hemisphere functioning in autistic children

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HEMISPHERE FUNCTIONING IN AUTISTIC CHILDREN Margot R. Prior and John L. Bradshaw (Department of Psychology, La Trobe University, Bundoora, and Department of Psychology, Monash University, Clayton) There is now considerable support for the theory that a severe and global language deficit underlies the childhood disorder known as autism (Rutter, 1974, Churchill, 1972; Hermelin and O'Connor, 1970; Prior, 1975). The syndrome· has many features in common with developmental aphasia (Savage, 1968; Churchill, 1972); although with amelioration or recovery, the outcome on the latter disorder is rather different from that in autism. A notable characteristic of many autistic children is a particular pattern of performance on intelligence tests, with verbal measures being almost invariably much below performance measures. Moreover, subtests in which functioning is generally least retarded amongst autistic children are those which are reputed to reflect right-hemisphere mediated abilities, viz. block design, object assembly and form-boards. It is also the case that the language performance of many autistic children is characterized by concre- teness, repetitiveness, and recognition without analysis - all considered right hemisphere functions. On the basis of abnormal pneumographic findings in 15 of 17 language retarded autistic children which indicated ventricular enlargement with the deficiency of brain substance in the left cerebral hemisphere, Hauser, DeLong and Rosman (1975) have suggested a major left-sided cerebral abnormality in these children. In support of their hypothesis they note that eight children were left-handed and three had no hand preferences. They further suggest that some motor and language functions had been 'taken over' by the right hemisphere. They present human adult ancf animal evidence linking temporal lobe damage to behavioural deficits similar to those observed in autistic children. Although these findings as yet lack replication and the argument is somewhat tenuous, it seems reasonable to explore hemisphere functioning further, in the search for possible causes of autism. Lesions of the left temporal lobe are known to impair ability to assimilate verbal auditory material (Milner, 1974) and this is without Cortex (1979) 15, 73-81.

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Page 1: Hemisphere Functioning in Autistic Children

HEMISPHERE FUNCTIONING IN AUTISTIC CHILDREN

Margot R. Prior and John L. Bradshaw

(Department of Psychology, La Trobe University, Bundoora, and Department of Psychology, Monash University, Clayton)

There is now considerable support for the theory that a severe and global language deficit underlies the childhood disorder known as autism (Rutter, 1974, Churchill, 1972; Hermelin and O'Connor, 1970; Prior, 1975). The syndrome· has many features in common with developmental aphasia (Savage, 1968; Churchill, 1972); although with amelioration or recovery, the outcome on the latter disorder is rather different from that in autism. A notable characteristic of many autistic children is a particular pattern of performance on intelligence tests, with verbal measures being almost invariably much below performance measures. Moreover, subtests in which functioning is generally least retarded amongst autistic children are those which are reputed to reflect right-hemisphere mediated abilities, viz. block design, object assembly and form-boards. It is also the case that the language performance of many autistic children is characterized by concre­teness, repetitiveness, and recognition without analysis - all considered right hemisphere functions.

On the basis of abnormal pneumographic findings in 15 of 17 language retarded autistic children which indicated ventricular enlargement with the deficiency of brain substance in the left cerebral hemisphere, Hauser, DeLong and Rosman (1975) have suggested a major left-sided cerebral abnormality in these children. In support of their hypothesis they note that eight children were left-handed and three had no hand preferences. They further suggest that some motor and language functions had been 'taken over' by the right hemisphere. They present human adult ancf animal evidence linking temporal lobe damage to behavioural deficits similar to those observed in autistic children. Although these findings as yet lack replication and the argument is somewhat tenuous, it seems reasonable to explore hemisphere functioning further, in the search for possible causes of autism. Lesions of the left temporal lobe are known to impair ability to assimilate verbal auditory material (Milner, 1974) and this is without

Cortex (1979) 15, 73-81.

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74 M. R. Prior and ]. L. Bradshaw

doubt a major impairment m all autistic children (Prior, Gajzago and Knox, 1976).

There are two schools of thought concerning the development of lateralization in young children and its relationship to language usage. According to one the right ear advantage (as shown in dichotic listening tasks) continues to increase until puberty (Lenneberg, 1967; Satz, Bakker, Teunissen, Goebel and van der Vlugt, 1975). Others however (Berlin, 1973; Geffen, 1976; Hiscock and Kinsbourne, 1977; Krashen, 1975) believe that lateralization of the language function is complete in normal children by the age of four to five years. However Porter and Berlin (1975) urge caution in interpreting developmental studies. Certainly there are left-right asymme­tries in the anatomy of the forebrains of neonates and even foetuses (Chi, Dooling and Gilles, 1977; Rubens, 1977; \Vitelson and Pallie, 1973) and Etus, (1975) has reported differences in the non-nutritive sucking reflexes of neonates to speech sounds presented to the left and right ears. Answers to this question may be sought for in studies of language disordered children showing various degrees of language competence. For example if lateralization is necessary for language acquisition one would expect to find evidence for left (or right) hemispheric dominance for speech signals in autistic children who have acquired language. If lateralization increases with language acquisition one would expect that the greater the level of language competence achieved the greater the strength of laterality in such children (allowing for ceiling and floor effects). Unfortunately the nature of the techniques available for the measurement of laterality is such that such measurement would be not be easy.

Although there has been speculation that children with specific learning difficulties, especially language based disabilities, may have abnormal 'cerebral dominance' (Witelson and Rabinovitch, 1972) there is very little reported research which could illuminate the difficulties of autistic cases. Sommers and Taylor (1972) found that more words and digits were reported from the left ears of a "dyphasic" group of children while the opposite was reported for normal subjects. However this paradoxical left ear preference shown by the dysphasic group was only significantly different from the normal group performance for dichotically presented digits. The perform­ance of children with auditory-linguistic deficits in the Witelson and Rabinovitch study (1972) did not support an hypothesis of lack of laterali­zation of speech functions per se. Like the aforementioned group, they showed a left-ear preference for digits and these authors suggest that the impaired children do show lateralization of speech function though indeed with perhaps a higher incidence of right hemisphere superiority for speech functions than shown in normal children. However this finding is qualified by the lack of right ear advantage in the normal control group.

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Because of the still controversial nature of current theories of hemi­spheric specialization (viz. is it absolute, partial or merely reflecting attentional biases, is the dichotomy verbal/visuospatial or the possibly more fundamental processing distinction of analytic/holistic?) (Bradshaw, Gates and Patterson, 1976 ), no particular hypotheses were formulated for this study. Rather, an attempt was made to examine ear advantage in a dichotic listening task and to relate performance to salient characteristics of autistic children such as mental age, handedness, verbal ability, language development history and task competence. What is known about the disabilities of autistic children might lead to hypothesis that because language deficits are central to the disorder, those children who learn to speak may do so because language functions are able to develop in the right hemisphere, whilst those who do not are more severely damaged perhaps bilaterally and are unable to make this transfer. Milner ( 197 4) and Krashen ( 197 3) have noted that with adults left lesions impair performance on verbal tests with little effect on spatial and configurational tests; however since autistic children frequently function below normal even on such right hemisphere functions and since a diagnosis of autism requires onset of the disorder before two years of age, then some right hemisphere damage must be implicated. Perhaps if the damage is not severe the right hemisphere can take over language functions (to the probable detriment of its visuospatial processing capacities) and therefore one would expect a higher probability of the development of language in cases whose right hemisphere functions are reasonably intact. There is support for this in that language is most likely to develop in those children who show a normal or near normal level of functioning on IQ (performance) tests. If this were the case a left ear advantage would be predicted in children with well developed language and no ear advantage predicted in children at early stages of language learning. It is worth noting that transfer of function is rare after five years of age (Krashen, 197 3) and autistic children almost never develop language after five or six years of age. In this paper we report an examination of hemisphere functioning in autistic children using measures of hand and foot preference and a dichotic listening task.

MATERIAL AND METHOD

Subjects

A total of 23 children who had previously been diagnosed as autlstlc was included in the study. In addition all subjects fulfilled the Prior, Boulton, Gaj­zago and Perry ( 1975) criteria for a diagnosis of autism; viz. aloneness from early in life, bizarre and obsessive behaviour, poor or absent eye contact and inability to use speech to communicate in a normal way. Three children proved

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76 M. R. Prior and ]. L. Bradshaw

unable to do the dichotic listening task because they did not understand what response was required and one child refused to speak during the session although she clearly understood the requirement and would point to pictures representing the stimuli. Thus 19 children actually completed the dichotic listening task. The mean chronological age (CA) of the group of 14 boys and 5 girls was 11 years, 1 month, ranging between 8 years 2 months and 13 years 10 months. Verbal mental age (MA) and IQ were assessed with the Peabody Picture Voca­bulary Test (PPVT) (Dunn, 1965). The mean MA was 6 years 9 months (range, 3 years 2 months to 14 years 2 months) with mean IQ, 68.

A control group of 19 right-handed normal primary school children was also tested. Their mean MA was 8 years 2 months and all IQs were in the normal range. There was no significant difference between the group in mean MA by t test. No child in either group had any apparent hearing problems.

Apparatus

Tests for handedness were as follows: demonstrate cleaning of teeth; write or draw on paper; throw a ball (3 times); kick a ball off the floor (3 times); strike or pretend to strike a match. In each case the object to be used was placed in front of the subject directly in his midline and he was asked to pick it up and complete the task.

The dichotic listening tape was prepared using the automatic alignment method of Vincent and Bradshaw (1975). Stimuli were 34 word pairs made up from single syllable items from the PPVT with no word being used more than twice and then each time in a different ear. The first ten word pairs were used for practice items, the remaining 24 being test pairs. The tape was played on a Sony reel to reel portable stereo recorder through earphones with the volume of stimuli reaching the ears varying between 70 and 75 dB.

Procedure

Cihldren were tested in a familiar room at their Day Centre or School in one session lasting from 20 to 30 minutes. They were first tested for hand preference, then given the dichotic listening task and finally the PPVT. For the dichotic listening test subjects were told to "Tell me just what you hear; tell me in a loud voice". Subjects were randomly assigned for presentation of either list to either right or left ear so that 10 subjects heard List A through the right ear and 9 subjects heard List A through the left ear.

Practice pairs were given until it was clear that the subject understood the task (in most cases immediately) before presentation of test pairs.

RESULTS

Handedness

All 23 autistic children were tested on the five handedness measures. The adoption of a criterion of at least 4 of the 5 tests showing a consistent hand preference gave 17 clearly right-handed subjects, no left-handed subjects and 6 showing a mixture of preferences. It is worth noting here

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that if only writing or drawing hand preference had been used as the meas­sure of handedness, then 21 subjects would have been classified as right­handed, and one would have been classed left-handed, although in this case all other tasks were done with the right hand. Those children with a mixture of preference were classed as such, generally because they were apparently developmentally immature and their preference reflected poor coordination and ability to do the task, rather than being a real indicator of preference. In the match striking task, an exercise which was apparently quite new to most of the children and thus perhaps a good measure of preference, 20 subjects preferred to try with the right hand. All 23 subjects used the right hand to demonstrate use of tooth brush. Left and mixed preferences were most often shown in throwing and kicking the ball and sometimes indicated poor skills in this area.

The relationship between handedness and laterality was examined in those 19 subjects who completed the dichotic listening task. The criterion for ear advantage was . the weaker one used by Berlin, Hughes, Lowe-Bell and Berlin ( 197 3) i.e. a difference of 2 or more in correct ear responses. Of the 15 subjects classed as right-handed, 6 showed a left ear advantage, 5 showed a right ear advantage and 4 showed no advantage. A Fisher Exact Test indicated no relationship between handedness and ear advantage.

Dichotic listening

In analysing the data (number of correct responses) for the control group a number of different methods were used (see Birkett, 1977) to ensure that the results were robust and not dependent on the method of analysis used. The results of these analyses are reported elsewhere (Davidson and Prior, 1978) and thus no details will be given here, but by analysis of variance, correlated samples t test, and using the formula (R- L)/(R + L) 100 [where R (or L) is the number of trials on which the correctly identified syllable was delivered to the right (or left) )ear] all produced a significant right ear advantage (p < .01) for the control group. Thus it was clear that this procedure with MA matched normal children produced the expected right ear advantage.

The performance of the autistic group was characterized by considerable individual differences. Five subjects showed a clear right ear advantage (an ear difference of 3 or more); seven subjects showed a left ear advantage, and the remaining seven no advantage for either ear. The mean number of errors on the task was 7.1 (S.D. 3.2). This was not different from that of the control group (mean 7.7, S.D. 3.4.) indicating parity of performance levels between the groups. No autistic child ever reported more than one word although one older girl of normal IQ level reported that she 'could hear

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78 M. R. Prior and ]. L. Bradshaw

another noise'. By contrast 5 normal children reported more than one word at least on some occasions.

There was no difference overall within the autistic group in numbers of words correctly reported from each ear (t = .35, n.s.). Additional analyses were carried out to examine the relationship between lateral preference and other relevant clinical variables. For these analyses the Fisher Exact Test was used with preference defined as a difference of 3 or more. There was a significant difference between lateralized (in terms of either left or right ear advantages) and non-lateralizated children with respect to the presence or absence of speech before the age of 5 years, with 11 of the former having speech and only 2 of the latter. A parallel result obtained when lateralized and non-lateralized children were compared in terms of either high or low IQ (arbitrarily set at above 65 and below 58). Thus there appeared to be a relationship between presence of speech before 5 and also IQ level and laterality. Of those 13 children with speech before 5, 6 showed a left ear advantage and 5 showed a right ear advantage. Of the 5 children with mental ages below 5~ years only 1 showed an (right) ear advantage. Of the four children with 'normal' IQ, two showed a left ear advantage (and were both right-handed) and two showed a right ear advantage (and were both right-handed). Of the three lowest functioning children with minimal language (IQ below 40), none showed any ear advantage and one showed mixed preference on the handedness tasks.

There was a significant excess of autistic children showing a left ear advantage when compared with the normal group (p < .01, Fisher Exact Test). Thus although heterogeneous within the group the autistic subjects were clearly different from normal subjects in terms of this excess of right hemisphere dominance for verbal stimuli. There were no sex differences within the group.

Error types

For both aut1st1c and control groups the kinds of errors made were unremarkable since with almost no exception they consisted of combinations of the two words heard e.g. kie for pie and key. Most involved a displa­cement of initial or final consonant and occasionally an intruded first consonant e.g. take for cake and coat.

DISCUSSION

Two findings of this study seem to be of particular importance in illuminating language disorder in childhood autism. These are firstly the finding of a significant excess of right hemisphere dominance for verbal stimuli, and secondly the relationship between dominance, speech develop-

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ment, and intelligence level. The excess of right dominanec in this group of autistic children which is similar to that found in earlier studies with language disordered children (Witelson and Rabinovitch, 1972; Sommers and Taylor, 1972) suggests that (a) there is experimental support for the hypothesized centrality of the language disorder in autism (Prior, 1975; Churchill, 1972); and (b) for at least a proportion of cases, language functions may be taken over or may develop in the right hemisphere perhaps as a results of impairment in left hemisphere functioning. Incidentally there was no real support in this study for the hypothesis (Witelson and Rabinovitch, 1972) that right-sided speech function is related to poorer visuospatial skills as all the right hemisphere dominant children here, for whom performance IQs were available had higher performance than verbal IQs with the particular pattern of strengths so frequently noted for autistic children such as block design and object assembly. However it must be noted that only for 2 of these children was performance IQ in the normal range.

It is now known that those autistic children most likely to achieve normal or near normaf adjustment are those with adequate language skills and absence of severe intellectual retardation (Rutter, 1974). In view of this and the facts that language in autistic children rarely begins to emerge after the age of 5 or 6 years, and lateralization of language function is probably complete by age 5, it seems a tenable hypothesis that the presence or absence of language lateralization might also be a good predictor of outcome in autism. For the theory of laterality and development this would be support for the suggestion that laterality precedes language development and that language emerges consequent upon the 'fixing' of hemisperic specialization.

The results of the handedness testing are somewhat at variance with earlier reports on handedness in autistic children (Colby and Parkinson, 1977; Boucher, 1977; Hauser et al., 1975) where a number of left­handed autistic children were noted. This contradiction may reflect sampling differences, level of retardation differences (since retardation and poor skills affect handedness measures) or perhaps differences in the methods used to estimate hand preference. It does however fit in with studies of normal subjects indicating that several measures of handedness will produce different results and that extreme care is necessary both in assessment and in inter­pretation in this area. It is worth noting that Boucher ( 1977) used a number of measures of handedness and did not find the expected excess of left-handed autistic subjects in a larger group of 46. The lack of relationship between handedness and hemisperic dominance in the present sample is in line with Kinsbourne's (1975) conclusion that there was not a close relationship between handedness and language lateralization. In any case since many autistic children are developmentally retarded and often poorly

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80 M. R. Prior and ]. L. Bradshaw

motivated with consequent poorly developed eye-hand and foot-hand coor­dination skills, it seems premature at this stage to make etiological inferences from handedness data.

The interpretation of the results of the dichotic listening task can at this stage only be speculative but it does at least suggest a difference in the process of language lateralization in autistic children, when compared with normals, which warrants further investigation. If autistic children do suffer from some kind of left hemisphere abnormality it would be as Sear­leman (1977) has noted, of considerable theoretical and clinical interest if the reasons for takeover by the right hemisphere in some cases but not in other could be discovered. A further point of note is the reported deficiencies in abstract linguistic abilities even in relatively well adjusted autistic adults suggesting incomplete transfer if it does occur (Searleman, 1977). However arguments concerning many aspects of the relationship between measures of laterality including dichotic listening continue to receive critical attention (e.g. Yates, 1972; Blumstein, Goodglass and Tartter, 1975; Freides, 1977; Birkett, 1977 ), and therefore further research with clinical groups of children will need to consider differences with respect to experimental paradigms as well as clinical issues.

SUMMARY

Recent research in childhood autism has provided support for the hypothe­sis that a central cognitive deficit involving severe language impairment underlies this disorder. In this study a group of autistic children were tested for handed­ness and for lateralization of speech function using a dichotic listening task. Contrary to earlier reports there were no left-handed children in the group although a number showed mixed preference. In the dichotic listening task using pairs of single syllable words the autistic group performed similarly to a matched group of normal children in terms of numbers of correct responses but over all did not show the right ear advantage characteristic of the normal children. There was a significant excess of right hemisphere dominance for verbal stimuli amongst the autistic children suggesting that for some at least, language functions had de­veloped in the right hemisphere. Lateralization was shown to be related to pre­sence or absence of speech before the age of 5 years and to IQ level.

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M. R. Prior, Department of Psychology, La Trobe University, Bundoora, Victoria, Australia.