Psychiatry Research. 10, 2 I-30 Elsevier

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Autistic Children’s Hand Preferences: Results From an Epidemiological Study of Infantile Autism

Christopher Gillberg

Received November 3, 1982; revised version received March 31, 1983; accepted April 18, 1983.

Abstract. Twenty-six autistic children, constituting a total population sample of children diagnosed in accordance with Rutter’s criteria as suffering from infantile autism, were assessed with regard to handedness and certain associated factors. They were compared with 52 age-, sex-, and IQ-matched controls. Sixty-two percent of the autistic children were non-right-handed compared with 37% of the controls. Left-handedness in autism was associated with an abundance of delayed echolalia. Heredity for left-handedness in some cases, and assumed brain damage and immature patterns of lateralization in others, were considered the cause of non-right-handedness in the autistic children. Computed tomographic (CT) brain scans and other neurobiological examinations did not provide evidence indicating clear-cut unilateral left hemisphere dysfunction in autism. Rather, a slight trend in the opposite direction (i.e., an association with right hemisphere dysfunction) was seen in the left-handed autistic children. The result points toward the need for further studies of handedness in autism.

Key Words. Infantile xtism, handedness, brain dysfunction.

Several studies (see McCann, 1981 for a recent review of the relevant literature) have attempted to analyze the relationship (if any) between left-handedness (or rather non-right-handedness) and the clinical syndrome of infantile autism. The results are conflicting (Boucher, 1977; Colby and Parkinson, 1977; Barry and James, 1978) but many authorities (e.g., Ricks and Wing, 1976) hold that the available evidence suggests a left hemisphere dysfunction in infantile autism. However, Hetzler and Griffin (1981) have recently concluded that bilateral brain (especially temporal lobe) dysfunction would be required for the classical syndrome of autism to arise.

The reported studies on handedness and autism have not been based on total population samples but on children referred to specific clinics. The method of ascer- tainment may, of course, be one of the reasons for the divergent findings.

The present study reports on handedness and various associated factors in a population sample of infantile autistic children. The main aims of the study have been to (1) test the hypothesis that there is a relationship between left-handedness and infantile autism; (2) analyze the importance of various contributory factors such as heredity and prenatal, perinatal, and neonatal conditions; (3) investigate possible phenomenological differences (especially regarding language development) in left- and right-handed children diagnosed as suffering from infantile autism; and (4)

Christopher Gillberg, M.D., is Assistant Professor, Barn-och S-402 35 GGteborg. Sweden.

0165-1781 83 $03.00 IQ 1983 Elsevier Science Publishers B.V.

ungdomspsykiatriska kliniken. Box 7284,

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correlate handedness in autistic children to morphological and neurophysiological findings.

Methods

Infantile Autistic Group. Twenty-six children (20 boys, 6 girls, boy:girl ratio q 3.3: 1) born in the years 1962-76 and living in Goteborg (a large industrial town on the Swedish west-coast, c. 450,000 inhabitants) region on a chosen census day (December 3 I, 1980) fulfilled Rutter’s (I 978) criteria for infantile autism and were therefore included in the present study. All 26 children had shown (I) early onset (before 30 months of age), (2) severe disturbance of ability to relate to people (out of keeping with intellectual level), (3) failure or delay and deviance of speech- language development (also out of keeping with intellectual capacity), and (4) insistence on sameness as demonstrated by stereotyped mannerisms and elaborate repetitive routines. The children had been screened in a total population study in the Goteborg region. In this screening all child psychiatrists, pediatricians, and other doctors working with children in the Gdteborg region had been contacted by letter and asked if they knew of any child with “infantile autism, childhood schizophrenia, childhood psychosis, mental retardation with autistic traits, severe disturbance of social relationships plus speech-language disorder or severe compulsive dis- order” born in the years 1962-76. All cases reported were (or had already been) extensively examined by the author, and parents and professionals were interviewed in detail about the child. For details of the epidemiological study, the reader is referred to Gillberg (in press a). In short, the estimated prevalence for infantile autism was 2.0 per 10,000, which is considered fairly accurate although a few cases with severe mental retardation and also a few of above average intelligence might have been missed. Other childhood psychosis cases, not fulfilling Rutter’s criteria, were about as rare as infantile autism, with the prevalence being estimated at 1.9 per 10,000.

Of the autistic children, 19% were in the normal or near-normal IQ range based on nonverbal testing, while 81% had tested IQs < 70 or were so severely retarded and disturbed as to be considered untestable.

Handedness was determined in the spring of 1983 (see below). All children were then in the age range of 7-21 years. Twenty-three percent (6/26) had developed epilepsy (one of these six children was of normal intelligence). One girl with autism, mild mental retardation, and epilepsy suffers from neurofibromatosis. One other child, a boy with severe mental retardation, has the same diagnosis. No child in the autism group suffers from any major gross motor handicap.

Control Group. For each autistic child, two children matched for age, sex, and IQ were chosen in the following way. Twenty-one of the autistic children were definitely mentally retarded with IQs ranging from 10 to 70. For these, a retarded group was selected from the register for the Board of Provisions and Services to the Mentally Retarded (BPSMR) by randomly choosing children of the same sex born in the same year and with an IQ not more than 5 units higher or lower than that of the autistic child. In Sweden, a mentally retarded person has to be registered at the BPSM R in order to obtain maximum help from society. Forty-two children were selected in this way.

For the five autistic children of normal or near-normal intelligence, comparison children (matched for age and sex with the autistic children) were randomly chosen from one school district in central Goteborg. The control group thus comprised 52 children, 40 boys and 12 girls. As in the autistic group, 19% were of normal or near-normal intelligence. Of the 81% of the mentally retarded control children, three (7Yo) (two boys and one girl) suffered from Down’s syndrome. None of the control children suffered from psychosis or”the triad of language and social impairment” described by Wing and Gould (1979).

Other Comparison Groups. In a total population study of perceptual, motor, and attentional deficits (Gillberg et al.. 1982) in Gdteborg. 42 children (33 boys and 9 girls), aged 7 years, were

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diagnosed as suffering from concomitant motor-perception-attention deficit, here referred to as MBD (minimal brain dysfunction) syndromes. All these children were of normal or near normal intelligence, and none was diagnosed as suffering from cerebral palsy. This MBD group of 42 children is used for comparison in the present study in certain instances.

In a population study of left-handedness in Goteborg (Gillberg et al., in press b) 22 left- handed boys, considered representative of all left-handed IO-year-old boys in Goteborg, and 23 left-handed girls, considered representative of all left-handed IO-year-old girls, were selected as a study group. This left-handed group will also be referred to for comparison in the present study.

Assessment of Handedness. The method for determining handedness described by Annett (1967) and referred to by Barry and James (1978) was used. The child’s hand preference when (I) pointing, (2) drawing, (3) throwing, (4) cutting, and (5) unscrewing the lid of ajar was observed. The child’s first attempt at each of these tasks was recorded. The child was considered left-handed if all the tasks were performed with the left hand, right-handed if all the tasks were performed with the right hand, and ambidextrous if neither of these categories applied.

Language Development of Autistic Children. Someautisticchildren werecompletely mute (6126 q 23%). All the others had shown echolalia for long periods of time. Most of them had grown out of the more extreme forms of repetitive noncommunicative speech, but in several instances there remained an abundance of deluyedecholuliu. This “diagnosis” was not scientifi- cally validated but was based on clinical judgments made by experienced clinical psychologists.

Reduced Optimal@ in the Prenatal, Perinatal, and Neonatal Periods. A list of 29 “optimal” conditions during pregnancy, delivery, and the neonatal period was checked for the autistic children and for the children in the MBD group and the left-handed group in order to reveal possible reductions of optimality in different groups. This method of studying prenatal, perinatal, and neonatal factors was introduced by Prechtl(l968, 1980). The same method has been used by the author in other neurodevelopmental studies (see, for example, Gillberg and Rasmussen, 1982). A high value for this factor indicates “reduced” optimality, e.g., there might have been bleeding in pregnancy, infections in pregnancy, generalized maternal edema, mater- nal proteinuria, asphyxia and hyperbilirubinemia in the child. A “reduced optimality score” of0 would indicate that all 29 conditions analyzed were optimal. A detailed survey of “reduced optimality” in the autistic children of the study has been published elsewhere (Gillberg and Gillberg, in press).

Social Class. Social class was assessed using a modified version of the Graffar classification system (Graffar, 1956), which takes account of parental occupational and educational level plus number of rooms per person. It is divided into three classes, with social class 1 being the highest.

Familial Sinistrality Score. A familial sinistrality score was computed by adding 1 point for all left-handed second-degree relatives and 2 points for left-handed first-degree relatives.

Other Parameters Studied. Computed tomographic (CT) scans of the brain were obtained in 23 (88%) of the 26 autistic patients. For details the reader is referred to Gillberg and Svendsen (1983). In the text “occipital petalia” refers to asymmetry of the brain in which the left or the right hemisphere is larger than the other hemisphere in the occipital region. “Right occipital petalia” means that the right hemisphere is larger.

Electroencephalographic (EEG) recordings (in the resting state and, in some cases, sleep recordings and recordings after hyperventilation and photic stimulation) were performed in 22 (85%) of the 26 cases. Auditory brainstem responses (ABRs) were recorded in 20 (77%) of the cases. For details, the reader is referred to Gillberg et al. (in press a).

Statistical Methods. Chi-square test (with Yates’ correction, if appropriate) was used when comparing group frequencies. Means were compared with Fisher’s exact test.

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Results

Rate of Left-Handedness. Sixty-two percent of the autistic children (16/26) were non-right-handed (Table 1). Non-right-handedness was accounted for by left- handedness in 6 of these 16 cases. The rates of non-right-handedness, and especially left-handedness, were lower in the other groups.

Table 1. Rates of handedness in autistic and other children

Study group Right-handedness Ambidexterity Left-handedness

Infantile autism 1 O/26 138% I 1 O/26 f 38%) 6/ 26 (23%11

Control group 33/52 (63% 1 16/52 (31%) 3/ 52 ( 6%)

Total population sample

of lo-year-old children2 8941985 (91%1 91/985 ( 9%)

1. < 0.05, autism p compared with control group 1x2 = 6.71, df= 21. 2. Results from epidemiological study of lo-year-old children concerning background factors in left- and

right-handedness ~Gillberg et al.. in press bl.

Hereditary Factors. Seven of the 26 autistic children (27%) had left-handed parents, brothers, or sisters. The proportion of children with left-handed first-degree relatives was about the same in the MBD group (31%), but very much smaller in a sample of non-MBD 7-year-old children (12%).

Sex Ratios. There was a marked preponderance of boys in the autistic group (boy:girl ratio in the whole group of autistic children q 3.3:l). All but one of the non-right-handed children were boys, which means that among right-handed autistic children, the boy:girl ratio was quite normal (1: 1) (Table 2). There were no corres- ponding differences between boys and girls in the control group.

Table 2. Sex ratios in various groups (boy: girl ratios)

Ambidextrous Right-handers children Left-handers

Infantile autism an = 261 1:l 9:l 6:0

Control group in = 521 3.1:1 7:l 0.5:l

Total population sample of

lo-year-old children l.l:l 1.6:1

1. Results from epldemiological study (Gillberg et al., In press bi referred to in Table 1.

Reduced Optimality in the Prenatal, Perinatal, and Neonatal Periods. There were no significant differences between left-handed, right-handed, and ambidextrous autistic children with regard to reduced optimality in the prenatal, perinatal, and neonatal period (Table 3). However, the left-handed autistic children tended to have somewhat lower scores than the others. and those three left-handed autistic children

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Table 3. Characteristics of left- and riaht-handed autistic children

Left-handers Ambidextrous (,n = 6) (n = 10)

Reduced optimality score ,’

Mean 4.5 6.0

SD 2.3 3.2

Maternal age at birth of child

Mean 31.2 30.0

SD 3.7 4.8

Sinistrality score

Mean 1.5 0.7

SD 1.8 1.1

Average/near average intelligence O/6 ( 0%) 3/10 (30%)

Mild-moderate mental

retardation 5/6 (83%) 3110 (30%)

Severe mental retardation l/6 (17%) 4/10 (40%)

Muteness 1 /6 (17%) 3110 (30%)

Abundance of delayed echolalia 5/6 (83%)’ ,,’ 2 / 10. (20%)

1. p < 0.02 when compared with right-handers; all other differences, NS.

Right-handers (n = 10)

5.9

1.8

31.2

6.1

0.4

1.3

2/10 (20%)

6110 (60%)

2110 (20%)

2110 (20%)

l/l0 (10%)

who had first-degree left-handed relatives had mean (k SD) reduced optimality scores that were particularly low (3.7 k 2.1). Left-handed children in the general population had mean (k SD) reduced optimality scores of 2.9 f 2.0 (Gillberg et al., in press b). Children with a diagnosis of MBD had mean (k SD) scores of 4.1 f 2.0. Corresponding scores in a random population sample of 7-year-old children without MBD were 2.7 f 1.4 (Gillberg and Rasmussen, 1982).

Social Class. The left-handed autistic children came from the lowest social class (class 3) in 67% (416) of the cases. The corresponding figure for the remaining autistic children was 55% ( 1 1 / 20).

Maternal Age. Maternal age at birth of the child was rather high in the whole of the autistic group. There were no obvious differences with regard to maternal age between the right- and the non-right-handed autistic children (Table 3).

Intellectual Capacity. Five out of six (83%) of the left-handed autistic children were in the mildly to moderately mentally retarded range. The corresponding proportions in the ambidextrous and right-handed autistic groups tended to be somewhat smaller-3 out of 10 (30%) and 6 out of 10 (60%), respectively.

Language Characteristics. A majority (83%) of the left-handed autistic children showed an abundance of delayed echolalia. This feature was rare in the ambidextrous

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and right-handed group of autistic children. The difference between left- and right- handed children in this respect was statistically significant at the 2% level (x2= 5.95, df q 1, Yates’ correction applied).

CT Scan Findings and ABR Results. There was a slight tendency for the left- handed autistic children to show more pathological findings on their CT scans than right-handed children. This was demonstrated by somewhat higher frequency figures for gross abnormalities (Table 4) and higher mean Evans’ ratios (higher values for this variable indicating central atrophy of the brain’). Right occipital petalia (i.e., the right hemisphere is larger in the occipital region) occurred in three out of six autistic left-handed children (50%), all of whom had left-handed first-degree relatives and in 3 out of 17 examined ambidextrous/ right-handed autistic children (none of whom had left-handed first-degree relatives). The three left-handed children and the three non- left-handed children with right occipital petalia showed low mean (f SD) reduced optimality scores (3.7 f 2.1) in both groups compared with the autistic group as a whole (5.6 f 2.5).

ABR results were very similar in the left-handed, ambidextrous, and right-handed autistic groups. Mean brainstem transmission time was equal in different groups. There were definitely abnormal ABR results in 17-25% of the cases in each handedness group of autistic children.

Table 4. CT scan findings in left- and right-handed autistic children

Left-handers Ambidextrous Right-handersl (n = 6) (n = 6) (n = 9)

Gross abnormalities Right occipital petalia

Left occipital petalia

Right frontal horn narrow

Both frontal horns narrow

Left frontal horn narrow

Evans’ ratio

216 (33%)s

316 (5~0%)~

0

l/6 (17%)

l/6 (17%)

l/6 (17%)

2f 8 (25%)

2/8 (25%)

0

318 (38%)

0

0

l/9 (11%)

l/9 (11%)

l/9(11%)

2/9 (22%)

0

0

Mean 0.260 0.260 0.245

SD 0.029 0.038 0.013

1. Only 8 of 10 ambidextrous and 9 of 10 right-l:anded children had a CT scan performed. 2. One of these two left-handers had gross changes in the right hemisphere; the other child had a widening of the

fourth ventricle. 3. All three cases had first-degree lefl-handed relatives. No differences reached the 5% level of significance.

Left Hemisphere Damage/Dysfunction in Autism. Two of the left-handed autistic children showed gross brain damage on the CT scan. One showed a widening

I, Evans’ ratio is computed by diwding the greatest distance between the lateral aspects of the frontal horns by the largest diameter in the frontal plane between the interior aspects of the skull.

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of the fourth ventricle and the other a defect in the right parietal region. A third left-handed autistic child showed EEG changes (spike and wave activity) indicative of right hemisphere dysfunction. Of the ambidextrous children, one showed a defect at the site of the right lateral geniculate body, and another a widening of the fourth ventricle. Of the right-handed autistic children, only one showed gross CT changes, which were located in the left hemisphere.

Discussion

All the children of the present study were 7 years old or more at the time of the handedness determination. Two-thirds of the left-handed autistic children were IO or older. Thus, it is unlikely that any large fraction of the non-right-handedness found could be accounted for by young age and immature patterns of lateralizaton.

The present results suggest that the proportion of non-right-handed children in an infantile autistic sample is indeed elevated when compared with other children. More than 60% of the autistic children of the total population sample compared with 37% of the age-, sex-, and IQ-matched control children showed non-right-handedness. As the control group was matched for mental age, the link between non-right-handedness and autism apparently is not with the mental retardation of autism but with some other mechanism more specific to autism. This conclusion is also suggested by the finding that severe mental retardation was no more common among the left-handed children with autism than among the right-handed children with autism.

With regard to heredity for left-handedness, the comparison group that most closely resembled the autism group was the MBD group. MBD as diagnosed in this context required the presence of both attentional deficit signs and motor/ perception dysfunc- tion. Several of the children in the MBD group showed “psychotic behavior” (Gill- berg, in press b), a diagnostic category with much in common with “the triad of social and language impairment” characterized by Wing and Gould [ 1~ IY). I ms tatter category is considered by Wing to represent a broader definition than “infantile autism” but with many of the characteristics of autism.

Some studies of handedness in infantile autism have reported results compatible with the present findings (Hauser et al., 1975; Colby and Parkinson, 1977; Hier et al., 1979). However, other researchers have failed to demonstrate a clear-cut relationship between left-handedness and autism (Boucher, 1977; Barry and James, 1978). A study by Prior and Bradshaw (1979) produced relatively high figures for non-right- handedness in autism, but these were not accounted for by left-handedness but exclusively by ambidexterity. The criteria for being diagnosed as left-handed in the Prior and Bradshaw study were somewhat different from those used here and included “kicking a ball with the left foot.” Many studies have shown that handedness and footedness are by no means strongly correlated (e.g., Rasmussen et al., in press), and it is quite possible that if the present study had used the same diagnostic criteria as used by Prior and Bradshaw, the results might have been more closely comparable. This discussion highlights the need for universal criteria for diagnosing handedness. It also shows that divergent results may be due to differences in diagnostic criteria. Neverthe- less, al/studies to date examining the correlation between handedness and autism have yielded results consonant with the hypothesis that autistic children tend to be less

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strongly lateralized in right-hand usage than normal children. Also, one must bear in mind that the other studies have not been on total population samples and the results are not immediately comparable with each other.

It appears that there are at least two major reasons for left-handedness in autism. One is heredity and the other is brain damage. The interesting finding that the three left-handed autistic children with “strong” heredity for left-handedness all showed a conspicuously large right hemisphere in the occipital region deserves special mention. It is possible that this reflects a common denominator for some cases of left- handedness in autism (i.e., hereditary right hemisphere “dominance”), but this conclu- sion is at most tentative and the findings are in need of further investigations (e.g., CT brain scans of parents of autistic children). Theextended pathological left-handedness model of Bishop (1980), which postulates that the proportion of left-handedness in brain-damaged populations is greater than in nondamaged groups and that left- handedness is often a sign of “shift” of handedness, is applicable in the discussion of the three left-handed autistic children without heredity for left-handedness. These three children showed rather high scores for reduced optimality in the prenatal, perinatal period. These reductions might point in the direction of brain damage in that group.

It was rather surprising to find that when unilateral brain dysfunction/ damage was demonstrated in the left-handed autistic children, it was always located in the right hemisphere. The damage found was not located in the motor cortex, but it is some- what unexpected that left hemisphere damage was not demonstrated in any case. However, it would be misleading to assume that most left-handers have a right hemisphere “dominance.” Milner et al. (1964) have shown that 6470 of “normal” non-right-handers have left hemisphere speech.

An abundance of delayed echolalia was typical of the left-handed autistic children, irrespective of whether the “hereditary” or the “nonhereditary” groups of left-handed autistic children were examined. Not much is known about the biological substrate for this fairly characteristic symptom in autism, but the link seen here with left- handedness calls for further exploration of the relationship between language func- tions and cerebral dominance in autism.

Ambidexterity in autism might be connected with hereditary factors in some cases, but might also be due to immature brain development, as suggested by Barry and James (1978).

Sex ratios in infantile autism have recently been the subject of a study by Wing (1981). Both the study of Wing and the studies of other authors have shown that the preponderance of boys in autism is not very strong among severely retarded children, but that with increasing IQ the proportion of boys becomes greater. In the present study there were interesting sex ratio differences between the left- and right-handed autistic groups. All the left-handed autistic children were boys, and the boy:girl ratio among right-handed autistic children was consistent with normal populations. This might indicate that autistic girls are more clearly “lateralized” in their brain functions than autistic boys. It might also be a sign that autism in boys is a rather different condition from autism in girls, despite similar symptomatology. The subject is a very difficult one and simple cause-and-effect relationships are not likely to be the ultimate result of the efforts made to disentangle the many clues.

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The results of the present study support the view that left-handedness is associated with some cases of infantile autism. However, no clear-cut relationship between left hemisphere dysfunction and autism could be demonstrated; rather, the results pointed in the direction of right hemisphere dysfunction in some left-handed autistic children. Left-handedness should not be regarded as proof of left hemisphere dysfunction in autism. Obviously some autistic children are left-handed because of hereditary fac- tors, others because of brain damage. Immature patterns of lateralizationPor brain damage leading to immaturity-are likely to account for the high proportion of ambidexterity seen. From the available evidence it would be premature to formulate any “umbrella” hyothesis with regard to autism and left hemisphere dysfunction. Further studies are needed on heredity (and just what it is that is inherited) and on the correlations between handedness, language, and autism before the importance of unilateral brain dysfunction in autism can be assessed.

Acknowledgments. This work has been supported by the Radda Barnens Riksforbund (The Swedish Save the Children Federation). Mrs. G. Jakobsson deserves special mention for brilliant secretarial assistance. Thanks are also due to Inger Winnergard, M.D., who gave invaluable help in the handedness determination. Birgit Borjesson and Anne Helgegren assisted in the data collection.

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