neurological and Electroencephalographic Correlative Studies in Infancy. New York, Grune & Stratton, Inc., 1964, pp 230-249 11. Penfield W, Jasper H: Epilepsy and the Functional Anatomy of the Human Brain. Boston, Little, Brown and Company, 1954. pp 116-126 12. Paillas JE, Vigouroux R, Darcourt G, et al: Considdrationssur I'dpilepsie occipitale: (A propos de 12 observations de ldsions occipitales operdes). Neurochirurgie 5:3-16, 1959 13. Huott AD, Madison DS, Niedermeyer E: Occipital lobe epilepsy: A clinical and electroencephalographic study. Eur Neurol 11 :325-339, 1974 14. Russel WR, Whkty CWM: Studies in traumatic epilepsy: 3. Visual fits. J Neurol Psychiatry 18:79-96, 1955
15.Marques Assis L, LivramentoJA, Cury M: Estudio clinico de 68casosde epilepsia occipital. Arch Neurol Psiquiat (S Paulo) 29:49-54, 1971 16. Ajmone Marsan C, Ralston B: The Epileptic Seizure: Its Functional Morphology and Diagnostic Significance. Springfidd, IL, Charles C Thomas, Publisher, 1957, pp 21 1-215 17. Bancaud J: Les crises dpileptiques d'origine occipitale (dtude st6rdo-dlectroencdphalographique). Rev Oto-Neuro-Ophthalmol 41 :299-311, 1969 18. Takeda A, Bancaud J, Talairach J: Concerning epileptic attacks of occipital origin. Electroencephalogr Clin Neurophysiol 28:647-648, 1970 19. Gastaut H: Un aspect mdconnu des ddcharges neuroniques occipitales: La crise oculo-clonique ou "nystagmus dpileptique," In Alajouanine PT (Editor): Activities of the Occipital Lobe. Paris, Masson, 1960, pp 169-185 20. Penfield W, Kristiansen K: Epileptic Seizure Patterns. Springfield, IL, Charles C Thomas, Publisher, 1951, pp 46-47 21. PenfieldW, RasmussenT: The Cerebral Cortexof Man:AClinical Study of Localizationof Function. New York, The Macmillan Company, 1950, pp 135-147 22. Critchley M: Types of visual perseveration: "Palinopsia" and "lllusoly Visual Spread." Brain 74:267-299, 1951 23. Bender MB: Neuro-ophthalmology. In Baker AB, Baker LH (Editors): Clinical Neurology. Volume I. Hagerstown, Harper & Row, Publishers, 1974, pp 38-39 24. Bender MB, Feldman M, Sobin AJ: Palinopsia. Brain 91:321, 1968 25. Marcus EM, Watson CW: Symmetrical epileptogenic foci in monkey cerebral cortex: Mechanisms of interaction and regional variations in capacity for synchronous discharge. Arch Neurol 19:99-116, 1968
NEUROLOGY May 1975
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Clinical ictal patterns in epileptic patients with occipital electroencephalographic foci BARRY I. LUDWIG and COSIMO AJMONE MARSAN Neurology 1975;25;463 DOI 10.1212/WNL.25.5.463 This information is current as of May 1, 1975 Updated Information & Services
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Neurology ® is the official journal of the American Academy of Neurology. Published continuously since 1951, it is now a weekly with 48 issues per year. Copyright © 1975 by the American Academy of Neurology. All rights reserved. Print ISSN: 0028-3878. Online ISSN: 1526-632X.
