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

Abstract

Background Deficits 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. Methods We 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. Results In 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. Limitations We 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. Conclusion Children 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.

Magnetoencephalography Studies of the Envelope Following Response During Amplitude-Modulated Sweeps: Diminished Phase Synchrony in Autism Spectrum Disorder

“…Examining a large cohort of 7–15-year-old boys, Edgar et al (2016) did not reveal group differences in ASSR, though bilateral associations with age were observed, as was a right hemispheric dominance of the ASSR responses. Similar age associations and lack of significant group differences have been reported in 7–12-year-old boys ( Stroganova et al, 2020 ) and in 5–7-year-old participants ( Ono et al, 2020 ). Given that the auditory system is still developing through early adulthood, with the 40 Hz ASSR reaching its maximum around 22 years of age ( Cho et al, 2015 ), it may not be surprising that atypical ASSR in neurodevelopmental disorders, such as ASD, do not manifest until later in their maturation ( De Stefano et al, 2019 ).…”

“…Studies in adults have suggested that the ASSR is largest in response to presentations in the gamma range particularly at 40 Hz ( Galambos et al, 1981 ; Picton et al, 2003 ). While the 40 Hz ASSR has been used to illustrate consistent gamma abnormalities in several neurodevelopmental disorders, principally schizophrenia ( Brenner et al, 2003 ; Hong et al, 2004 ; Light et al, 2006 ; Hamm et al, 2011 ; Lenz et al, 2011 ; Edgar et al, 2014 ), studies focused on ASD have been more inconsistent ( Rojas et al, 2006 ; Wilson et al, 2007 ; Edgar et al, 2016 ; Ono et al, 2020 ; Seymour et al, 2020 ; Stroganova et al, 2020 ).…”

40-Hz Auditory Steady-State Response (ASSR) as a Biomarker of Genetic Defects in the SHANK3 Gene: A Case Report of 15-Year-Old Girl with a Rare Partial SHANK3 Duplication

“…The 40-Hz ASSR deficit occurs in non-psychotic first-degree relatives of patients with schizophrenia [61] and ASD [59], which is consistent with an effect of familial or genetic risk factors. However, recent larger sample studies in children with ASD did not confirm ASSR reduction [62,63]. Such discrepancy might be related to the well-known heterogeneity of the ASD population.…”

Disturbed Balance of Inhibitory Signaling Links Hearing Loss and Cognition

“…In autism patients and animal models, the reduced inhibition is said to reduce reliability (increasing variability) of signal transformation and the signal-to-noise ratio (Dinstein et al, 2012;Haigh et al, 2016). Interestingly, deficits in fast auditory processing are also reported in nearly normal-hearing children that have ASD (Fitch et al, 2013;Foss-Feig et al, 2017), and here, deficits in fast auditory processing are linked to markedly delayed and displaced auditory steady-state responses (Stroganova et al, 2020), or with rapid spectral-ripple discrimination deficits (Ankmnal Veeranna et al, 2019).…”