J Autism Dev Disord (2008) 38:15741580 DOI 10.

1007/s10803-008-0540-3

ORIGINAL PAPER

Language Abilities of Children with Asperger Syndrome

Esko Toppila Teija Kujala Minna Laakso Satu Saalasti Tuulia Lepisto Taina Nieminen-von Wendt Lennart von Wendt Eira Jansson-Verkasalo

Published online: 7 March 2008 Springer Science+Business Media, LLC 2008

Abstract Current diagnostic taxonomies (ICD-10, DSMIV) emphasize normal acquisition of language in Asperger syndrome (AS). Although many linguistic sub-skills may be fairly normal in AS there are also contradictory ndings. There are only few studies examining language skills of children with AS in detail. The aim of this study was to study language performance in children with AS and their age, sex and IQ matched controls. Children with AS had signicantly lower scores in the subtest of Comprehension of Instructions. Results showed that although many linguistic skills may develop normally, comprehension of language may be affected in children with AS. The results

suggest that receptive language processes should be studied in detail in children with AS. Keywords Asperger syndrome Language Comprehension of instructions Executive dysfunction

Introduction Asperger syndrome (AS) is a lifelong neurobiological disorder of social interaction and behaviour. It belongs to the continuum of autistic spectrum disorders (ASD) (Frith 2004; Wing 1981; Gillberg and Gillberg 1989; Klin et al. 2000). The ICD-10 or DSM-IV diagnosis of AS is based on the following behavioural criteria: Qualitative impairment in social interaction, restricted repetitive and stereotyped patterns of behaviour, interests and activities, and no clinically signicant general delay in language or cognitive development (WHO 1993; APA 1994). Difculties of communication and social interaction are the core of all autistic disorders. Clear explanations for these difculties are yet to be resolved. Research on communication in children with AS has mainly focused on pragmatic disorders since most of these children have problems in interactive language use, with respect to both language production and comprehension (Adams et al. 2002; Bishop 1989; Ghaziuddin and Gerstein 1996; Tager-Flusberg 1999; Koning and McGill-Evans 2001; Landa 2000; Shriberg et al. 2001). Accordingly, the speech of individuals with AS is uent but pragmatically impaired. Also, interpretation of utterances is literal (Rapin and Dunn 2003), causing difculties in understanding idioms (Kerbel and Grunwell 1998), humour (Ozonoff and 1993, 1995). Miller 1996), metaphors and irony (Happe Speech is often syntactically impeccable and atypical for

T. Kujala E. Jansson-Verkasalo S. Saalasti T. Lepisto Cognitive Brain Research Unit, Department of Psychology, University of Helsinki, Helsinki, Finland L. von Wendt S. Saalasti T. Lepisto Department of Child Neurology, Helsinki University Central Hospital, Helsinki, Finland S. Saalasti (&) M. Laakso Department of Speech Sciences, University of Helsinki, P.O. Box 9, Helsinki 00014, Finland e-mail: satu.saalasti@helsinki. E. Toppila Finnish Institute of Occupational Health, Helsinki, Finland T. Nieminen-von Wendt Department of Adolescent Psychiatry, Jorvi Hospital, Espoo, Finland T. Nieminen-von Wendt Medical Centre Dextra, Helsinki, Finland E. Jansson-Verkasalo Faculty of Humanities, Logopedics, University of Oulu, Oulu, Finland

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the chronological age of the children (Attwood 1998; Ghaziuddin et al. 2000; Rapin and Dunn 2003). Furthermore, individuals with AS display substantial difculties in the production and comprehension of speech prosody (Koning and McGill-Evans 2001; Shriberg et al. 2001). However, it is not yet known to what extent the difculties in communication are actually due to linguistic problems. Current diagnostic taxonomies exclude problems in language development in AS (ICD-10; DSM IV). Although many linguistic sub-skills have been shown to be fairly normal in AS (Frith 2004), there are also contradictory ndings. For example, Gillberg and Gillberg (1989), Tantam (1988) and Wing (1981) suggest that delays in language development may be associated with AS. The vocabulary of children with AS has been described as adult like (Attwood 1998). In contrast, adults with AS were shown to perform below chronological age in tests of receptive and expressive vocabulary (Howlin 2003). Furthermore, in spite of uent verbal expression, problems in understanding semantics, as in multiple word meanings, are typical in AS (Kerbell and Grunwell 1998). Problems with receptive language have been reported to be more common than impairments in expressive language among individuals of the whole ASD group (Kjelgaard and Tager-Flusberg 2001; Rapin and Dunn 2003). The denition of language and the aspects of language that are considered may contribute to the opposite ndings in earlier studies (Tager-Flusberg 1999, 2004; Bartlett et al. 2005). Furthermore, there are only few studies investigating language development and linguistic skills in children with AS in detail. So far, there is no consensus on the fundamental psychological or neural decits underlying the impairments of communication and language in AS. Cognitive impairments of individuals with AS are much less severe than in autism (Ozonoff et al. 1991). It has been shown, however, that individuals with AS have decits in executive functions (Joseph et al. 2005), and at the pivotal level of perceptual processing (Iarocci and McDonald 2006; Nieminen-von Wendt 2005). Furthermore, the central auditory processing is altered in children with AS, as indicated by studies using event-related brain potentials et al. 2006). (Jansson-Verkasalo et al. 2003, 2005; Lepisto Although pivotal and central auditory processing are atypical in children with AS, it is not yet known whether these decits contribute to language comprehension at the behavioural level, and in different kinds of conditions. It is possible that language comprehension is normal in silent, laboratory like situations. Problems in auditory processing and language comprehension may arise, however, in challenging listening conditions, such as those including background noise, as found in adults with high-functioning autism (HFA) or with AS (Alcantara et al. 2004) or when there are many speakers.

The question of the role and nature of language impairment in AS remains inadequately outlined in previous studies. The purpose of the present study was to make a detailed exploration of the language competence of schoolaged children with AS. We hypothesized that difculties in language development would manifest as poorer performance in the selected measures of language. In particular, we expected that children with AS would perform below average in receptive subtests of the selected language measures. Furthermore, we measured the effect of noise to language comprehension.

Methods Participants The participants of the study were 22 children with AS (16 boys and 6 girls; mean age 8.9 years, range 7.0 10.4 years). Children were recruited from the Helsinki University Central Hospital (HUCH, population catchment area 1.4 million), and the Helsinki Asperger Center at the private medical centre Dextra. AS was clinically diagnosed, based on Autism Spectrum Screening Questionnaire (Ehlers et al. 1999), the Autism Diagnostic InterviewRevised (Lord et al. 1994), and the Autism Diagnostic Observation Schedule (Lord et al. 2000). Diagnoses were made by experienced teams of professionals (child neurologist, neuropsychologist and registered nurse), and the diagnosis was only nalized after agreement in the group responsible for the diagnostic procedure. Only children who met the ICD-10 (WHO 1993) criteria for AS, and had acquired language within the normal milestones (words at the age of 1 year and sentences at the age of 2 years) were included in the study. Furthermore, the children included in the study had no reported hearing difculties and no other diagnosed neuropsychiatric conditions, learning disabilities (dysphasia, dyslexia) or depression. The participants of the control group were 23 healthy children (17 boys and 6 girls) recruited from normal elementary schools from Helsinki. Their mean age was 9.0 years (range 7.610.6 years). Parents received an introductory letter on the experiment through teachers. Information on childrens health and development was obtained by a questionnaire completed by the parents. The children included in the control group had a history of typical neurological development: no learning difculties and no severe neurological conditions had been reported in their families. All the children had a full scale IQ (WISCIII, Wechsler 1991) of at least 85. There was no statistical difference between groups in IQ (Table 1). IQ testing (WISC-III, Wechsler 1991) was performed either as a part

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of the diagnostic procedures or as a separate session within this study similarly as for the controls. Behavioural Measures of Language Abilities Childrens language abilities were measured extensively (Table 2). Vocabulary and naming abilities were measured with the Finnish version (Laine et al. 1997) of the Boston Naming Test (Kaplan et al. 1983), in which the children were asked to name pictures. If they were unable to name them, they were given semantic and nally phonetic prompts to help the word nding process. The Rapid Automized Naming Test (Ahonen et al. 1999) was conducted to measure the word nding process in more detail. In this speeded naming task children were asked to name colours and mixed symbols (letters, numbers and colours). The two word nding tests were selected because of their relevance to speech comprehension and semantic processing. Furthermore, selected subtests tapping various language abilities were selected from the Finnish Developmental Neuropsychological Evaluation (NEPSY; Korkman et al. 1997), NEPSY is a standardized neuropsychological test battery for children, and was recently demonstrated to be a reliable method for nding different neurocognitive phenotypes in ASD (Hooper et al. 2006). The Sentence Repetition subtest measures the linguistic short-term memory. Verbal Fluency evaluates verbal expression, uency and inventiveness. In the Word Fluency task children are asked to say as many words as possible in a certain

semantic or phonetic category in one minute. The Nonword Repetition task measures childrens ability to analyse and reproduce phonological knowledge. The Phonological Processing subtest ascertains childrens ability to perceive word structure. In this test children are asked to change the syllable or phoneme structure of different words. Subtest of Comprehension of Instruction evaluates verbal comprehension and auditory working memory. Children are given verbal instructions, according to which they have to touch coloured geometrical gures. The Comprehension of Sentences subtest evaluates knowledge of syntactic structures of language. In this subtest children are required to answer to syntactically complex questions. Auditory processing was further evaluated by measuring sentence comprehension in background noise. Two different noises, cafeteria noise and white noise, were used in the study in the background of the sentence comprehension subtest. The cafeteria noise was recorded in a cafeteria using a DAT tape recorder (TASCAM, USA). A recording microphone BK4139, (Bruel & Kjaer, Denmark) was used. After the recording the signal was transferred into the computer. In the computer the noise amplitude was stratied so that the amplitude variation was less than 2 dB. The 1 s mean frequency spectrum of the signal was also shaped to be the same in the recording. The white noise, used in a separate condition, was ltered to have the same spectrum as the cafeteria noise and the amplitude was adjusted to the same level. The signal-to-noise ratio was adjusted to 0 dB. Procedure

Table 1 Ages and IQs of the children participating in the study AS (n = 22) M (SD) Age Verbal IQ Performance IQ Full-scale IQ 8.9 (0.9) 112 (17.3) 104 (17.1) 108 (13.5) Controls (n = 23) M (SD) 9.0 (0.7) 112 (12.9) 108 (12.7) 110 (10.4) p-value 0.66 0.95 0.29 0.62

The p-values were obtained by one-way ANOVA

Table 2 Language tests used and language functions measured Test NEPSY Language ability Phonological processing Comprehension of instructions Sentence comprehension Non-word repetition Fluency Sentence repetition Boston naming test Rapid automized naming Naming Speeded naming

Testing was carried out between 9.00 and 17.00 at the Cognitive Brain Research Unit of the Department of Psychology, University of Helsinki. All subjects were given a simple written outline of the procedure to help them to follow the course of the session. Two different testing orders were used to avoid order effects and changed alertness. The children had at least one break during which they were offered snacks. The language testing alone took altogether 12 h. The expenses of all participants were reimbursed. Written consent was obtained from all the parents. The study was approved by the ethical board of the Department of Psychology and the ethical committee of HUCH. Statistical Analysis Raw scores were used in the between-group analysis. Oneway analyses of variance (ANOVA) were conducted separately for each subtest in order to evaluate whether the groups differed signicantly on the language skills. The relationship of the group with variables was further analysed using effect size statistics (ETA squared). The

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intergroup difference in sentence comprehension was tested using two-way ANOVA for repeated measures with Group as a between-subject factor and Noise (cafeteria noise 9 white noise) as a within-subject factor. Missing data value of one participant in the control group was replaced by the mean score of all of the subtest scores of the group in two subtests (in the two noise conditions of Sentence Comprehension subtest). The criterion p-value of 0.05 was used to establish statistical signicance. However, because multiple statistical tests were performed, we applied a Bonferroni correction yielding a corrected a = 0.0038.

Results Children with AS scored signicantly lower than the controls in the Comprehension of Instructions test (F(1,43) = 10.98, p = 0.002, ETA squared = 0.203) (Table 3, Fig. 1). The range of the scores in this test was also greater in the group of children with AS than in the control group. According to effect size statistics, the grouping variable explains 20.3% of variance in the dependent variable. Moreover, children with AS tended to perform worse than their controls in the Phonological Processing subtest (F(1,43) = 4.10, p = .049, ETA squared = 0.087) (Table 3). Instead, the children with AS performed similarly to their controls on the, uency (semantic and phonetic uency), naming, speeded naming, non-word repetition and sentence repetition tasks (Table 3). The background noise had similar effects on the sentence comprehension in both groups (Table 3). Although both groups appeared to obtain
Fig. 1 Box-and-Whisker plot graph of differences between groups in the subtest of Comprehension of Instructions. Children with AS scored signicantly (p = 0.002) lower than the controls in the Comprehension of Instructions test. The range of the scores is greater in the group of children with AS than in the control group

lower scores in the cafeteria condition than in the silent and white noise conditions, this effect was not statistically signicant.

Discussion Signicant differences between the children with AS and their controls were found in the Comprehension of Instructions subtest. Children with AS scored signicantly

Table 3 Mean scores, standard deviations (SD) and p-values of subtests of language skills (one-way ANOVA) Language subtest AS Mean Phonological processing Comprehension of instructions Non-word repetition Fluency Semantic uency Phonetic uency Sentence comprehension Sentence comprehension in cafeteria noise Sentence comprehension in white noise Sentence repetition Naming Speeded naming of colours Speeded naming of mixed symbols 29.82 23.77 9.86 40.91 27.27 13.27 16.36 14.77 16.77 28.09 47.00 51.95 51.90 SD 3.71 2.07 2.51 14.37 9.30 6.78 2.42 2.67 2.35 2.04 6.10 10.63 13.02 Controls Mean 31.78 25.57 11.00 45.48 29.22 16.61 16.30 15.82 17.27 27.65 45.91 48.89 46.95 SD 2.75 1.53 1.45 12.22 6.90 6.70 2.08 2.38 1.98 1.94 6.01 10.41 12.59 0.049 0.002 0.068 0.256 0.429 0.104 0.930 0.178 0.450 0.465 0.551 0.335 0.201 p-value

Note that higher score reects better result except in Speeded Naming in which it is the opposite

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lower than their controls. No other signicant differences were found on the language measures used in this study. Our results showed that children with AS had more difculties in following verbal instructions when compared with typically developing children, as suggested by their signicantly lower scores on the Comprehension of Instructions subtest of NEPSY. In this test, the children were asked to identify gures with different shapes and colours. The particular subtest is developed from the TOKEN test (DeRenzi and Vignolo 1962) and assesses comprehension of verbal commands with increasing complexity. Performing well in the Comprehension of Instructions subtest requires, in addition to language skills, short-term memory, attention, motor planning and spatial perception. Well-functioning working memory skills are needed for selecting, maintaining and manipulating relevant information in the execution of an action (Russell et al. 1999). Therefore, it is possible that lower scores in children with AS when compared to their controls would be due to decient short-term memory. However, children with AS scored similarly to the controls in the Sentence Repetition subtest that measures auditory short-term memory. Thus, decits in short-term memory alone cannot explain the poorer performance in the Comprehension of Instructions test. Lower scores in the Comprehension of Instructions subtest may be linked to decits in self-regulation, and planning and execution of a motor action once the linguistic information has to be put into action. Executive dysfunctions have long been associated with AS (Russell et al. 1999). Further support for this suggestion comes from our result on the subtest in Phonological Processing, where children with AS had lower scores than their controls (the result was not, however, statistically signicant). As in the subtest of Comprehension of Instructions, execution of this subtest requires executive functions as in working memory, planning and self-regulation. Joseph et al. (2005) suggest, however that executive dysfunctions are not directly related to language impairment in autistic disorders. Rather, decits in executive functions in autistic individuals are in part due to a failure to use language as inner speech to plan and direct their behaviour. Consequently, it is possible that difculty in using inner speech in directing performance contributed to the performance on the subtests of Comprehension of Instructions as well as in Phonological Processing. Childrens receptive language ability was also measured with the Sentence Comprehension test. The performances of the two groups did not differ in this test, even when conducted in noise. It is possible that the Sentence Comprehension test is not as sensitive as the Comprehension of Instructions test and therefore does not involve the same

level of difculty. The Sentence Comprehension subtest evaluates knowledge of syntactic structures of language, the test being a straightforward test in responding to syntactically complex questions. Furthermore, good performance on this subtest does not require executive functions as does the subtest of Comprehension of Instructions. The results thus suggest that linguistic processing of sentence structures in not problematic in children with AS. However, language comprehension in everyday situations, where many factors contribute to comprehension, may still be atypical. Linguistic information is interpreted in a given context. Individuals with HFA and AS have been found to have difculty in integrating linguistic information with a context (Jolliffe and Baron-Cohen 2000) which might explain the lower scores of children with AS in our results, too. Jolliffe and Baron-Cohen (2000) studied linguistic information processing in the framework of weak central and Frith 2006) and the coherence theory of autism (Happe problems were suggested to result from the tendency to focus on details and not to integrate information coherently. In our study, children had to be able to disengage from details (single concepts) of the instructions heard and perform on the basis of the whole sentence. It is possible that children with AS paid too much attention to single words, due to which meaning of the whole sentence was not comprehended as well as in the control group. Thus, the meaning of the instruction heard had to be integrated with an action for which coherent linguistic processing is required. In our study, the factors contributing to language comprehension were not studied. Therefore more detailed studies are needed to reveal whether comprehending verbal instructions is linked, for example, to weak central coherence. The size of our group was limited and the differences in raw scores were small. Therefore, the results should be generalized with caution. However, the results were in accordance with our hypothesis and earlier ndings (Kjelgaard and Tager-Flusberg 2001; Rapin and Dunn 2003). Impairments in receptive language skills have been reported in more capable individuals with autism (Kjelgaard and Tager-Flusberg 2001; Rapin and Dunn 2003). The result is relevant when planning intervention for individuals with AS. Moreover, the result gives motivation for future studies on different stages of language comprehension. With the selected behavioural measures of language a limited range of linguistic subskills could be studied. The tests used in our study are instruments for clinical use, therefore more sensitive tests should be used in the future, and also the more primary level of perception should be carefully scrutinized. Together with language measures, measures controlling executive functions such as memory and attention would be useful for interpreting the results.

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1579 Ghaziuddin M., & Gerstein, L. (1996). Pedantic speaking style differentiates Asperger syndrome from high-functioning autism. Journal of Autism and Developmental Disorders, 26(6), 585 595. Ghaziuddin, M., Thomas, P., Napier, E., Kearney, G., Tsai, L., Welch, K., & Fraser, W. (2000). Brief report: Brief syntactic analysis in Asperger syndrome: A preliminary study. Journal of Autism and Developmental Disorders, 30(1), 6770. Gillberg, C., & Gillberg, C. (1989). Asperger syndromeSome epidemiological considerations: A research note. Journal of Child Psychology and Psychiatry, 30(4), 631638. , F. G. E. (1993). Communicative competence and theory of Happe mind in autism: A test of relevance theory. Cognition, 48, 101 119. , F. G. E. (1995). Understanding minds and metaphors: Insight Happe from the study of gurative language in autism. Metaphor and Symbolic Activity, 10, 275295. , F., & Frith, U. (2006). The weak coherence account: DetailHappe focused cognitive style in autism spectrum disorders. Journal of Autism and Developmental Disorders, 36(1), 625. Howlin, P. (2003). Outcome in high-functioning adults with autism with and without early language delays: Implications for the differentiation between autism and Asperger syndrome. Journal of Autism and Developmental Disorders, 33(1), 313. Hooper, S. R., Poon, K. K., Marcus, L., & Fine, C. (2006). Neuropsychological characteristics of school-age children with high-functioning autism: performance on the NEPSY. Child Neuropsychology, 12, 299305. Iarocci, G., & McDonald, J. (2006). Sensory integration and the perceptual experience of persons with autism. Journal of Autism and Developmental Disorders, 36(1), 7790. eponiene _ , R., Kielinen, M., Suominen, K., Jansson-Verkasalo, E., C ntti, V., Linna, S.-L., Moilanen, I., & Na a ta nen, R. (2003). Ja Decient auditory processing in children with Asperger syndrome, as indexed by event-related potentials (ERPs). Neuroscience Letters, 338, 197200. a ta nen, Jansson-Verkasalo, E., Kujala, T., Jussila, K., Moilanen, I., Na R., Suominen, K., & Korpilahti, P. (2005). Similarities in the phenotype of auditory processing in children with Asperger syndrome and their parents. European Journal of Neuroscience, 22, 986990. Jolliffe, T., & Baron-Cohen, S. (2000). Linguistic processing in highfunctioning adultswith autism or Asperger syndrome. Can global coherence be achieved? A further test of central coherence theory. Psychological Medicine, 30, 11691187. Joseph, R. M., McGrath, L. M., & Tager-Flusberg, H. (2005). Executive dysfunction and its relation to language ability in verbal school-age children with autism. Developmental Neuropsychology, 27(3), 361379). Kaplan, E. F., Goodglass, H., & Weintraub, S. (1983). The Boston naming test (2nd edn). Philadelphia: Lea & Febiger. Kerbel, D., & Grunwell, P., (1998). A study of idiom comprehension in children with semantic-pragmatic difculties. Part II: Between-groups results and discussion. International Journal of Language and Communication Disorders, 33, 2344. Kjelgaard, M., & Tager-Flusberg, H. (2001). An investigation of language impairment in autism: Implications for genetic subgroups. Language and Cognitive Processes, 16, 287308. Klin, A., Volkmar, F. R., & Sparrow, S. S. (2000). Diagnostic issues in Asperger syndrome. In Klin, A., Volkmar, F. R., & Sparrow, S. S (Eds.) Asperger syndrome (pp. 2571). New York: The Guilford Press. Korkman M., Kirk U., & Kemp, S. L. (1997). NEPSY: Lasten neuropsykologinen tutkimus. [The NEPSY: the Finnish Developmental Neuropsychological Evaluation]. Helsinki, Finland: Psykologien kustannus Oy.

Furthermore, response inhibition and error correction strategies of children with AS should be measured to investigate the self-regulation capabilities of children with AS. The motivation for the present study was to ascertain whether school-aged children with AS have decits in language performance and whether these difculties as such contribute to their communication difculties. Our results showed that there are subtle differences in linguistic ability between children with AS and their typically developing controls in language reception. These problems in language reception may have an effect on social behaviour and may contribute to the problems of communication of these children. Further studies are needed to better explore this connection. In sum, language competence is a complex issue that has to be taken into account when looking at social interaction difculties in AS.
Acknowledgments We wish to thank all the children and their parents for participating in this study. We also thank psychology student Marjaana Saarivuo for performing the WISC-III on the control children. We would also like to thank Professor Marit Korkman for valuable comments. The research was supported by the Arvo and Foundation, Finland, and the Finnish-Swedish doctor Lea Ylppo association, Finland.

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