Elsevier

Clinical Neurophysiology

Volume 119, Issue 8, August 2008, Pages 1720-1731
Clinical Neurophysiology

Deficient brainstem encoding of pitch in children with Autism Spectrum Disorders

https://doi.org/10.1016/j.clinph.2008.01.108Get rights and content

Abstract

Objective

Deficient prosody is a hallmark of the pragmatic (socially contextualized) language impairment in Autism Spectrum Disorders (ASD). Prosody communicates emotion and intention and is conveyed through acoustic cues such as pitch contour. Thus, the objective of this study was to examine the subcortical representations of prosodic speech in children with ASD.

Methods

Using passively evoked brainstem responses to speech syllables with descending and ascending pitch contours, we examined sensory encoding of pitch in children with ASD who had normal intelligence and hearing and were age-matched with typically developing (TD) control children.

Results

We found that some children on the autism spectrum show deficient pitch tracking (evidenced by increased Frequency and Slope Errors and reduced phase locking) compared with TD children.

Conclusions

This is the first demonstration of subcortical involvement in prosody encoding deficits in this population of children.

Significance

Our findings may have implications for diagnostic and remediation strategies in a subset of children with ASD and open up an avenue for future investigations.

Introduction

Autism Spectrum Disorders (ASD) refers to the cluster of disorders including autism, Asperger Disorder, and Pervasive Developmental Disorder Not Otherwise Specified (PDD-NOS). Impairment in pragmatic (socially contextualized) language is a hallmark of all ASD. Prosodic elements of spoken language, including alterations in pitch, duration and amplitude at the word and phrase levels, convey pragmatic information including the importance of a particular word, the requirement for a response to an utterance, or the speaker’s affective state. Whereas aberrant prosodic elements – poor inflection, excessive or misaligned stress, monotonous intonation – are known to characterize the expressive language of individuals with ASD (McCann and Peppe, 2003), less is known about the potential contribution of a neurological source to this receptive prosody deficit. Prosody in autism has been extensively investigated at cognitive and behavioral levels (Hobson, 1986, Shriberg et al., 2001, Rapin and Dunn, 2003, Paul et al., 2005) but a better understanding of the underlying neurophysiology is warranted. Specifically, subcortical responses to prosodic speech have never been studied in individuals with ASD.

Although data addressing brainstem involvement are lacking, studies using cortical-evoked potentials in patients on the autism spectrum (specifically Asperger Disorder) have demonstrated deficient encoding of speech and related this deficit to poor receptive prosody. For example, adults with Asperger Disorder who were presented with a woman’s name uttered neutrally or with scornful, sad, or commanding affect had relative difficulty identifying the emotional connotations compared with controls, and also showed significant differences in mismatch negativity (MMN, a response reflecting encoding of acoustic change) including longer latencies, smaller amplitudes, and fewer elicited responses (Kujala et al., 2005). In a second study (Korpilahti et al., 2007), boys with Asperger Disorder were presented with a woman’s name at two different fundamental frequencies (f0) to express either tender or commanding affect. Their N1 responses (reflecting stimulus onset) were both delayed and reduced in amplitude compared with controls, and their MMN responses were earlier, larger, and had atypical laterality. The most recent study using the MMN in this population showed an enhanced response (amplitude) in individuals with ASD in a constant-feature discrimination for both pitch and vowel stimuli, whereas this effect disappeared when the condition involved deciphering phonemes with pitch variations (Lepisto et al., 2008). These data are similar to earlier work by Lepisto and colleagues, indicating that adults and children with Asperger Disorder (Lepisto et al., 2006), as well as children with autism (Lepisto et al., 2005), had enhanced MMN responses to sounds that deviated in pitch from the standard stimulus. In this study, both the standard and deviant stimuli had constant pitch for the duration of the sound. However, they also showed reduced P3a responses (involuntary orienting response) to changes in pitch in speech, albeit non-variant, within the syllable.

Pitch is the psychophysical correlate of f0 and is determined by the rate of vocal fold vibration. The auditory brainstem encodes frequency components of speech with high fidelity such that the f0 and its harmonics can be extracted from the passively elicited auditory brainstem response (Galbraith et al., 2004a, Krishnan et al., 2004, Krishnan et al., 2005, Kraus and Nicol, 2005, Musacchia et al., 2007, Wong et al., 2007). Accurate brainstem encoding of the pitch contour of a speech syllable is crucial for producing and perceiving both linguistic meaning (e.g., statement versus question) and emotional affect in speech.

An emergent body of literature has demonstrated that pitch tracking in the auditory brainstem is experience-dependent, malleable and linked to the processing of higher order cognitive factors such as language and music. For example, adult native speakers of a tonal language (Mandarin) demonstrated more precise brainstem pitch encoding than did non-native speakers (Krishnan et al., 2004, Krishnan et al., 2005). Similarly, brainstem frequency-following responses (FFR) more faithfully encoded stimulus f0 contour and demonstrated more robust phase locking in musicians than in non-musicians (Musacchia et al., 2007, Wong et al., 2007). Finally, brainstem pitch tracking can be improved by short-term training (Song et al., 2008).

Because click-evoked auditory brainstem responses have historically been used to detect abnormal auditory encoding of sound in the clinical setting, most existing ASD research assesses the integrity of the auditory brainstem via this method (Klin, 1993, Rapin and Dunn, 2003). However, work from our laboratory has demonstrated that some children with language-based learning problems exhibit deficient brainstem encoding of speech stimuli despite normal encoding of click stimuli (Banai et al., 2005, Song et al., 2006, Johnson et al., 2007, Russo et al., in press). Thus, speech stimuli have been shown to be more sensitive and hence more useful than click stimuli for the detection of subtle abnormalities in the processing of language. This finding could be particularly relevant to children with ASD because the transient and periodic dimensions of speech stimuli convey prosodic as well as phonetic information.

To test the hypothesis that faulty brainstem representation of variations in pitch contributes to the impaired prosody in ASD, we compared responses to speech syllables with descending and ascending pitch contours in a population of children with ASD to those of a control population of typically developing (TD) children.

Section snippets

Methods

The Institutional Review Board of Northwestern University approved all research and consent and assent were obtained from the parent(s) or legal guardian(s) and the child.

Children were acclimated to the testing circumstances prior to experimental data collection. They were allowed to visit the laboratory and interact with the tester on multiple occasions. Some children brought an electrode home with them to better familiarize themselves with the neurophysiological procedure.

Age, sex and intelligence considerations

Because of the variability in age and intelligence, we considered these variables in preliminary statistical analyses. Further, due to the greater incidence of ASD in males versus females, our ASD group included a majority of male participants. Since sex differences can occur in brainstem responses (Jerger, 1980, Rupa and Dayal, 1993), we also evaluated effects of sex. The distribution of age did not vary between groups and therefore it is unlikely to be a contributing factor to any of the

Discussion

Using speech syllables with variable pitch, we have demonstrated deficient brainstem encoding of pitch in a subgroup of verbal children with ASD. Specifically we found that these children with ASD had aberrant, non-direction-specific pitch tracking (increased frequency and Slope Error) and reduced neural phase locking to the stimulus (poorer autocorrelations) compared to TD children. These results were detected in children over a restricted age range, with normal peripheral hearing and

Acknowledgements

We thank the children who participated in this study and their families. We also acknowledge Jane Hornickel for her work on the harmonics analyses.

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    Financial interests: This research was supported by NIH R01 DC01510 and the Hugh Knowles Center. The authors declare that they have no competing financial interests.

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