Research ReportThe discrimination of and orienting to speech and non-speech sounds in children with autism
Introduction
Autism is a pervasive neurodevelopmental disorder characterized by impairments in social interaction and in communication, and by restricted, repetitive patterns of behavior [5], [68]. About 50% of patients fail to develop useful spoken language [31], and those who do develop speech show marked abnormalities in their language development [57], [64]. Neuroimaging studies have revealed abnormal cortical activation patterns in the auditory processing areas in response to sounds both in adults [8], [51] and in children [9], [12] with autism. In the present study, the cortical processing of speech and non-speech sounds in children with autism was studied by recording auditory event-related potentials (ERP).
ERPs, extracted from the electroencephalogram (EEG), provide a non-invasive and accurate way of monitoring the timing and stages of auditory perception. In adults, the ERP waveform to a repeated sound consists of P1, N1, and P2 peaks, while in children, the response typically consists of P1, N2, and N4 peaks when the stimulus rate is faster than 1 s [16], [17], [22]. These responses reflect sound detection and the transient encoding of the physical stimulus features [16], [22]. The N1 component has been widely studied in individuals with autism, but the results have been inconsistent (for a review, see [10]), while P1 has been reported to be diminished in adults with autism [13], and a similar trend has been shown in children [18].
Sound-feature encoding is the first step of auditory cortical processing. It is followed by auditory discrimination, which can be studied by measuring ERPs to occasional infrequent changes (deviants) in a sequence of repeated standard stimuli. If the change is perceptually discriminable, it elicits an ERP called mismatch negativity (MMN). MMN [54] peaks at about 150–250 ms after change onset, and the larger the stimulus change, the earlier and larger the MMN [53]. Although MMN is modulated by attention [67], it is elicited even when the subject is not attending to the stimuli [53]. Furthermore, even under conditions of inattention, MMN amplitude and latency closely parallel an individual's active discrimination performance [4], [44]. MMN is therefore a useful tool for studying cortical auditory discrimination in clinical populations such as those with autism.
Auditory discrimination abilities in people with autism have so far been mainly investigated using pitch deviants. Gomot et al. [32] reported shortened MMN latencies to pitch changes (1000 Hz vs. 1100 Hz) in simple tones in a group of 15 mentally retarded children with autism, suggesting higher brain reactivity to pitch deviancy in them. Consistent with this, Ferri et al. [28] showed that the MMN amplitude for simple tone pitch changes (1000 Hz vs. 1300 Hz) was larger in children and adolescents with autism and mental retardation than in controls. Čeponienė et al. [18] found similar MMN amplitudes in children with autism (without mental retardation) and their controls for pitch changes (deviants 10% higher) in vowels, acoustically matched non-speech vowel counterparts, and simple tones. In contrast, MMN amplitude for pitch changes (1000 Hz vs. 1500 Hz) was diminished in children with tuberous sclerosis complex (TSC) and autism as compared to those with TSC only [60]. However, in this study, all of the subjects with autism had lesions involving one or both temporal lobes, as is usually the case in those with TSC who develop autism. Furthermore, all of the participants had epilepsy and were under medication, which may have confounded the results.
Neurophysiological data suggesting enhanced or normal pitch discrimination abilities in autism correspond with behavioral studies showing that musically untrained individuals with autism have an excellent pitch memory, and outperform controls in identifying pitches, detecting pitch changes in melodies, and disembedding familiar labeled tones from within musical chords [11], [35], [36], [49], [50]. Good pitch-perception skills in those with autism may be related to the enhanced perceptual processing of local stimulus features that has been reported in this disorder [48], and are possibly associated with more accurate and robust pitch representations in the sensory memory [11]. Furthermore, pitch sensitivity might partly explain the auditory hypersensitivity that is highly prevalent in individuals with autism [55].
In addition, two studies have measured the MMN for phoneme changes in children with autism. Kemner et al. [39] reported corresponding MMN amplitudes for vowel change (/oy/ vs. /ay/) in high-functioning children with autism and their controls. This study used unusually long interstimulus intervals (4–6 s), however, which may have confounded the results. Recently, Kuhl et al. [43] recorded MMN to consonant changes in CV-syllables (/wa/ vs. /ba/) in 29 preschool children with autism spectrum disorders and their controls. They found that MMN was diminished in amplitude in the autism spectrum group, suggesting deficits in the discrimination of consonants.
For salient sound changes, MMN is followed by the P3a, an ERP index of involuntary attention switch [1], [26], [27], [62]. It is triggered by infrequent, attention-catching stimuli, and the larger the change, the larger the P3a [69]. Its role in involuntary attention switching has been investigated in studies in which P3a-eliciting changes in unattended sound sequences disturbed performance in a simultaneous visual task that the subject was carrying out [1], [26], [33]. In addition, an enhanced P3a has been reported in patient groups characterized by increased distractibility [38], [56]. On the other hand, diminished P3a amplitudes have been found in patients with focal brain lesions and an impaired ability to orient to stimuli [42].
The P3a elicited by highly attention-catching novel sounds has been reported to be diminished in amplitude in adolescents with autism [20], but enhanced in children [28]. Recently, the P3a elicited by considerably less attention-catching pitch changes was shown to be differentially affected by speech and non-speech sounds. Čeponienė et al. [18] found that children with autism had no P3a to pitch changes in vowels, whereas their P3a to corresponding changes in acoustically matched complex sounds and in simple tones did not differ from that of the controls. The authors suggested that there may be a speech sound-specific orienting deficit in autism. Interestingly, Gervais et al. [30] reported diminished brain activation to vocal sounds in five adults with autism, whereas the activation to non-vocal, environmental sounds was normal. When they asked their subjects afterwards to describe what sounds they had heard, the controls reported hearing equally many vocal and non-vocal sounds, whereas those with autism had a much better recall of non-vocal stimuli, suggesting an attentional bias towards non-vocal sounds. Similarly, Kuhl et al. [43] reported that, whereas control children showed no preference between infant-directed speech and its computer-synthesized non-speech analogs, preschoolers with autism spectrum disorders showed a strong listening preference for non-speech signals. Converging evidence of impaired orienting to speech in individuals with autism has been reported in other studies, too [7], [23], [25], [40], although some have also reported impaired attention shifting and orienting for non-speech auditory stimuli [3], [21], [23], [25]. Nevertheless, these deficits might be more evident for speech than non-speech stimuli [23], [25], [52].
The goal of the present study was to determine how speech and non-speech sounds are encoded, discriminated, and oriented to by school-aged children with autism as compared with controls. To this end, the MMN and P3a were recorded for pitch, duration, and vowel changes in speech stimuli, and for corresponding changes in acoustically matched non-speech stimuli. Furthermore, the ERPs elicited by speech and non-speech standard stimuli were examined.
Section snippets
Standard-sound ERPs
Both speech and non-speech standard stimuli elicited a waveform consisting of the P1, N2, and N4 peaks (Fig. 1, Table 1) that were highly significant in both groups (controls: t(14) = 9.00 to −14.46, P < 0.000001; children with autism: t(14) = 6.40–13.40, P < 0.0001). Three-way ANOVAs (Group × AP × LT) indicated that the children with autism had a diminished P1 amplitude frontocentrally for speech (Group: F(1,28) = 5.38, P < 0.03; Group × AP: F(2,56) = 5.94, P < 0.02) and non-speech stimuli
Sound encoding in children with autism
In both groups, standard stimuli elicited similar P1, N2, and N4 waveforms as typically obtained in school-aged children [16]. Consistent with the results of earlier studies, no latency differences in the standard-sound ERPs were found between the groups [18], [32], indicating that sound-feature encoding was as fast in the children with autism as in their controls. However, the standard-sound ERPs were diminished in amplitude in the children with autism particularly frontocentrally. Significant
Participants
Fifteen children (mean age 9.4, range 7.3–11.10; 13 boys) fulfilling the ICD-10 [68] and DSM-IV [5] criteria for Autistic Disorder participated in the study. The diagnoses had been made at the Helsinki University Central Hospital (HUCH) or at the Central Hospital of Central Finland by experienced clinicians. The mean total score of the group on the CARS scale [59] was 32.9 (SD 2.2). All the children were unmedicated, and had no EEG, MRI, or chromosomal abnormalities. Two of them had co-morbid
Acknowledgments
This research was supported by the Academy of Finland (70252) and the Finnish Cultural Foundation. Reija Alen, MD helped in recruiting some of the patients. We express our warmest thanks to all the children and their parents for their participation.
References (69)
- et al.
A method for generating natural-sounding speech stimuli for cognitive brain research
Clin. Neurophysiol.
(1999) - et al.
The neuroanatomical substrate of sound duration discrimination
Neuropsychologia
(2002) - et al.
Cortical auditory evoked potentials in autism: a review
Int. J. Psychophysiol.
(2004) - et al.
Blood flow response to auditory stimulations in normal, mentally retarded, and autistic children: a preliminary transcranial Doppler ultrasonographic study of the middle cerebral arteries
Biol. Psychiatry
(1992) - et al.
Midlatency auditory evoked responses: P1 abnormalities in adult autistic subjects
Electroencephalogr. Clin. Neurophysiol.
(1992) Brainstem, cerebellar and limbic neuroanatomical abnormalities in autism
Curr. Opin. Neurobiol.
(1997)- et al.
Autism: processing of novel auditory information assessed by event-related brain potentials
Electroencephalogr. Clin. Neurophysiol.
(1984) - et al.
The mismatch negativity and the P3a components of the auditory event-related potentials in autistic low-functioning subjects
Clin. Neurophysiol.
(2003) - et al.
Brain activity index of distractibility in normal school-age children
Neurosci. Lett.
(2001) Inadequate cortical feature maps: a neural circuit theory of autism
Biol. Psychiatry
(1997)
The neural representation of time
Curr. Opin. Neurobiol.
Auditory event-related brain potentials in autistic children and three different control groups
Biol. Psychiatry
Decreased response to novel stimuli after prefrontal lesions in man
Electroencephalogr. Clin. Neurophysiol.
The mismatch negativity as an index of temporal processing in audition
Clin. Neurophysiol.
Attentional skills during the first 6 months of age in autism spectrum disorder
J. Am. Acad. Child Adolesc. Psych.
Early selective attention effect on evoked potential reinterpreted
Acta Psychol.
Electrophysiological evidence of abnormal activation of the cerebral network of involuntary attention in alcoholism
Clin. Neurophysiol.
Update on the language disorders of individuals on the autistic spectrum
Brain Dev.
Autism in tuberous sclerosis: evoked potential evidence for a deficit in auditory sensory processing
Clin. Neurophysiol.
Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man
Electroencephalogr. Clin. Neurophysiol.
Processing of novel sounds and frequency changes in the human auditory cortex: magnetoencephalographic recordings
Psychophysiology
Attention function and dysfunction in autism
Front. Biosci.
The accuracy of sound duration representation in the human brain determines the accuracy of behavioural perception
Eur. J. Neurosci.
Diagnostic and Statistical Manual of Mental Disorders
Cerebral asymmetry and the development of early infantile autism
J. Autism Child. Schizophrenia
Perception of complex sounds: abnormal pattern of cortical activation in autism
Am. J. Psychiatr.
Perception of complex sounds in autism: abnormal auditory cortical processing in children
Am. J. Psychiatr.
Enhanced pitch sensitivity in individuals with autism: a signal detection analysis
J. Cogn. Neurosci.
Clinical and macroscopic correlates of minicolumnar pathology in autism
J. Child Neurol.
Minicolumnar pathology in autism
Neurology
Children's auditory event-related potentials index sound complexity and “speechness”
Int. J. Neurosci.
Maturation of cortical sound processing as indexed by event-related potentials
Clinl. Neurophysiol.
Speech-sound-selective auditory impairment in children with autism: they can perceive but do not attend
Proc. Natl. Acad. Sci. U. S. A.
Impairment in shifting attention in autistic and cerebellar patients
Behav. Neurosci.
Cited by (235)
Processing of auditory novelty in human cortex during a semantic categorization task
2024, Hearing ResearchProcessing of acoustic and phonological information of lexical tones at pre-attentive and attentive stages
2024, Language, Cognition and NeuroscienceA Preliminary Study Characterizing Subcortical and Cortical Auditory Processing and Their Relation to Autistic Traits and Sensory Features
2024, Journal of Autism and Developmental Disorders