Folia Psychiatrica et Neurologica Japonica, Vol, 30, No. 3, 1976
Clinical Features Related with Centrencephalic EEG Abnormality Norihiro Miyaishi, M.D. Department of Neurology, Institute of Neurological Science, Tottori University School of Medicine, Yonago INTRODUCTION Main interest is usually concentrated on ictal symptoms when paroxysmal EEG abnormality is found. And this kind of clinical category is identified with some types of epilepsy. Non-ictal or continuous symptom, not coexisting with any type of epileptic symptom, is easily spoken of as epileptoid, interictal or subclinical symptoms, if patients have the similar EEG abnormality seen in epilepsy. The psychical or psychiatric symptom found together with EEG abnormality stimulates usually search-efforts concentrating on personality and psychodynamic mechanism. It seems that EEG abnormality of the patients who have psychical or psychiatric problems scarcely attracts attention. Focal EEG abnormality, like temporal focal discharges, is easily accepted to connect with the psychical symptoms in the conception of epilepsy, and the psychical symptoms are regarded as epileptic nature. But there are many problems still remaining unsolved when the similar psychical or psychiatric symptom is seen in the patient with centrencephalic EEG abnormality. The centrencephalic EEG abnormality, in this paper, comprised the followings; bilateral diffuse synchronous spike and wave, 3-61sec spike and wave, 6/sec small spike and wave, 614/sec positive spikes and bilateral diffuse _____
Received for publication May 14, 1976.
synchronous slow bursts. It is well known that the patient with these EEG discharges, not necessarily suffering from the ictal symptom, has various kinds of symptom of either physical or psychical. However, when the interpretation of the centrencephalic EEG findings as an excessive neuroral discharge is valid, this interpretation can hardly justify that the ictal symptom is the only means to determine the pathophysiological foundation of the electric-clinical correlation. To clarify the clinical features of patients with psychical symptom, one or a few consultations result not rarely in errors, especially when the symptom is related to EEG abnormality. It must be considered, furthermore, that physical and psychical symptoms can be modified in the developmental course of the same individual. For this reason, it may be the best way to see patients from early childhood through the adult period for understanding the clinical characteristics. In this paper, the correlation between the clinical features and EEG findings was studied in patients in the six to 10 and 11 to 24 age brackets. SUBJECTS AND METHODS A total of 204 subjects were available in this study. They were divided into two series. The first series comprised 154 children ranging in age from six to 10 years, the average
N. Miyaishi
264
age being 8.5. They were consulted, because of school underachievements, in order to decide whether special education curriculum could be useful ,or not. Neither physical handicap nor environmental factor was thc cause of bad school records. They were again divided into two groups according to IQ, and one group had 84 children whose 10 was above 90, while the other group of 70 children showed IQ below 85. IQ was measured by Suzuki-Binkt Tests. Besides school underachievements, various physical symptoms together with behavior problems were observed in the 154 children. Their symptoms and behavior deviation were confirmed by the authors and supported by their school teachers and parents. Behavior problems were sorted according to the modified program from Stevens's original one.ln The
15
10
5
quality and quantity of behavior problems were carefully evaluated. The second series of subjects consisted of 50 patients who had been hospitalized once during the previous three years. The agerange was 11 to 24 years with an average of 18. All of them had centrencephalic EEG findings, 6-14/sec positive spikes. The clinical observation was extended from their developmental course through the post-hospitalization period. Particular attention was paid to suicidal attempt and personality and developmental environment to clarify the underlying mechanism of the desire for suicide. EEG's were taken on eight- and 12-channel ink-writing recorders. The activating procedures of hyperventilation, photic stimulation and the intravenous injection of di-
10
numbers I Shortalbntlonspan I Dlrtrutlon a
M
Exploslw
: Clumsy
I
limldlty
i Hvprmnw
*
Aguresrhn Wwttlg
4
:
~awfrurtratlon lmpulrlvb
B
I
8 I
n 7c
lrolrtlon
u i 2 1
' @posMt 1
Stwnmrln Wlthdrwn
* * *
Fig. 1: Varieties and incidence of behavior problems.
Centrencephalic EEG Abnormality phenhydramine at dose level of 1 mg/kg body weight were used. RESULTS
1. The First Series (1)
Varieties and incidence of behavior problems (Fig. 1)
Among 84 children with IQ above 90, 72 (83%) had some varieties. These behavior problems could result from the disorder of attention. Out of 70 children with IQ below 85, 53 (76%) had other varieties of behavior problems. Hypoactivity and clumsiness showed a high incidence of 14 and 1 1 respectively. Although these two were thought to be the usual properties of low intelligent children, they were not rarely found in the present group of children with I0 above 90.
265
ache, abdominal pain, vomiting, increased fever of unknown cause and itching. They recurred in 38% of the children with IQ above 90, and in 43% of those with IQ below 85. Vegetative symptoms and behavior problems in the same individual were common. Thirty-one percent of a total of 154 children suffered from both of them, whereas 9% had the former only.
(3) Varieties of EEG abnormalities (Table 1) Some degree of EEG abnormality was seen in 77% of 154 children. There were borderline or slightly abnormal EEG’s in 50 cases (32%), cortical focal spike (C.F.S.) in I8 (12%), generalized diffuse synchronous in 25 (17%), 6-14 spike and wave (G.S.) positive spike or phantom spike and wave (P(h)S) in 22 (14%), and multi focus (M.F.) in 3. As to the abnormalities of centrencephalic origin, they were seen in 47 children
(2) Associated symptoms (Figs. 2. a, b)
(31 %).
Past history was studied back through the date of children’s birth. Several vegetative symptoms were pointed out, such as head-
(4) The relation between EEG abnormalities and behavior problems The distribution of EEG abnormalities in
Tdal
in
131I
imi
I91 1101
1%)
Table 1: Varieties of EEG Abnormalities
EEG findings
No. %
B . L . 4 1 . abn.
50 (32) 18 i 1 2 j
C.F.S.
\
G.S.
P(h)S.
M.F.
Norm. Total
Behavior Deviation Behavior Deviation Autonomic Symptom
154
B.L.41. abn.; Borderhewslight abnormal
Autonomic Symptom alone no Symptom
3 ( 2) 36 (23)
h 0
=
1.0. >Po
1.0.
< 85
total 84 total 70
Fig. 2: Varieties of clinical symptoms.
C.F.S.;Cortical focal spike G.S.; Generalized bilateral spike and wave P(h)S.; Positive spike or phantom spike and wave M.F.;Multifocus Norm.; Normal
N. Miyaishi
266
the varieties of behavior problems was illustrated (Fig. I). There was no significant correlation of the EEG abnormalities with a certain behavioral property. The relation between EEG abnormalities and clinical types
(5)
Then, four clinical types were arranged according to whether either or both of behavior problems and vegetative symptoms, or neither, were found in patients. And, the percentage of EEG abnormalities was shown in each clinical type. (Fig. 3) In the type which showed behavior problems only, borderline or slightly abnormal EEG’s were most dominant, having the percentage of 38. On the other hand, the EEG abnormalities of centrencephalic origin were most common in the type with both of behavior problems and vegetative symptoms, and also in the type with vegetative symptoms alone, showing 46% and 43%, respectively. The relation between clinical types and EEG abnormalities
(6)
The proportion of each clinical type in each kind of EEG abnormalities was illustrated. (Fig. 4) The clinical type only with behavior problems shared 58% of borderline or slightly abnormal EEG’s. This type shared also 61 % of cortical focal spikes. On the other hand, the clinical type with both of behavior problems and vegetative symp-
toms occupied 48% of G.S., and also 45% of P(h)S. Fifty-eight percent was shared by the type only with behavior problems in normal EEG category. This finding could suggest that behavior problems which developed only from vegetative symptoms had a close relation to the centrencephalic EEG abnormalities.
2. The Second Series (1)
Varieties and incidence of behavior problems (Table 2)
In 50 patients of this series, there were some varieties of behavior problems. They were school refusal in 14 cases, suicidal attempt in 10, short-range or compulsive behavior and misdeed, etc. These problems usually attracted attention to the underlying sociopathic peculiarities.
(2) Affective aspect (Table 3) The emotional properties of patients were summarized from the overall survey from childhood through the period after their hospital discharge. Anxiety, depressiveness, or aggressiveness became evident, but none of them could be the essential properties of the patients. A psychiatric study was made
B 1.5.1
Abn
Canlrancephallc C F S
Bollador Dwlltlon GS
BCh D N +
Aulon Dlsl
OW
Autonom Dlsl
Na Sympl
Fig. 3: The relation between symptoms and EEG.
PlhlS
Cantlonceph~llc
M f
Norm
Fig. 4: The relation between EEG and
symptoms.
Centrencephalic EEG Abnormality
267
on patients of this series. Neither neurosis nor psychopathy was pointed out. A certain psychological condition, which was not similar to any category of psychosis, was considered in 18 cases.
the reverse was rare. In some stage, both of vegetative symptoms and behavior problems coexisted. They occurred at the same time in some individuals, but independently in the same number of cases.
(3) Varieties of vegetative symptoms and their correlation to behavior problems (Table 4)
(4)
In each individual, physical symptoms, especially vegetative ones were scrutinized in relation to his emotional properties, psychological condition and behavior problems. Chronic headache was noteworthy among vegetative symptoms, being found in 24 patients. The developmental or transitional process of vegetative symptoms and behavior problems was looked over back through his infant period. The results were illustrated on the lower part of Table 4. In the earlier stage, some vegetative symptoms were dominant, whereas in the later stage, behavior problems became evident. Thus, it seemed that vegetative symptoms changed into behavior problems during the course of illness. This correlation was seen in 21 patients and
Table 2: Varieties and Incidence of
Behavior Problems Behavior problems School refusal Suicidal attempt Short-rangecompulsive behavior Misdeed sexual behavior steal Idleness- taciturnity Regression Unsettled employment Eccentricity Psychomotoric excitement Runaway-wandering Hyperactive ( A total of 50 cases)
Ten cases of suicidal attempt
One killed herself and nine were survivals. The age-range of these 10 cases was 15 to 24 years, and nine cases were females. The properties in personality were studied. Egocentricity or self-assertiveness was seen in five cases. But no significant value was given. Intelligence was normal in most cases. Their developinental environment was investigated. Five cases were the youngest child, two were brought up by their grandmothers and two lost either of their parents early in life. Six were schoolgirls and four were workers. The ways used by them were medical drug in five cases, knives in two, automobile in one, and city gas in one. In one remainder, it was unclear how she killed herself. Psychological condition at the time of suicidal attempt was studied. Two cases were impulsive, two had been in anxiety or
Table 3: Affective Properties of 50 Patients with Six and 14 Positive Spikes Anxiety Depressiveness Nervousness Low frustration tolerance Irritability Hypochondry Emotional instability Restlessness Regression Tension Impulsiveness Withdrawn Fear Aggression Ill-humored
12 11 10 9 8 7
5 4 4 3 3 2 2 1 1
-___
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268
established. If patients have some other symptoms different from epileptic attacks, the clinical significance of the epileptic EEG discharges could not be so clearly determined. There are a good number of patients who show the epileptic EEG discharges but no epileptic attacks. To clarify this kind of clinical feature, a synthetic investigation based on semiology, intelligence, affective or behavioral problems and environmental
depressiveness for a long time, two had been hysteric, and one had some strange consciousness. DISCUSSION When some epileptic manifestations of the classic category of epilepsy are seen in patients with the so-called epileptic EEG discharges, diagnosis as epilepsy would be easily
Table 4: The Mode of Onset of Symptoms Varieties of physicalsymptoms
.
No.
Headache 24 Vomiting 6 Dizziness 5 Insomnia 4 Head congestion 4 Abdominal pain 4 Dyspnea 4 Cenesthesie 4 Irritable colon 3 Urticaria 2 Tinnitus 2 Exhaustion 1 Somnolent 1 Sensation of urinary retention 1 Myalgie 1 Palpitation 1 Unknown febrile 1 Total
Continu- Epious sodic 8
6 1
4 2 1 3 1
1 2
Ictal
-
10
5 5
Unchange- Diver- Changeable sity able 13 2
3 1
2
3
3 4 1 1
1 1 3 1 1 1 1 1
2 1
I
2
4 2 2 1 1 2 1 2 1 1
1
2 1
1 1
1 1
1 1
23
9
12
1 1
33
35
27
The developmental or transitional process of symptoms vegetative symptoms -+ psychical or behavioral problems 21 psychical or behavioral problems -+ vegetative symptoms 3 The appearance of both vegetative and psychical or behavioral prob1ems: at the some period 14 each independently 12 alternatively 2
6
Centrencephalic EEG Abnormality survey is necessary. Paroxysmal seizure discharge of the EEG is nothing more than an excessive neuroral discharge within the brain. Clinical manifestation would be produced from ,the cooperative function of the primary location of the neuroral excessive discharge and its circumferential locations within the brain. The present study was aimed at clarifying new clinical entity other than epilepsy and the meaning of epileptic EEG's in it. Two series of subjects were compared with each other.
269
bursts could not always mean EEG abnormality. These findings should be estimated with every regard to the developmental process of the brain and age distribution.' m Therefore, EEG findings other than paroxysmal seizure discharge were put aside from the consideration in this study. Behavior problems associated with the EEG seizure discharges have been studied with regard to the semiological difference according to the location of cerebral lesion.8 fl It was well known that the temporal cortex could bring out certain behavior problems.2 And there were several works con1. The First Series cerned with the centrencephalic EEG findings. (a) The characteristics of symptoms The properties of behaviors were pointed Behavior problems of the children of this out in those works, and impulsiveness," series were estimated mainly from the qualihyperactivity," psychopathy7 l 2 lfi and agtative and quantitative analysis. This analysis g r e s s i ~ e n e s s and , ~ ~ abnormal behavior probwas useful enough to find up the characterlems14 20 such as stealing and misdeed were istics of the behavior problems of this series where such sociopathic problems as misdeed assumed to correspond to certain EEG findings. But, after all, it was scarcely deterwere scarcely found. mined that what kind of behavioral properIt was concluded that the behavior probties and what type of EEG findings could lems were understood to be limited to the correspond to each other. extent of the estimation. Most children The present study resulted also in negative showed learning disability as a common on this question and no distinctive correlafeature, and it was supposed to result from tion was detected between particular bebehavior problems. The behavior problems havioral properties and certain EEG findwere one of the most principal symptoms in ings. Summarized overall, the most importhis series. Various symptoms concerning tant results were supposed that all the bethe vegetative nervous system were next to havioral properties might correlate definitely behavior problems. These vegetative symptoms were seen in 41 % of the children. The to the mechanism itself from which any type relation between vegetative symptoms and of the centrencephalic EEG abnormalities learning disability or behavior problems was could originate. investigated, paying particular attention to The relation among clinical symptoms, EEG abnormality. behavior problems and vegetative symptoms, and the EEG characteristics were summar(b) The relation between clinical characterized as follows: Children who had behavior istics and EEG findings problems but no vegetative symptoms In the discussion on EEG abnormality, it showed frequently borderline EEG's or is not needless to say that consideration must slightly abnormal EEG's but rarely paroxysbe based on the various points of view. mal seizure discharges. And it is noticeable Dysrhythmic basic waves and slow wave that those who had vegetative symptoms but
270
N. Miyaishi
no behavior problems or those who had both of vegetative symptoms and behavior problems had paroxysmal EEG discharges. especially the centrencephalic EEG findings. It was supposed that the delay of the developmental process of the brain might play an important role in the primary basis of behavioral deviation, and that vegetative symptoms, corresponding directly to the centrencephalic EEG abnormalities, could promote the behavioral deviation with the cooperation of some disorders of consciousness, attention and affection.
series of patients other than school refusal and suicidal attempt. Most of these behavior problems were paroxysms in their nature but non-acquired. The duration of these paroxysms varied in time even in the same individual. A good number of studies suggested the relation between the positive spikes in the EEG and behavioral abnormalities, but the final clinical significance of this positive spikes was not yet established. Henryfi made a historical review on the positive spikes from many previous literatures and described that psychiatrically the positive spikes could hardly show a correspondence with certain particular event of behavior problems. Then, 2. The Second Series he stated that this EEG discharge could be (a) Clinical symptoms more easily expected from clinical petit ma1 Antisocial troubles were a common rea- epilepsy. We found the positive spikes in a son for clinical consultation in young per- wide variety of clinical events, supporting his sons whose EEG's were abnormal. The opinion to some extent. To clarify the parsubjects of this series, selected from those, ticular role of the positive spikes, a longwere admitted to our hospital for further term study would be necessary on every paphysical and psychical studies. In addition tient back through his birth to follow up to sociopathic behavioral deviations, affec- contact, because some symptom may change tive disorders and vegetative disturbances into other symptom during the course of his were the main clinical symptoms. The be- growth. havioral deviations produced some affairs which forced the patients into maladjust- (b) Some relations among the varieties of clinical symptoms ment at home, school or business. This The relation between one another of three was exactly different from the behavior problems of the children aged below 10. The clinical varieties, vegetative symptoms, affecsocial affairs they committed were composed tive disturbances and behavior problems was of school refusal in 11 patients, suicidal shown in Table 4. In case patients were attempt in 10 and misdeed in four. The mis- younger, headache and abdominal pain were deed included sexual delinquency and steal- commoner than affective or behavioral dising. In I 1 cases of school refusal who were orders, whereas the latter became commoner 13-17 years old, some complex develop- when the patients were older. Several pamental history, domestic trouble or bad re- tients had been admitted to hospital with the lation between friends were found. These chief complaints of some vegetative symptroubles have attracted some workers' atten- toms when they were younger and were tion" as an exact cause of school refusal. again admitted several years later because of But some other causal reason should be con- behavior problems. Vegetative symptoms were non-ictal on sidered in our cases of school refusal. The same causal mechanism seen in the cases of some occasions and ictal on other occasions suicidal attempt was assumed. Several kinds in most patients and not always fixed on a of behavior problems were found in this certain same organ. In the patients who had
Centrencephalic EEG Abnormality the positive spikes, vegetative symptoms were not yet a certain factor determining whether they were primary or derivative symptoms. But this question did not deny that the vegetative symptoms could play an essential role to produce the behavior problems or the excessive affective expression. Suicidal attempt gave the approach for the mechanism of the behavioral deviation and the positive spikes. Twenty percent of the patients with the 6-1 4/sec positive spikes tried suicidal attempt. Several events, personality distortion or psychological conflicts could be considered as a direct cause of suicidal attempt. But these events were seen more widely not only in suicidal attempt but also in other behavior problems. Physical stress resulting from head injury or vegetative dysfunction was also thought to activate the suicidal attempt. But, it was pointed out as the most interesting fact that some cases experienced a strange feeling, a clouding of consciousness or a psychomotor like an episode at the exact time when they performed suicidal attempt, and that in other cases serious affective disorders were observed. Nobody was diagnosed as depression. A case died from suicidal attempt. Most cases had little volition for a sure deathlXand unadequate tools were chosen. It was concluded that the suicidal attempt for them was something other than the act of killing oneself. But it was supposed to result from particular types of affective disorders or behavior problems."' As the modern convenience advances more, the number of people with social maladjustment may increase. This serious social problem must be studied not only from the viewpoint of social pathology but also from the biological viewpoint. The abnormal EEG discharges of centrencephalic nature proposed an important biological indicator for affective and behavioral abnormalities. Three clinical varieties, vegetative symptoms, affec-
27 1
tive disorders and behavior problems might be thought to result from a certain pathological process within the brain. And this pathological process might ejaculate occasionally the EEG discharges of centrencephalic nature. To explain the pathophysiology of the affective disorders of the patients with the centrencephalic EEG phenomenon, the followings appeared to be necessary. (1) The clinical symptoms resulted from both physical and affective reactions. On some occasions, one of the two reactions exceeded the normal range and the other did not, and on the other occasions, the latter exceeded the normal limits but the former did not.
(2) Many activating factors were supposed in physical symptoms and the duration of the symptoms varied time to time in the same individual patients. This suggests that when the overreaction of the vegetative nervous system resulted in the physical symptoms, the affective reaction was limited to the normal extent. (3) Reversely, when the affective reaction exceeded the normal range, resulting in various affective disorders and behavior problems, the reaction of the vegetative nerve system was limited to the normal extent, presenting no physical symptoms. In addition to these basic explanations, the location of cerebral alternation and personal disposition should be argued before the differences of clinical features were considered. The varieties in psychiatric manifestations would depend upon the varieties in the correlative action between the cortex and the subcortex within the brain. The cortical excessive discharge of the EEG, resulting from the excessive function of a certain location of the cerebral cortex, might present an explosion of symptom which represents exactly the intrinsic function of the
N. Miyaishi
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location of the cortex. On the other hand, the EEG discharges of centrencephalic nature usually never show this kind of correlation between the location of EEG discharge and the location within the brain. These EEG discharges should be considered as a mediative physiologic indicator that suggests a pathognomonic figure in the mechanism of the connection or the regulation between the physical and affective reactions. SUMMARY The clinical and electroencephalographical observations were performed on the two series of subjects and some relations between the EEG paroxysins of centrencephalic nature and clinical features were obtained.
( I ) One series comprised 154 children with the age-range of six to 10 years complaining of some learning disability. The abnormal EEG paroxysms of centrencephalic nature were found in 3 1 % of them. Behavior deviation and vegetative symptoms were the main clinical symptoms, appearing in 83% and 40% of these children respectively. It was supposed that children with both behavior deviation and vegetative symptoms and also those with vegetative symptoms alone had a close relation with the centrencephalic EEG paroxysms, and that learning disability might result from these two main symptoms. (2) The other series was composed of 50 patients in whom the age varied from 11 to 24 years, mainly 15-16, and 6-14/sec positive spikes were found. The behavior problems of these patients had the qualities which brought more practical sociopathic behaviors, and this was an exact difference from the behavior problems in the former series of children. In addition, vegetative disturbances and affective disorders were observed, and they are considered to relate to
the behavior problems. The vegetative disturbances might play a role as an activating factor and the affective disorders as an underlying factor in the developing process of the behavior problems. Finally, it is concluded that although the fundamental clinical varieties of behavioral, affective and vegetative dysregulations were observed in the patients who had the centrencephalic EEG paroxysms, these three varieties were dependent on one another during the development of the individual patients. REFERENCES 1 Brill, N . Q . and Seidemann, H.: The EEG of normal children, Amer J Psychiat, 98: 250, 1941. 2 Bingley, T.: Mental symptoms in temporal
lobe gliomas, Acta Psychiat Scand, 33: 1, 1958. 3 Cazzullo, E. J.: Psychiatric aspects of epilepsy, Int J Neurol, 1: 53, 1959. 4 Gastaut, H.: So-called psychomotor and temporal epilepsy, Epilepsia, 2: 59, 1953. 5 Henry, C. E.: Positive spike discharges in
6 7
S
9
the EEG and behavior abnormality, In G. H. Glaser (Ed.), EEG and behavior, Basic Book, New York, 315, 1963. Higgins, J. W.: Behavioral changes during intercerebral ejectrical stimulation, A.M.A. Arch Neurol Psychiat, 76: 399, 1956. Hill, D.: EEG in episodic, psychotic and psychopathic behavior: classification of data, EEG Clin Neurophysiol, 4: 419, 1952. Kanner, L.: Child psychiatry, Springfield, Illinois, U.S.A. 1935. Klinkerfuss, G. H. rr al.: Electroencephalographic abnormalities of children with hyperkinetic behavior, Neurology, IS: 883,
1965. 10 Low, N. L.: Electroencephalogram in children, Amer J Dis Child, 65: 898, 1943. 11 Miller, D. L.: School phobia, New York State, J Med, 72: 1160, 1972. 12 Nicholson, J. M. and Knott, J. R.: Sleep EEG’s in psychiatric patients, EEG Clin
Centrencephalic EEG Abnormality Neurophysiol, 9: 375, 1957. 13 Ohara, K.: Suicide in children: a viewpoint from family pathology, Clin Psychiat, 5: 375, 1963, (in Japanese). 14 Schwade, E. D. and Otto, 0.: Homicide as a manifestation of thalamic or hypothalamic disorder with abnormal electroencephalographic findings, Wis Med J, St: 171. 1953. 15 Schwade, E. D. and Geiger, S. G.: Abnor-
mal electroencephalographic findings in severe behavior disorders, Dis Nerv Syst, 17: 307, 1956. 16 Small, J. G.: The six per second spike and
27 3
wave, A psychiatric population study, EEG Clin Neurophysiol, 24: 561, 1968. 17 Stehle, H. C.: Thalamic dysfunction involved in destructive-aggressive behavior directed against persons and property, EEG Clin Neurophysiol, 12: 264, 1960. 18 Stevens, J. R.: Behavior disorder of childhood and the electroencephalogram, Arch Neurol, 18: 160, 1968. 19 Struve, F. A. et al.: Electroencephalographic correlates of suicide ideations and attempts, Arch Gen Psychiat, 27: 363, 1972. 20 Walker, A. E.: Murder or epilepsy, J Nerv Ment Dis, 133: 430, 1961.
Clinical Features Related with Centrencephalic EEG Abnormality Norihiro Miyaishi, M.D. Department of Neurology, Institute of Neurological Science, Tottori University School of Medicine, Yonago INTRODUCTION Main interest is usually concentrated on ictal symptoms when paroxysmal EEG abnormality is found. And this kind of clinical category is identified with some types of epilepsy. Non-ictal or continuous symptom, not coexisting with any type of epileptic symptom, is easily spoken of as epileptoid, interictal or subclinical symptoms, if patients have the similar EEG abnormality seen in epilepsy. The psychical or psychiatric symptom found together with EEG abnormality stimulates usually search-efforts concentrating on personality and psychodynamic mechanism. It seems that EEG abnormality of the patients who have psychical or psychiatric problems scarcely attracts attention. Focal EEG abnormality, like temporal focal discharges, is easily accepted to connect with the psychical symptoms in the conception of epilepsy, and the psychical symptoms are regarded as epileptic nature. But there are many problems still remaining unsolved when the similar psychical or psychiatric symptom is seen in the patient with centrencephalic EEG abnormality. The centrencephalic EEG abnormality, in this paper, comprised the followings; bilateral diffuse synchronous spike and wave, 3-61sec spike and wave, 6/sec small spike and wave, 614/sec positive spikes and bilateral diffuse _____
Received for publication May 14, 1976.
synchronous slow bursts. It is well known that the patient with these EEG discharges, not necessarily suffering from the ictal symptom, has various kinds of symptom of either physical or psychical. However, when the interpretation of the centrencephalic EEG findings as an excessive neuroral discharge is valid, this interpretation can hardly justify that the ictal symptom is the only means to determine the pathophysiological foundation of the electric-clinical correlation. To clarify the clinical features of patients with psychical symptom, one or a few consultations result not rarely in errors, especially when the symptom is related to EEG abnormality. It must be considered, furthermore, that physical and psychical symptoms can be modified in the developmental course of the same individual. For this reason, it may be the best way to see patients from early childhood through the adult period for understanding the clinical characteristics. In this paper, the correlation between the clinical features and EEG findings was studied in patients in the six to 10 and 11 to 24 age brackets. SUBJECTS AND METHODS A total of 204 subjects were available in this study. They were divided into two series. The first series comprised 154 children ranging in age from six to 10 years, the average
N. Miyaishi
264
age being 8.5. They were consulted, because of school underachievements, in order to decide whether special education curriculum could be useful ,or not. Neither physical handicap nor environmental factor was thc cause of bad school records. They were again divided into two groups according to IQ, and one group had 84 children whose 10 was above 90, while the other group of 70 children showed IQ below 85. IQ was measured by Suzuki-Binkt Tests. Besides school underachievements, various physical symptoms together with behavior problems were observed in the 154 children. Their symptoms and behavior deviation were confirmed by the authors and supported by their school teachers and parents. Behavior problems were sorted according to the modified program from Stevens's original one.ln The
15
10
5
quality and quantity of behavior problems were carefully evaluated. The second series of subjects consisted of 50 patients who had been hospitalized once during the previous three years. The agerange was 11 to 24 years with an average of 18. All of them had centrencephalic EEG findings, 6-14/sec positive spikes. The clinical observation was extended from their developmental course through the post-hospitalization period. Particular attention was paid to suicidal attempt and personality and developmental environment to clarify the underlying mechanism of the desire for suicide. EEG's were taken on eight- and 12-channel ink-writing recorders. The activating procedures of hyperventilation, photic stimulation and the intravenous injection of di-
10
numbers I Shortalbntlonspan I Dlrtrutlon a
M
Exploslw
: Clumsy
I
limldlty
i Hvprmnw
*
Aguresrhn Wwttlg
4
:
~awfrurtratlon lmpulrlvb
B
I
8 I
n 7c
lrolrtlon
u i 2 1
' @posMt 1
Stwnmrln Wlthdrwn
* * *
Fig. 1: Varieties and incidence of behavior problems.
Centrencephalic EEG Abnormality phenhydramine at dose level of 1 mg/kg body weight were used. RESULTS
1. The First Series (1)
Varieties and incidence of behavior problems (Fig. 1)
Among 84 children with IQ above 90, 72 (83%) had some varieties. These behavior problems could result from the disorder of attention. Out of 70 children with IQ below 85, 53 (76%) had other varieties of behavior problems. Hypoactivity and clumsiness showed a high incidence of 14 and 1 1 respectively. Although these two were thought to be the usual properties of low intelligent children, they were not rarely found in the present group of children with I0 above 90.
265
ache, abdominal pain, vomiting, increased fever of unknown cause and itching. They recurred in 38% of the children with IQ above 90, and in 43% of those with IQ below 85. Vegetative symptoms and behavior problems in the same individual were common. Thirty-one percent of a total of 154 children suffered from both of them, whereas 9% had the former only.
(3) Varieties of EEG abnormalities (Table 1) Some degree of EEG abnormality was seen in 77% of 154 children. There were borderline or slightly abnormal EEG’s in 50 cases (32%), cortical focal spike (C.F.S.) in I8 (12%), generalized diffuse synchronous in 25 (17%), 6-14 spike and wave (G.S.) positive spike or phantom spike and wave (P(h)S) in 22 (14%), and multi focus (M.F.) in 3. As to the abnormalities of centrencephalic origin, they were seen in 47 children
(2) Associated symptoms (Figs. 2. a, b)
(31 %).
Past history was studied back through the date of children’s birth. Several vegetative symptoms were pointed out, such as head-
(4) The relation between EEG abnormalities and behavior problems The distribution of EEG abnormalities in
Tdal
in
131I
imi
I91 1101
1%)
Table 1: Varieties of EEG Abnormalities
EEG findings
No. %
B . L . 4 1 . abn.
50 (32) 18 i 1 2 j
C.F.S.
\
G.S.
P(h)S.
M.F.
Norm. Total
Behavior Deviation Behavior Deviation Autonomic Symptom
154
B.L.41. abn.; Borderhewslight abnormal
Autonomic Symptom alone no Symptom
3 ( 2) 36 (23)
h 0
=
1.0. >Po
1.0.
< 85
total 84 total 70
Fig. 2: Varieties of clinical symptoms.
C.F.S.;Cortical focal spike G.S.; Generalized bilateral spike and wave P(h)S.; Positive spike or phantom spike and wave M.F.;Multifocus Norm.; Normal
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266
the varieties of behavior problems was illustrated (Fig. I). There was no significant correlation of the EEG abnormalities with a certain behavioral property. The relation between EEG abnormalities and clinical types
(5)
Then, four clinical types were arranged according to whether either or both of behavior problems and vegetative symptoms, or neither, were found in patients. And, the percentage of EEG abnormalities was shown in each clinical type. (Fig. 3) In the type which showed behavior problems only, borderline or slightly abnormal EEG’s were most dominant, having the percentage of 38. On the other hand, the EEG abnormalities of centrencephalic origin were most common in the type with both of behavior problems and vegetative symptoms, and also in the type with vegetative symptoms alone, showing 46% and 43%, respectively. The relation between clinical types and EEG abnormalities
(6)
The proportion of each clinical type in each kind of EEG abnormalities was illustrated. (Fig. 4) The clinical type only with behavior problems shared 58% of borderline or slightly abnormal EEG’s. This type shared also 61 % of cortical focal spikes. On the other hand, the clinical type with both of behavior problems and vegetative symp-
toms occupied 48% of G.S., and also 45% of P(h)S. Fifty-eight percent was shared by the type only with behavior problems in normal EEG category. This finding could suggest that behavior problems which developed only from vegetative symptoms had a close relation to the centrencephalic EEG abnormalities.
2. The Second Series (1)
Varieties and incidence of behavior problems (Table 2)
In 50 patients of this series, there were some varieties of behavior problems. They were school refusal in 14 cases, suicidal attempt in 10, short-range or compulsive behavior and misdeed, etc. These problems usually attracted attention to the underlying sociopathic peculiarities.
(2) Affective aspect (Table 3) The emotional properties of patients were summarized from the overall survey from childhood through the period after their hospital discharge. Anxiety, depressiveness, or aggressiveness became evident, but none of them could be the essential properties of the patients. A psychiatric study was made
B 1.5.1
Abn
Canlrancephallc C F S
Bollador Dwlltlon GS
BCh D N +
Aulon Dlsl
OW
Autonom Dlsl
Na Sympl
Fig. 3: The relation between symptoms and EEG.
PlhlS
Cantlonceph~llc
M f
Norm
Fig. 4: The relation between EEG and
symptoms.
Centrencephalic EEG Abnormality
267
on patients of this series. Neither neurosis nor psychopathy was pointed out. A certain psychological condition, which was not similar to any category of psychosis, was considered in 18 cases.
the reverse was rare. In some stage, both of vegetative symptoms and behavior problems coexisted. They occurred at the same time in some individuals, but independently in the same number of cases.
(3) Varieties of vegetative symptoms and their correlation to behavior problems (Table 4)
(4)
In each individual, physical symptoms, especially vegetative ones were scrutinized in relation to his emotional properties, psychological condition and behavior problems. Chronic headache was noteworthy among vegetative symptoms, being found in 24 patients. The developmental or transitional process of vegetative symptoms and behavior problems was looked over back through his infant period. The results were illustrated on the lower part of Table 4. In the earlier stage, some vegetative symptoms were dominant, whereas in the later stage, behavior problems became evident. Thus, it seemed that vegetative symptoms changed into behavior problems during the course of illness. This correlation was seen in 21 patients and
Table 2: Varieties and Incidence of
Behavior Problems Behavior problems School refusal Suicidal attempt Short-rangecompulsive behavior Misdeed sexual behavior steal Idleness- taciturnity Regression Unsettled employment Eccentricity Psychomotoric excitement Runaway-wandering Hyperactive ( A total of 50 cases)
Ten cases of suicidal attempt
One killed herself and nine were survivals. The age-range of these 10 cases was 15 to 24 years, and nine cases were females. The properties in personality were studied. Egocentricity or self-assertiveness was seen in five cases. But no significant value was given. Intelligence was normal in most cases. Their developinental environment was investigated. Five cases were the youngest child, two were brought up by their grandmothers and two lost either of their parents early in life. Six were schoolgirls and four were workers. The ways used by them were medical drug in five cases, knives in two, automobile in one, and city gas in one. In one remainder, it was unclear how she killed herself. Psychological condition at the time of suicidal attempt was studied. Two cases were impulsive, two had been in anxiety or
Table 3: Affective Properties of 50 Patients with Six and 14 Positive Spikes Anxiety Depressiveness Nervousness Low frustration tolerance Irritability Hypochondry Emotional instability Restlessness Regression Tension Impulsiveness Withdrawn Fear Aggression Ill-humored
12 11 10 9 8 7
5 4 4 3 3 2 2 1 1
-___
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established. If patients have some other symptoms different from epileptic attacks, the clinical significance of the epileptic EEG discharges could not be so clearly determined. There are a good number of patients who show the epileptic EEG discharges but no epileptic attacks. To clarify this kind of clinical feature, a synthetic investigation based on semiology, intelligence, affective or behavioral problems and environmental
depressiveness for a long time, two had been hysteric, and one had some strange consciousness. DISCUSSION When some epileptic manifestations of the classic category of epilepsy are seen in patients with the so-called epileptic EEG discharges, diagnosis as epilepsy would be easily
Table 4: The Mode of Onset of Symptoms Varieties of physicalsymptoms
.
No.
Headache 24 Vomiting 6 Dizziness 5 Insomnia 4 Head congestion 4 Abdominal pain 4 Dyspnea 4 Cenesthesie 4 Irritable colon 3 Urticaria 2 Tinnitus 2 Exhaustion 1 Somnolent 1 Sensation of urinary retention 1 Myalgie 1 Palpitation 1 Unknown febrile 1 Total
Continu- Epious sodic 8
6 1
4 2 1 3 1
1 2
Ictal
-
10
5 5
Unchange- Diver- Changeable sity able 13 2
3 1
2
3
3 4 1 1
1 1 3 1 1 1 1 1
2 1
I
2
4 2 2 1 1 2 1 2 1 1
1
2 1
1 1
1 1
1 1
23
9
12
1 1
33
35
27
The developmental or transitional process of symptoms vegetative symptoms -+ psychical or behavioral problems 21 psychical or behavioral problems -+ vegetative symptoms 3 The appearance of both vegetative and psychical or behavioral prob1ems: at the some period 14 each independently 12 alternatively 2
6
Centrencephalic EEG Abnormality survey is necessary. Paroxysmal seizure discharge of the EEG is nothing more than an excessive neuroral discharge within the brain. Clinical manifestation would be produced from ,the cooperative function of the primary location of the neuroral excessive discharge and its circumferential locations within the brain. The present study was aimed at clarifying new clinical entity other than epilepsy and the meaning of epileptic EEG's in it. Two series of subjects were compared with each other.
269
bursts could not always mean EEG abnormality. These findings should be estimated with every regard to the developmental process of the brain and age distribution.' m Therefore, EEG findings other than paroxysmal seizure discharge were put aside from the consideration in this study. Behavior problems associated with the EEG seizure discharges have been studied with regard to the semiological difference according to the location of cerebral lesion.8 fl It was well known that the temporal cortex could bring out certain behavior problems.2 And there were several works con1. The First Series cerned with the centrencephalic EEG findings. (a) The characteristics of symptoms The properties of behaviors were pointed Behavior problems of the children of this out in those works, and impulsiveness," series were estimated mainly from the qualihyperactivity," psychopathy7 l 2 lfi and agtative and quantitative analysis. This analysis g r e s s i ~ e n e s s and , ~ ~ abnormal behavior probwas useful enough to find up the characterlems14 20 such as stealing and misdeed were istics of the behavior problems of this series where such sociopathic problems as misdeed assumed to correspond to certain EEG findings. But, after all, it was scarcely deterwere scarcely found. mined that what kind of behavioral properIt was concluded that the behavior probties and what type of EEG findings could lems were understood to be limited to the correspond to each other. extent of the estimation. Most children The present study resulted also in negative showed learning disability as a common on this question and no distinctive correlafeature, and it was supposed to result from tion was detected between particular bebehavior problems. The behavior problems havioral properties and certain EEG findwere one of the most principal symptoms in ings. Summarized overall, the most importhis series. Various symptoms concerning tant results were supposed that all the bethe vegetative nervous system were next to havioral properties might correlate definitely behavior problems. These vegetative symptoms were seen in 41 % of the children. The to the mechanism itself from which any type relation between vegetative symptoms and of the centrencephalic EEG abnormalities learning disability or behavior problems was could originate. investigated, paying particular attention to The relation among clinical symptoms, EEG abnormality. behavior problems and vegetative symptoms, and the EEG characteristics were summar(b) The relation between clinical characterized as follows: Children who had behavior istics and EEG findings problems but no vegetative symptoms In the discussion on EEG abnormality, it showed frequently borderline EEG's or is not needless to say that consideration must slightly abnormal EEG's but rarely paroxysbe based on the various points of view. mal seizure discharges. And it is noticeable Dysrhythmic basic waves and slow wave that those who had vegetative symptoms but
270
N. Miyaishi
no behavior problems or those who had both of vegetative symptoms and behavior problems had paroxysmal EEG discharges. especially the centrencephalic EEG findings. It was supposed that the delay of the developmental process of the brain might play an important role in the primary basis of behavioral deviation, and that vegetative symptoms, corresponding directly to the centrencephalic EEG abnormalities, could promote the behavioral deviation with the cooperation of some disorders of consciousness, attention and affection.
series of patients other than school refusal and suicidal attempt. Most of these behavior problems were paroxysms in their nature but non-acquired. The duration of these paroxysms varied in time even in the same individual. A good number of studies suggested the relation between the positive spikes in the EEG and behavioral abnormalities, but the final clinical significance of this positive spikes was not yet established. Henryfi made a historical review on the positive spikes from many previous literatures and described that psychiatrically the positive spikes could hardly show a correspondence with certain particular event of behavior problems. Then, 2. The Second Series he stated that this EEG discharge could be (a) Clinical symptoms more easily expected from clinical petit ma1 Antisocial troubles were a common rea- epilepsy. We found the positive spikes in a son for clinical consultation in young per- wide variety of clinical events, supporting his sons whose EEG's were abnormal. The opinion to some extent. To clarify the parsubjects of this series, selected from those, ticular role of the positive spikes, a longwere admitted to our hospital for further term study would be necessary on every paphysical and psychical studies. In addition tient back through his birth to follow up to sociopathic behavioral deviations, affec- contact, because some symptom may change tive disorders and vegetative disturbances into other symptom during the course of his were the main clinical symptoms. The be- growth. havioral deviations produced some affairs which forced the patients into maladjust- (b) Some relations among the varieties of clinical symptoms ment at home, school or business. This The relation between one another of three was exactly different from the behavior problems of the children aged below 10. The clinical varieties, vegetative symptoms, affecsocial affairs they committed were composed tive disturbances and behavior problems was of school refusal in 11 patients, suicidal shown in Table 4. In case patients were attempt in 10 and misdeed in four. The mis- younger, headache and abdominal pain were deed included sexual delinquency and steal- commoner than affective or behavioral dising. In I 1 cases of school refusal who were orders, whereas the latter became commoner 13-17 years old, some complex develop- when the patients were older. Several pamental history, domestic trouble or bad re- tients had been admitted to hospital with the lation between friends were found. These chief complaints of some vegetative symptroubles have attracted some workers' atten- toms when they were younger and were tion" as an exact cause of school refusal. again admitted several years later because of But some other causal reason should be con- behavior problems. Vegetative symptoms were non-ictal on sidered in our cases of school refusal. The same causal mechanism seen in the cases of some occasions and ictal on other occasions suicidal attempt was assumed. Several kinds in most patients and not always fixed on a of behavior problems were found in this certain same organ. In the patients who had
Centrencephalic EEG Abnormality the positive spikes, vegetative symptoms were not yet a certain factor determining whether they were primary or derivative symptoms. But this question did not deny that the vegetative symptoms could play an essential role to produce the behavior problems or the excessive affective expression. Suicidal attempt gave the approach for the mechanism of the behavioral deviation and the positive spikes. Twenty percent of the patients with the 6-1 4/sec positive spikes tried suicidal attempt. Several events, personality distortion or psychological conflicts could be considered as a direct cause of suicidal attempt. But these events were seen more widely not only in suicidal attempt but also in other behavior problems. Physical stress resulting from head injury or vegetative dysfunction was also thought to activate the suicidal attempt. But, it was pointed out as the most interesting fact that some cases experienced a strange feeling, a clouding of consciousness or a psychomotor like an episode at the exact time when they performed suicidal attempt, and that in other cases serious affective disorders were observed. Nobody was diagnosed as depression. A case died from suicidal attempt. Most cases had little volition for a sure deathlXand unadequate tools were chosen. It was concluded that the suicidal attempt for them was something other than the act of killing oneself. But it was supposed to result from particular types of affective disorders or behavior problems."' As the modern convenience advances more, the number of people with social maladjustment may increase. This serious social problem must be studied not only from the viewpoint of social pathology but also from the biological viewpoint. The abnormal EEG discharges of centrencephalic nature proposed an important biological indicator for affective and behavioral abnormalities. Three clinical varieties, vegetative symptoms, affec-
27 1
tive disorders and behavior problems might be thought to result from a certain pathological process within the brain. And this pathological process might ejaculate occasionally the EEG discharges of centrencephalic nature. To explain the pathophysiology of the affective disorders of the patients with the centrencephalic EEG phenomenon, the followings appeared to be necessary. (1) The clinical symptoms resulted from both physical and affective reactions. On some occasions, one of the two reactions exceeded the normal range and the other did not, and on the other occasions, the latter exceeded the normal limits but the former did not.
(2) Many activating factors were supposed in physical symptoms and the duration of the symptoms varied time to time in the same individual patients. This suggests that when the overreaction of the vegetative nervous system resulted in the physical symptoms, the affective reaction was limited to the normal extent. (3) Reversely, when the affective reaction exceeded the normal range, resulting in various affective disorders and behavior problems, the reaction of the vegetative nerve system was limited to the normal extent, presenting no physical symptoms. In addition to these basic explanations, the location of cerebral alternation and personal disposition should be argued before the differences of clinical features were considered. The varieties in psychiatric manifestations would depend upon the varieties in the correlative action between the cortex and the subcortex within the brain. The cortical excessive discharge of the EEG, resulting from the excessive function of a certain location of the cerebral cortex, might present an explosion of symptom which represents exactly the intrinsic function of the
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location of the cortex. On the other hand, the EEG discharges of centrencephalic nature usually never show this kind of correlation between the location of EEG discharge and the location within the brain. These EEG discharges should be considered as a mediative physiologic indicator that suggests a pathognomonic figure in the mechanism of the connection or the regulation between the physical and affective reactions. SUMMARY The clinical and electroencephalographical observations were performed on the two series of subjects and some relations between the EEG paroxysins of centrencephalic nature and clinical features were obtained.
( I ) One series comprised 154 children with the age-range of six to 10 years complaining of some learning disability. The abnormal EEG paroxysms of centrencephalic nature were found in 3 1 % of them. Behavior deviation and vegetative symptoms were the main clinical symptoms, appearing in 83% and 40% of these children respectively. It was supposed that children with both behavior deviation and vegetative symptoms and also those with vegetative symptoms alone had a close relation with the centrencephalic EEG paroxysms, and that learning disability might result from these two main symptoms. (2) The other series was composed of 50 patients in whom the age varied from 11 to 24 years, mainly 15-16, and 6-14/sec positive spikes were found. The behavior problems of these patients had the qualities which brought more practical sociopathic behaviors, and this was an exact difference from the behavior problems in the former series of children. In addition, vegetative disturbances and affective disorders were observed, and they are considered to relate to
the behavior problems. The vegetative disturbances might play a role as an activating factor and the affective disorders as an underlying factor in the developing process of the behavior problems. Finally, it is concluded that although the fundamental clinical varieties of behavioral, affective and vegetative dysregulations were observed in the patients who had the centrencephalic EEG paroxysms, these three varieties were dependent on one another during the development of the individual patients. REFERENCES 1 Brill, N . Q . and Seidemann, H.: The EEG of normal children, Amer J Psychiat, 98: 250, 1941. 2 Bingley, T.: Mental symptoms in temporal
lobe gliomas, Acta Psychiat Scand, 33: 1, 1958. 3 Cazzullo, E. J.: Psychiatric aspects of epilepsy, Int J Neurol, 1: 53, 1959. 4 Gastaut, H.: So-called psychomotor and temporal epilepsy, Epilepsia, 2: 59, 1953. 5 Henry, C. E.: Positive spike discharges in
6 7
S
9
the EEG and behavior abnormality, In G. H. Glaser (Ed.), EEG and behavior, Basic Book, New York, 315, 1963. Higgins, J. W.: Behavioral changes during intercerebral ejectrical stimulation, A.M.A. Arch Neurol Psychiat, 76: 399, 1956. Hill, D.: EEG in episodic, psychotic and psychopathic behavior: classification of data, EEG Clin Neurophysiol, 4: 419, 1952. Kanner, L.: Child psychiatry, Springfield, Illinois, U.S.A. 1935. Klinkerfuss, G. H. rr al.: Electroencephalographic abnormalities of children with hyperkinetic behavior, Neurology, IS: 883,
1965. 10 Low, N. L.: Electroencephalogram in children, Amer J Dis Child, 65: 898, 1943. 11 Miller, D. L.: School phobia, New York State, J Med, 72: 1160, 1972. 12 Nicholson, J. M. and Knott, J. R.: Sleep EEG’s in psychiatric patients, EEG Clin
Centrencephalic EEG Abnormality Neurophysiol, 9: 375, 1957. 13 Ohara, K.: Suicide in children: a viewpoint from family pathology, Clin Psychiat, 5: 375, 1963, (in Japanese). 14 Schwade, E. D. and Otto, 0.: Homicide as a manifestation of thalamic or hypothalamic disorder with abnormal electroencephalographic findings, Wis Med J, St: 171. 1953. 15 Schwade, E. D. and Geiger, S. G.: Abnor-
mal electroencephalographic findings in severe behavior disorders, Dis Nerv Syst, 17: 307, 1956. 16 Small, J. G.: The six per second spike and
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wave, A psychiatric population study, EEG Clin Neurophysiol, 24: 561, 1968. 17 Stehle, H. C.: Thalamic dysfunction involved in destructive-aggressive behavior directed against persons and property, EEG Clin Neurophysiol, 12: 264, 1960. 18 Stevens, J. R.: Behavior disorder of childhood and the electroencephalogram, Arch Neurol, 18: 160, 1968. 19 Struve, F. A. et al.: Electroencephalographic correlates of suicide ideations and attempts, Arch Gen Psychiat, 27: 363, 1972. 20 Walker, A. E.: Murder or epilepsy, J Nerv Ment Dis, 133: 430, 1961.
