P3 responses to prosodic stimuli in adult autistic subjects

doi:10.1016/0168-5597(91)90139-O

Electroencephalography and Clinical Neurophysiology/Evoked Potentials Section

Volume 80, Issue 6, November–December 1991, Pages 561-571

https://doi.org/10.1016/0168-5597(91)90139-O Get rights and content

Abstract

Autistic persons are known to have serious abnormalities in speech prosody. The present study attempted to ascertain whether autistic persons could discriminate and/or recognize prosodic contrasts in auditory stimuli. A group of 11 adult autistic subjects with normal IQ and an age-matched group of normal subjects were studied electrophysiologically and behaviorally during presentations of prosodic and phonemic stimuli. The cognitive P3 potential was recorded in response to rare (20%)/frequent (80%) presentations of phonemic stimuli, ‘ba/pa’, linguistic-prosodic stimuli, ‘Bob’. (statement)/‘Bob?’ (question), and emotional-prosodic stimuli, ‘Bob’ (happy)/‘Bob’ (happy)/’Bob’ (angry). Behaviorally, auditory discrimination was tested by requiring a button-press response to each presentation of the rare target stimulus and cognitive association was tested by requiring a match between the verbalized stimulus and an appropriate picture/word.

Contrary to our hypothesis, the autistic subjects generally showed normal P3 responses to all stimuli and performed at a normal level in all behavioral tests. However, a significant autistic P3 response to the phoneme ‘pa’ was not demonstrated. This surprising result was reexamined and shown to reflect an unusually large autistic response to ‘pa’ as the frequent stimulus in the first recording block, this initial hyper-reactivity prevented a ‘frequent/rare’ differential when ‘pa’ was presented as the rare stimulus in a later recording block. In the P3 latency window, both the autistic and control groups showed the largest amplitude responses to emotional-prosodic stimuli; neither the N1 nor P2 showed these stimulus effects. Thus, ‘emotional sounds’ appear to be particularly effective in activating the neural substrate of the P3 generator system.

Overall, these data indicate remarkably normal P3 and behavioral processing of prosodic stimuli by the high-functioning autistic subjects of this study.

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Thus, while explicit task performance may not be impaired in AS, two recent electrophysiological (ERP) studies (Korpilahti et al., 2007; Kujala, Lepistö, Nieminen-von Wendt, Näätänen, & Näätänen, 2005) suggest fundamental processing differences between AS and non-clinical participants in early processing stages (e.g. reduced N1, Korpilahti et al., 2007). But then again, there is also evidence that later processing stages may not differ between individuals with ASD and non-clinical controls in an emotion discrimination task (Erwin et al., 1991). Thus, part of the reason for the inconsistencies in emotional prosody perception could be demands on explicit versus implicit processing, and current research has examined the effect of experimental task set-up directly in high functioning individuals with ASD.
Emotional prosody provides important cues for understanding the emotions of others in every day communication. Asperger's syndrome (AS) is a developmental disorder characterised by pronounced deficits in socio-emotional communication, including difficulties in the domain of prosody processing. We measured pupillary responses as an index of emotional prosodic processing when 15 participants with AS and 19 non-clinical control participants listened to positive, negative and neutral prosodic sentences. This occurred under a spontaneous and an explicit task instruction. In the explicit processing condition, the AS group and the non-clinical controls showed increased pupil dilations to positively and negatively intoned sentences when judging the valence of that prosodic sentence. This suggests higher processing demands for emotionally arousing information, as the effect was not found in comparison to neutrally intoned sentences. In the spontaneous processing condition, controls also responded with increased pupil dilations to positively intoned sentences, whilst individuals with AS showed increased pupil dilations to negative sentences. The latter result is further supported by diminished ratings of emotionally intense sentences in the AS group compared to healthy controls. Perception and recognition of positively valenced sentences in individuals with AS appears impaired and dependent on the general task set-up. Diminished pupil dilations in spontaneous positive processing conditions as well as reduced positive valence ratings give strong indications for a general negative processing bias of verbal information for adult individuals diagnosed with AS.
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We report findings concerning the understanding of prosody in Asperger Syndrome (AS), a topic which has attracted little attention and led to contradictory results. Ability to understand grammatical prosody was tested in three novel experiments. Experiment 1 assessed the interpretation of word stress, Experiment 2 focused on grammatical pauses, and Experiment 3 tested the discrimination of the question contour. Acoustic tasks were also used to assess the perception of pitch, duration, intensity and prosodic contours. AS participants performed as well as typically developing controls in all our tasks. This provides support in favour of the view that grammatical prosody is spared in Asperger Syndrome.
Audiologic and electrophysiologic evaluation in children with psychiatric disorders
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Individuals with psychiatric disorders can present perception, attention and memory deficits, raising doubts about peripheral and/or central hearing loss. Thus, the aim of this study is to describe the audiological and electrophysiological results of individuals with psychiatric disorders, looking for peripheral and/or central auditory disorders. Methods: 20 individuals with autism and Asperger syndrome and 20 individuals without psychiatric disorders from eight to 19 years of age, were submitted to audiological and electrophysiological evaluation. Results: No alterations were observed on the audiological evaluation in all the individuals. In ABR, 50% of individuals with autism and 30% with Asperger syndrome presented alterations. Significant statistical differences were observed between the groups in the quantitative analysis. All groups presented alterations in AMLR and P300. In AMLR, no significant statistical differences were observed between the groups in the qualitative and quantitative analyses. In the P300, we noticed significant statistical differences between Asperger and control groups in the quantitative analysis. Conclusions: A high occurrence of alterations in auditory evoked potentials was seen in children with psychiatric disorders, although in some analysis it was observed a non-statistically significant difference when comparing study and control groups. We stress the need for a more careful investigation of the auditory function in this population.
Resolving ambiguity: A psycholinguistic approach to understanding prosody processing in high-functioning autism
2008, Brain and Language
Individuals with autism exhibit significant impairments in prosody production, yet there is a paucity of research on prosody comprehension in this population. The current study adapted a psycholinguistic paradigm to examine whether individuals with autism are able to use prosody to resolve syntactically ambiguous sentences. Participants were 21 adolescents with high-functioning autism (HFA), and 22 typically developing controls matched on age, IQ, receptive language, and gender. The HFA group was significantly less likely to use prosody to disambiguate syntax, but scored comparably to controls when syntax alone or both prosody and syntax indicated the correct response. These findings indicate that adolescents with HFA have difficulty using prosody to disambiguate syntax in comparison to typically developing controls, even when matched on chronological age, IQ, and receptive language. The implications of these findings for how individuals with autism process language are discussed.
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The question of etiology in autism remains elusive primarily due to the fact that autism does not result from a single dysfunction but is multi-faceted in nature. Investigations into etiology have ranged from identifying abnormalities in the genome to describing structural/functional brain abnormalities. Bearing in mind the risk of over-simplification, there is still utility in isolating a specific deficit to examine its etiologic contribution. It is known that individuals with autism have difficulty processing auditory information at the cortical level but this is not consistently seen subcortically. In recent years, cortical auditory processing has been extensively researched using event-related potentials (ERPs); however, these results in relation to autism have not been reviewed. This paper will examine this literature and discuss implications for future research.
The mismatch negativity and the P3a components of the auditory event-related potentials in autistic low-functioning subjects
2003, Clinical Neurophysiology
Objective: In order to understand better the psychophysiological basis of auditory processing abnormalities in autism, we decided to study two automatic components of the auditory event-related potentials (ERPs): the mismatch negativity (MMN)—a component of the ERP which is recorded when, during repetitive auditory stimulation, rare changes are introduced—and the novelty-related P3a which is recorded as a response to unexpected novel events occurring in a sequence of repetitive stimuli.
Methods: Ten male subjects, mean age 12.3 years (SD 4.95), affected by autism and mental retardation were admitted to this study. All patients were also mentally retarded. Ten normal male subjects, mean age 12.2 years (SD 3.94), were used as controls. Auditory evoked potentials were recorded from 19 scalp electrodes (10–20 system), and stimuli were presented in sequences consisting of 2000 tones (70 dB, $ISI =800 ms$ ). Three types of stimuli were presented: (1) standard stimuli (1000 Hz tones, 80% of total stimuli), (2) deviant stimuli (1300 Hz tones, 10% of total stimuli), and (3) novel stimuli (complex and non-monotonal, 10% of total stimuli). To quantify the MMN, the evoked response to the standard tones was subtracted from the corresponding deviant stimulus response and its amplitude and latency at peak were measured over Fz, Cz and Pz; similarly, the P3a component of the ERP was obtained by subtracting the response to the standard tone from that to the novel stimuli and its amplitude and latency at peak were measured over Fz, Cz and Pz. Also, the amplitude and latency at peak for the N1 component of the auditory evoked potential obtained with the standard stimuli were measured over Fz, Cz and Pz. The correlation between age and MMN and P3a amplitude was also analyzed.
Results: N1 showed significantly shorter latencies in the autistic groups. MMN elicited by deviant stimuli, but not that elicited by novel stimuli, was found to be significantly larger in autistic children than in normal controls. P3a showed higher amplitude in autistic subjects than in normal controls during childhood; the opposite was observed during young adulthood.
Discussion: Our findings indicate that significant changes in ERPs can also be seen in non-cooperative individuals with autism and mental retardation, which might be different from the changes already reported for high-functioning autistic subjects and deserve further insight. These changes show developmental modifications that should be taken into consideration when analyzing data from autistic subjects.

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^☆: This work was supported by USPHS Grants HD05958 and HD04612.

¹: The authors wish to thank Andrew Russell, M.D., Linda Bott, Ph.D. and Cathy Sammons, M.S.W. for their diagnostic evaluation of the autistic subjects.

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Main articleP3 responses to prosodic stimuli in adult autistic subjects☆

Abstract

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Psychiat. Res.

Psychiat. Res.

Electroenceph. clin. Neurophysiol.

Language patterns of German and English autistic adolescents

Prosodic development in normal and autistic children

Communication deficits in the adolescent with autism, schizophrenia, and language-learning disabilities

Animal models of event-related potentials

Abnormal P1 potentials in autistic subjects

Soc. Neurosci. Abst.

The assessment of affection disorders in children and adolescents by semi-structured interview. Test-retest reliability of the schedule for affection disorders and schizophrenia for school-age children, present episode version

Arch. Gen. Psychiat.

Main article
P3 responses to prosodic stimuli in adult autistic subjects☆