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 abnormalities 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, this auditory response may reflect vocal pitch processing abnormalities in ASD. The SF, however, has never been studied in people with this disorder. 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 selective left-hemispheric abnormalities at the level of the core auditory cortex when processing spectrally complex periodic sound. The observed neural deficit may contribute to speech perception difficulties experienced by children with ASD, including their poor perception and production of linguistic prosody.

The age‐related changes in 40 Hz Auditory Steady‐State Response and sustained Event‐Related Fields to the same amplitude‐modulated tones in typically developing children: A magnetoencephalography study

“…In accordance with the previous findings (Edgar et al, 2016; Maurizi et al, 1990; Poulsen et al, 2009; Stapells et al, 1988; Stroganova et al, 2020), we showed a relationship between the strength of 40 Hz ASSR and children's age. Specifically, the results revealed the age‐related increase of 40 Hz ITPC in the right hemisphere in our sample of 7‐to‐12‐year‐old children, and this corresponds to studies which showed a monotonic enhancement of both power and ITPC of auditory gamma oscillations from childhood to the early adolescence (Edgar et al, 2016; Poulsen et al, 2009).…”

“…The analysis of phase consistency across the trials (or ITPC)—a robust measure of the neural response to periodic auditory signal (Tan et al, 2015)—revealed a right hemispheric dominance of 40 Hz ASSR, indicating that the ITPC‐value was higher in the right auditory ROI. This is in line with the previous studies in both children (Edgar et al, 2016; Poulsen et al, 2009; Stroganova et al, 2020) and adults (Pellegrino et al, 2019; Ross et al, 2005). Some authors hypothesized that this asymmetry can be explained by the fact that the right auditory cortex is specialized for processing the temporal periodicity of the sound (Ross et al, 2005).…”

“…Contrary to Edgar and colleagues' MEG study (Edgar et al, 2016) with the similar age‐range group, we detected a clear 40 Hz ASSR in all children from our sample, whereas in Edgar et al (2016) study, 40 Hz ASSR was not observed in the majority of children. Importantly, in a more recent study (Stroganova et al, 2020), 40 Hz ASSR has also been detected in most of the children. Stroganova et al (2020) speculated that, in comparison to Edgar et al (2016) study, they could detect a clear steady‐state 40 Hz gamma response in most children owing to methodological differences, such as, for example, the type of the stimuli (clicks instead of the amplitude‐modulated tones), stimulus presentation (monaural instead of binaural), and source localization methods (sLORETA instead of single dipole modeling).…”

“…The similar age‐related increase in the power of 40 Hz ASSR was shown in another study with 56 typically developing children aged 7–14 years old (Edgar et al, 2016), although, as the authors mentioned, 40 Hz ASSR was not observed in the majority of participants. In a more recent study, Stroganova et al (2020) also have shown the monotonic increase of 40 Hz ASSR with age in a group of 7‐to‐12‐year‐old typically developing boys ( N = 35). In the only longitudinal study, Poulsen and colleagues (2009) aimed to compare the amplitude of 40 Hz ASSR in children aged 10 and then 11.5 years of age.…”

“…There are several studies in children, using MEG/EEG, which focus on the age‐related changes in auditory gamma oscillations, using 40 Hz Auditory Steady‐State Response, or 40 Hz ASSR (Aoyagi et al, 1994; Cho et al, 2015; Edgar et al, 2016; Maurizi et al, 1990; Poulsen et al, 2009; Rojas et al, 2006; Seymour et al, 2020; Stapells et al, 1988; Stroganova et al, 2020). According to this paradigm, participants are presented with amplitude‐modulated tones or click trains at a regular gamma frequency, usually at 40 Hz (Pellegrino et al, 2019; Thut et al, 2011).…”