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Aggression and epilepsy
Journal of Psychosomatic Research, Vol. 13, pp. 229 to 236. Pergamon Press, 1969. Printed in Northern Ireland
AGGRESSION
AND
EPILEPSY
DAVID C. TAYLOR*
IF THEREare specific cerebral mechanisms concerned with the regulation of aggressive behaviour in man these mechanisms might be amenable to study through various types of cerebral dysfunction. The more stereotyped the form and the more focal the location of the dysfunction the better the model would be. There are several advantages to studying the model offered by chronic epilepsy. The location and severity of the disorder can be assessed to some extent, so that these variables can be related to their effect on personality. The chronic course allows consideration of the duration of the dysfunction, as well as variations of effect with its age of onset. And it usually allows the sufferer to attempt, at least, to engage in the business of everyday life, so that the individual reveals his personality in the context of society at large. In addition, in recent years some epilepsy has been treated by standardised cerebral surgery the effects of which can be assessed. The traditional belief that 'epileptics' are unduly 'aggressive' has been refined into a finding, frequently repeated, that patients with temporal lobe epilepsy are unusually prone to mental disorders and that amongst these disorders overtly aggressive and rude behaviour is the most common single entity. The neurophysiological basis of this type of epilepsy was developed alongside other significant research into the functions of the limbic system which were outlined in Papez [1] theories of the mechanism of emotion and in the work of Kluver and Bucy [2] in the monkey. Thus a parallel might be drawn between the effects of focal functional disturbances in the temporal lobe in man together with the effects of its extirpation, and the results of stimulation and ablation of the homologous regions in animals. There are several serious limitations to the relevance of these studies to man. There is, as has been mentioned previously by Hill [3] the serious problem of interspecies differences. There is the problem that in stimulation studies marked variations in behaviour can be produced from zones only millimetres apart so that no true parallel can be found in the relatively crude electro-physiological studies in man. There is the problem of what constitutes aggression in man. The animal experimentalist has chosen to study well defined observable units of behaviour the frequency of which is recordable. The psychiatrist usually has a loosely defined notion of aggression often depending on subjective judgment or on behaviour reported at second hand. Even restricting the meaning of aggression to overtly aggressive displays all that emerges from many reports is that a proportion of epileptics have a troublesome bad temper. Whether this is on the same continuum as the passivity-aggressiveness shown in agonistic displays in animals or whether bad temper can usefully be separated from the more sophisticated, displaced, sublimated aspects of aggression in human psychology remains a matter for speculation. From the neurophysiological * H o n . C o n s u l t a n t Psychiatrist, Park Hospital for Children, Old R o a d , H e a d i n g t o n , Oxford; a n d Medical R e s e a r c h Officer, H u m a n D e v e l o p m e n t R e s e a r c h U n i t , University o f Oxford. 229
230
DAWD C. TAYLOR
viewpoint the variety of behaviours allowable as aggressive according to the definition of Dollard et al. [4], and the alternatives for displaced aggression apparent in Freudian psychology, are retrogressive since it is probable that a wider range of mechanisms is involved in the selection of these complex responses than would be necessary for the exhibition of any given satisfactorily defined aggressive act. Thus a broad enough definition of aggression will frustrate any correlation between the locus of a cerebral abnormality and the personality. In the same way, despite the interest of some individual cases, for heuristic purposes the ictus itself cannot be viewed as an aggressive act. For these reasons the relationship between 'aggression' and 'epilepsy' will be explored through studies where there was a reasonably limited definition of aggression and where the nature of the epilepsy and its accompanying electrical disturbances was carefully described and was referable to those limbic areas which have excited most interest. Whilst no study made prior to the description of psychomotor epilepsy by Gibbs, Gibbs and Lennox [5] has the precision of electroencephalographic support, it is probable, from descriptive accounts, that the 'petit mal' of Falret [6] in which the patient felt overwhelmed, the helpless victim of violent urges, and the 'psychic epilepsy' of the late 19th century, in which there were sudden compulsions to violent verbal or physical outburst, both occurred in patients subject to temporal lobe discharges. Violence was a feature of the episodic, short duration, epileptic mania described by Gowers [7]. Instances of violent actions during automatisms are evident in several of the case histories cited by Jackson [8]; for example, the young boot-black who threw his shoe-box at a policeman was fined for his first offence but was later sent to a lunatic asylum. From a different starting point Davenport [9] concluded that violent temper was inherited especially in families with epileptic members. In an early study of the electroencephalographic correlates of psychopathic personality, Hill and Watterson [I0] confirmed Davenport's finding by showing that a family history of bad temper was three times more common in aggressive than nonaggressive psychopaths and indeed had a firmer hereditary basis than epilepsy itself in their patients. Using Schneider's definition of psychopathy with Henderson's sub groups they showed, by given EEG criteria, that an abnormal EEG existed in 65 per cent of their aggressive psychopaths as compared with 32 per cent of the inadequate personalities, and 15 per cent of their controls. The EEG montage at that time would not allow precise localisation of these abnormalities but the study did suggest a neurophysiological basis to abnormal behaviour. "One can have little doubt that an abnormal EEG constitutes for its possessor a handicap in the business of biological adaptation, failure of which may show itself as in our present series in undesirable, asocial behaviour . . . . In view of the similarity between the aggressive behaviour of psychopaths and the normal bad temper response to frustration in young children the suggestion that the abnormality in the EEG in these cases is produced by a failure of development in the central nervous system is very tempting. It fits with our psychiatric, biological and social conception of psychopathic personalities". Gibbs, Gibbs and Fuster [11] explored the personality features of 300 patients with psychomotor epilepsy selected by EEG criteria. Forty two per cent showed severe personality disorder and in addition 3 per cent had attempted suicide and 9 per cent were psychotic. This group of patients, the authors remark, "were poorly
Aggression and epilepsy
231
tolerated by the community". They concluded that "in view of the high association of personality disorder with psychomotor epilepsy it seems reasonable to attribute much of what has been called the epileptic personality to disturbance of the anterior temporal areas". That the relevant abnormality was not limited to the anterior region of the lobe in mentally disturbed patients was evident in the work of Rey, Pond and Evans [12] who culled 59 cases with no obvious aetiological factor from a search of 3,000 EEGs for patients with temporal lobe discharges. Sixty eight per cent of these patients conformed to a description of shy, egocentric and irritable and 49 per cent showed overt pathological aggression. Over 50 per cent had a family history of mental disorder. "They are children in their EEGs and their personalities, though chronologically grown up", they wrote, and they pursued the explanatory hypothesis set up earlier by Hill that the essential defect was a failure of cerebral maturation. The abnormalities were most evident in the posterior part of the left temporal lobe, from which, according to Grey Walter, the theta activity disappears last in normal infants. This lateralisation was supported in their 'epileptic' patients by the preponderance of verbal discrepancies in the Wechsler tests. From a later study by Hill [13] it would seem that whilst anterior foci are more likely to be associated with epilepsy and disturbances of consciousness, the more posterior foci are more frequently associated with abnormal personality, psychopathic aggression, and antisocial behaviour. These findings are confirmed in the work of Hughes et al. [14] who found that infrequent grand mal, autonomic changes, and psychic manifestations as well as behaviour disorders were associated with a more posterior locus. Where the EEG abnormalities were bilateral they tended to be more obvious on the left side. The authors believed that the posterior loci were associated with hippocampal lesions and the anterior loci with amygdala damage. Gastaut [15] too believed that the hippocampal form of temporal lobe epilepsy was the most common and most associated with behaviour disorders. These findings would be consistent with the neuropathology of temporal lobe epilepsy where the most common lesion, mesial temporal sclerosis, most regularly affects the hippocampus [16, 17]. In 1953 Hill [18] dismissed the idea that epilepsies of central origin and those of focal origin outside the temporal lobes had any specific psychological aspects since he believed that when seen in psychiatric clinics such patients were usually of low I.Q. and poor social background. Such a view of the general effects of poor environment was amply justified by the study of Grunberg and Pond [19] who showed that the incidence of disturbed background was far higher in the general run of epileptics with behaviour disorder than in those without. It must, however, be remembered that the incidence of disturbed backgrounds in patients with temporal lobe epilepsy is notably high. In our own recent study [20] 40 per cent of patients had at least one first degree relative with mental disorder, 27 per cent were bereft of at least one parent before the age of 15 years, and 36 per cent were not domiciled in their appropriate homes. It was Bailey who first performed temporal lobectomy for the relief of epilepsy in patients 'whose need for help was desperate'. These patients differed from Penfield's in that the abnormalities in the temporal lobes were presumed to be purely functional. In this country Mr. Murray Falconer in association with Professor Hill began performing temporal lobectomies in 1952. The high prevalence of psychiatric 3
232
DAVID C. TAYLOR
disorders in the patients is evident in the published studies emanating from this work and indeed, it has been accepted that, at times, personality disturbances which had resisted treatment were an added reason for operation [21]. Character disorders of the type already described were the most common single psychiatric entity; 18 of the first 27 patients reported on were so affected [22], and of these at least 11 were aggressive. Post operative depression, interpreted as a 'turning-in' of the aggressive behaviour, was common, 5 of these patients needed ECT. James [23] showed that in 28 per cent of the first 72 patients operated aggression dominated the clinical picture. All but one of these patients had been either excluded from school, or admitted to hospital, or appeared in court for aggressive behaviour. In all but one case the epilepsy had started before the age of 13 and the mean age at onset, at 6.4 yr, was 8 yr less than in his marginal/normal group. The prognosis for this group was excellent, and strongly related to relief from epilepsy. In social terms the effect of surgery was to change the number considered well adjusted from 1 preoperatively to 14 out of 20 at follow-up. The subject was further extended by Serafetinides [24] in a series of 100 patients. He agreed that aggression was a feature of those with early onset epilepsy and that these patients also tended to be operated on earlier. But he found a substantial predominance of males in the aggressive group and 25 of the 36 aggressive patients were operated on the left side. In a recent study [20] we were concerned mainly to assess the effect of operation on the social adjustment of our patients but a clinical assessment of personality was also made retrospectively from the pre-operative notes and again at the follow-up interview. One hundred consecutive English-speaking patients, including 50 never previously reported, were considered. Pre-operatively 48 were considered psychopathic according to the same criteria used by Hill and Watterson [10] but 10 had an additional diagnosis. These 48 patients were characterised by being predominantly of male sex (38 out of 48 compared with 25 of the remaining 52), they showed an excess in the lower social classes, were of lower full scale I.Q. and had poorer interpersonal relationships. They were younger at the time of onset of their epilepsy and 28 of the 48 were operated on the left side compared with 20 of the remaining 52. (/9 < 0-05, Chi Squared = 3.9). Twenty seven of these patients were noted as showing overt aggression, not merely as some part of their life histories but as a feature of their current pre-operative mental state. Examination of these patients revealed that their parents and to some extent they themselves were in excess in the lower social classes. The full scale I.Q. was significantly lower than for non-aggressive patients, and one third of them compared to one fifth of the remainder had required special schooling or had their school careers grossly disrupted (see Table 1.]. Forty one per cent had been permanently separated from at least one parent before the age of 15 (Table 1). Their general social adjustment was extremely poor. In the figure the social adjustment scores are a total of 7 items of social adjustment and are arrayed each in a locus determined by the pre and post operative score. Whilst aggressive patients are grossly under-represented in those reasonably adjusted pre-operatively they contribute equally with the remainder to those who improved. Of the 7 individual items which made this total score the greatest difference between aggressive patients and the rest came in their intra-family relationships (Table 2). There were important
Aggression and epilepsy
233
TABLE I.--BACKGROUND FACTORS Aggressive
Others
%
%
N = 27
N=
66 93 48 41 41 59 33
Operated before 24 years of age Age of onset epilepsy 1st or 2nd decade Parental social class 4,5 or 0 F.S.I.Q. 89 or less Bereft before age 15 Patients' social class 4,5 or 0 Schooling, special or disturbed
37 71 27 23 22 40 21
CHANGES IN I N D I V I D U A L SOCIAL ADJUSTMENT SCORES P R E - T O - P O S T OPERATIVE RATING SOCIAL ADJUSTMENT 15
10
~,~ Stayed • Good •4 • •••k 0
•
POST-OPERATIVE 20
b
OQ• ~ 1 •
•
30
25
Worsened from Nor mdl SCOre
(22)
32
(12)
©
•
>
D% 00
•0 O
•
•0
• O
0
%
O D
••
0
20 •0 0
O•
•
•
•
©.• ©,
•
m
2~ ,~
0
. ll'O•
© 0 •
"'4
IL
•
•
25
© 0
?,
O
Improved IO Normal Score
k
•
m
(28)
0 • •4• • 0 "• 0•0
o S,o.o~g. (37>
AGGRESSIVE NON-AGGRESSIVE
0 •
FIG. 1. Pre-operative social score: Below 15 Above 15
Aggressive 4 23
Others 30 43
Chi Squared = 4.95 p < 0.05 Post-operative social score: Below 15 Above 15
Aggressive
Others
I1 16
40 33
Chi Squared = 0.636
N.S.
•
" "-,,
73
Chi squared • 7"02 5"07 4"43 3"86 3"54 3"03 1"13
234
DAVID C. TAYLOR TABLE 2.---INDIVIDUAL ITEMS OF SOCIAL ADJUSTMENT
(maximum score = 5)
Family relationships 1 or 2 Use of leisure 1 or 2 Non-family relationships 1 or 2 Never institutionalised Domiciled at home Work adjustment 1 or 2 Sexual adjustment 1 or 2
Aggressive % N = 27
Others % N ~ 73
Chi squared*
15 26 19 41 52 22 30
52 45 40 60 69 34 27
9"7 3-69 3"06 3-03 2-36 1"3 0'05
* Yates correction where one cell was 5 or less. (For a full description of the protocols see Taylor and Falconer [201.) differences in non-family relationships, the use made of leisure and the extent of institutionalisation suffered. There was no difference between the sexual adjustment of the aggressive and non-aggressive patients (Table 2). It was noted that the aggressive patients were more frequently operated upon in their late teens and early twenties and the 9 patients who improved their social scores to below 15 were all operated in the decade between 16 and 26. In this sub group, however, left and right sided operations are equally represented, outcome for seizures and the pathological findings were the same as in the whole series. There are several conclusions to be drawn. Firstly although 'aggressiveness' is rather difficult to define the consistent incidence of about one third in these studies, separately made by 5 different author groups, suggests that it is a distinguishable feature in these patients. That this is not entirely parochial is confirmed by the 38 per cent incidence in the survey by Preston and Atack [25] and the 36 per cent incidence in Ounsted, Lindsay and N o r m a n ' s study [26]. Secondly although these patients all suffered focal, temporal lobe dysfunction only one third w e r e so affected. The consensus of several studies is that those affected tend to be of male sex, low class, low intelligence, and more frequently disturbed on the left side of the brain. The importance of left temporal lobe damage has recently been emphasized in a variety of studies [27-29]. Thirdly these factors can be brought together in a coherent way. Early onset epilepsy brings a child to specialist attention at an age when conduct disorders are the rule for disturbed children, before paranoid and depressive mechanisms are used, and they are brought to operation at a stage in their development when their aggression is out of hand. Our own current research is suggesting that epilepsies following on prolonged convulsions either 'febrile' or in response to cerebral infection tend to damage the left hemisphere more before the age of 2 years and the right hemisphere more thereafter. Thus in a group of patients with early onset epilepsy the incidence of left cerebral damage would tend to be maximised. In addition, cerebral damage sustained young is more 'destructive' of I.Q. than when sustained older. Further the vast majority of temporal lobe epilepsy of onset before 4 yr is due to mesial temporal sclerosis. Thus the good prognosis which is generally given for aggressive patients could be a product of the generally good prognosis for patients with this lesion whether aggressive or not [17]. In our own study [20] whilst it was found that overt pathological aggression was reduced there was no general tendency towards 'taming' and the relief of mental disorders seemed to come, though not invariably, with relief of epilepsy.
Aggression and epilepsy
235
O n the other h a n d alternative responses to frustration and social failure are frequent in the long term follow-up o f these patients. These need not be interpreted as a redirection o f libidinal energy but as responses to continuing frustration. In a mean follow-up o f 5 yr in our own series o f 100 patients, 37 had a further period o f mental hospital treatment, 5 per cent o f the patients had committed suicide, and a further 2 had performed ritual self mutilations. This suicide rate is only comparable with that in other less selected series o f epileptics [30, 31]. N o evidence could be found, and clinical experience does n o t suggest, that any f o r m o f agonistic display occurs in the course o f a seizure other than a u t o n o m i c changes [32]. Williams [33] described only one patient in a series o f 100 for w h o m anger was an aura. It seems in the light o f this review more parsimonious to conclude that aggressiveness in these patients is less the result o f interference with mechanisms specifically controlling aggressive behaviour than that the defect is one o f learning. They have m a n y reasons to fail to learn; they are damaged early, in structures o f vital significance to learning, their social origins suggest that example and training might be defective. Schooling is disrupted and institutionalisation frequent. This learning failure is evident in inappropriate social responses which are misinterpreted as aggressive releasing the causal chain o f reaction and expectation. It will constitute a major source o f frustration a m o n g s t the wide variety o f frustrations contingent u p o n being epileptic [34]. It is essential to realize that perhaps the most " p a t h o l o g i c a l " aspect o f this overtly aggressive behaviour is its failure as a useful social mechanism. Acknowledgements--I am grateful to Mr. Murray A. Falconer for his support and encouragement
in studying his patients at the Guys-Maudsley Neurosurgical Unit. The basic data were collected during the tenure of a grant given jointly by the Governors of Guys, and the Royal Bethlem and Maudsley Hospitals. The author is currently Medical Officer in the Human Development Research Unit of the University of Oxford, which is supported by the Department of Education and Science and the Department of Employment and Productivity. REFERENCES 1. PAPEZJ. W. A proposed mechanism of emotion. Archs. Neurol. Psychiat. 38, 725 (1937). 2. KLLWERH. and Buoy P. C. Preliminary analysis of the functions of temporal lobes in monkeys. Archs. Neurol. Psychiat. 42, 979 (1939). 3. HILLD. In The Natural History of Aggression. Carthy J. D. and Ebling F. J. (Eds). Academic Press, London (1964). 4. DOLLARDJ., DOOB L. W., MILLERN. E., MOWRERO. n. and SEARSR. R. Frustration and Aggression, Yale University Press (1939). 5. GraBs F. A., GIBBSE. L. and LENNOXW. G. Epilepsy: a paroxysmal cerebral dysrhythmia. Brain 60, 377 (1937). 6. FALRETJ. De l'6tat mental des 6pileptiques. Archs. G~n. M~d. 16, 666; 17, 461 ; 18, 423 (1860, 1861). 7. GOWERSW. R. Epilepsy and Other Chronic Convulsive Disorders, Churchill, London (1881). 8. JACI(SONJ. H. Temporary mental disorders after epileptic paroxyms. In Selected Writings of John Hughlings Jackson, p. 119, James Taylor (Ed). Staples Press (1958). 9. DAVENPORTC. The feebly inhibited: violent temper and its inheritance. J. Nerv. Ment. Dis. 42, 593 (1915). I0. HILL J. D. and WATTERSOND. Electroencephalographic studies of psychopathic personalities. J. NeuroL Paychiat. 5, 47 (1942). 11. GIBBSE. L., GIBBSF. A. and FtrSTERB. Psychomotor epilepsy. Archs. Neurol. Psychiat. 60, 331 (1948). 12. REY H., PONDD. A. and EVANSC. Clinical and electroencephalographic studies of temporal lobe function. Proc. R. Soc. ivied. 42, 891 (1949).
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DAVID C. TAYLOR
13. HILL D. EEG in episodic psychotic and psychopathic behaviour: a classification of data. Electroenceph. Clin. Neurophysiol. 4, 419 (1952). 14. HUOHESJ. R., SCHLAGENHAtrFFR. E., CtJRTINM. J. and BROWNV. F. Electroclinical correlation in temporal lobe epilepsy with emphasis on inter-areal analysis of the temporal lobe. Electroeneeph. Clin. Neurophysiol. 13, 333 (1961). 15. GASTAtrrH. So-called 'psychomotor' and 'temporal' epilepsy. Epilepsia 2, 59 (1953). 16. MAR6ERISONJ. H. and CORSELLISJ. A. N. Epilepsy and the temporal lobes; a clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain 89, 499 (1966). 17. FALCONERM. A. and TAYLORD. C. Surgical treatment of drug resistant temporal lobe epilepsy due to mesial temporal sclerosis: etiology and significance. Archs. Neurol. 19) 353 (1968). 18. HILL D. Psychiatric Disorders of Epilepsy, Med. Press. 20, 473 (1953). 19. GRtmBER6 F. and POND D. A. Conduct disorders in epileptic children. J. Neurol. Neurosurg. Psychiat. 20, 65 (1957). 20. TAYLORD. C. and FALCONERM. A. Changes in clinical, socio-economic and psychological adjustment after temporal lobectomy for epilepsy. Br. J. Psychiat. 114, 1247 (1968). 21. FALCONERM. A., HILL D., MEYERA. and WILSONJ. L. Clinical, radiological and EEG correlations with pathological changes in temporal lobe epilepsy and their significance in surgical treatment. Temporal Lobe Epilepsy, pp. 369-410, Baldwin M. and Bailey P. (Eds). Chas. C. Thomas, Springfield, Ill. (1958). 22. HILL J. D., POND D. A., MrrCHELL W. and FALCONERM. A. Personality changes following temporal lobectomy for epilepsy. J. Ment. Sci. 103, 18 (1957). 23. JA~IESI. P. Temporal lobectomy for psychomotor epilepsy. J. Ment. Sci. 106, 543 (1960). 24. SERArETINIOESE. A. Aggressiveness in temporal lobe epilepsies and its relation to cerebral dysfunction and environmental factors. Epilepsia 6, 33 (1965). 25. PRESTOND. W. and ATACICE. A. Temporal Lobe Epilepsy: a clinical study of 97 cases. Can. Med. Assoc. J. 9, 1256 (1964). 26. OUNSTEDC., LrNDSAYJ. and NORMANR. Biological Factors in Temporal Lobe Epilepsy, Clinics in Developmental Medicine, No. 22, Heineman, London (1966). 27. FLOg HENRYP. Psychosis and Temporal Lobe Epilepsy. M.D. Thesis, Edinburgh University, unpublished. 28. LISHMANW. A. Psychiatric disability after head injury: the significance of brain damage. Proc. R. Soc. Med. 59, 261 (1966). 29. MNt;r,.HINS. S. and DINABtrRGE. Y. Epileptiform manifestations in early right sided and left sided lesions of the brain in children. Zh. Nevropat. Psikiat. Korsakov. 65, 1073 (1965). (Excerpta Medica, English summary). 30. LtrND M. Die Mortalitiit yon Epileptikern, Sonderdr. Medsche Sachverst (1968). 31. KROHNW. Causes of death among epileptics. Epilepsia 4, 315 (1963). 32. GLooR P. Aggression and Defense. Neural Mechanisms and Social Patterns. UCLA Forum in Medical Science No. 7, 118, Clemente C. D. and Lindsley D. B. (Eds). Univ. Calif. Press (1967). 33. WILLthMSD. The gtructure of emotions reflected in epileptic experience. Brain 79, 29 (1956). 34. TAYLORD. C. Some psychiatric aspects of epilepsy. Paper given to the Conference "The Clinical Significance of the Temporal Lobe", Royal College of Physicians and Surgeons of Glasgow, March, 1968. In Press.
AGGRESSION
AND
EPILEPSY
DAVID C. TAYLOR*
IF THEREare specific cerebral mechanisms concerned with the regulation of aggressive behaviour in man these mechanisms might be amenable to study through various types of cerebral dysfunction. The more stereotyped the form and the more focal the location of the dysfunction the better the model would be. There are several advantages to studying the model offered by chronic epilepsy. The location and severity of the disorder can be assessed to some extent, so that these variables can be related to their effect on personality. The chronic course allows consideration of the duration of the dysfunction, as well as variations of effect with its age of onset. And it usually allows the sufferer to attempt, at least, to engage in the business of everyday life, so that the individual reveals his personality in the context of society at large. In addition, in recent years some epilepsy has been treated by standardised cerebral surgery the effects of which can be assessed. The traditional belief that 'epileptics' are unduly 'aggressive' has been refined into a finding, frequently repeated, that patients with temporal lobe epilepsy are unusually prone to mental disorders and that amongst these disorders overtly aggressive and rude behaviour is the most common single entity. The neurophysiological basis of this type of epilepsy was developed alongside other significant research into the functions of the limbic system which were outlined in Papez [1] theories of the mechanism of emotion and in the work of Kluver and Bucy [2] in the monkey. Thus a parallel might be drawn between the effects of focal functional disturbances in the temporal lobe in man together with the effects of its extirpation, and the results of stimulation and ablation of the homologous regions in animals. There are several serious limitations to the relevance of these studies to man. There is, as has been mentioned previously by Hill [3] the serious problem of interspecies differences. There is the problem that in stimulation studies marked variations in behaviour can be produced from zones only millimetres apart so that no true parallel can be found in the relatively crude electro-physiological studies in man. There is the problem of what constitutes aggression in man. The animal experimentalist has chosen to study well defined observable units of behaviour the frequency of which is recordable. The psychiatrist usually has a loosely defined notion of aggression often depending on subjective judgment or on behaviour reported at second hand. Even restricting the meaning of aggression to overtly aggressive displays all that emerges from many reports is that a proportion of epileptics have a troublesome bad temper. Whether this is on the same continuum as the passivity-aggressiveness shown in agonistic displays in animals or whether bad temper can usefully be separated from the more sophisticated, displaced, sublimated aspects of aggression in human psychology remains a matter for speculation. From the neurophysiological * H o n . C o n s u l t a n t Psychiatrist, Park Hospital for Children, Old R o a d , H e a d i n g t o n , Oxford; a n d Medical R e s e a r c h Officer, H u m a n D e v e l o p m e n t R e s e a r c h U n i t , University o f Oxford. 229
230
DAWD C. TAYLOR
viewpoint the variety of behaviours allowable as aggressive according to the definition of Dollard et al. [4], and the alternatives for displaced aggression apparent in Freudian psychology, are retrogressive since it is probable that a wider range of mechanisms is involved in the selection of these complex responses than would be necessary for the exhibition of any given satisfactorily defined aggressive act. Thus a broad enough definition of aggression will frustrate any correlation between the locus of a cerebral abnormality and the personality. In the same way, despite the interest of some individual cases, for heuristic purposes the ictus itself cannot be viewed as an aggressive act. For these reasons the relationship between 'aggression' and 'epilepsy' will be explored through studies where there was a reasonably limited definition of aggression and where the nature of the epilepsy and its accompanying electrical disturbances was carefully described and was referable to those limbic areas which have excited most interest. Whilst no study made prior to the description of psychomotor epilepsy by Gibbs, Gibbs and Lennox [5] has the precision of electroencephalographic support, it is probable, from descriptive accounts, that the 'petit mal' of Falret [6] in which the patient felt overwhelmed, the helpless victim of violent urges, and the 'psychic epilepsy' of the late 19th century, in which there were sudden compulsions to violent verbal or physical outburst, both occurred in patients subject to temporal lobe discharges. Violence was a feature of the episodic, short duration, epileptic mania described by Gowers [7]. Instances of violent actions during automatisms are evident in several of the case histories cited by Jackson [8]; for example, the young boot-black who threw his shoe-box at a policeman was fined for his first offence but was later sent to a lunatic asylum. From a different starting point Davenport [9] concluded that violent temper was inherited especially in families with epileptic members. In an early study of the electroencephalographic correlates of psychopathic personality, Hill and Watterson [I0] confirmed Davenport's finding by showing that a family history of bad temper was three times more common in aggressive than nonaggressive psychopaths and indeed had a firmer hereditary basis than epilepsy itself in their patients. Using Schneider's definition of psychopathy with Henderson's sub groups they showed, by given EEG criteria, that an abnormal EEG existed in 65 per cent of their aggressive psychopaths as compared with 32 per cent of the inadequate personalities, and 15 per cent of their controls. The EEG montage at that time would not allow precise localisation of these abnormalities but the study did suggest a neurophysiological basis to abnormal behaviour. "One can have little doubt that an abnormal EEG constitutes for its possessor a handicap in the business of biological adaptation, failure of which may show itself as in our present series in undesirable, asocial behaviour . . . . In view of the similarity between the aggressive behaviour of psychopaths and the normal bad temper response to frustration in young children the suggestion that the abnormality in the EEG in these cases is produced by a failure of development in the central nervous system is very tempting. It fits with our psychiatric, biological and social conception of psychopathic personalities". Gibbs, Gibbs and Fuster [11] explored the personality features of 300 patients with psychomotor epilepsy selected by EEG criteria. Forty two per cent showed severe personality disorder and in addition 3 per cent had attempted suicide and 9 per cent were psychotic. This group of patients, the authors remark, "were poorly
Aggression and epilepsy
231
tolerated by the community". They concluded that "in view of the high association of personality disorder with psychomotor epilepsy it seems reasonable to attribute much of what has been called the epileptic personality to disturbance of the anterior temporal areas". That the relevant abnormality was not limited to the anterior region of the lobe in mentally disturbed patients was evident in the work of Rey, Pond and Evans [12] who culled 59 cases with no obvious aetiological factor from a search of 3,000 EEGs for patients with temporal lobe discharges. Sixty eight per cent of these patients conformed to a description of shy, egocentric and irritable and 49 per cent showed overt pathological aggression. Over 50 per cent had a family history of mental disorder. "They are children in their EEGs and their personalities, though chronologically grown up", they wrote, and they pursued the explanatory hypothesis set up earlier by Hill that the essential defect was a failure of cerebral maturation. The abnormalities were most evident in the posterior part of the left temporal lobe, from which, according to Grey Walter, the theta activity disappears last in normal infants. This lateralisation was supported in their 'epileptic' patients by the preponderance of verbal discrepancies in the Wechsler tests. From a later study by Hill [13] it would seem that whilst anterior foci are more likely to be associated with epilepsy and disturbances of consciousness, the more posterior foci are more frequently associated with abnormal personality, psychopathic aggression, and antisocial behaviour. These findings are confirmed in the work of Hughes et al. [14] who found that infrequent grand mal, autonomic changes, and psychic manifestations as well as behaviour disorders were associated with a more posterior locus. Where the EEG abnormalities were bilateral they tended to be more obvious on the left side. The authors believed that the posterior loci were associated with hippocampal lesions and the anterior loci with amygdala damage. Gastaut [15] too believed that the hippocampal form of temporal lobe epilepsy was the most common and most associated with behaviour disorders. These findings would be consistent with the neuropathology of temporal lobe epilepsy where the most common lesion, mesial temporal sclerosis, most regularly affects the hippocampus [16, 17]. In 1953 Hill [18] dismissed the idea that epilepsies of central origin and those of focal origin outside the temporal lobes had any specific psychological aspects since he believed that when seen in psychiatric clinics such patients were usually of low I.Q. and poor social background. Such a view of the general effects of poor environment was amply justified by the study of Grunberg and Pond [19] who showed that the incidence of disturbed background was far higher in the general run of epileptics with behaviour disorder than in those without. It must, however, be remembered that the incidence of disturbed backgrounds in patients with temporal lobe epilepsy is notably high. In our own recent study [20] 40 per cent of patients had at least one first degree relative with mental disorder, 27 per cent were bereft of at least one parent before the age of 15 years, and 36 per cent were not domiciled in their appropriate homes. It was Bailey who first performed temporal lobectomy for the relief of epilepsy in patients 'whose need for help was desperate'. These patients differed from Penfield's in that the abnormalities in the temporal lobes were presumed to be purely functional. In this country Mr. Murray Falconer in association with Professor Hill began performing temporal lobectomies in 1952. The high prevalence of psychiatric 3
232
DAVID C. TAYLOR
disorders in the patients is evident in the published studies emanating from this work and indeed, it has been accepted that, at times, personality disturbances which had resisted treatment were an added reason for operation [21]. Character disorders of the type already described were the most common single psychiatric entity; 18 of the first 27 patients reported on were so affected [22], and of these at least 11 were aggressive. Post operative depression, interpreted as a 'turning-in' of the aggressive behaviour, was common, 5 of these patients needed ECT. James [23] showed that in 28 per cent of the first 72 patients operated aggression dominated the clinical picture. All but one of these patients had been either excluded from school, or admitted to hospital, or appeared in court for aggressive behaviour. In all but one case the epilepsy had started before the age of 13 and the mean age at onset, at 6.4 yr, was 8 yr less than in his marginal/normal group. The prognosis for this group was excellent, and strongly related to relief from epilepsy. In social terms the effect of surgery was to change the number considered well adjusted from 1 preoperatively to 14 out of 20 at follow-up. The subject was further extended by Serafetinides [24] in a series of 100 patients. He agreed that aggression was a feature of those with early onset epilepsy and that these patients also tended to be operated on earlier. But he found a substantial predominance of males in the aggressive group and 25 of the 36 aggressive patients were operated on the left side. In a recent study [20] we were concerned mainly to assess the effect of operation on the social adjustment of our patients but a clinical assessment of personality was also made retrospectively from the pre-operative notes and again at the follow-up interview. One hundred consecutive English-speaking patients, including 50 never previously reported, were considered. Pre-operatively 48 were considered psychopathic according to the same criteria used by Hill and Watterson [10] but 10 had an additional diagnosis. These 48 patients were characterised by being predominantly of male sex (38 out of 48 compared with 25 of the remaining 52), they showed an excess in the lower social classes, were of lower full scale I.Q. and had poorer interpersonal relationships. They were younger at the time of onset of their epilepsy and 28 of the 48 were operated on the left side compared with 20 of the remaining 52. (/9 < 0-05, Chi Squared = 3.9). Twenty seven of these patients were noted as showing overt aggression, not merely as some part of their life histories but as a feature of their current pre-operative mental state. Examination of these patients revealed that their parents and to some extent they themselves were in excess in the lower social classes. The full scale I.Q. was significantly lower than for non-aggressive patients, and one third of them compared to one fifth of the remainder had required special schooling or had their school careers grossly disrupted (see Table 1.]. Forty one per cent had been permanently separated from at least one parent before the age of 15 (Table 1). Their general social adjustment was extremely poor. In the figure the social adjustment scores are a total of 7 items of social adjustment and are arrayed each in a locus determined by the pre and post operative score. Whilst aggressive patients are grossly under-represented in those reasonably adjusted pre-operatively they contribute equally with the remainder to those who improved. Of the 7 individual items which made this total score the greatest difference between aggressive patients and the rest came in their intra-family relationships (Table 2). There were important
Aggression and epilepsy
233
TABLE I.--BACKGROUND FACTORS Aggressive
Others
%
%
N = 27
N=
66 93 48 41 41 59 33
Operated before 24 years of age Age of onset epilepsy 1st or 2nd decade Parental social class 4,5 or 0 F.S.I.Q. 89 or less Bereft before age 15 Patients' social class 4,5 or 0 Schooling, special or disturbed
37 71 27 23 22 40 21
CHANGES IN I N D I V I D U A L SOCIAL ADJUSTMENT SCORES P R E - T O - P O S T OPERATIVE RATING SOCIAL ADJUSTMENT 15
10
~,~ Stayed • Good •4 • •••k 0
•
POST-OPERATIVE 20
b
OQ• ~ 1 •
•
30
25
Worsened from Nor mdl SCOre
(22)
32
(12)
©
•
>
D% 00
•0 O
•
•0
• O
0
%
O D
••
0
20 •0 0
O•
•
•
•
©.• ©,
•
m
2~ ,~
0
. ll'O•
© 0 •
"'4
IL
•
•
25
© 0
?,
O
Improved IO Normal Score
k
•
m
(28)
0 • •4• • 0 "• 0•0
o S,o.o~g. (37>
AGGRESSIVE NON-AGGRESSIVE
0 •
FIG. 1. Pre-operative social score: Below 15 Above 15
Aggressive 4 23
Others 30 43
Chi Squared = 4.95 p < 0.05 Post-operative social score: Below 15 Above 15
Aggressive
Others
I1 16
40 33
Chi Squared = 0.636
N.S.
•
" "-,,
73
Chi squared • 7"02 5"07 4"43 3"86 3"54 3"03 1"13
234
DAVID C. TAYLOR TABLE 2.---INDIVIDUAL ITEMS OF SOCIAL ADJUSTMENT
(maximum score = 5)
Family relationships 1 or 2 Use of leisure 1 or 2 Non-family relationships 1 or 2 Never institutionalised Domiciled at home Work adjustment 1 or 2 Sexual adjustment 1 or 2
Aggressive % N = 27
Others % N ~ 73
Chi squared*
15 26 19 41 52 22 30
52 45 40 60 69 34 27
9"7 3-69 3"06 3-03 2-36 1"3 0'05
* Yates correction where one cell was 5 or less. (For a full description of the protocols see Taylor and Falconer [201.) differences in non-family relationships, the use made of leisure and the extent of institutionalisation suffered. There was no difference between the sexual adjustment of the aggressive and non-aggressive patients (Table 2). It was noted that the aggressive patients were more frequently operated upon in their late teens and early twenties and the 9 patients who improved their social scores to below 15 were all operated in the decade between 16 and 26. In this sub group, however, left and right sided operations are equally represented, outcome for seizures and the pathological findings were the same as in the whole series. There are several conclusions to be drawn. Firstly although 'aggressiveness' is rather difficult to define the consistent incidence of about one third in these studies, separately made by 5 different author groups, suggests that it is a distinguishable feature in these patients. That this is not entirely parochial is confirmed by the 38 per cent incidence in the survey by Preston and Atack [25] and the 36 per cent incidence in Ounsted, Lindsay and N o r m a n ' s study [26]. Secondly although these patients all suffered focal, temporal lobe dysfunction only one third w e r e so affected. The consensus of several studies is that those affected tend to be of male sex, low class, low intelligence, and more frequently disturbed on the left side of the brain. The importance of left temporal lobe damage has recently been emphasized in a variety of studies [27-29]. Thirdly these factors can be brought together in a coherent way. Early onset epilepsy brings a child to specialist attention at an age when conduct disorders are the rule for disturbed children, before paranoid and depressive mechanisms are used, and they are brought to operation at a stage in their development when their aggression is out of hand. Our own current research is suggesting that epilepsies following on prolonged convulsions either 'febrile' or in response to cerebral infection tend to damage the left hemisphere more before the age of 2 years and the right hemisphere more thereafter. Thus in a group of patients with early onset epilepsy the incidence of left cerebral damage would tend to be maximised. In addition, cerebral damage sustained young is more 'destructive' of I.Q. than when sustained older. Further the vast majority of temporal lobe epilepsy of onset before 4 yr is due to mesial temporal sclerosis. Thus the good prognosis which is generally given for aggressive patients could be a product of the generally good prognosis for patients with this lesion whether aggressive or not [17]. In our own study [20] whilst it was found that overt pathological aggression was reduced there was no general tendency towards 'taming' and the relief of mental disorders seemed to come, though not invariably, with relief of epilepsy.
Aggression and epilepsy
235
O n the other h a n d alternative responses to frustration and social failure are frequent in the long term follow-up o f these patients. These need not be interpreted as a redirection o f libidinal energy but as responses to continuing frustration. In a mean follow-up o f 5 yr in our own series o f 100 patients, 37 had a further period o f mental hospital treatment, 5 per cent o f the patients had committed suicide, and a further 2 had performed ritual self mutilations. This suicide rate is only comparable with that in other less selected series o f epileptics [30, 31]. N o evidence could be found, and clinical experience does n o t suggest, that any f o r m o f agonistic display occurs in the course o f a seizure other than a u t o n o m i c changes [32]. Williams [33] described only one patient in a series o f 100 for w h o m anger was an aura. It seems in the light o f this review more parsimonious to conclude that aggressiveness in these patients is less the result o f interference with mechanisms specifically controlling aggressive behaviour than that the defect is one o f learning. They have m a n y reasons to fail to learn; they are damaged early, in structures o f vital significance to learning, their social origins suggest that example and training might be defective. Schooling is disrupted and institutionalisation frequent. This learning failure is evident in inappropriate social responses which are misinterpreted as aggressive releasing the causal chain o f reaction and expectation. It will constitute a major source o f frustration a m o n g s t the wide variety o f frustrations contingent u p o n being epileptic [34]. It is essential to realize that perhaps the most " p a t h o l o g i c a l " aspect o f this overtly aggressive behaviour is its failure as a useful social mechanism. Acknowledgements--I am grateful to Mr. Murray A. Falconer for his support and encouragement
in studying his patients at the Guys-Maudsley Neurosurgical Unit. The basic data were collected during the tenure of a grant given jointly by the Governors of Guys, and the Royal Bethlem and Maudsley Hospitals. The author is currently Medical Officer in the Human Development Research Unit of the University of Oxford, which is supported by the Department of Education and Science and the Department of Employment and Productivity. REFERENCES 1. PAPEZJ. W. A proposed mechanism of emotion. Archs. Neurol. Psychiat. 38, 725 (1937). 2. KLLWERH. and Buoy P. C. Preliminary analysis of the functions of temporal lobes in monkeys. Archs. Neurol. Psychiat. 42, 979 (1939). 3. HILLD. In The Natural History of Aggression. Carthy J. D. and Ebling F. J. (Eds). Academic Press, London (1964). 4. DOLLARDJ., DOOB L. W., MILLERN. E., MOWRERO. n. and SEARSR. R. Frustration and Aggression, Yale University Press (1939). 5. GraBs F. A., GIBBSE. L. and LENNOXW. G. Epilepsy: a paroxysmal cerebral dysrhythmia. Brain 60, 377 (1937). 6. FALRETJ. De l'6tat mental des 6pileptiques. Archs. G~n. M~d. 16, 666; 17, 461 ; 18, 423 (1860, 1861). 7. GOWERSW. R. Epilepsy and Other Chronic Convulsive Disorders, Churchill, London (1881). 8. JACI(SONJ. H. Temporary mental disorders after epileptic paroxyms. In Selected Writings of John Hughlings Jackson, p. 119, James Taylor (Ed). Staples Press (1958). 9. DAVENPORTC. The feebly inhibited: violent temper and its inheritance. J. Nerv. Ment. Dis. 42, 593 (1915). I0. HILL J. D. and WATTERSOND. Electroencephalographic studies of psychopathic personalities. J. NeuroL Paychiat. 5, 47 (1942). 11. GIBBSE. L., GIBBSF. A. and FtrSTERB. Psychomotor epilepsy. Archs. Neurol. Psychiat. 60, 331 (1948). 12. REY H., PONDD. A. and EVANSC. Clinical and electroencephalographic studies of temporal lobe function. Proc. R. Soc. ivied. 42, 891 (1949).
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