Left hemispheric deficit in the sustained neuromagnetic response to periodic click trains in children with ASD

T A Stroganova,A O Prokofyev,D E Goiaeva,K S Komarov,T S Obukhova,T M Ovsiannikova,O V Sysoeva,E V Orekhova

doi:10.1186/s13229-020-00408-4

Abstract

BackgroundDeficits in perception and production of vocal pitch are often observed in people with autism spectrum disorder (ASD), but the neural basis of these deficits is unknown. In magnetoencephalogram (MEG), spectrally complex periodic sounds trigger two continuous neural responses—the auditory steady state response (ASSR) and the sustained field (SF). It has been shown that the SF in neurotypical individuals is associated with low-level analysis of pitch in the ‘pitch processing center’ of the Heschl’s gyrus. Therefore, alternations in this auditory response may reflect atypical processing of vocal pitch. The SF, however, has never been studied in people with ASD.MethodsWe used MEG and individual brain models to investigate the ASSR and SF evoked by monaural 40 Hz click trains in boys with ASD (N = 35) and neurotypical (NT) boys (N = 35) aged 7–12-years.ResultsIn agreement with the previous research in adults, the cortical sources of the SF in children were located in the left and right Heschl’s gyri, anterolateral to those of the ASSR. In both groups, the SF and ASSR dominated in the right hemisphere and were higher in the hemisphere contralateral to the stimulated ear. The ASSR increased with age in both NT and ASD children and did not differ between the groups. The SF amplitude did not significantly change between the ages of 7 and 12 years. It was moderately attenuated in both hemispheres and was markedly delayed and displaced in the left hemisphere in boys with ASD. The SF delay in participants with ASD was present irrespective of their intelligence level and severity of autism symptoms.LimitationsWe did not test the language abilities of our participants. Therefore, the link between SF and processing of vocal pitch in children with ASD remains speculative.ConclusionChildren with ASD demonstrate atypical processing of spectrally complex periodic sound at the level of the core auditory cortex of the left-hemisphere. The observed neural deficit may contribute to speech perception difficulties experienced by children with ASD, including their poor perception and production of linguistic prosody.

Highlights

Deficits in perception and production of vocal pitch are often observed in people with autism spectrum disorders (ASD), but the neural basis of these abnormalities is unknown
Variability of Mental Processing Index (MPI) scores was high in the ASD sample and ranged from ‘very low’ to ‘higher than the average’ scores on all three scales
We found that in children, to adults [18], the sustained neural response to temporally regular 40 Hz clicks consists of two superimposed neural signals: the Auditory Steady State Response (ASSR) and slowly developing negative DC shift, referred to as the Sustained Field

Summary

Introduction

Deficits in perception and production of vocal pitch are often observed in people with autism spectrum disorders (ASD), but the neural basis of these abnormalities is unknown. Neuroimaging studies have shown that atypical development in children with ASD may originate from an early aberration of the temporal cortex maturation, which is specific to the left hemisphere [3] It remains unknown, when and where in the brain a left-hemispheric speech processing deficit arises in individuals with ASD. One of the most intriguing aspect of this problem is whether such a lateralized deficit exists already at the low level of cortical hierarchy – in the regions of the auditory core confined by the Heschl’s gyrus [4] that extracts the periodicity/pitch from the acoustic input This ‘low-level’ neurofunctional deficit may manifest itself in different ways. Given that the individuals with ASD, regardless of their IQ and general language skills, have abnormalities in perception of pitch in speech signals, as well as difficulties with production of adequately intonated speech [13, 14], a putative low-level neural deficit in encoding of temporal regularity in this clinical group merits careful investigation

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