A behavioural and electroencephalographic study of autistic children

1. Psychiar. Rex, 1965, Vol. 3, pp. 181-197.

A BEHAVIOURAL

Pergamon Press

Ltd.Printed inGreat Britain.

AND ELECTROENCEPHALOGRAPHIC

STUDY OF AUTISTIC CHILDREN S. J. HUTT*, CORINNEHUTT, D. LEE and C. OUNSTED Park Hospital for Children, Oxford, England (Received 18 March 1965) (Revised 7 June 1965)

INTRODUCTION IN 1943 KANNER,~ describing the clinical features of 11 cases, delineated a syndrome of childhood which he called ‘early infantile autism’. More recently EISENBERG and KANNER~ have summarized the early findings, enumerating 5 characteristic features of the syndrome : (a) the inability to relate to people ‘from the beginning of life’; (b) failure to use language in order to communicate; (c) an obsession for maintaining sameness; (d) preoccupation with objects; (e) evidence of ‘good cognitive potentialities’. In the same paper these authors go on to say: “in the light of experience with a ten-fold increase in clinical material, we would now isolate these two pathognomic features, both of which must be present: extreme self-isolation and the obsessive insistence on the preservation of sameness, features that may be regarded as primary. . . . ” The aims of the present study are (i) to describe and quantify the ‘free-field’ behaviour of such a group of children; (ii) to present an analysis of their electroencephalograms including some preliminary telemetry data; and (iii) to suggest a possible neurophysiological hypothesis to account for the two sets of findings. The patients studied were ten children, nine boys and one girl whose average age was 3 years 10 months. The criteria for their inclusion in the study were (i) that in each case the diagnosis of autism should have been made independently by at least two clinicians; and (ii) that none of the patients should have evidence of anatomical cerebral damage. The possibility of misclassification is an ever present hazard in all research employing nosological entities. Having decided, however, to accept the diagnosis of autism made by the two clinicians, it was strictly adhered to, despite any possible reservations on the part of the writers. In retrospect, it appears that all children manifested the first four of the diagnostic signs listed by EISENBERGand KANNER (idem) including the two ‘primary’ features. It is debatable whether all children showed evidence of ‘good cognitive potentialities’. This however is the most difficult feature to assess, since these children are largely *Present address: Research Fellow, St. Catherine’s College, Oxford. 181

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non-verbal and react adversely to the social programming involved in formal psychological testing. In view of the diagnostic problems therefore, it was thought desirable to present brief biographies of the ten children. CASE

HISTORIES

Case 1. No. 1810. A boy. Date of birth 29.3.60. He was referred to this hospital when the teachers at his nursery school found him unmanageable. The father was a university lecturer. He was described as a schizoid personality and the mother as cool and detached. There was a younger healthy brother. A maternal uncle suffered from schizophrenia. There was a history of glandular fever in the first trimester of the pregnancy. The child was born at term and there was no history of perinatal injury; birth weight was 8 lb 4 oz. He was lively at birth, he sat at 6 months and walked at 13 months. He babbled at 8 months but there was no more development in speech until the age of 2 years, when he began to use a few words meaningfully. As an infant he rocked the cot SO much it had to be nailed to the floor; he habitually spun himself around. Much of his play was occupied with buttons, rings, doors and switches. Both at home and at his nursery school he did not play or mix with other children. At the age of 2 he was seen by the school Medical Officer who advised against his admission to nursery school as he spoke no meaningful words and was overactive. He was then referred to the department of otorhinolaryngology. An adequate audiogram could not be obtained; the hearing therapist was unable to demonstrate any hearing loss. He obeyed a few simple commands. For a period he had habitually assumed strange postures. He showed distress on deviation from the usual route when out walking. He was referred to this hospital from the ENT department in November 1962 on account of his unstable behaviour with a request for suggestions regarding schooling. A diagnosis of Kanner’s syndrome was made. The parents, however, were extremely resistant to further investigations being made on the child. The father denied that any disability existed and insisted on his return to nursery school. He was re-referred in January 1963, and at interview the child spent most of his time racing up and down the corridor, opening and closing the door, which he could do with great dexterity. He was able to do the Form Board for circles and triangles but perseverated on this activity and started to scream when attempts were made to remove it from him. His verbal utterances at this time were meaningless. He alerted to unusual sounds and was able to obey simple commands. He was, however, non-communicating and paid no attention to either his father or to the examining doctor. Father again denied any disability and refused child’s admission to hospital. Out-patient contact-was maintained and the parents-finally agreed to admission in November 1963. Physical examination revealed no abnormality; skull X-ray report: no lesions seen, pituitary fossa intact, sutures appear normal. Case 2. No. 1971. A boy. Date of birth 25.8.59. In April 1963, at the age of 3% he was referred to this hospital as his overactivity and failure to make normal progress were causing his parents some distress. The father was a firm manager who had been educated at public school; the mother was trained as a teacher. Both parents were described as cool and detached. There were two older female sibs, one of whom was adopted, and a younger male sibling-all these were healthy. During the pregnancy the father had German measles and the mother was given gamma-globulins during the first trimester. Delivery was natural at full term and birth weight was 8 lb 2 oz. The boy sat at 17 months and walked at 22 years, but did not speak. When he had learned to walk, he spent his time trudging up and down a room and picking up and dropping toys. He showed no constructive play and was grossly overactive. He had unprovoked screaming bouts. He was unresponsive to pain. He did not learn to feed himself and was doubly incontinent. He became distressed in strange places. He was inattentive to adults and did not play with other children. He had been investigated at other hospitals for possible deafness but was thought by the paediatricians to be autistic. When seen in May 1963, he avoided outstretched arms; he spent his time spinning toys, chewing or wandering around the room. He grunted but spoke no words. Physical examination revealed general hypotonia and unsteady gait, but was otherwise normal. He was psychometrically untestable, but a Vineland Social age of 20 months was obtained. Final assessment was autism, together with some retardation. Case 3. No. 2066. A boy. Date of birth 27.5.59. He was referred to this hospital by the paediatricians as he seemed ‘to be in a world of his own’ and did not play with other children. His father was a motor mechanic; the mother was described as shy. They lived with the maternal grandparents. The patient was the youngest of three boys, the other two being healthy. Pregnancy and the neonatal period were normal; birth weight was 6 lb 12 oz. The child sat up at 6 months,

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stood at 1 year and walked at 16 months. He learned to feed himself and developed clean habits. He acquired a small vocabulary but used this less and less. He was described as an exceptionally good baby. He played little with toys, but liked running and jumping. Any articles or toys he was given he rotated or juggled in a characteristic manner. He did not progress in speech or social responses. He was referred to this hospital in July 1963 at the age of 4 years. Audiometry revealed no hearing loss. He did not play with a toy nor did he appear to be interested in what was going on around him. At times he wriggled his hands. Clinical examination revealed no significant abnormality. On admission in September 1963, he was described as a manneristic, severely anxious, autistic child. After admission he was noticed to be producing a whispering noise in conjunction with his hand rotations. He obtained a Vineland Social age of 23 years. Case 4. No. 1587. A girl. Date of birth 28.10.58. She was referred to this hospital when the mother found her increasingly difficult to manage at home on account of her frequent screaming attacks. The father was in a parachute regiment; he was not a jovial person, and was frequently irritable. The mother when seen was very depressed. The patient was the youngest of three girls. The child was born 8 weeks prematurely and birth weight was 4 lb; she breathed at once although there was some respiratory distress. Tube feeds were needed and following this she was slow to suck. She was mildly jaundiced in the neonatal period. When she was a year old she was admitted to the hospital with bronchial pneumonia. Following this her feeding had been very slow and she had great difficulty with solids. She was slow in all her milestones and did not speak. She had frequent screaming attacks. At times she sat rocking herself, poking her ears or playing with her hair, and was completely inaccessible. Often she made moaning sounds. However, there were periods when she laughed when cuddled. She neither played with toys nor engaged in any constructive play. She was admitted in April 1962, at the age of 34. On admission her behaviour alternated between screaming attacks with no detectable precipitating factors, and periods of rocking, with rhythmic movements of her fingers. She rarely obeyed commands and did not speak. When an attempt was made to test her psychologically she took no notice of toys, her only activities being to throw things or to ensure that certain objects were in their right place; she became distressed if they were removed. She made a monotonous repetitive ‘ah eee’ verbalisation. If left alone she would sit flicking her lip or a nearby object. Physical examination revealed hypotonia but no other abnormality. A report of her air encephalogram stated ‘margins of lateral ventricles somewhat rounded and ventricles themselves though symmetrical may be slightly enlarged; cortical markings within normal limits for the age. Remaining parts of ventricular system appear normal.’ The diagnosis was retardation and autism. Case 5. No. 1699. A boy. Date of birth 13.3.60. The complaints were that the child seemed completely indifferent to other human beings, and had spoken no distinguishable words since the age of 15 months. The father was a research engineer. Both parents were described as shy and reserved. Birth was normal, but soon afterwards the mother became ill and was unable to look after the child. She died of sarcoma of the spleen when he was 1 year old. He walked at 15 months and spoke a few words. He was doubly incontinent. He played with toys for hours on his own, particularly with objects that rotated. He had frequent bouts of screaming and would sometimes scream solidly through the whole night. He played for long periods pouring water from a bucket, repeating the movement over and over again. The child had been attending nursery school but the staff were worried about him as they found him unresponsive. It was thought that he was deaf as he made no responses to sound. In June 1962, he was referred to the paediatricians who thought him probably not deaf, and in July 1962, he was referred to this hospital. At interview he displayed considerable dexterity in manipulating objectsfitting them together or spinning them. It was noticed that he averted from social contact and at times when thwarted he would hit himself on the face. The final assessment described him as an autistic child. Case 6. No. 1489. A boy. Date of birth 13.10 56. Parents complained that he lived in a world of his own, and would not co-operate at school. The father was an accountant and the mother a bank clerk prior to marriage. The father was very neat and tidy and tended to be upset by the noise of the children. The patient had an older sister and a younger brother. In March 1963, the father was admitted to a psychiatric hospital with a diagnosis of schizophrenia. Pregnancy and birth were normal; birth weight was 7 lb. The child sat at 8 months, walked at 22 months, and said a few words at 9 months but stopped speaking altogether at a year. He was dry and clean at 2fyears. He was described as a good baby. He rocked himself to sleep every night; he spun objects and hummed the same tune repeatedly. He occasionally spun himself around until he was giddy. He banged his head.

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In July 1960, he was referred to the paediatricians because he was not talking. Subsequently at the age of 4 years he came under observation at a Child Guidance Centre and was considered to be suffering from schizophrenia. There were episodes of overactivity and outbursts of shouting; he appeared to be more interested in things than in people. He rocked himself incessantly and had a mannerism of the mouth. In October 1961, he was referred to this hospital by the school Medical Officer for further investigation. On admission his behaviour was manneristic; he postured and from time to time explored his body either by masturbation, by gentle tongue movements or rocking gently to and fro. His main play activities were with wheels and water. He did not speak. He was also nocturnally enuretic. The diagnosis on admission was Kanner’s syndrome. Case 7. No. 1979. A boy. Date of birth 10.3.58. Complaints were failure to respond to sounds, absence of speech, failure to show normal interest in people and absence of normal response to injury. The child had been adopted at 3f months. There was no known history of mental illness in either side of his real family. The adoptive father was an army captain: he was described as an obsessional worker, slow to lose his temper. The adoptive mother was a stable and warm person. The child sat at 10 months, walked at 23 years but did not speak. He was clean and dry by the age of 2. He was a passive baby and never liked being cuddled; he ignored noises and made little distinction between people. At the beginning of 1959, when he was 9 months old, he was referred to the paediatricians through a children’s department on account of his failure to respond to sounds; this failure had first been noticed at 6 months. He was described by the paediatricians as a normal, lively intelligent baby but who made very little response to sound. He was seen by the audiologists in 1960, who did not consider him deaf, but subsequent interviews indicated less response to sound. A month later the psychologists noticed that he showed little interest in people and that he was developmentally backward. At this time too, the parents reported that he was becoming more withdrawn, ignoring touch as well as sound. He was seen again by ENT specialists in September 1960, when he still seemed unresponsive to sound. Six months later the audiologist reported that the boy at interview took no notice of anybody in the room, played only with toys which he could spin and avoided his gaze. He suggested to the parents that the boy was mentally disturbed and not backward. At the end of 1962 when he was 4% years, he was described by the school Medical Officer as a case of schizophrenic syndrome of childhood. In May 1963, he was referred to this hospital. On admission he was seen to be assuming strange postures; he showed some communication by means of gestures. In play he was attracted to water and to objects he could spin. He had many unusual mannerisms, and he walked on tip-toe most of the time. A neurological examination revealed no positive signs. The diagnosis was autism with possibly other complicating factors. Case 8. No. 1522. A boy. Date of birth 11.1.58. The parents were concerned that the child was not developing speech, that he appeared completely cut-off and made no response to being called. The father was a schoolmaster, born in Australia and educated at public school in England; he was a very shy person. The mother was a drama teacher. There was an older brother who was friendly, talkative and showing some anxiety about his brother. The maternal grandmother was said to have had a senile paranoid illness. Pregnancy was normal; birth weight was 7 lb. 10 oz. Milestones were normal: the child used a cup at 7 months, crawled at 8 months, and walked at 18 months. He spoke a few words at 23 years, but developed little speech since then. He was clean and dry at 3, but had relapsed recently. It was a long time before the parents could get a smiling photograph of him. They began to worry about the boy when he was 2+ years old because of his lack of development: his speech was minimal, his behaviour dreamy, and he would wander around, staring out of the windows for long periods, and make little response to either of the parents. At other times he became more lively and would like to sit on his mother’s lap, although he did not make any response to his mother as a person. He occasionally played with toys, but not very constructively. From 18 months onwards he became progressively more dreamy. He could, however, feed and dress himself. He obeyed simnle commands. If frustrated he would scream for long periods. He would constantlygrind his teeth. In July 1961, he was referred to the paediatricians because of his delayed progress. He was subsequently seen by the ENT snecialist who did not think him deaf. In January 1962. he was referred to this hospital by the paediatricians who suspected him of being psychotic. At interview the parents stated that the child had made no improvement over the past two years. During the interview the child wandered restlessly round the room, returned to his mother, sat with her for a few minutes and then wandered off again. He did not look at her or at the doctor. After admission he was noticed to be either grinding his teeth or sucking his fingers constantly. He paid no attention to the other children and at times was completely inaccessible. He had occasional temper tantrums, particularly if the routine was altered or he could not get what he wanted.

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ELECTROENCEPHALOGRAPHIC STUDYOF AUTISTICCHILDREN

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Case 9. No. 2153. A boy. Date of birth 7.5.60. The mother complained that they had always found him a difficult child; they were unable to communicate with him. He wandered aimlessly most of the time and had become difficult with food. The father was an actor and the mother too had been an actress prior to marriage. The patient was the third of four boys. Pregnacy and birth were uneventful; birth weight was 7 lb. In the early months he was an easy happy baby. He walked at 16 months and said a few words at 20 months, but nothing more since then. The mother found that from the age of about 18 months she could not communicate with the boy, but he would play alone in the garden for long periods. In June 1963, at the age of 3, he was referred for hearing evaluation; the test results were equivocal. Two months later he was referred to an ENT department in London; the specialist concluded that the child suffered from high-tone loss and recommended that he should be visited by a teacher of the deaf. In October 1963, he was seen at school for deaf children where it was noted that he reacted sharply to each new stimulus except the voice but when the sounds were repeated his responses were few and inconsistent. He was next referred to a hospital audiology unit, whose report stated “If there is a defect of hearing it is so minimal as not to be significant in the context of his present condition”. Late in October 1963, he was referred to this hospital for further investigation. At interview the parents reported that the child was not interested in people; he was not a cuddly child and did not require much attention. He rocked his bed; he like stroking furry objects. He was more active than any of the other children and the mother thought he was also less sensitive to painful stimuli. He was beginning to understand simple commands. During the interview he spent much time turning the light switch on and off and opening and closing the door. He was extremely overactive and disliked being frustrated in his activities. He occasionally grimaced, but allowed himself to be picked up. The diagnosis was autism. Case 10. No. 2047. A boy. Date of birth 28.4.59. He was referred to this hospital as a very disturbed, withdrawn, timid child who uttered only stereotyped phrases. He was the illegitimate son of a barrister who was undergoing Freudian analysis and was described as extremely disturbed. The mother, a graduate, had been a journalist; she was suspected of suffering from schizophrenia. The mother’s husband, the patient’s step-father, had had two previous admissions to psychiatric hospitals, and was currently under psychiatric care. He was a university lecturer. Birth was natural and at full term; birth weight was 9 lb. The child walked at 14 months and by the age of 2 years had ‘phenomenal’ speech, but this did not develop further. He was dry at 18 months, but was not clean even by the age of 2. The child had always been uninterested in people, and tended to avoid contact and even the mother’s gaze. He would cling if picked up, but the mother did not feel there was any affection in this. He assumed strange postures, grimaced and manifested ritualistic behaviour. He frequently scrutinized his hands and fingers and at times smacked himself rather violently. He became frightened in new situations ; he sometimes engaged in echolalia or repetitive movements. At home he was underactive and ‘lived in a world of his own’. His behaviour at nursery school was similar and he often talked and laughed to himself. The teachers had suspected deafness as they found it difficult to attract his attention. He did not mix with the other children. He suddenly developed a fear of the lavatory. He was referred to this hospital in July 1963, at the age of 4% years. The first interview was interspersed by perseverative dialogue between mother and child which in turn was punctuated by neologisms. The child himself made many indistinct utterances in a perseverative manner; he showed some finger mannerisms. He played with toys only briefly. Although he sat on his mother’s lap, at no time did he look directly at her. Physical examination revealed no abnormalities; skull X-ray report: no lesions seen, pituitary fossa within normal limits. BEHAVIOURAL

ANALYSIS

Method A method of recording and analyzing the free-field behaviour of children has been described in detail elsewhere,394 together with details of its reliability and limitations. In brief, children were observed individually through a one-way screen, and a continuous behaviour commentary was made on to magnetic tape. The variables recorded were: (i) Visual fixation, i.e. direction of fixations which lasted 1.5 sets or more; (ii) Locomotion, i.e. manner of changing position with reference to the floor covering;

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(iii) Manipulation-what objects were manipulated and how; this included both handling objects and moving them with the feet; (iv) ‘Gestures’. Gestures were defined as bodily movements which did not bring the child into contact with selected parts of the physical environment, e.g. rocking, picking the nose, waving the arms. By using a stylized dictation, it was possible to describe the behaviour as it occurred. The beginning and end of different activities were recognized by the recruitment and relaxation of muscle groups. It was thus possible subsequently to time activities from the tape recording. (A similar type of analysis has been employed by CHAPPLE et a15 in the study of the behaviour of adult schizophrenics). The children were observed in four situations: A, B, C and D, each session lasting 3 minutes. (1) A was a waiting room in which they had all been previously, but which on this occasion was empty except for fixtures like the sink and light switches; (2) in B a box of coloured blocks was placed in the room; (3) in C a female adult (who was known to the subjects), sat passively in a corner of the room; the blocks were also present; (4) in D the adult attempted to engage the child in building a standard design with the blocks. These four situations were presented one after the other in four different orders. The child was left free to wander around the room and the door was left unlocked so he could leave the room if he wished. The data were analyzed in terms of the duration of visual fixations and manipulatory activities, and of the time spent in different activities, i.e. in gestures, locomotion, exploration of the room, block-play and ‘social responses’. Wherever appropriate, comparisons on the behavioural measures are made with six non-autistic children who were in-patients for relatively minor behaviour disorders. These children had been studied previously and will henceforward be referred to as ‘normals’. The mean age of the normal group was 4 years, that of the autists 3 years 10 months. Since the data did not fulfil the requirements of a parametric test, the significance of differences between the groups was tested by the Mann-Whitney U test, significance levels used being for a two-tailed test.

RESULTS

Although the 10 cases were remarkably similar with regard to clinical features, six of these children showed marked and characteristic stereotypies. Since stereotypy was their predominant activity it was decided to examine separately the behaviours of the children who showed stereotypies and those who did not; these two sub-groups are subsequently referred to as the St group and N-St group respectively. The proportions of time spent in four different types of behaviour by these two sub-groups relative to the normals are shown in Fig. 1. (i) Gestures. These included (a) movements of body-parts, e.g. hand-flicking, rocking,

A BEHAVIOURAL AND ELECTROENCEPHALOGRAPHIC STUDYOF AUTISTICCHILDREN AUTISTS

NORMALS

GP

GP N-ST

,

,x_ ._._._. _._._

ST

_.

,/

V’.” .*

A

I3

C

D

A

B

C

D

A

B

C

D

FIG. 1. Proportions of time spent in different activities by normals and two sub-groups of autists.

(b) patterns of movements, e.g. dancing, shrugging while walking, and (c) body manipulations, e.g. nose-picking, rubbing. Although gestures included stereotypies, the two were not synonymous. Stereotypies have been defined as “repetition, in an invariant pattern, of certain movements having no observable goal” (HUM and HuTT~). It was found

that:

(a) as the environment was made more complex the amount of gesturing decreased in the normal and N-St groups; (b) as the environment was made more complex the amount of gesturing increased in general in the St group, except in D ; (c) in D the adult was able to intervene more actively to inhibit some of the stereotypy; (d) normal and N-St groups did not differ significantly from each other in any of the four situations ; (e) the difference between the St group and the other two groups was significant in B (p = O-01), C (p = 0.01) and D Cp = 0.02). (ii) Locomotion. All children showed more locomotion (i.e. walking, running or crawling) when they were alone in the unfurnished room. Locomotion was nearly always accompanied by visual exploration of the environment. In C and D only one of the normals, the youngest, showed any locomotion, whereas half the autists continued to move about. None of the differences between normals and autists were significant. (iii) Manipulation of$xtures. When in the empty room, the normals and non-stereotypers spent more than a third of their time operating light switches, taps and other fixtures. Group St spent relatively little time in such active exploration, the differences between this group and the other two groups being significant at the 5 per cent level. As other potential stimuli were introduced this activity decreased in all children. Only one normal continued to manipulate the light switches in C and D; again it was the youngest. (iv) Block-play. When the blocks were present, block play was the predominant activity in both the normal and N-St groups. Group St on the other hand spent any appreciable time with the blocks only in the presence of the active adult. The three groups differed from

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one another significantly in B (p = 0.05) and C (p = 0.05), but not in D. In the autistic children it was the increase in the amount of block-play from C to D that was significant, whereas in the normals it was the increase from B to C. Constructive play was distinguished from non-constructive play in terms of the motor activities recruited. Thus, constructive play involved attempts to make some design or structure, whereas non-constructive play involved of banging the blocks, throwing them, or picking them up singly. The normal group showed increasing amounts of constructive play from B (25 per cent) to D (43 per cent). The autists as a group showed no constructive play in B, hardly any in C (4 per cent) and very little more in D (9 per cent.) In other words, whereas Group St largely ignored the blocks in B and C, Group N-St played with the blocks in all three situations, but mostly non-constructively. (v) Social responses. These included visual fixations upon the adult, and responses which involved some physical contact with her. The normals showed these responses for 12 per cent of the time in C, and 7 per cent of the time in D; the autists for 6.5 per cent and 7.5 per cent respectively. The normals showed many more active approaches to the adult in C than did the autists, but the figures are too small for statistical comparison. (vi) VisualJixations. The duration of fixations which lasted 1.5 seconds or more could be reliably timed. The mean duration of visual fixations in the autists and normals is shown in Fig. 2. (The St and N-St groups were not significantly different: they were therefore Visual

30

25

20

I5

IO

.

-. \I

l ,X-_

fixations

x---x

Normals

Autists

,x -XR'

L 5

FTG. 2.

Mean duration of visual fixation in autistic and normal children.

combined.) The two groups were very similar in A, but in B the normals fixated mainly on the blocks, in C both on the blocks and the adult, and in D again more on the blocks than the adult. The autists, however, showed very brief visual fixations in all four situations,

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but these were generally interspersed with fairly long periods of scanning, i.e. where fixation was too brief to be measured or where it was uncertain as to what stimulus was being fixated. Scanning represented 30 per cent of the visual behaviour of the autists, but only 10 per cent of the normals. The differences between the visual fixations of normals and autists was significant in B (p = 0.002), C (p = 0.02) and D (p = 0.02). (vii) Manipulutory activity. Different ways of using or handling the same stimulus were regarded as different manipulatory activities. The mean duration of such activities is shown in Fig. 3. (Again the two autist sub-groups were combined since they did not differ significantly from each other). Manipulatory

activity l

J FIG. 3.

-

Normals

I

I

I

_L

A

B

C

D

Mean duration of manipulatory activity in autistic and normal children.

Once again the two groups were very similar in A, where the objects of manipulation were fixtures in the room. In B the normals spent fairly long periods in block manipulation, in C these were interrupted by social responses, and in D block manipulation was shared by subject and adult. The autists, however, showed short manipulatory activities in all situations, these activities generally having a desultory appearance, i.e. absence of clear cut-off points. The difference between the two groups was significant in B (p = 0*004), C (p = 0.002) and D (p = O-02). ELECTROENCEPHALOGRAPHY (1)

Routine EEGs Waking EEGs are carried out on all patients in our hospital, and in many cases sleeping EEGs are also made. Records are subsequently analyzed using a standard data coding system specially developed for this purpose. In the present study all children had had at

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least two resting EEGs and seven had sleeping EEGs. Since the young autist is a particularly difficult child to examine in the waking state, a procedure was used which has been found valuable in obtaining records from severely disturbed children. The child was examined either whilst sitting up in a comfortable chair with eyes open, or sitting on the lap of an adult. Passive eye closure was subsequently obtained for variable periods during the record. An adequate number of artefact-free periods was obtained jn this manner from all children. The child either wore a conventional rubber head-band with saline pad electrodes; or electrodes were attached using Shackle rubber suction cups. Eight bipolar recordings were simultaneously made from the frontal, temporal, parietal and occipital areas of the right and left hemisphere respectively. The EEGs were recorded on an Offner type T machine. TABLE 1. SUMMARYOF RESTINGEEGFINDINGS

Cases

1

Dominant rhythm

Secondary rhythms

Focal/ localized rhythms (resting record)

Focal site of 3

Spikes or spike/ wave occurrence

General description

of record

nil

nil

nil

medium voltage irregular theta dominated record

2*

unstable irregular theta nil

nil

nil

nil

3*

nil

nil

4*

nil

nil

5

nil

low voltage irregular record (<2OpV); no dominant rhythm low voltage irregular record (<2OpV); no dominant rhythm low voltage irregular record (<2OpV); no dominant rhythm low voltage irregular record ( <2OpV) ; with occasional bilateral beta medium voltage alpha dominated record with bilateral beta

fi*

bilateral beta bilateral beta

paroxysmal delta nil

front0 temporal

nil nil

nil

nil

nil

nil

nil

nil

nil

I*

unstable irregular alpha nil

8

nil

nil

nil

nil

9

nil

nil

nil

nil

10*

nil

nil

nil

nil

low voltage irregular record (<2OpV); no dominant rhythm low voltage irregular record (<2OpV); no dominant rhythm medium voltage irregular record (>2OpV); no dominant rhythm low voltage irregular record (<2OpV) ; no dominant rhythm

* = Gp St The main characteristics of the records obtained are summarized in Table 1. The records showed predominantly generalized low voltage irregular activity (t20pV) without any established rhythms. They thus resembled the ‘flat’ EEG described by ADAMS’ or the ‘desynchronized’ adult EEG described by many authors, said to be associated with states of high central arousal. Eye closure either made no difference whatever (see Fig. 4) or in one child, produced a fairly stable alpha rhythm. Since a large number of young children seen in our department also have been examined

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under these rather unusual conditions, it was possible to check on the probability of obtaining similar records from a successive unselected sample of children of the same age referred with psychiatric disorders other than autism. In a consecutive sample of 60 children only one had a ‘fiat’ EEG. Even with eyes open, the records of the control children were

r-r

6

c;

FIG. 4. (Case 5) Waking EEG record showing low voltage irregular activity with no established rhythm and not modified by passive eye closure. Similar records were obtained in seven other children of the autistic group.

generally of higher voltage than those of the autistic children and genetally contained a dominant rhythm. Whilst remembering that the children referred to our hospital represent a highly selected sample, there is some evidence that from the EEG point of view the 10 autistic children studied represented a statistically unusual group, and that their EEG records could hardly be attributed to an artefact of the recording situation. (2) Telemetry duta Two children (Cases 3 and 7) were studied simultaneously behaviourally, using the procedure already described, and electroencephalogr aphically by means of a ‘I elevar’ radio link. This consists of two units, each the size of a half-penny, containing pre-amplifiers, transmitters and batteries. The units were tucked under the patient’s collar leaving two short lengths of wire protruding, which were attached to suction cup electrodes fixed to the right and left occiputs respectively. Signals from the transmitters were picked up by the Televar receiver, an FM receiver with multi-directional aerial, which was in the adjacent observation room. The EEGs were recorded on an Offner type T machine. The children were studied under three sets of conditions corresponding with environments A, B and D in the previous

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section ; the three environments were presented in reverse order to one child (S3). Behavioural recordings were made as before; these were subsequently transcribed, timed and matched against the appropriate EEG tracing. The EECJ record was then divided into ‘epochs’ according to the length of the accompanying behaviour. An epoch was defined as a section of the EEG tracing whose beginning and end points coincided with the initiation and cessation respectively of a category of motor behaviour. Each epoch was assessed independently by two of us, without knowledge of the accompanying behaviour. The duration of activity in the delta, theta, alpha and beta bands was measured, as well as the amount of low voltage irregular activity. It was thus possible to determine the bio-electric activity which accompanied each motor activity as well as the total amount of bio-electric activity of each type. Epochs which were technically dubious were timed, but not assessed. No precise temporal association could be demonstrated between particular activities and specific patterns of EEG activity. In practice there were few instances where any one activity was accompanied by a single EEG rhythm. Especially during the more prolonged behaviours, the EEG would show first one rhythm and then another, or a rhythm would begin during one activity and continue into another. If, however, the total duration of activity in each EEG category is considered, an interesting trend emerges. We shall consider in the present analysis one type of behaviour pattern, stereotypies.6 Table 2 shows the frequency and duration of bouts of stereotypy in relation to the total duration of desynchronized activity in the EEG in each environment. We defined ‘desynchronized’ as low voltage irregular activity or low voltage beta activity. Owing to an idiosyncracy of Case 7, it was not possible to complete condition D: this whole session was spent in removing the adult’s shoes. TABLE 2.

FREQUENCYAND DURATIONOF BOUTSOF STEREOTYPY M RELATIONTO DESYNCHRONIZED ACTIVITYIN THE EEG

Case

Environments A

Frequency of stereotypy bouts Percentage time

stereotypy

Desynchrony as percentage of assessable

s3

S7

5 0

B 13 14

D 12 -

s3

12.8 0

29.5

54.1

46.6

S3 s7

26.5 56.7

38.0 74.6

70.9 -

s7

-

record

As ment; Both were

in the main study, least stereotypy occurred in the relatively unstructured environthere was again a significant increase in the time spent in stereotypy in environment B. children showed a corresponding increase in the frequency with which stereotypies initiated in environment B. The slight drop in the amount of stereotypy shown by

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Case 3 in environment D may again suggest that the adult is able to ‘break up’ the pattern of stereotypy by engaging the child in play with the blocks. The amount of EEG desynchronization was also related to the structure of the environment. Both children showed less EEG desynchronization in the empty room as compared with the more structured environments. Case 3 showed greatest EEG desynchronization in the social situation, D, and it is of interest that in this environment the telemetry EEG was similar to that obtained in the laboratory. It seems, therefore, that in general stereotypy is more likely to occur in those situations where electrocortical activation is greater. The present analysis, however, was based on visual inspection of the EEG, thus the association should be regarded only as suggestive. More precise formulation must await the use of automatic EEG analysis and suitable data handling techniques.

DISCUSSION

These 10 autistic children appeared to have many clinical features and biographical details in common-they withdrew from social contact, their activities were centred on mechanical toys or those which allowed repetitive movement, most of them were suspected of deafness and lacked speech, many of them became very upset on change of routine or situation. Electrophysiologically they seemed to be a remarkably homogeneous group : 8 out of 10 had an identical EEG coding, the probability of this code occurring in a non-autistic population being extremely low. In certain aspects of their ‘free-field’ behaviour too, t.he autistic children exhibited characteristics which differentiated them from other children of their own age. Their visual fixations and manipulatory activities were brief in all situations, whereas the mean durations of activities in the normals changed relative to the situation. Both groups, however, were remarkably similar in the empty room. Thus, it is not the brevity of activities that is significant in itself in the autistic group, but the absence of change relative to situation. In respect of these duration measures the autists were similar to a group of brain-damaged children who had been similarly investigated,4 but whereas the latter were characterized by their abrupt ‘attention-switching’, the autists were distinguished by an almost desultory merging of one activity into the next. Moreover, the visual behaviour of the autists included a considerable amount of scanning, where often it was impossible to say what stimulus was being fixated. When, however, an analysis was made of the kind of activities recruited in the different situations, the autists no longer appeared to be such a completely homogeneous group. Rather there were six children who showed characteristic and persistent stereotypies and four who did not. In the former sub-group gesturing was generally the predominant activity. It is interesting to note that the proportion of time spent in gesturing in A by Gp St, although considerably more than that spent by normals of their own age, is the same as that spent by older normal children in the same situation.4 The gestures of the latter were largely bodymanipulations and complex patterns of movement, analogous to the behaviour shown by adults in sensory deprivation experiments.8 Once the environment was structured, however,

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gestures dropped out of the repertoire of the normal children. Here again it is not the high level of gesturing in Gp St that is important in itself, but the persistence of the high level despite environmental changes. The predominance of gesturing also had a reciprocal effect on the levels of other behaviours and it was not until the active adult intervened that the behaviour of Gp St became more like that of the normal children: the level of gesturing dropped and was overtaken by block-play. On the other hand the N-St group behaved much more like the normals. This suggests that in terms of motor behaviour alone, autistic children who do not show stereotypies may be much more like their normal peers than is commonly supposed. Thus, it might be said that the structure of behaviour in Gp N-St is similar to that of the normals and different from Gp St. It is important to note, however, that in both autistic sub-groups the greatest change (e.g. in block-play) occurred at the intervention of the adult whereas in the normal group the mere presence of the adult was sufficient to effect this change. Nevertheless, the fact that the social stimulus was able to effect a marked change in the behaviour of the autistic children in D showed that these children were by no means socially unresponsive. In a closer analysis of their social behaviour, HUTT and OuNsnd suggest that most autists fail to gaze fixate a social partner, but in all other respects, their social responses are morphologically similar to those of normal children. Much evidence from animal studies indicates that behavioural withdrawal and stereotyped behaviour occur in states of high arousal. It has been suggested that in these autistic children too, and in particular in those who engage in stereotypies, the non-specific activity of the ascending reticular system is at a chronically high level, perhaps due to some biochemical/metabolic lesion.6y10 The EEG findings may offer independent evidence of the level of arousal. The laboratory EEG records of eight children contained irregular activity with no established rhythms, and in seven of these cases their voltage was less than 2OpV. They thus resembled the ‘flat’ records described by ADAMS’ which were found to have a very low frequency of occurrence in the normal population over 10 years of age and to be almost absent in children under the age of 10 years. They also resemble the ‘desynchronized’ or ‘activated’ EEG described by several workers and thought to be a manifestation of increased electrocortical bombardment from the reticular system. A review of the relevant evidence has recently been made by LINDSLEY.~~ The majority of records made by us on children with Kanner’s syndrome fall within the ‘flat’ EEG range. It is unlikely that the flat records are an artefact of the circumstances under which the records are made. Although most records have to be made with eyes open, eye closure, whether active or passive, does not generally alter the records. Moreover, records made upon non-autistic children under the same conditions are generally of higher voltage and show greater organization even with eyes open. It has been shown that even when children of this age are actively engaged in exploring a room, there is gradual emergence of an established rhythm within approximately 2 minutes of entering the room.12 The telemetry data so far available suggest that a social situation (and the laboratory EEG is such a situation) would be expected to produce a more activated EEG record than a non-social situation. Only two children had EEGs containing what could be regarded as an established rhythm, Case 1 an unstable diffuse theta rhythm and Case 6 an unstable bioccipital alpha

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rhythm. In both cases the voltage of the records was again low. Whilst we have seen alphadominated records only infrequently in autistic children, they have been reported by HEWER et al.13in 88 per cent of their cases. LANDOLT~~regards these findings as a special manifestation of ‘forced normalization’ of the EEG during psychotic episodes; he quotes LOEB and GIBERTI who suggest that hyperactivity of centrencephalic structures, e.g. the ‘waking centre’ of the reticular formation, may be responsible for forced normalization. In general, therefore, we may postulate that records which are predominantly desynchronized or of higher frequency than is generally found in children of this age group may be evidence of a higher level of electrocortical activation or arousal. Since, however, the seven sleeping records were within normal limits for the age group, it would follow that the hypothesis of a high level of arousal in these children applies only to the waking state. Except when the adult intervened, those children who showed stereotyped behaviour explored their environment consistently less than the other autists, i.e. stereotypy and exploration seem to be antithetical activities. GLICKMAN~~ suggests that the reticular activating system of the brain-stem, in maintaining the non-specific activity of the CNS, may also act as a threshold-mechanism governing exploratory behaviour. In these children, therefore, if central arousal is already at a very high level (Gp St) exploratory activity, which results in increasing arousal potential16 is unlikely. Exploratory activity is only observed when there is relative sensory deprivation. Stereotypies probably act as a safety device to prevent further sensory input, having a neurophysiological effect analogous to PAVLOV’S ‘supramaximal inhibition’, thereby protecting the organism from the deleterious consequences of excessive excitation.16 Supportive evidence for this kind of functional mechanism is afforded by the telemetry data; in the empty room, where sensory input is at a minimum, level of stereotypy is low and the EEG shows relatively little desynchronization; as stimuli are introduced stereotypy increases as does the amount of low voltage irregular rhythm in the EEG. Many of these autistic children were originally suspected of peripheral deafness, some of them actually being referred to us via ENT clinics. Yet audiometry, where this has been possible, has seldom revealed any loss of hearing. Their threshold for painful stimuli also appears to be higher than that of normal children. Experiments by HERNANDEZ-PEON and his colleagues]rJs showed that stimulation of certain parts of the reticular formation of the cat would block activity in sensory pathways whose receptors are simultaneously stimulated. Similarly an experiment by JOUVET and DESMEDT~~indicated that blocking could occur at the co&ear nucleus upon stimulation of certain points of the R.A.S. It is possible that in autistic children similarly a chronically high level of A.R.A.S. activation produces blocking of sensory pathways, thus accounting for their reduced sensitivity to sound, to pain and perhaps even for their visual scanning rather than fixations on specific stimuli. The hypothesis of high non-specific arousal could be tested by the use of different drug regimes. STRETCHES has suggested that “any drug that raises arousal thresholds for exteroceptive stimuli will lead, within certain limits, to an increase in exploratory behaviour”. On this basis, administration of any drug whose action is to depress the activity of the reticular system should reverse the levels of stereotypy and exploratory activity. Finally, it is necessary to caution against the description of behaviour as ‘pathological’

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or ‘abnormal’ (other than in a purely statistical sense). Behaviour by itself cannot be pathological if it is shown to be in the repertoire of normal individuals. In fact, in a qualitative analysis of the kinds of motor patterns recruited by these autistic children, we were unable to find any that did not occur in the repertoire of normal children. Even the stereotypies consisted of patterns shown by other children, except that in the autists they were deployed with increasing frequency and sometimes increasing intensity. If our hypothesis regarding the underlying neurophysiological disorder is correct, far from being ‘pathological’, these behaviours may indeed serve a ‘useful’ function for the individual.

SUMMARY

Short biographies are given of 10 children, age 3 to 6 years, diagnosed as suffering from Kanner’s Syndrome (early infantile autism). An analysis was made of the free-field activities of these children compared with a group of normal children of similar age. Electroencephalographic studies were also carried out on all 10 children, and in two it was possible to carry out simultaneous behavioural and EEG observations by means of telemetry. The children were observed for three minute periods in four environments of varying complexity: A. an empty room; B. the same room with toy wooden blocks present; C. blocks plus passive adult; D. blocks plus active adult. Except in A the visual fixations and manipulatory activities were of significantly shorter duration in the autistic children than in the normals, lacked clear ‘cut-off’ points and showed relatively little variability between environments. The autistic children as a whole showed virtually no constructive play in contrast with the normals, though more time was spent in contact with play materials in the social environments. Changes in the time spent in locomotion, gesturing, block-play and manipulation of other objects in the environment showed that the autistic children were acutely responsive to changes in their environment, including the presence of the social stimulus. If the autistic children were subdivided into those who characteristically showed stereotypies and those who did not, the latter sub-group showed a behaviour structure which was very similar to that of the normals, whereas the stereotypy sub-group was clearly differentiated from both the normal children and the non-stereotypy sub-group. Eight autistic children had waking EEG records characterized by low voltage irregular activity without any established rhythms; one child, a record containing irregular alpha and another unstable theta activity. Two of the children with ‘flat’ laboratory EEGs showed more rhythmic, higher voltage records when their EEGs were telemetred in environment A. They also showed less stereotyped behaviour. In environments B and D they showed progressively more irregular EEG activity and more stereotypy. The hypothesis is advanced that autistic children are in a chronically high state of physiological arousal. The findings of the present study and those of other workers are discussed with respect to this hypothesis.

Acknowledgements-The first and second authors are in receipt of grants from the Oxford Regional Hospital Board and Nuffield Foundation respectively, whose support is gratefully acknowledged. We are grateful to Dr. MARCEL KINSBOURNE for helpfully criticizing an earlier version of the manuscript.

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