Abstract
Optimal brain sensitivity to the fundamental frequency (F0) contour changes in the human voice is important for understanding a speaker’s intonation, and consequently, the speaker’s attitude. However, whether sensitivity in the brain’s response to a human voice F0 contour change varies with an interaction between an individual’s traits (i.e., autistic traits) and a human voice element (i.e., presence or absence of communicative action such as calling) has not been investigated. In the present study, we investigated the neural processes involved in the perception of F0 contour changes in the Japanese monosyllables “ne” and “nu.” “Ne” is an interjection that means “hi” or “hey” in English; pronunciation of “ne” with a high falling F0 contour is used when the speaker wants to attract a listener’s attention (i.e., social intonation). Meanwhile, the Japanese concrete noun “nu” has no communicative meaning. We applied an adaptive spatial filtering method to the neuromagnetic time course recorded by whole-head magnetoencephalography (MEG) and estimated the spatiotemporal frequency dynamics of event-related cerebral oscillatory changes in beta band during the oddball paradigm. During the perception of the F0 contour change when “ne” was presented, there was event-related de-synchronization (ERD) in the right temporal lobe. In contrast, during the perception of the F0 contour change when “nu” was presented, ERD occurred in the left temporal lobe and in the bilateral occipital lobes. ERD that occurred during the social stimulus “ne” in the right hemisphere was significantly correlated with a greater number of autistic traits measured according to the Autism Spectrum Quotient (AQ), suggesting that the differences in human voice processing are associated with higher autistic traits, even in non-clinical subjects.
Highlights
Recent cognitive theories of autism spectrum disorder (ASD) have emphasized the importance of considering the cognitive and social deficits of individuals with ASD and the aspects of the intact or even enhanced cognitive abilities [1,2,3,4,5]
If we employed a conservative method to control the FWE rate using the cluster size (P FWE-corrected,0.10), there was a significant event-related de-synchronization (ERD) in the beta band associated with the deviant stimulus ‘‘nu’’ during the 300–500 ms time window, whereas there were no significant ERDs associated with the deviant stimulus ‘‘ne’’ in any of the time windows
We demonstrated that higher activation in the right temporal lobe during the social stimulus ‘‘ne’’ was associated with more autistic traits measured by Autism Spectrum Quotient (AQ) and no significant positive correlation was found between the brain activation and the prevalence of autistic traits for the non-social stimulus ‘‘nu.’’ The region where brain activation was associated with more autistic traits was located a few centimeters forward of the regions where significant brain activation was observed during deviant stimuli compared with the standard stimuli/ne/for the deviant syllables/Ne/
Summary
Recent cognitive theories of autism spectrum disorder (ASD) have emphasized the importance of considering the cognitive and social deficits of individuals with ASD and the aspects of the intact or even enhanced cognitive abilities [1,2,3,4,5]. The over-functioning of brain regions typically involved in primary perceptual functions was recently considered an autistic perceptual endophenotype, and ‘‘the Enhanced Perceptual Functioning (EPF) model’’ [2,6] has been proposed to explain the superiority of the perceptual flow of information (e.g., enhanced low-level discrimination) in ASD individuals This model is supported by previous neurophysiological studies demonstrating hypersensitivity for auditory change detection of low-level auditory stimuli in subjects with Asperger syndrome (i.e., an autism spectrum condition), reflected in the enhanced mismatch negativity (MMN) for deviant sounds [7,8]. A twin study demonstrated that autistic traits are continuously distributed and moderately to highly heritable in the general population, suggesting that these observations might be arbitrary where cutoffs are made between research designations of ‘‘affected’’ vs ‘‘unaffected’’ with ASD [10] This continuum was revealed using tools such as the Social Responsiveness Scale (SRS) [13] or the Autism Spectrum Quotient (AQ) [9].
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