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Language and auditory processing in autism Michael Siegal and Mark Blades Department of Psychology, University of Sheffield, Western Bank, Sheffield S10 2TP, UK
Autism is characterized by varying degrees of disorders in language, communication and imagination. What are the prospects for making sense of this heterogeneous condition? Advances in identifying phenotypes in relation to subgroups within autism, based on disproportionate language impairment, have been recently reported by Tager-Flusberg and Joseph. The symptom severity of these subgroups requires investigation for underlying deficits, such as in auditory processing. Other recent reports support the view that a deficit in auditory processing might be a key factor in autism. The absence of ‘theory of mind’ (ToM) reasoning (which includes the ability to infer the beliefs of others) has often been proposed to characterize the nature of autistic spectrum disorders [1– 3]. However, it is now apparent that performance on ToM tasks will not lead to a full understanding of autism. For one thing, some children diagnosed as autistic pass the tasks whereas others who are not autistic fail. Furthermore, children often display the symptoms of autism before the age at which they can usually be tested for whether they show ToM understanding (see Box 1). Because the ToM hypothesis falls short of a full account of autism, new research directions have emerged with results that might eventually be seen to complement the ToM account. Here we describe a recent set of studies designed to enable the delineation of autistic phenotypes. These serve to draw together a number of recent findings, and point to a connection between autism and auditory processing. Language and phenotypes in autism A recent thematic issue of Philosophical Transactions of the Royal Society [4] showcases 12 articles that represent the vanguard of recent autism research. Of particular note is a set of studies described by Tager-Flusberg and Joseph [5] that take a significant step towards the differentiation of autistic phenotypes on the basis of language impairment. Tager-Flusberg and Joseph subdivided 47 children with autism aged 6 – 13 years (mean age, 8 yrs 11 mths) into three groups: those high on verbal IQ relative to nonverbal IQ, those high on non-verbal IQ relative to verbal IQ, and those with equal verbal and non-verbal IQ scores. Consistent with evidence that the level of language ability is linked to the severity of autism [6,7], Tager-Flusberg and Joseph found that low verbal IQ was correlated with the lack of communication and reciprocal social interaction that is symptomatic of autism. In addition, children with high non-verbal IQ relative to verbal IQ showed less Corresponding author: Michael Siegal (
[email protected]). http://tics.trends.com
reciprocal social interaction than those in the other two groups. According to this analysis, children who have low verbal ability, especially when this is combined with relatively high non-verbal ability, present severe symptoms of autism. This view is supported by other observations that Tager-Flusberg and Joseph report in their article. For example, the children with autism who exhibit disproportionately low verbal ability also possess a significantly larger head circumference than other children with autism. Many children with autism also share the characteristics of children without autism who have a Specific Language Impairment (SLI), in that both groups exhibit similar patterns of grammatical errors. Magnetic resonance brain scans also reveal that children with autism, like children with SLI, can show a difference in brain asymmetry. In normal children, the left hemisphere language areas are enlarged relative to the size of the homologous regions in the right hemisphere. In both children with autism and children with SLI, this asymmetry can be reversed. Finally, recent work has frequently implicated gene loci known to be associated with language impairment in autism [8,9], and Tager-Flusberg and Joseph note that studies on the genetics of language have yielded similarities in the linkage between language and autism, and language and SLI. The connection with audition Frith and Happe´ have perceptively described how specific impairments can give rise to a number of ‘downstream’ developmental effects that might appear as more general deficits [10]. In our view, one key gatekeeper for later development involves the auditory processing through which children normally come to encounter language. Consistent with Tager-Flusberg and Joseph’s conclusion that the severity of autism is characterized by disproportionate language impairment, children with autism have been shown to have difficulties in extracting the linguistic information received through auditory perception – information that is vital for participating in conversations and for recognizing that the minds of others are repositories of mental states that might differ from reality. A range of recent studies, mostly investigating school-aged children and adolescents, points to abnormalities in the hearing of those with autism. Although some have hyperacusis [11], many others have subtle auditory impairments and, for example, show asymmetrical patterns of activity in the olivocochlear system involved in detection of speech-in-noise [12,13]. From early infancy, hearing is a fundamental basis for the orientation of attention [14]. Children with autism who
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Box 1. Autism and the assessment of theory of mind ToM is usually assessed using measures such as the ‘Sally-Ann task’ [1], in which children are told a story that is acted out with puppets. One puppet (Sally) places a marble in a basket and then leaves the scene. While she is away a second puppet (Ann) takes the marble out of the basket and puts it in a box. Then Sally returns, and the child is asked where Sally will look for the marble. By the age of 4 years, most normally developing children correctly reply that Sally will look in the basket, indicating that they have an understanding of false beliefs (Sally believes that the marble is in the basket, but that is now not the case), which is central to ToM reasoning. In contrast to typically developing children, most children with autism with a mental age of 4 years fail false-belief tasks [6]. This difference in performance between typically developing children and children with autism originally prompted suggestions that false-belief tasks might be diagnostic of autism, and that deficits in understanding other minds might be an explanation for autistic behaviour. However, although the ToM hypothesis does usefully contribute to an understanding of some aspects of autism, it cannot be completely sustained for several reasons. First, in many studies a significant proportion of young children with autism do succeed on false-belief tasks and therefore false belief cannot be diagnostic of autism [20]. Second, some children who are not autistic (e.g. children who are blind or late-signing deaf) show protracted difficulties on false-belief tasks beyond the age of 4 years [21,22]. Third, some children with autism can now be identified as early as 18 months of age from patterns of behaviours such as atypical gaze, and lack of pretend play [20,23], well before the age when ToM deficits would be expected.
have abnormalities in hearing may be unable to engage jointly in attention with speakers – a skill that can be regarded as ‘pivotal’ in autism [15]. Several recent studies using a variety of techniques have further supported the view that a deficit in auditory processing might be an underlying factor in autism. In the same thematic issue of Philosophical Transactions on autism, Plaisted et al. [16] report an experiment involving eight individuals with autistic spectrum disorders, aged 13 – 28 years (mean, 18 yrs 3 mths). The participants were required to detect whether a signal occurred in the first or second interval of a trial comprising bursts of masking noises. The auditory filter shapes of the subjects were abnormally wide, indicating that a larger discrepancy between the frequencies of a signal and a masking sound is required for those with autism to hear the signal. In another study that sought to examine auditory processing in autism, Ceponiene et al. [17] used cortical event-related brain potentials. Nine children with autism aged 6 – 12 years (mean, 8 yrs 9 mths) were exposed to tone and vowel stimuli. Three types of electrophysiological measurements were recorded: auditory sensory ERPs, the mismatch negativity component, and the P3a component. The auditory sensory ERP is assumed to reflect sound frequency or intensity, the mismatch negativity component to indicate detection of infrequent ‘deviant’ sounds as distinct from repetitive ‘standard’ sounds, and the P3a component to indicate the involuntary orientation of attention to salient events in the environment. Differences in auditory sensory ERPs between the children with autism and a normal control group were not quite significant and, unlike in previous research [18], there was no significant difference in mismatch negativity. http://tics.trends.com
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Fig. I. An example of a theory-of-mind task used with deaf children. Children were shown a picture of a boy fishing, and in this example the boy has caught a boot. The children were then shown four pictures (a fish, a boot, and two distracter objects) and asked, in sign language, to point to the picture that showed what the boy was thinking (it should be the fish, assuming that the boy has not yet pulled in his line to reveal the boot, which the viewer however can see). Reproduced with permission from Ref. [3].
Figure I illustrates an example of a task used with deaf children. Using this and similar tasks, Woolfe et al. [24] found that late-signing deaf children who were 4 years or older had difficulty indicating what the boy in the picture was thinking. Therefore lack of ToM, as expressed in falsebelief tasks by children who have a mental age of at least 4 years, is not unique to autism.
However, for the children with autism, unlike for the control group, changes in vowel pitch (although not tones) elicited no significant P3a. On this basis, Ceponiene et al. conclude that their impairment in auditory processing is at the attentional rather than the sensory level and that children with autism might have an attentional deficit in orienting to the ‘speechness’ quality of sounds as represented by vowels. Conclusion Research on autism always needs to be considered with appropriate caveats. The ages of the children in the studies mentioned here are variable, the measures given differ, and the sample sizes are often small. Bearing these considerations in mind, we can conclude that evidence is accumulating that children whose language is severely impaired, especially relative to their non-verbal intelligence, are at risk of developing severe symptoms of autism. At the same time, other research suggests that children with autism have deficits in auditory processing that preclude participation in conversation with others, which possibly lead to downstream impairments on ToM tasks, and excessive interest in objects at the expense of people. The diagnosis of barriers to auditory processing promises to identify the nature of the social isolation of children with autism. Research in this area holds the eventual prospect of gaining a deeper insight into the mystery of autism and developmental disorders more generally, with a focus on remediation through improved auditory processing. There are now indications that training in auditory processing can help language and reading problems in dyslexia [19], and similar interventions might eventually be shown to be of benefit to those with autism.
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Acknowledgements We are grateful to Peter Mitchell, Dave Moore and Danielle Ropar for discussions on this topic.
References 1 Baron-Cohen, S. et al. (1985) Does the autistic child have a ‘theory of mind’? Cognition 21, 37 – 46 2 Gallagher, H.L. and Frith, C.D. (2003) Functional imaging of ‘theory of mind’. Trends Cogn. Sci. 7, 77 – 83 3 Siegal, M. and Varley, R. (2002) Neural systems involved in ‘theory of mind’. Nat. Rev. Neurosci. 3, 463– 471 4 Frith, U. and Hill, E.L., eds (2003) Autism: Mind and Brain. Themed issue of Philos. Trans. R. Soc. Lond. Ser. B (Vol. 358, No. 1430), The Royal Society 5 Tager-Flusberg, H. and Joseph, R.M. (2003) Identifying neurocognitive phenotypes in autism. Philos. Trans. R. Soc. Lond. Ser. B 358, 303 – 314 6 Bailey, A. et al. (1996) Autism: towards an integration of clinical, genetic, neuropsychological, and neurobiological perspectives. J. Child Psychol. Psychiatry 37, 89 – 126 7 Happe´, F. (1995) The role of age and verbal ability in the theory of mind task performance of subjects with autism. Child Dev. 66, 843 – 855 8 Alarcon, M. et al. (2002) Evidence for a language quantitative trait locus on chromosome 7q in multiplex autism families. Am. J. Hum. Genet. 70, 60 – 71 9 Folstein, S.E. and Rosen-Sheidley, B. (2001) Genetics of autism: complex aetiology for a heterogeneous disorder. Nat. Rev. Genet. 2, 943 – 955 10 Frith, U. and Happe´, F. (1998) Why specific developmental disorders are not specific: on-line and developmental effects in autism and dyslexia. Dev. Sci. 1, 267 – 272 11 Rosenhall, U. et al. (1999) Autism and hearing loss. J. Autism Dev. Disord. 29, 349 – 357 12 Collet, L. et al. (1993) Objective auditory dysfunction in infantile autism. Lancet 342, 923 – 924
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13 Khalfa, S. et al. (2001) Peripheral auditory asymmetry in infantile autism. Eur. J. Neurosci. 13, 628 – 632 14 Mendleson, M.J. and Haith, M.M. (1976) The relation between audition and vision in the newborn. Monogr. Soc. Res. Child Dev. 41, Serial No. 167 15 Charman, T. (2003) Why is joint attention a pivotal skill in autism? Philos. Trans. R. Soc. Lond. Ser. B 358, 315 – 324 16 Plaisted, K. et al. (2003) Towards an understanding of the mechanisms of weak central coherence effects: experiments in visual configural learning and auditory perception. Philos. Trans. R. Soc. Lond. Ser. B 358, 375 – 386 17 Ceponiene, R. et al. (2003) Speech-sound-selective auditory impairment in children with autism: they can perceive but do not attend. Proc. Natl. Acad. Sci. U. S. A. 100, 5567– 5572 18 Gomot, M. et al. (2001) Auditory mismatch process in children with autism: an ERP topographic study. Int. J. Psychophysiol. 41, 197 – 235 19 Temple, E. (2002) Brain mechanisms in normal and dyslexic readers. Curr. Opin. Neurobiol. 12, 178 – 183 20 Charman, T. (2000) Theory of mind and the early diagnosis of autism. In Understanding Other Minds: Perspectives from Autism and Cognitive Neuroscience, 2nd edn, (Baron-Cohen, S. et al., eds), Oxford University Press 21 Hobson, R.P. and Bishop, M. (2003) The pathogenesis of autism: insights from congenital blindness. Philos. Trans. R. Soc. Lond. Ser. B 358, 335 – 344 22 Peterson, C.C. and Siegal, M. (2000) Insights into theory of mind from deafness and autism. Mind Lang. 15, 123 – 145 23 Osterling, J.A. et al. (2002) Early recognition of 1-year-old infants with autism spectrum disorder versus mental retardation. Dev. Psychopathol. 14, 239– 251 24 Woolfe, T. et al. (2002) Signposts to development: theory of mind in deaf children. Child Dev. 73, 768 – 778 1364-6613/$ - see front matter q 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S1364-6613(03)00194-3
| Book Review
A mature view of autism Autism: Explaining the Enigma by Uta Frith, Blackwell Publishing, 2nd Edn, 2003. £15.99 (pbk) (249 pages) ISBN 0 631 22901 9
Simon Baron-Cohen Autism Research Centre, Cambridge University, Downing Street, Cambridge, CB2 3EB, UK
Uta Frith’s new, second edition of her beautiful book on autism is very welcome. The first edition, published in 1989, was very well received by both the academic community, practitioners in the autism field, and by families. It was reprinted 10 times in paperback, and has been translated into many languages. How could she improve on it? And yet she has. She recognized that in the intervening decade, autism research had blossomed, and that this new edition was an opportunity to see quite how well the two main theories that she is well-known for have fared, in the light of a lot of new data. First, take the mindblindness theory (that people with autism are unable to imagine what other people are thinking). Frith’s view is that in the past decade, this Corresponding author: Simon Baron-Cohen (
[email protected]). http://tics.trends.com
theory has been strengthened, and she reviews the evidence in detail and in very accessible style. Further, she goes beyond the extreme picture of mindblindness to hint at those people with autism-spectrum conditions who have ‘compensated’ for their lack of what she calls an ‘intuitive’ mentalizing ability by developing what she calls a ‘conscious’ mentalizing ability. Her conclusion is that now we have a cognitive explanation of the key triad of impairments, shown in Fig. 1a. Frith then considers the weak-central-coherence theory. In the first edition of her book, she proposed this new idea to explain a set of symptoms in autism that the mindblindness theory could not explain: the narrow attention to detail, the ‘islets of ability’ or even talents, and the detachment from, or immunity to, context. A decade later, her conclusion is that this theory too has fared well in the light of further experimentation, such that we now have a cognitive account of the ‘non-triad’ symptoms (Fig. 1b).