Research in Autism Spectrum Disorders

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1 Research in Autism Spectrum Disorders 5 (2011) Contents lists available at ScienceDirect Research in Autism Spectrum Disorders Journal homepage: Review A review of behavioural and electrophysiological studies on auditory processing and speech perception in autism spectrum disorders Birgitt Haesen a,1, Bart Boets a,b,1, *, Johan Wagemans c a Leuven Autism Research Consortium, Child and Adolescent Psychiatry, University of Leuven (K.U. Leuven), Herestraat 49 - Box 7003, 3000 Leuven, Belgium b Centre for Parenting, Child Welfare & Disabilities, University of Leuven (K.U. Leuven), Vesaliusstraat 2 - Box 3765, 3000 Leuven, Belgium c Laboratory of Experimental Psychology, University of Leuven (K.U. Leuven), Tiensestraat Box 3711, 3000 Leuven, Belgium ARTICLE INFO ABSTRACT Article history: Received 5 November 2010 Accepted 12 November 2010 Keywords: Autism spectrum disorder Auditory processing Speech perception Local processing Global processing This literature review aims to interpret behavioural and electrophysiological studies addressing auditory processing in children and adults with autism spectrum disorder (ASD). Data have been organised according to the applied methodology (behavioural versus electrophysiological studies) and according to stimulus complexity (pure versus complex tones versus speech sounds). In line with the weak central coherence (WCC) theory of autism we aimed to investigate whether individuals with ASD show a more locally and less globally oriented processing style in the auditory modality. To avoid the possible confound of stimulus complexity, this influence was taken into account as an additional hypothesis. The review reveals that the identification and discrimination of isolated acoustic features (in particular pitch processing) is generally intact or enhanced in individuals with ASD, for pure as well as for complex tones and speech sounds. It thus appears that the local processing advantage is not influenced by stimulus complexity. Individuals with ASD are also less susceptible to global interference of speech-like material. A deficit in global auditory processing, however, is less universally confirmed. We propose that the observed pattern of auditory enhancements and deficits in ASD may be related to an atypical pattern of right hemisphere dominance. As the right and left hemisphere are relatively more specialized in spectral versus temporal auditory processing, respectively, right hemisphere dominance in ASD could provoke enhanced pitch and vowel processing, whereas left hemisphere deficiencies might explain speech perception problems and temporal processing deficits. ß 2010 Elsevier Ltd. All rights reserved. Contents 1. Introduction General characteristics of the reviewed studies Behavioural studies of auditory processing in autism spectrum disorders Pure tones Complex tones Acoustic features of speech sounds Speech perception: integration of acoustic features * Corresponding author at: Leuven Autism Research Consortium, University of Leuven (K.U. Leuven), Herestraat 49, Box 7003, 3000 Leuven, Belgium. Tel.: ; fax: address: bart.boets@ped.kuleuven.be (B. Boets). 1 Both authors equally contributed to this study and should be regarded as joint first authors /$ see front matter ß 2010 Elsevier Ltd. All rights reserved. doi: /j.rasd

2 702 B. Haesen et al. / Research in Autism Spectrum Disorders 5 (2011) ERP and ERF studies of auditory processing in autism spectrum disorders Pure tones Complex tones Acoustic and phonetic features of speech sounds A tentative synthesis Pure tone processing Complex tone processing Acoustic and phonetic processing of speech Local versus global auditory processing in ASD The role of stimulus complexity Atypical brain lateralization and atypical auditory processing Conclusion Acknowledgements References Introduction The term autism spectrum disorders (ASD) refers to a spectrum of early onset neurodevelopmental disorders, which are characterized by limitations in social, communicative and everyday functioning. Autism is the core disorder and is defined by impairments in social interaction, as well as language and communication difficulties and stereotyped behaviours, interests and activities. Other disorders of the ASD-continuum do not meet all of these criteria. Individuals diagnosed with Asperger syndrome, for example, do not show impairments in language development, although they do have difficulties using language in social situations (American Psychiatric Association, 1994; Eigsti & Shapiro, 2003; Kanner, 1943). In addition to the variation in presence and severity of these deficits, people with ASD also show considerable variation in intellectual ability, ranging from mental retardation to the level of being highly gifted. Within the group of autistic children and adults a distinction can be made between high functioning autism (HFA: IQ 70 or above) and low functioning autism (LFA: IQ below 70) (Tsai, 1992). Visual, tactile and auditory perceptual abnormalities, such as hyper- or hyposensitivity, are often reported (Talay-Ongan & Wood, 2000). In this literature review we will focus on auditory processing and speech perception in ASD. Several theories attempt to explain the autistic pattern of auditory symptoms. Relevant for this review is the theory of Weak Central Coherence (WCC), which postulates that people with ASD have difficulties to integrate information into a meaningful whole while their ability to process detailed information is enhanced or at least preserved (Frith, 2003; Frith & Happé, 1994; Happé, 1999). An alternative, more moderate view of local versus global processing in ASD was suggested by the Enhanced Perceptual Functioning theory (EPF) (Mottron & Burack, 2001; Mottron, Dawson, Soulières, Hubert, & Burack, 2006). The EPF theory also hypothesizes enhanced local processing in ASD, similar to the WCC theory, but does not expect a general deficiency in global processing. The theory suggests that global processing is optional in individuals with ASD and not mandatory as it is in general populations. In the visual modality, convincing evidence of superior local processing in individuals with ASD has been put forward (Behrmann et al., 2006; Dakin & Frith, 2005; Happé & Frith, 2006; Plaisted, Saksida, Alcántara, & Weisblatt, 2003; Simmons et al., 2009), although research findings regarding impaired global processing of visual material are mixed (Dakin & Frith, 2005; Happé, 1999; Happé & Frith, 2006; Plaisted et al., 2003; Simmons et al., 2009). Some evidence exists for intact global processing of simple visual stimuli, but impaired global processing for more complex visual stimuli (Simmons et al., 2009). The main hypothesis we want to investigate is whether or not the theory of WCC applies to auditory perceptual processing in ASD. On the basis of this theory, we expect that the auditory processing style of individuals with ASD will be more locally and less globally oriented. In other words, we expect them to show enhanced local auditory perception (e.g., the processing of isolated acoustic features, like pitch or intensity) and poorer processing of global auditory features (e.g., the integration of acoustic features into a global percept, which is necessary for speech perception, for instance). Given that local versus global processing is often entangled with stimulus complexity, we additionally investigated the influence of stimulus complexity on the auditory processing performance of individuals with ASD (see Samson, Mottron, Jemel, & Belin, 2006, for a similar approach). Throughout the review we therefore categorized the studies based on the complexity of the stimuli that have been used, i.e. pure tones versus complex tones versus speech material. Local processing was expected to be enhanced in individuals with ASD regardless of stimulus complexity. Global processing could be intact for more simple auditory stimuli and impaired for more complex auditory stimuli, in accordance with findings regarding global visual processing in ASD. In this review we will be focusing on auditory and speech processing in ASD. It is important, however, to note that auditory and speech processing are generally embedded in a broader context of social communication. As stated earlier, individuals with ASD have difficulties with communication and social functioning, e.g. problems with spoken and receptive language and with interpreting emotions and intentions of other people. It has been shown that young children with ASD do not show the same orientation to speech as seen in typically developing children (Kuhl, Coffey-Corina, Padden, & Dawson, 2005). Orientation to speech plays an important role in learning to comprehend and process speech, as well as in developing oral language and communication. It might be argued whether a deviant pattern of social orientation is the cause or the

3 B. Haesen et al. / Research in Autism Spectrum Disorders 5 (2011) consequence of deviances in auditory orientation and auditory processing in individuals with ASD. With this review we aim to provide a state-of-the-art overview of studies investigating auditory processing and speech perception in ASD, but we do not aim to make any claims regarding the causal nature of the complex interrelations between social orientation, auditory processing and speech perception. 2. General characteristics of the reviewed studies The participants in the studies included in this review were diagnosed with autism or Asperger syndrome, according to the Diagnostic and Statistical Manual of Mental Disorders (DSM) or the International Statistical Classification of Diseases and Related Health Problems (ICD) criteria. They differed in age, gender and intelligence. Most participants were male, due to the fact that ASD is more prevalent in males than in females (Bryson, 1996). Studies with children and with adults were included, low-functioning as well as high-functioning. In all included studies, controls were matched for age, gender and (non-verbal) IQ, unless otherwise specified. Both behavioural and electrophysiological studies were reviewed. An electrophysiological technique often used to investigate auditory processing is the recording of event-related potentials (ERP) or event-related fields (ERF). ERPs are recorded by means of electro-encephalography (EEG) and ERFs by means of magnetoencephalography (MEG). An ERP waveform typically consists of peaks and valleys which are named by their polarity (P for positive, N for negative) and the time elapsed after the appearance of the stimulus. Auditory evoked potentials (AEP), which are used to trace the responses that are produced by auditory stimuli, are a subclass of ERPs. Evoked potentials can be divided into short latency, middle latency and long latency responses. The short latency responses include cochlear potentials and auditory brainstem responses and occur at less than 10 ms after stimulus onset. The middle latency responses, occurring between 10 ms and 50 ms, comprise slow waves of auditory brain stem responses and the earliest components reflecting auditory cortical processing. Every component with a latency above 50 ms is considered a long latency response (Eggermont, 2007). Early components reflect modality specific processing (0 150 ms), whereas the late cortical components (150 ms or later) are less dependent on stimulus characteristics, but more dependent on, for example, task characteristics (e.g., N2 and P3). The N1 and P1 responses are early components that are often measured in ERP studies; they are thought to reflect initial cortical processing of different features of auditory stimuli (Eggermont, 2007; Samson et al., 2006). The mismatch negativity (MMN) and the mismatch field (MMF) are auditory evoked potentials that are elicited if an infrequent stimulus occurs within a stream of standard stimuli; they are a measurement of automatic, preconscious change detection. An oddball paradigm where the infrequent sound deviates from the standard sound in some feature(s) (e.g., pitch, duration) is often used to investigate MMN or MMF. It occurs at about ms from the onset of the infrequent sound and is obtained by subtracting the ERP responses to the standard frequent sound from those elicited by the non-standard sound (Näätänen & Winkler, 1999; Samson et al., 2006). At a higher level attention and memory related processes are involved, reflected by the late latency P3 component. This response occurs about 300 ms after the presentation of the stimulus and is elicited when discriminating deviant and standard sounds. There are two subcomponents, which are related to passive versus active attention. The P3a component is elicited when individuals involuntary orient their attention to the stimuli, whereas the P3b is only apparent when an active response to sound stimuli is required (Samson et al., 2006). The N4 component is typically elicited by potentially meaningful changes in stimuli and occurs at approximately 400 ms after presentation of a deviant stimulus. It is thought to play an important role in language processing and semantics. The N4 amplitude will be more prominent when a word is more difficult to integrate in a certain context (Hagoort, 2003). In particular, for speech perception it seems to be related to the semantic integration of words in a sentence context (Barber & Carreiras, 2005). The magnetic equivalents of the electroencephalographic evoked responses that reflect initial auditory cortical processing are the M50 and the M100. The M100 magnetic field is comparable to the N1 that was described earlier; the M50 is analogous to the Pa/P1 complex of the electroencephalographic evoked responses (Oram Cardy, Ferrari, Flagg, Roberts, & Roberts, 2004). In the majority of the reviewed ERP and ERF studies initial cortical sound processing is examined (e.g., N1, P1, M50, M100) as well as sound discrimination (MMN, MMF). Some studies also investigate higher level attentional (P3, P3a) and semantic processes (N4). In the majority of studies included in this review the sound stimuli were presented binaurally through either headphones or loudspeakers. In the behavioural studies an active response was required, while in most electrophysiological studies participants were not asked to respond. In most cases they were watching a (silent) video to keep them from consciously attending to the sounds. Studies were selected by means of Web of Science and PSYCInfo databases, based on the key words speech perception, auditory perception, sound perception, speech processing, auditory processing, sound processing, speech discrimination, auditory discrimination or sound discrimination in combination with autism or Asperger. Initially, 115 studies were found in the PSYCInfo database and 179 studies on Web of Science. Case studies were excluded from the obtained studies and only ERP, ERF and behavioural studies were selected. Additional studies were selected through inspection of reference lists. A further selection was made based upon inspection of the abstracts and only those articles which were relevant to our hypothesis were included in this review.

4 704 B. Haesen et al. / Research in Autism Spectrum Disorders 5 (2011) Details about the 43 studies included in this review can be found in Supplementary Table 1, arranged according to the applied methodology and stimulus complexity. This table offers an organized overview of the literature, and provides information about participant characteristics, stimulus parameters, main results and their interpretation. 3. Behavioural studies of auditory processing in autism spectrum disorders 3.1. Pure tones The most prominent auditory symptoms reported in people with ASD are abnormal behavioural reactions to environmental sounds and increased sensitivity to loudness (Frith & Baron-Cohen, 1987). Khalfa et al. (2004) found enhanced perception and reduced tolerance to loudness in children with autism in response to pure tones. Children with autism showed reduced auditory dynamic ranges due to lower loudness discomfort levels (hyperacusis). Other behavioural studies with pure tones showed enhanced pitch sensitivity in individuals with ASD. Bonnel et al. (2003) used a same different discrimination task and a low high categorisation task to assess pitch perception in children and adolescents with HFA. The individuals with HFA showed enhanced pitch discrimination and pitch categorisation abilities, and they also obtained similar performance levels on both tasks. This contrasts with the controls, who performed more poorly on the categorisation task than the discrimination task. More recently, Bonnel et al. (2010) found enhanced pitch discrimination of static pure tones in a group of individuals with autism, but not in individuals with Asperger syndrome. Thus, superior pitch discrimination seemed characteristic to only those individuals with ASD who also showed significant language problems. It has previously been suggested that an association might exist between reduced salience of language, a non-speech preference bias and (enhanced) auditory processing abilities (Heaton, 2003; Kuhl et al., 2005). Enhanced pitch discrimination for pure tones was also found in a study by Jones et al. (2009), but only for a subgroup of adolescents with ASD that had higher IQs and delayed onset of first words. Jones et al. concluded that this might suggest the presence of a specific phenotype. Apart from frequency discrimination, Jones et al. also investigated intensity and duration discrimination, but found no differences between autistic subjects and controls. Oades, Walker, Geffen, and Stern (1988) found that children with autism reacted faster but performed poorer than controls, while discriminating pure tones with pitch differences in background white noise Complex tones Musical savants are more common among individuals with ASD than in non-clinical populations (Rimland & Fein, 1988). They have been shown to possess absolute pitch skills and superior processing of musical stimuli in general (Miller, 1989). Processing of complex, musical stimuli has also been investigated in non-savant individuals with ASD. Intact or superior processing of musical stimuli has been found in ASD for pitch discrimination. In a study by Järvinen-Pasley and Heaton (2007) individuals with HFA or Asperger syndrome discriminated pitch in speech speech, speech music and music music conditions. There was no difference between individuals with HFA or Asperger syndrome and controls when asked to make same different judgements of pitch in musical forms, suggesting intact processing of pitch in music. Heaton (2005) found intact pitch contour discrimination for six-tone musical contours in children with HFA, and another behavioural study by Järvinen-Pasley, Pasley, and Heaton (2008) and Järvinen-Pasley, Wallace, Ramus, Happé, andheaton(2008) found superior performance for participants with autism or Asperger syndrome when judging five-tone musical contours. Mottron, Peretz, and Ménard (2000) found enhanced (absolute) pitch processing in individuals with ASD when making same different judgements of melodies that were contour preserved (participants had to rely on absolute pitch to judge the melody pairs). Pitch contour processing was intact, in accordance with Heaton (2005), as shown by the effective use of contour as a discrimination cue for contour-violated melodies. Mottron et al. concluded that their findings evidenced enhanced local processing and intact pitch contour processing, which was considered to be global processing in this study. In a study by Foxton et al. (2003) individuals with ASD made same different judgments of pitch contours in five-tone musical stimuli. In contrast with other studies, these authors interpreted pitch contour processing as a local processing activity. They argued that a pitch contour consists of a series of simple pitch directions and that the contour can be obtained by simply adding together these local features. In this study global referred to the conditions were contour, absolute pitch values and their timing were combined. Three conditions with increasing interference were created in this experiment; a no-interference condition (matched in terms of relative time points of change and actual pitches), a local pitch interference condition (matched in terms of time points of change, but not the actual pitches) and a local pitch and timing interference condition (mismatched in terms of both the relative time points of change and the actual pitches). In contrast to controls, the ASD group showed no deterioration in performance when discriminating pitch contours in these three conditions. Individuals with ASD were thus not susceptible to auditory global interference (of both time and actual pitch changes on local pitch contour processing), whereas controls were. Another study using complex musical material found better retrieval and identification of pitch in a condition of individual, labelled tones for children with autism (Heaton, 2003). Disembedding of the tones seemed to be dependent on pre-exposure and labelling of the tones. In one condition participants had to disembed familiar labelled tones from within musical chords, in the other condition participants had to disembed unlabelled tones. When demands were made on long-term pitch memory (familiar, labelled tones condition) children with autism were superior. When not able to rely on

5 B. Haesen et al. / Research in Autism Spectrum Disorders 5 (2011) long-term pitch memory (not pre-exposed, unlabelled tones condition) children with autism and controls were both equally captured by the global qualities of the chords. Heaton, Hudry, Ludlow, and Hill (2008) and Heaton, Williams, Cummins, and Happé (2008) did not observe enhanced pitch memory or pitch interval processing of musical stimuli in their total sample of children with HFA or LFA, but only in a subsample. This subgroup was characterized by outstanding block design performance and lower vocabulary scores. It was suggested by the authors that the development of superior pitch processing in autism may be associated with an early atypical local processing bias. Auditory processing has also been investigated for non-musical, complex stimuli. Superior complex tone pitch discrimination of children with ASD was found in a study by Gomot, Belmonte, Bullmore, Bernard, and Baron-Cohen (2008). Reaction times and number of hits were considered when discriminating pitch of complex tones. The children with ASD reacted faster with similar accuracy, hence showing enhanced pitch discrimination. Bonnel et al. (2010) found intact pitch discrimination of static and modulated complex tones. Non-vocal timbre and loudness discrimination were investigated as well, and were also found to be intact both for static and modulated complex tones. Two studies investigated duration discrimination of complex tones. Lepistö et al. (2006) demonstrated diminished hitrates in Asperger syndrome compared to controls for duration discrimination. In a behavioural sound identification test by Lepistö, Nieminen-von Wendt, von Wendt, Näätänen, and Kujala (2007) the Asperger syndrome group performed as accurately as controls, but had slower reaction times to the different pairs for duration and non speech pitch differences. However, according to Lepistö et al. (2007) this finding may be attributed to a different response strategy since no difference was found in MMN latency Acoustic features of speech sounds Several studies demonstrated intact or enhanced perceptual processing of acoustic features of speech in individuals with ASD. As earlier described, Järvinen-Pasley and Heaton (2007) investigated pitch discrimination in children with HFA or Asperger syndrome in speech speech, speech music and music music conditions. The clinical group showed similar pitch sensitivity in all three conditions. Controls, on the other hand, showed deterioration in performance in the speech speech and especially the speech music conditions as compared to the music music condition. The researchers concluded that pitch information in speech stimuli has more salience for children with autism or Asperger syndrome than for the nonclinical group. Auditory perceptual processing appears thus to be more domain-general in ASD, and less dependent on the nature of the presented stimuli (speech versus music). Alternatively, it could also have been the case that controls, but not children with HFA or Asperger syndrome, were more captured by the linguistic information in speech stimuli. Heaton, Hudry, et al. (2008) and Heaton, Williams, et al. (2008) investigated pitch contour discrimination in monosyllabic real words and monosyllabic nonsense words for 10 different vowel sounds. Non-speech pitch contours were also created. Children with ASD showed enhanced pitch contour discrimination across different auditory stimuli classes (words, nonsense words and non-speech pitch contours). Both groups showed poorer discrimination of pitch contour when the stimuli were speech-like (both words and nonsense words), compared to non-speech pitch contour stimuli. The authors thus suggested that speech, rather than semantic content, could be the cause of poorer pitch discrimination. Järvinen-Pasley, Pasley, et al. (2008) and Järvinen-Pasley, Wallace, et al. (2008) found superior pitch contour processing in speech in children with ASD. They presented sentence stimuli with four distinct pitch contours accompanied by visual response slides. The visual response slides included correct and incorrect pitch contour symbols, and correct and incorrect linguistic choices. Children with ASD made more accurate perceptual judgements than controls, which evidences superior perceptual processing of speech, but no differences between groups were found for linguistic responses. In both groups linguistic processing was the primary processing mode, although this tendency towards linguistic processing (over perceptual processing) was weaker in children with ASD than in controls. In another study, children with HFA and Asperger syndrome showed superior perceptual processing of speech (and music) stimuli when matching pitch patterns (Järvinen-Pasley, Pasley, et al., 2008; Järvinen-Pasley, Wallace, et al., 2008). Neither the control group nor the clinical group showed evidence of semantic interference upon perceptual processing ability. However, when identifying rhythm patterns, children with HFA or Asperger syndrome were not hindered by semantic information whereas controls did show evidence of semantic capture. This supports the evidence of superior perceptual processing of speech in autism. Apart from findings showing enhanced pitch and rhythm perception of speech sounds, there is also some evidence of diminished duration discrimination. In a behavioural sound discrimination study by Lepistö et al. (2006) decreased hit rates were found for duration changes of vowels (and complex tones) in a group of children with Asperger syndrome. This finding suggests a deficit in their duration discrimination abilities. In a parallel study Lepistö et al. (2007) administered a behavioural sound identification test and found that the group of children with Asperger syndrome had slower reaction times to different pairs for vowel-duration and phonetic discrimination. However, they were as accurate as controls. As mentioned before, these results are most likely due to a different response strategy, as there was no difference in MMN between the Asperger syndrome group and controls. Besides pitch, loudness and non-vocal timbre discrimination Bonnel et al. (2010) also focused on vocal timbre discrimination. They discovered that individuals with autism or Asperger syndrome and controls were equally capable of discriminating vocal timbre of vocal tones (vowel-like stimuli), in silence as well as in noise, and for both static and modulated vocal tones. Even under these different circumstances vocal timbre processing thus seems to be intact.

6 706 B. Haesen et al. / Research in Autism Spectrum Disorders 5 (2011) In a study by Stewart and Ota (2008) autistic traits were measured in a normal population and phoneme discrimination in relation to linguistic content was investigated. A word non-word speech continuum was used to measure the influence of linguistic features on phoneme perception. In general, participants tended to shift their segment identification towards the real word end of the continuum (in this case towards/kiss/rather than/giss/and towards/gift/rather than/kift/). The effect appeared to be negatively correlated with autistic traits (measured on the basis of Autism Spectrum Quotient scores). This suggests that individuals with autistic traits were less likely to be affected by linguistic features in their phonetic perception Speech perception: integration of acoustic features The abovementioned studies concern processing of isolated acoustic features of speech sounds (such as, e.g. pitch). Yet, speech perception in general (like the perception of words or sentences) requires the integration of a variety of acoustic features. Studies investigating the perception of words or sentences as a whole or investigating the perceptual integration of several acoustic features are scarce. Two behavioural studies have investigated speech-in-noise perception. Groen et al. (2009) aimed to study spectro-temporal processing in children with HFA. Two-syllable words were presented in four different types of background noise: pink noise, amplitude modulated pink noise, moving ripple and amplitude modulated moving ripple. For both the controls and the children with HFA, temporal dips in the background noise allowed better speech perception, whereas spectro-temporally more complex ripple sounds decreased the perception of speech. However, the gain in speech perception of pink noise with temporal dips relative to pink noise without temporal dips was smaller in children with HFA than in controls. No differences between groups were found when integrating auditory fragments presented in spectral dips in ripple sounds. The authors concluded that spectral processing is intact in children with HFA, whereas temporal processing is abnormal. These findings, according to the authors, support the complexityspecific hypothesis of the EPF model (e.g. Samson et al., 2006). The complexity specific hypothesis predicts that perception of simple low-level stimuli and local features will be enhanced in autism, while perception of more complex and global information is expected to be spared or impaired. A second study investigating speech-in-noise perception in an integrative manner was carried out by Alcántara, Weisblatt, Moore, and Bolton (2004). They presented sentence stimuli in five different background noise conditions: a female talker, steady speech-shaped noise, speech-shaped noise with temporal dips, steady speech-shaped noise with regularly spaced spectral dips, and speech-shaped noise with temporal and spectral dips. Alcántara et al. found that individuals with HFA or Asperger syndrome made use of both temporal and spectral dips to perceive speech in noise. However, they benefitted less from temporal dips compared to controls. This is consistent with the findings of Groen et al. (2009), who found intact spectral but abnormal temporal processing of children with HFA. 4. ERP and ERF studies of auditory processing in autism spectrum disorders 4.1. Pure tones Pitch discrimination has been investigated most commonly and several studies point in the direction of enhanced pitch discrimination in individuals with ASD. Using an oddball paradigm Gomot, Giard, Adrien, Barthélémy, and Bruneau (2002) found that children with autism had shortened MMN latencies to pitch changes, and thus concluded that children with autism were superior in pitch perception. Ferri et al. (2003) also found enhanced pitch discrimination of pure tones in low functioning autistic children, reflected by an enhanced MMN for deviant pure tone sounds. The N1 latency of children with LFA was shorter, which implies that initial auditory cortical processing was abnormal, possibly faster. In a study by Čeponienè et al. (2003), using pure tones, complex sounds and vowel sounds, pitch discrimination was found to be largely intact, but not enhanced, regardless of the acoustic complexity. Likewise cortical sound perception, as measured by N2, N4 and P1, was intact. N2 and N4 were normal, P1 showed a tendency to be smaller but this difference was not significant. However, the evidence of enhanced pitch discrimination in individuals with ASD is not unequivocal. Jansson-Verkasalo et al. (2003) found delayed MMN in children with Asperger syndrome to changes in pure tone and syllable pitch. This effect was larger for pure tones. Abnormalities in initial auditory cortical processing were also found: P1 and N2 were diminished. In another study children with Asperger syndrome were compared with their fathers and mothers regarding pitch discrimination and sound encoding (Jansson-Verkasalo et al., 2005). This study aimed to investigate whether hereditary aspects of the Asperger syndrome extend to the auditory system. Children with Asperger syndrome, as well as their fathers and mothers, showed abnormal initial auditory cortical processing. Abnormal pitch discrimination was also present, but only in children with Asperger syndrome and their fathers, not in their mothers. In children with Asperger syndrome this was reflected by a diminished N2 and N4 amplitude, a prolonged P1 and N4 latency, a shorter N2 and a prolonged MMN2 latency. Their fathers had a prolonged P1 latency, enhanced N2 amplitude, a shorter MMN1 latency and a prolonged MMN2 latency. Their mothers showed a prolonged P1 and N1 latency. In an ERF study of low functioning individuals with autism a diminished MMF total power was found when discriminating pitch of pure tones (Tecchio et al., 2003). These results indicate abnormal pitch discrimination. However, no abnormalities in initial auditory cortical processing were found: there was no difference between controls and the LFA group in M100 latency or amplitude. In another ERF study by Oram Cardy, Flagg,

7 B. Haesen et al. / Research in Autism Spectrum Disorders 5 (2011) Roberts, and Roberts (2005) children with autism showed a prolonged MMF latency to pitch changes in pure tones, though M50 and M100 did not differ from controls. Thus, this evidences intact initial auditory cortical processing, but delayed pitch discrimination of pure tones. A study by Oram Cardy et al. (2004) found that initial auditory cortical processing was intact, as no differences in M50 or M100 between children with ASD and typically developing children were found for sequences of pure tones. Both in typically developing children and in children with ASD the M50 dominated the auditory evoked field relative to M100. In a group of adults without ASD the pattern was reversed: M100 dominated relative to M50. No ASD adult group was included in this study, thus it could not be investigated whether adults with ASD would show a similar reversed pattern of activation as adults without ASD. Oram Cardy, Flagg, Roberts, Brian, et al. (2005), Oram Cardy, Flagg, Roberts, and Roberts (2005) and Oram Cardy, Flagg, Roberts, and Roberts (2008) investigated language and auditory processing in autistic children versus language-impaired children (SLI). In the first study, pairs of 1 khz tones were separated by a 150 ms silent gap (Oram Cardy, Flagg, Roberts, Brian, et al., 2005; Oram Cardy, Flagg, Roberts, and Roberts, 2005). The ERF responses of four groups were compared: an autism group, an Asperger group, a language impaired group and a typically developing group. In all groups identifiable M50 and M100 responses were elicited by the first tone. To the second tone, however, fewer than 44% of the children with autism and 34% of the children with SLI showed an identifiable M50 or M100 response. The children with Asperger syndrome, who had no language impairment, and the controls showed identifiable responses to both the first and the second tone. Thus, the impairments found in this study reflect rapid temporal processing difficulties and, as suggested by the authors, may rather be associated with language impairment and not with ASD in se. In a second study by Oram Cardy et al. (2008) languageimpaired children, including those with autism, had a prolonged latency of M50 in the right hemisphere (not in the left), when listening to series of 1 khz tones. With every millisecond increase in right hemisphere M50 latency, the odds of language impairment increased with 3%. In addition, behavioural measures indicative of receptive and expressive language impairments were associated with prolonged M50 and M100 latencies. The authors suggested that right hemisphere auditory processing may be a key dysfunction underlying the overlap between individuals with ASD and individuals with selective language impairment. These findings provide evidence for a specific relationship between delayed auditory evoked fields of non-speech auditory stimuli (in the right hemisphere) and impaired language development. Oades et al. (1988) presented pure tones in a background of white noise to individuals with autism and controls, who had to discriminate pitch changes. Abnormalities in initial auditory cortical processing were found: individuals with autism showed a more varied distribution of amplitude maxima for all ERP components and they had shorter N1 latencies and enhanced N1 amplitudes. The latter was particularly the case for rare non-targets compared to standards and deviant sounds. Intensity (loudness) and duration perception have also been investigated for simple tones, though not as frequently as pitch perception. Bruneau, Roux, Adrien, and Barthélémy, (1999) investigated auditory evoked potentials to pure tones of varying intensities in low functioning children with autism and in typically developing and mentally retarded children. Bruneau and colleagues found abnormalities of N1b and N1c. N1b is a fronto-central component and was diminished in amplitude for all intensities in the autism group. N1c is a temporal component and was also diminished in amplitude for the autism group, as well as prolonged. For controls the bilateral N1c peak amplitude increased with increasing intensities but in the autism group this effect was only present on the right side. This might suggest a right hemispheric dominance in auditory processing in autistic individuals. Hemispheric effects have also been found in other studies, as will be discussed below. In a replication study the same pure tones of varying intensity were again presented to a group of low functioning children with autism and a control group (, Bruneau, Bonnet-Brilhault, Gomot, Adrien, & Barthélémy, 2003). The LFA group showed diminished N1c amplitudes and longer N1c latencies in both the left and right hemisphere. However, for the 80 db stimulus the N1c amplitude was significantly greater on the right hemisphere than on the left in participants with LFA, in controls the reverse pattern was found, but it did not reach significance. These abnormalities confirm that intensity processing is abnormal in LFA-children. As suggested by the authors of the study, these results might indicate a dysfunction at the level of the auditory association cortex, including the superior temporal gyrus. The superior temporal gyrus, the superior temporal sulcus, and in particular the left posterior superior temporal sulcus, are important for auditory processing and speech perception (i.e., analyzing rapidly changing auditory input and deriving meaning from it) (Redcay, 2008; Scott & Johnsrude, 2003). Lepistö et al. (2009) used pure tones of varying intensities to investigate auditory stream segregation in Asperger syndrome. The researchers used three different conditions: an oddball condition, a segregated and an integrated condition. The oddball condition used two tones, one standard and one deviant tone, to measure discrimination abilities. In the segregated condition two tones, which clearly differed in pitch from the oddball tones, were presented between the tones of the oddball paradigm. The resulting two sound streams shared the same intensity range but could be clearly separated on the basis of their frequency. This segregation allows the detection of the deviant oddball intensity. The integrated condition was similar to the segregated condition, but the intervening tones had a frequency that was much closer to that of the oddball tones. This results in one sound stream instead of two separated streams. The Asperger group showed a diminished MMN in the segregated condition; however, intensity discrimination was intact when stream segregation was not required. Thus, children with Asperger syndrome appear to be less efficient in auditory stream segregation, which, as proposed by Lepistö et al. (2009), might have implications for the perception of speech in noisy environments. Initial auditory cortical processing was intact in these children as reflected by a normal P1 and P2 response. The difference in MMN can therefore not be ascribed to differences in basic auditory feature processing.

8 708 B. Haesen et al. / Research in Autism Spectrum Disorders 5 (2011) Kasai et al. (2005) investigated duration discrimination of pure tones using an ERF methodology. No differences in MMF were found between adults with autism and controls. This study suggests that duration discrimination in autistic adults is intact. However, thus far no other electrophysiological studies have investigated duration discrimination of pure tones Complex tones Čeponienè et al. (2003) found largely intact processing and discrimination of pitch in high-functioning children with autism, regardless of the acoustic complexity. A normal MMN compared to controls was found for complex tones (as well as for pure tones and vowels). In a study by Lepistö et al. (2005) enhanced pitch discrimination was found in children with autism, reflected by an enhanced MMN for pitch changes in complex tones. The same experiment also investigated duration discrimination of nonspeech vowel analogues and non-speech vowel analogues discrimination (as an equivalent to the phonetic changes in the vowel condition). Shorter MMN latencies to non-speech vowel analogue changes were found, supporting the evidence of enhanced non-speech vowel analogue discrimination. However, the ability to discriminate duration changes of complex non-speech vowel analogues appears to be impaired. Lepistö et al. (2005) also found abnormal initial auditory cortical processing for complex tones, as reflected by diminished P1 and P2 amplitudes. However, Whitehouse and Bishop (2008) found no abnormalities in initial auditory cortical processing of complex tones. Children with Asperger syndrome, like children with autism, showed diminished MMNs for duration changes of complex tones compared to controls (Lepistö et al., 2006) Acoustic and phonetic features of speech sounds There are several studies using vowels that show enhanced or intact pitch discrimination. Čeponienè et al. (2003) found intact initial auditory cortical processing and pitch discrimination for vowels (as well as for complex and simple tones) in a clinical group of high functioning children with autism compared to controls. Another three studies also investigated pitch discrimination of vowels, in addition to duration and phoneme discrimination of vowels (Lepistö et al., 2005, 2006, 2007). These studies used the same sound stimuli, but the clinical and control groups differed. When children with Asperger syndrome were presented with vowels /a/ or /o/ and were asked to discriminate pitch, phoneme or duration, they showed an enhanced MMN for pitch changes and a diminished MMN for duration changes (Lepistö et al., 2006). No group differences in phoneme discrimination were found between the Asperger group and the control group. Cortical sound processing appeared to be defective, as reflected by a diminished N4. Another study, using a clinical group of children with autism, also demonstrated deficient auditory cortical processing (diminished P1 and N4), as well as enhanced pitch discrimination (Lepistö et al., 2005). Thus, similarities in vowel processing seem to exist between children with autism and children with Asperger syndrome. Adults with Asperger syndrome also showed an enhanced MMN for pitch changes in vowels, similar to children with autism and Asperger syndrome (Lepistö et al., 2007). However, adults with Asperger syndrome also showed an enhanced MMN for duration changes, whereas the children with autism or Asperger syndrome showed an intact or diminished ability to discriminate vowel duration changes. Lepistö et al. (2008) investigated pitch and phoneme discrimination of vowels in children with autism using a constant feature and a varying feature oddball paradigm. The constant feature condition was a classical oddball design, whereas in the varying feature condition the stimuli varied in pitch in the sequences with phoneme deviants and in phonemes in the sequences with pitch deviants. Lepistö et al. (2008) found enhanced MMN for pitch changes in both paradigms, but only found enhanced phoneme discrimination in the constant-feature paradigm. The authors suggest that these findings could implicate enhanced discrimination of spectral auditory information (vowel discrimination also depends on spectral processing), but that the advantage in phoneme discrimination is lost when the context of the vowels is speech-like and requires an abstraction of invariant speech features from varying input. However, Kasai et al. (2005) found deficient phoneme discrimination of vowels in adults with autism, even when the task did not require extracting invariant speech features from varying inputs. This deficit was reflected by the delayed MMF, predominantly in the left hemisphere, when discriminating phonemes. Duration discrimination was also considered in this study, but no abnormalities were found when discriminating duration changes in vowels. A study by Oram Cardy, Flagg, Roberts, Brian, et al. (2005) and Oram Cardy, Flagg, Roberts, and Roberts (2005) with children with autism also found a delayed MMF for phonetic changes. In this same study pitch discrimination of vowels also resulted in delayed MMF, which is inconsistent with previously described studies that investigated pitch discrimination of vowels. Initial cortical sound processing was intact in this study. Whitehouse and Bishop (2008), on the other hand, found a deficit in initial auditory cortical processing in children with autism. The MMN of phoneme discrimination was intact, which differs from the findings of Oram Cardy, Flagg, Roberts, Brian, et al. (2005), Oram Cardy, Flagg, Roberts, and Roberts (2005) and Kasai et al. (2005). The findings regarding the processing and discrimination of syllables appear to be contradictory. In a study by Jansson- Verkasalo et al. (2003) phonetic discrimination of syllables and initial auditory cortical processing of pure tones and syllables were impaired in children with Asperger syndrome, though the latter impairment was more severe for pure tones. In a study by Russo, Zecker, Trommer, Chen, and Kraus (2009) syllable processing was investigated in a quiet condition and in a condition with background noise. Children with ASD were less efficient than controls in their auditory cortical processing of syllables, with or without noise. The ASD group, as opposed to controls, did not deteriorate in syllable processing in the noisy

9 B. Haesen et al. / Research in Autism Spectrum Disorders 5 (2011) condition compared to the quiet condition. The authors suggest that this might be due to the fact that responses were already severely impaired in the quiet condition. Kemner, Verbaten, Cuperus, Camfferman, and van Engeland (1995) investigated syllable discrimination in high functioning children with autism. No differences in MMN or N1 between participants with autism and controls were found, suggesting largely intact initial auditory cortical processing and discrimination of syllables. Kuhl et al. (2005) found impaired syllable discrimination, in line with Jansson-Verkasalo et al. (2003) and Russo et al. (2009). However, Kuhl et al. were able to associate their findings with a non-speech sound preference. Apparently, the majority of pre-school children with ASD preferred non-speech sounds over motherese speech. Motherese speech is a form of speech with special characteristics (e.g., higher pitch) that is typically used to talk to babies and young children. If children with ASD were divided into subgroups according to their non-speech versus speech preference, it was shown that impaired syllable discrimination was associated with a non-speech preference. The children with ASD who preferred motherese speech showed the same syllable discrimination abilities as controls. The association found in this study suggests an important link between social processing and speech perception. 5. A tentative synthesis The literature concerning auditory processing in autism spectrum disorders is diverse. The studies use different classes of stimuli, different criteria to select participant groups and different methodologies and equipment. Generally, there is much variance in results and conclusions, but similarities can also be seen when comparing the outcomes of behavioural and electrophysiological studies Pure tone processing Behavioural studies (Bonnel et al., 2003, 2010; Jones et al., 2009) as well as ERP and ERF studies (Čeponienè et al., 2003; Ferri et al., 2003; Gomot et al., 2002; Oram Cardy et al., 2004) have shown enhanced pitch processing and discrimination of pure tones. The electrophysiological findings, however, are not unequivocal as some ERP or ERF studies have also shown deficient pure tone pitch processing and discrimination in ASD (Jansson-Verkasalo et al., 2003, 2005; Oram Cardy, Flagg, Roberts, Brian, et al., 2005; Oram Cardy, Flagg, Roberts, and Roberts, 2005; Tecchio et al., 2003). Intensity discrimination of pure tones has also been investigated by both research approaches, but the number of studies is scarce. One behavioural study found enhanced intensity perception (Khalfa et al., 2004) and one study found intact, but not enhanced, intensity discrimination of pure tones (Jones et al., 2009). Electrophysiological intensity processing of pure tones was intact in one study when stream segregation was not required (Lepistö et al., 2009). However, in two other electrophysiological studies intensity processing of pure tones was deficient (Bruneau et al., 1999, 2003). These different outcomes could probably be explained by differences in participant selection: Bruneau et al. (1999) and Bruneau et al. (2003) studied a group of very young mentally retarded children with autism, whereas the other studies either tested a group of children with Asperger syndrome (Lepistö et al., 2009) or a group of children with autism or ASD with mixed IQs (Khalfa et al., 2004; Jones et al., 2009). Duration discrimination of pure tones has been investigated by one behavioural (Jones et al., 2009) and one electrophysiological study (Kasai et al., 2005). Both studies found evidence of intact duration discrimination of pure tones. More research is needed to further substantiate these findings Complex tone processing Both behavioural and electrophysiological findings seem to provide evidence for enhanced, or at least intact, pitch processing of complex tones. Behavioural studies have demonstrated intact or enhanced processing and discrimination of complex musical and non-musical stimuli in individuals with ASD (Bonnel et al., 2010; Järvinen-Pasley & Heaton, 2007; Järvinen-Pasley, Pasley, et al., 2008; Järvinen-Pasley, Wallace, et al., 2008; Mottron et al., 2000). Pitch memory and labelling were enhanced in children with HFA, in accordance with findings showing enhanced pitch perception (Heaton, 2003). Disembedding of tones from chords was superior in ASD compared to controls, but only when disembedding was dependent on pitch memory and labelling (Heaton, 2003). ERP/ERF studies also found intact or enhanced pitch discrimination of complex tones (Čeponienè et al., 2003; Kujala et al., 2007; Lepistö et al., 2005, 2006, 2007). Research of other features than pitch discrimination is scarce for complex tones. In the behavioural approach there is some evidence for intact intensity discrimination and non-vocal timbre discrimination of complex tones in individuals with autism (Bonnel et al., 2010). In the electrophysiological approach there is some support for deficient duration discrimination in children with ASD but intact duration discrimination in adults with ASD (Lepistö et al., 2005, 2006, 2007) Acoustic and phonetic processing of speech Behavioural and electrophysiological studies have shown enhanced, or at least intact, pitch processing of speech sounds. Behavioural studies found intact or superior pitch processing and pitch contour processing in individuals with ASD when using phoneme, word or sentence stimuli (Heaton, Hudry, et al., 2008; Heaton, Williams, et al., 2008; Järvinen-Pasley &