Journal of Abnormal Child Psychology, 1973, 1, 3, pp. 267-279
Some Psychological Correlates of Generalized and Focal Epilepsy in Children z CLAIRE B. LOWRY AND SUSAN B. CAMPBELL 2
The McGill University, Montreal Children's Hospital Research Institute School-aged children with two types of epilepsy, generalized and focal, were compared with normal children of the same age, sex, and IQ on measures of cognitive style, attention, motor control, and behavioral pathology. Epileptic children were found to employ less efficient cognitive strategies and to have longer reaction times and poorer control of fine motor movements than have normal children. Children with generalized epilepsy were more impaired than were normal children when sustained motor pertbrmance was required. Mothers of children with generalized epilepsy reported more behavior problems than did control mothers on an objective checklist. These results suggest special educational methods for the treatment and education of epileptic children.
Despite the prevalence o f epilepsy in children, there is surprisingly little research on the cognitive and behavioral correlates o f this disorder. Ires (1970) has reported a higher evidence o f learning disorders in epileptic children, while others have suggested that behavior'problems (Graham & Rutter, 1968) and hyperactivity (Ounsted, 1965) are frequent concomitants o f epilepsy. Few attempts have been made, however, to use unbiased samples, objective measures, or well-matched control ~ o u p s . Moreover, the different types o f epilepsy are seldom considered separately.
1The research reported in this paper was supported by Grant No. MA-4505 from the Medical Research Council of Canada. Grateful thanks are extended to Dr. Katherine Metrakos, Director of the Convulsive Disorder Clinic, Montreal Children's Hospital, who screened epileptic subjects and gave us her enthusiastic support. The Diagnostic Test Center was most helpful in providing blood serum levels on the clinical sample. We wish to thank the Notre Dame de Grace and Westmount branches of the Y.M.C.A. for access to control
mbjects. 2Requests for reprints should be sent to Dr. Susan B. CampbeLl, Department of Psychology, Montreal Children's Hospital, 2300 Tupper Street, Montreal 108, Quebec. 267
Copyright Q 1973 by V. H. Winston & Sons, Inc.
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The present study was designed to investigate patterns of cognitive style, attention, and motor control, as well as incidence of behavior disorders in two groups of epileptic children and a matched group of normal children. Since epileptic children are reported to have learning difficulties despite intellectual functioning within the average range (Ires, 1970), it was thought that epileptic-normal comparisons on these particular measures might clarify group differences in psychological functioning. SCOPE OF THE STUDY
Cognitive Style Recently a growing body of data in experimental psychology has linked problem solving to individual differences in cognitive style or strategies of task solution. For example, Kagan (1965a) found that individual differences in speed of decisionmaking, a style he calls reflection-impulsivity, are related to inductive reasoning skills, motor activity, and reading errors. Field dependenceindependence (Witkin, Dyk, Faterson, Goodenough, & Karp, 1962) reflects individual differences in the ability to focus on relevant stimulus attributes and relates to a range of cognitive and personality traits. Broverman, D. M., Broverman, I. K., and Klaiber (1966) noted that automatization or individual differences in the ability to respond rapidly to simple repetitive tasks is similarly related to attention and persistence. Thus, these facets of cognitive style appear to be pervasive aspects of problem solving which reflect differences in attentional and impulse control rather than specific cognitive skills. Furthermore, a study of the cognitive styles of hyperactive children (Campbell, Douglas, & Morgenstern, 1971) found that these children employ less efficient cognitive strategies than do normal children. Since epileptic children are often described as hyperactive, it seemed that a controlled study of the cognitive styles of epileptic children might provide data about their problem-solving strategies and suggest directions for educational planning.
Attention School performance often demands that children sustain attention for brief periods of time and that they respond quickly to the onset of a stimulus, for example, the teacher giving oral directions. Several studies have shown that children with nervous disorders such as hyperactivity are impaired in their ability to attend for brief periods (Cohen, 1970). Thus it seemed reasonable to examine the performance of children with generalized and focal epilepsy on a reaction-time task requiring a rapid response to stimulus onset.
PSYCHOLOGICAL CORRELATES OF EPILEPSY
Motor Control Although a review of the literature revealed little empirical evidence on the performance of epileptic children on motor tasks, Tellegen (1965) has reported that epileptic adults perform more poorly than do normal subjects on motor tests. Similarly, the clinical reports of Graham and Rutter (1968) suggest that problems of motor control are more common among epileptic children than among normal groups. Studies of other groups of children with suspected brain dysfunction, such as hyperactive children and retarded children, indicate that the clinical groups perform more poorly than do controls (Ellis, 1963; Knights & Hinton, 1969). Knights and Hinton have suggested that impulsivity and distractibility are correlated with poor performance on tasks requiring sustained fine motor control. Thus, children with generalized and focal epilepsy were compared with normal children on measures of motor performance. Behavior Problems Clinical surveys suggest that epileptic children exhibit a larger number of behavior problems than do normal children (Graham & Rutter, 1968; Ounsted, 1965; Pond, 1961). These data, however, have been obtained from clinical interviews and case histories and have failed to differentiate types of epilepsy. Despite the methodological limitations of these reports, they consistently find roughly a 25% prevalence of behavior problems in their epileptic samples (Werry, 1972). Given these clinical findings, an additional aim of this research was to compare the prevalence of behavior difficulties in two samples of epileptic and normal children using a relatively objective measure of behavior problems. Thus, in summary, it was expected that children with generalized epilepsy and those with focal epilepsy would show less efficient strategies of problem solving on measures of cognitive style, would perform more poorly on measures of sustained motor control, would show longer reaction times, and would be reported to exhibit more behavior problems than did matched normal children. METHOD Subjects A total of 21 children diagnosed as epileptic and 21 control children participated in this study. The clinical group were all being followed as outpatients at the Montreal Children's Hospital Convulsive Disorder Clinic. All potential epileptic subjects were screened by a child neurologist to determine whether they met the criteria for inclusion in the study. Subjects were accepted into the study only if epilepsy was the chief complaint, they were currently on anticonvulsant medication, and an EEG recorded during the past year was abnormal.
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So that results would not be contaminated by other problems, epiletic children were carefully selected. Thus, subjects were not included if their epilepsy appeared to be secondary to some gross sign of brain damage such as a tumor or cerebral palsy. Children diagnosed as neurotic or psychotic were excluded from the sample, as were subjects who exhibited any behavior problems severe enough to warrant psychiatric treatment. Children referred for psychological evaluation of learning difficulties were also excluded. Only children of at least dull normal intelligence were included (WlSC IQ of 85 or above). All subjects were living at home, except one who was living with his sibling in a foster home. Since it was not ethically possible to stop anticonvulsant medication, all epileptic subjects were on some combination of anticonvulsant drugs. Of the 21 children in the clinical group, 15 were diagnosed as having generalized epilepsy, the remaining six as having focal epilepsy. Subjects were predominantly from lower middle and middle class backgrounds. The control groups consisted of children who attended schools or summer day camps in the Montreal area. The parents of each child were contacted by letter or telephone, and if they agreed to participate in the study an appointment was made. Children with a history of psychiatric or learning difficulties were excluded. Only children who matched an epileptic child on age, sex, estimated WlSC IQ, and socioeconomic status were included in the final control group. The generalized epilepsy group consisted of eight boys and seven girls. Their ages ranged from 5 years, 11 months, to 11 years, 11 months, with a mean of 9 years, 1 month. Each control subject was matched with an epileptic child on age and sex. The ages of the controls ranged from 6 years, 7 months to 12 years, 7 months. The mean age of the control group was 9 years, 1 month, identical to that of the epileptic group. IQ scores of the epileptic subjects ranged from 94 to 138 with a mean of 109.2, while the IQs of the control subjects ranged from 94 to 131 with a mean of 109.1. Obviously these samples were well matched on these variables. The six subjects with focal epilepsy, three boys and three girls, ranged in age from 5 years, 0 months, to 11 years, 3 months, with a mean of 7 years, 9 months. Their controls, likewise matched on age and sex, ranged in age from 5 years, 2 months, to 11 years, 7 months. The mean age of the control group was 8 years, 0 months. The IQ scores of the focal group ranged from 106 to 125 with a mean of 115.8 while the IQs of their controls ranged from 100 to 125, with a mean of 113.7. Test Administration
Each child was seen individually at the Montreal Children's Hospital for approximately one hour of testing.
PSYCHOLOGICAL CORRELATES OF EPILEPSY
The Matching Familiar Figures Test (Kagan, 1965a) was used to measure reflection-impulsivity. It consisted of 12 sets of pictures of familiar objects and animals. Subjects were shown a standard stimulus and were required to choose the one picture from among the six alternatives that matched it. Up to six trials were allowed per item. Variables scored were latency to first ! response and number of errors. Fidd dependence-independence. The Children's Embedded Figures Test (Karp & Konstadt, 1963) was used to measure field dependence-independence. The child was required to locate two simple figures embedded in more complex designs. The score was the total number of figures correctly located. Only one trial was allowed per item, and there was no time limit. Since the 25 items were arranged in order of increasing difficulty, testing was discontinued after five consecutive failures. Prior to administration of the test items, there was a i demonstration of the embedding process as outlined in the test manual. Automatization. The measures of automatization were speed of color naming and errors on the Color Distraction Test (Santostefano & Paley, 1964) which consisted of 10 x 15-in. cards With pictures of lettuce, bananas, apples, and grapes in random order, 50 per I card. Card I consisted of red apples, green lettuce, blue grapes, and yellow bananas. Once it was established that the subject knew the color names, he was merely required to name all the colors on the card, in order, as fast as possible. Card II consisted of the same stimuli in the same order and color with the addition of 50 black and white peripheral pictures of familiar objects, meant to be diitracting. The child was instructed to name the colors and ignore the black and white pictures. Card III was made up of the same stimuli in the same order, but al! were in a contradictory color. Bananas were either blue, red, or green, but noi yellow, and so on. The subject was instructed to name the color that should be there, rather than the one which appeared. Speed of color naming and errors Were recorded for all three cards. Attention. A simple reaction-time task was used to investigate the ability to 9 I maintain attention for brief perlads of time. Reaction time was measured by a precise timer (Standard Electrici Time Company, Model S-I) graduated to .01 sec. Red and white lights were used as stimuli. They could be illuminated separately by the examiner, and !hey automatically started the timer. The lights were activated in random order, but the same order was used for all subjects. Depression of a pushbutton directly in front of the child extinguished the stimulus and stopped the timer. Hence the reaction time for each trial was equal to the length of time between illumination of the stimulus by the experimenter and its extinction by the subject. Five practice trials were given. A simple reaction-time score was obtained by taking the average of scores over the 20 test trials. There was a lapse of from 6 to 16 seconds between trials, with a mean intertrial interval of 12 seconds, iSubjects were warned 2 seconds prior to the start of each trial. The subject's dqminant hand was used on all trials, arid he was
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required to begin each trial with his hand at a fixed distance from the pushbutton. He was instructed to push the button as fast as possible, once the stimulus light came on. Motor performance. The Lafayette stylus maze was used to measure motor steadiness during motion. The subject was required to run a stylus through a maze which had blind alleys blocked. The maze was wired so that a light was activated whenever the stylus came into contact with the maze. A total of four trials was given, two for each hand. The number of contacts made on each trial was recorded and the score was the average over the two trials for each hand. Subjects were instructed to follow the path with the stylus, to try not to touch the sides, and to go very carefully. A pegboard test was used to evaluate motor control when sustained performance was ~equired. The apparatus consisted of a 6 x 4-in. board and 25 pegs. Subjects were told to insert the pegs individually, as rapidly as possible. The variable scored was the length of time required to complete the pegboard. A stopwatch was activated and stopped when the final peg was inserted. One trial was given for each hand. Behavior problems, The Behavior Problem Checklist (Quay & Peterson, 1967) was used as the measure of psychopathology. It was completed at the time of testing by the parent (usually the mother) accompanying the child to the hospital. In a few cases, this was not possible and the checklist was returned by mail a few days later. Parents were instructed to indicate whether a ~ven behavior constituted a problem and, if so, whether they considered it mild or severe. It was scored according to the manual on four factors: conduct problem, personality problem, inadequacy-immaturity, and socialized delinquency. Intelligence. The vocabulary subtest of the Wechsler Intelligence Scale for Children was administered according to standard instructions (Wechsler, 1949) to obtain an estimate of IQ.
Cognitive Style Reflection-impulsivity. To achieve homogeneity of variance, reaction time scores on the Matching Familiar Figures Test were converted to logarithms and analyzed using a t test for correlated samples. Children with generalized epilepsy were more impulsive than normal children. They responded significantly faster (t = 2.46; d[ = 14; p ( . 0 5 ) and made significantly more errors (t = 5.47; dr= 14; p ( . 0 0 1 ) than control children. Children with focal epilepsy were also more impulsive than normal children with significantly shorter latency scores (t = 3.87; df = 5; p ~ .02) and more errors (t = 4.87; df = 5; p ~ .01).
PSYCHOLOGICAL CORRELATES OF EPILEPSY
Field dependence-independence. Scores
on the Children's Embedded Figures Test were analysed using a t test for matched groups. Children with generalized epilepsy isolated significantly fewer embedded figures than did control children (t = 5,12; d f = 14; p < .001) as did children with focal epilepsy (t = 8.07; dr= 5; p < .01). Automatization. To correct for extreme scores, speed of color naming on the Color Distraction Test was converted to logarithms and error scores were converted to log (x + 1). The results from one child with generalized epilepsy had to be discarded since the experimenter made an error in timing her performance. Hence, all analyses of the Color Distraction Test were carried out on 14 subjects with generalized epilepsy and their controls. A two-way analysis of variance with repeated measures across cards and paired subjects indicated that the difference between groups in color naming speed was not significant (F = 1.59). A t test for matched groups, however, indicated that children with generalized epilepsy made significantly more color naming errors on the three cards combined than did normal controls (t = 3.23; df = 13; p < .01). One child with focal epilepsy refused to complete the Color Distraction Test. Thus all analyses were carried out on five subjects with focal epilepsy and their controls. A two-way analysis of variance with repeated measures indicated that children with focal epilepsy took significantly longer to name the colors on all three cards (F = 28.13; d.C"= 1/8; p < .01). The two groups did not differ, however, in number of errors in color naming (t = .06; df = 4). These data are summarized in Table 1.
Attention Data for the reaction-time task were analyzed using a t test for matched groups. Children with generalized epilepsy had significantly longer reaction times than did normal control children (t = 7.49; df = 14; p < .001), as did children with focal epilepsy (t = 3 . 4 7 ; d f = 5;p < .05). These data may be found in Table 2.
Motor Control Data for the maze task were anlayzed using a two-way analysis of variance with repeated measures. Children with generalized epilepsy showed poorer motor control when performance required careful movement of the hand. They made significantly more contacts with the edges of the maze than did control children ( F = 30.81; df = 1/28; p < . 0 1 ) . Within subjects, the effect of hand-on-maze performance indicated that the performance was superior with the dominant hand for both groups (F = 5.97; df = 1/28: p < .05). Children with focal epilepsy were also found to exhibit poorer motor control than did normal
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TABLE 1 MEANS AND STANDARD DEVIATIONS OF COGNITIVE STYLE COMPARISONS OF EPILEPTIC AND NORMAL CHILDREN Group i I i
Reflection-impulsivity (Matching Familiar Figures Test) Number of children Mean reaction time Standard deviation
(SD) Mean n u m b e r errors SD Field-dependence (Children's Embedded Figures Test) Number of children Mean number correct SD Automatization (Color Distraction Test) Number of children Mean naming time in seconds Mean, Card I SD Mean, Card II SD Mean, Card III SD Mean number errors Mean, Card I i SD Mean, Card II SD Mean, Card III SD
3.7 18.2 8.8
22.8 8.0 3.9
3.1 21.0 8.9
24.6 8.0 6.5
15 12.6 5.5
15 19.9 3.3
6 9.0 3.9
6 17.8 3.6
56.5 32.0 67.4 48.8 114.5 78.7
46.4 15.4 48,3 16,5 86.3 27.6
67.0 13.2 61.4 8.9 112.7 35.0
39.9 12.9 42.1 10.7 71.2 13.7
1.6 1.3 1.1 1.2 1.8 1.5
2.8 1.9 2.4 1.3 2.6 2.5
1.8 1.5 2.6 2.7 2.8 2.8
2.4 1.6 3.4 2.3 4.8 5.8
Note.-Means and standard deviation of raw score data.
PSYCHOLOGICAL CORRELATES OF EPILEPSY
TABLE 2 MEANS AND STANDARD DEVIATIONS OF RAW DATA ON ATTENTION AND MOTOR CONTROL MEASURES Group Measure
Reaction Time (RT) Task Mean RT in seconds SD Maze Dominant hand Mean number contacts SD Nondominant hand Mean number contacts SD Pegboard Dominant hand Mean completion time in seconds SD Nondominant hand Mean completion time in seconds SD
Generalized epileptic N = 15
Control N = 15
Focal epileptic N=6
children on this task since they made significantly more contacts with the maze (F ; 17.26; dr= 1/10;p < .01). The comparison o f dominant and nondominant hands failed to reach significance (F = 4.86; df = 1/ 10). Since the completion-time scores on the pegboard task were not normally distributed, they were transformed to logarithms and analyzed using a two-way analysis of variance with repeated measures. Children with generalized epilepsy had poorer motor control than did normal children when sustained performance was required. They also took significantly longer to complete the pegboard task (F = 33.60; df = 1/28; p < .01). The effect of hand on performance was also significant, since it took longer to complete the pegboard with the nondominant hand (F = 15.25; dr= 1 / 2 8 ; p < .01). The children with focal epilepsy did not differ from normal children on the pegboard task (F = .14; dj"= 1/10) and the
LOWRY AND CAMPBELL TABLE 3 MEANS AND STANDARD DEVIATIONS OF FACTOR SCORES ON THE BEHAVIOR PROBLEM CHECKLIST
Conduct problem Mean SD Personality problem Mean SD Inadequacy-immaturity Mean SD Socialized delinquency Mean SD
Generalized epileptic N=I1
hand effect failed to attain significance (F = .01; d f = 1/10). These data are summarized in Table 2.
Behavior Problems Four parents in the group of generalized epileptic children failed to complete the Behavior Problem Checklist. Thus all analyses were carried out on 11 epileptic children and their controls. Children with generalized epilepsy were described as having more problems on the inadequacy-immaturity factor than were normal children. This difference was significant only when a one-tailed test was used (t = 1.95; d f = 10; p < .05). Contrary to expectation, there were no differences on the remaining three factors. Moreover, no significant differences were found between children with focal epilepsy and control children on these measures. These data are summarized in Table 3.
Discussion Groups of children with generalized and focal epilepsy performed differently from normal children of the same age, sex, and IQ. Epileptic children responded more slowly on a reaction-time task and had poorer control of fine motor
PSYCHOLOGICAL CORRELATES OF EPILEPSY
movements on a stylus-maze task. Children with generalized epilepsy also performed more poorly than normals on a pegboard task requiring sustained motor activity. Both groups of epileptic children also tended to employ less efficient cognitive styles than did their normal controls. They were more impulsive and more field dependent. While children with generalized epilepsy made more errors than did controls on a measure of rapid serial naming, children with focal epilepsy performed this task more slowly ~han controls, suggesting that both groups of epileptic children do more poorly on some aspects of automatization. Surprisingly few differences were found on the Behavior Problem Checklist. Although children with generalized epilepsy were reported to show more problems in the area of inadequacy-immaturity, children with focal epilepsy did not differ from controls on any of the factors. Thus, mothers of children with generalized epilepsy reported a short attention span, laziness in school, excessive daydreaming, and passivity more frequently than did control mothers. There was no evidence of more hyperactivity or aggressive acting-out behavior in this epileptic sample. The failure to find any statistically significant differences between children with focal epilepsy and their controls perhaps reflects the small sample size. Since there is generally a fair amount of group overlap on this measure, group differences are difficult to obtain when samples are small. The investigators are currently planning to enlarge the sample of children with focal epilepsy. Difficulties in attention and motor control, as well as inefficient cognitive strategies, may in part account for the high frequency of learning problems observed in epileptic children by other investigators (Ives, 1970). Impulsive responding in the face of cognitive uncertainty has been related to reading ability (Kagan, 1965b) and inductive reasoning skills (Kagan, Pearson, & Welch, 1966) in normal children. Similarly, a field-dependent approach has been associated with poor performance on measures of visual-perceptual organization (Witkin et al., 1962). Weak automatization has also been linked to academic skills that involve rote learning, e.g., the mechanics of reading, writing, and arithmetic (Broverman et al., 1966). Similarly, children who have poor motor control and tend to respond slowly to stimulus onset would be expected to do poorly in school. Motor skills obviously would affect writing skills, while a delay in orienting to new input would suggest that the child misses much of what is going on in the classroom. This is confirmed by the checklist data for the generalized epileptic subjects whose mothers report a high frequency of daydreaming and short attention span. Although more research relating cognitive functioning to the actual school performance and problem behavior of epileptic children is sorely needed, these results do suggest that special educational techniques may be necessary to optimize the classroom performance and learning ability of many epileptic
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children. For example, training in perceptual and motor skills appears indicated, as does the use of memory aids when tasks require rote learning. Finally, hyperactive children have been successfully trained to decrease impulsive responding (Palkes, Stewart, & Kahanna, 1968); such training seems applicable to epileptic children as well. ~EFERENCES Broverman, D. M., Broverman, I. K., & YAaiber, E. L. Ability to automatize and automatization cognitive style: A validation study. Perceptual and Motor Skills, 1966, 23, 419--437. Campbell, S. B., Douglas, V. I., & Morgenstern, G. Cognitive styles in hyperactive children and the effect of methylphenidate. Journal o f Child Psychology and Psychiatry, 1971, 12, 55-67. Cohen, N. J. Psychological concomitants of hyperactivity in children. Unpublished doctoral dissertation, McGill University, 1970. Ellis, N. Handbook o f mental deficiency. New York: McGraw-Hill, 1963. Graham, P., & Rutter, M. Organic brain dysfunction and childhood psychiatric disorders. British Medical Journal, 1968, 106, 695-700. Ives, D. Learning difficulties in children with epilepsy. British Journal o f Disorders o f Communication, 1970, 5, 77-84. Kagan, J. Individual differences in the resolution of response uncertainty. Journal of Personality and Social Psychology, 1965, 2, 154-t 60. (a) Kagan, J. Reflection-impulsivity and reading ability in primary grade children. Child Development, 1965, 36, 609-628. (b) Kagan, J., Pearson, L., & Welch, L. Conceptual impulsivity and inductive reasoning. Child Development, 1966, 37, 583-594. Karp, S. A., & Konstadt, N. Manual for the Children's Embedded Figures Test. New York: Cognitive Tests, 1963. Knights, R. M., & Hinton, G. The effects of methylphenidate (Ritalin) on motor skills and behavior of children with learning problems. Journal o f Nervous and Mental Disease, 1969, 148, 643--653. Ounsted, C. The hyperactive syndrome in epileptic children. Lancet, 1965, 269, 303-31 I. Palkes, H., Stewart, M., & Kahanna, B. Porteus maze performance of hyperactive boys after training in self-directed verbal commands. Child Development, 1968, 39, 817-829. Pond, D. Psychiatric aspects of epileptic and brain-damaged children. British Medical Journal, 1961,2, 1377-1382. Quay, H. C., & Peterson, D. R. Manual for the Behavior Problem Checklist. Unpublished manuscript (mimeographed). Champaign, IU., 1967. Santostefano, S., & Paley, E. Development of cognitive controls in children. Child Development, 1964, 35, 939-949. Tellegen, A. The performance of chronic seizure patients on ~the General Aptitude Test Battery. Journal o f Clinical Psychology, 1965, 21, 100-184.
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Wechsler, D. Manual for the Wechsler Intelligence Scale for children. New York: Psychological Corporation, 1949. Werry, J. S. Organic factors in childhood psychopathology. In H. C. Quay & J. S. Werry (Eds.), Psychopathological disorders of childhood. New York: Wiley, 1972. Witkin, H. A., Dyk, R. B., Faterson, H. F., Goodenough, D. R., & Karp, S. A. Psych ological differentiation. New York: Wiley, 1962.