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

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...

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Autores principales: Stroganova, T. A., Komarov, K. S., Sysoeva, O. V., Goiaeva, D. E., Obukhova, T. S., Ovsiannikova, T. M., Prokofyev, A. O., Orekhova, E. V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7775632/
https://www.ncbi.nlm.nih.gov/pubmed/33384021
http://dx.doi.org/10.1186/s13229-020-00408-4
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author Stroganova, T. A.
Komarov, K. S.
Sysoeva, O. V.
Goiaeva, D. E.
Obukhova, T. S.
Ovsiannikova, T. M.
Prokofyev, A. O.
Orekhova, E. V.
author_facet Stroganova, T. A.
Komarov, K. S.
Sysoeva, O. V.
Goiaeva, D. E.
Obukhova, T. S.
Ovsiannikova, T. M.
Prokofyev, A. O.
Orekhova, E. V.
author_sort Stroganova, T. A.
collection PubMed
description 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.
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spelling pubmed-77756322021-01-04 Left hemispheric deficit in the sustained neuromagnetic response to periodic click trains in children with ASD Stroganova, T. A. Komarov, K. S. Sysoeva, O. V. Goiaeva, D. E. Obukhova, T. S. Ovsiannikova, T. M. Prokofyev, A. O. Orekhova, E. V. Mol Autism Research 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. BioMed Central 2020-12-31 /pmc/articles/PMC7775632/ /pubmed/33384021 http://dx.doi.org/10.1186/s13229-020-00408-4 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Stroganova, T. A.
Komarov, K. S.
Sysoeva, O. V.
Goiaeva, D. E.
Obukhova, T. S.
Ovsiannikova, T. M.
Prokofyev, A. O.
Orekhova, E. V.
Left hemispheric deficit in the sustained neuromagnetic response to periodic click trains in children with ASD
title Left hemispheric deficit in the sustained neuromagnetic response to periodic click trains in children with ASD
title_full Left hemispheric deficit in the sustained neuromagnetic response to periodic click trains in children with ASD
title_fullStr Left hemispheric deficit in the sustained neuromagnetic response to periodic click trains in children with ASD
title_full_unstemmed Left hemispheric deficit in the sustained neuromagnetic response to periodic click trains in children with ASD
title_short Left hemispheric deficit in the sustained neuromagnetic response to periodic click trains in children with ASD
title_sort left hemispheric deficit in the sustained neuromagnetic response to periodic click trains in children with asd
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7775632/
https://www.ncbi.nlm.nih.gov/pubmed/33384021
http://dx.doi.org/10.1186/s13229-020-00408-4
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