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Auditory encoding abnormalities in children with autism spectrum disorder suggest delayed development of auditory cortex

BACKGROUND: Findings of auditory abnormalities in children with autism spectrum disorder (ASD) include delayed superior temporal gyrus auditory responses, pre- and post-stimulus superior temporal gyrus (STG) auditory oscillatory abnormalities, and atypical hemispheric lateralization. These abnormali...

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Autores principales: Edgar, J. Christopher, Fisk IV, Charles L., Berman, Jeffrey I., Chudnovskaya, Darina, Liu, Song, Pandey, Juhi, Herrington, John D., Port, Russell G., Schultz, Robert T., Roberts, Timothy P. L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4696177/
https://www.ncbi.nlm.nih.gov/pubmed/26719787
http://dx.doi.org/10.1186/s13229-015-0065-5
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author Edgar, J. Christopher
Fisk IV, Charles L.
Berman, Jeffrey I.
Chudnovskaya, Darina
Liu, Song
Pandey, Juhi
Herrington, John D.
Port, Russell G.
Schultz, Robert T.
Roberts, Timothy P. L.
author_facet Edgar, J. Christopher
Fisk IV, Charles L.
Berman, Jeffrey I.
Chudnovskaya, Darina
Liu, Song
Pandey, Juhi
Herrington, John D.
Port, Russell G.
Schultz, Robert T.
Roberts, Timothy P. L.
author_sort Edgar, J. Christopher
collection PubMed
description BACKGROUND: Findings of auditory abnormalities in children with autism spectrum disorder (ASD) include delayed superior temporal gyrus auditory responses, pre- and post-stimulus superior temporal gyrus (STG) auditory oscillatory abnormalities, and atypical hemispheric lateralization. These abnormalities are likely associated with abnormal brain maturation. To better understand changes in brain activity as a function of age, the present study investigated associations between age and STG auditory time-domain and time-frequency neural activity. METHODS: While 306-channel magnetoencephalography (MEG) data were recorded, 500- and 1000-Hz tones of 300-ms duration were binaurally presented. Evaluable data were obtained from 63 typically developing children (TDC) (6 to 14 years old) and 52 children with ASD (6 to 14 years old). T1-weighted structural MRI was obtained, and a source model created using single dipoles anatomically constrained to each participant’s left and right STG. Using this source model, left and right 50-ms (M50), 100-ms (M100), and 200-ms (M200) time-domain and time-frequency measures (total power (TP) and inter-trial coherence (ITC)) were obtained. RESULTS: Paired t tests showed a right STG M100 latency delay in ASD versus TDC (significant for right 500 Hz and marginally significant for right 1000 Hz). In the left and right STG, time-frequency analyses showed a greater pre- to post-stimulus increase in 4- to 16-Hz TP for both tones in ASD versus TDC after 150 ms. In the right STG, greater post-stimulus 4- to 16-Hz ITC for both tones was observed in TDC versus ASD after 200 ms. Analyses of age effects suggested M200 group differences that were due to a maturational delay in ASD, with left and right M200 decreasing with age in TDC but significantly less so in ASD. Additional evidence indicating delayed maturation of auditory cortex in ASD included atypical hemispheric functional asymmetries, including a right versus left M100 latency advantage in TDC but not ASD, and a stronger left than right M50 response in TDC but not ASD. CONCLUSIONS: Present findings indicated maturational abnormalities in the development of primary/secondary auditory areas in children with ASD. It is hypothesized that a longitudinal investigation of the maturation of auditory network activity will indicate delayed development of each component of the auditory processing system in ASD. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13229-015-0065-5) contains supplementary material, which is available to authorized users.
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spelling pubmed-46961772015-12-31 Auditory encoding abnormalities in children with autism spectrum disorder suggest delayed development of auditory cortex Edgar, J. Christopher Fisk IV, Charles L. Berman, Jeffrey I. Chudnovskaya, Darina Liu, Song Pandey, Juhi Herrington, John D. Port, Russell G. Schultz, Robert T. Roberts, Timothy P. L. Mol Autism Research BACKGROUND: Findings of auditory abnormalities in children with autism spectrum disorder (ASD) include delayed superior temporal gyrus auditory responses, pre- and post-stimulus superior temporal gyrus (STG) auditory oscillatory abnormalities, and atypical hemispheric lateralization. These abnormalities are likely associated with abnormal brain maturation. To better understand changes in brain activity as a function of age, the present study investigated associations between age and STG auditory time-domain and time-frequency neural activity. METHODS: While 306-channel magnetoencephalography (MEG) data were recorded, 500- and 1000-Hz tones of 300-ms duration were binaurally presented. Evaluable data were obtained from 63 typically developing children (TDC) (6 to 14 years old) and 52 children with ASD (6 to 14 years old). T1-weighted structural MRI was obtained, and a source model created using single dipoles anatomically constrained to each participant’s left and right STG. Using this source model, left and right 50-ms (M50), 100-ms (M100), and 200-ms (M200) time-domain and time-frequency measures (total power (TP) and inter-trial coherence (ITC)) were obtained. RESULTS: Paired t tests showed a right STG M100 latency delay in ASD versus TDC (significant for right 500 Hz and marginally significant for right 1000 Hz). In the left and right STG, time-frequency analyses showed a greater pre- to post-stimulus increase in 4- to 16-Hz TP for both tones in ASD versus TDC after 150 ms. In the right STG, greater post-stimulus 4- to 16-Hz ITC for both tones was observed in TDC versus ASD after 200 ms. Analyses of age effects suggested M200 group differences that were due to a maturational delay in ASD, with left and right M200 decreasing with age in TDC but significantly less so in ASD. Additional evidence indicating delayed maturation of auditory cortex in ASD included atypical hemispheric functional asymmetries, including a right versus left M100 latency advantage in TDC but not ASD, and a stronger left than right M50 response in TDC but not ASD. CONCLUSIONS: Present findings indicated maturational abnormalities in the development of primary/secondary auditory areas in children with ASD. It is hypothesized that a longitudinal investigation of the maturation of auditory network activity will indicate delayed development of each component of the auditory processing system in ASD. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13229-015-0065-5) contains supplementary material, which is available to authorized users. BioMed Central 2015-12-30 /pmc/articles/PMC4696177/ /pubmed/26719787 http://dx.doi.org/10.1186/s13229-015-0065-5 Text en © Edgar et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.
spellingShingle Research
Edgar, J. Christopher
Fisk IV, Charles L.
Berman, Jeffrey I.
Chudnovskaya, Darina
Liu, Song
Pandey, Juhi
Herrington, John D.
Port, Russell G.
Schultz, Robert T.
Roberts, Timothy P. L.
Auditory encoding abnormalities in children with autism spectrum disorder suggest delayed development of auditory cortex
title Auditory encoding abnormalities in children with autism spectrum disorder suggest delayed development of auditory cortex
title_full Auditory encoding abnormalities in children with autism spectrum disorder suggest delayed development of auditory cortex
title_fullStr Auditory encoding abnormalities in children with autism spectrum disorder suggest delayed development of auditory cortex
title_full_unstemmed Auditory encoding abnormalities in children with autism spectrum disorder suggest delayed development of auditory cortex
title_short Auditory encoding abnormalities in children with autism spectrum disorder suggest delayed development of auditory cortex
title_sort auditory encoding abnormalities in children with autism spectrum disorder suggest delayed development of auditory cortex
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4696177/
https://www.ncbi.nlm.nih.gov/pubmed/26719787
http://dx.doi.org/10.1186/s13229-015-0065-5
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