Altered human voice processing in the frontal cortex and a developmental language delay in 3- to 5-year-old children with autism spectrum disorder

Yuko Yoshimura,Norio Hayashi,Chiaki Hasegawa,Yoshio Minabe,Takashi Ikeda,Daisuke N Saito,Manabu Oi,Hirokazu Kumazaki,Gerard B Remijn,Tetsuya Takahashi,Mitsuru Kikuchi,Hirotoshi Hiraishi

doi:10.1038/s41598-017-17058-x

Abstract

The inferior frontal and superior temporal areas in the left hemisphere are crucial for human language processing. In the present study, we investigated the magnetic mismatch field (MMF) evoked by voice stimuli in 3- to 5-year-old typically developing (TD) children and children with autism spectrum disorder (ASD) using child-customized magnetoencephalography (MEG). The children with ASD exhibited significantly decreased activation in the left superior temporal gyrus compared with the TD children for the MMF amplitude. If we classified the children with ASD according to the presence of a speech onset delay (ASD - SOD and ASD - NoSOD, respectively) and compared them with the TD children, both ASD groups exhibited decreased activation in the left superior temporal gyrus compared with the TD children. In contrast, the ASD - SOD group exhibited increased activity in the left frontal cortex (i.e., pars orbitalis) compared with the other groups. For all children with ASD, there was a significant negative correlation between the MMF amplitude in the left pars orbitalis and language performance. This investigation is the first to show a significant difference in two distinct MMF regions in ASD – SOD children compared with TD children.

Highlights

Autism spectrum disorder (ASD) comprises a set of neurodevelopmental disorders characterized by deficits in social communication and restrictive and repetitive patterns of behaviour, interests, and activities
We investigated the mismatch field (MMF) evoked by voice changes during speech in young children with autism spectrum disorder (ASD) and a speech onset delay (AS-SOD), children with ASD without a speech onset delay (AS-NoSOD), and age-matched typically developing (TD) control participants
The current study investigated the cortical pre-attentive discrimination of changes in speech tone in 3- to 5-year-old TD children and children with ASD

Summary

Introduction

Autism spectrum disorder (ASD) comprises a set of neurodevelopmental disorders characterized by deficits in social communication and restrictive and repetitive patterns of behaviour, interests, and activities. Accumulating electrophysiological evidence suggests that deficits in the discrimination of rapid sound changes are associated with impaired speech processing in children with ASD3 as well as developmental language disorders[4,5,6,7]. MMN/MMF is considered an indicator of change detection and has been used to probe speech discrimination[13,14,15,16]. Using source-localizing methods, MMN/MMF has been reported to be generated by temporal and frontal lobe sources, with the former being associated with change detection and the latter with involuntary switching of attention to sound changes[10]. Atypical MMN/MMF responses have been reported in populations with developmental language disorders[4,24] as well as children with ASD3,22,25–37. Numerous auditory electrophysiological studies have primarily focused on MMF in older children with ASD (older than 6 years); to our knowledge, no previous magnetoencephalography (MEG) studies have focused on analysis of the MMF source in younger children with ASD (age 6 and under)

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Conclusion