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Aberrant brain oscillatory coupling from the primary motor cortex in children with autism spectrum disorders

Autism spectrum disorder (ASD) often involves dysfunction in general motor control and motor coordination, in addition to core symptoms. However, the neural mechanisms underlying motor dysfunction in ASD are poorly understood. To elucidate this issue, we focused on brain oscillations and their coupl...

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Autores principales: An, Kyung-min, Ikeda, Takashi, Hasegawa, Chiaki, Yoshimura, Yuko, Tanaka, Sanae, Saito, Daisuke N., Yaoi, Ken, Iwasaki, Sumie, Hirosawa, Tetsu, Jensen, Ole, Kikuchi, Mitsuru
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7838765/
https://www.ncbi.nlm.nih.gov/pubmed/33494029
http://dx.doi.org/10.1016/j.nicl.2021.102560
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author An, Kyung-min
Ikeda, Takashi
Hasegawa, Chiaki
Yoshimura, Yuko
Tanaka, Sanae
Saito, Daisuke N.
Yaoi, Ken
Iwasaki, Sumie
Hirosawa, Tetsu
Jensen, Ole
Kikuchi, Mitsuru
author_facet An, Kyung-min
Ikeda, Takashi
Hasegawa, Chiaki
Yoshimura, Yuko
Tanaka, Sanae
Saito, Daisuke N.
Yaoi, Ken
Iwasaki, Sumie
Hirosawa, Tetsu
Jensen, Ole
Kikuchi, Mitsuru
author_sort An, Kyung-min
collection PubMed
description Autism spectrum disorder (ASD) often involves dysfunction in general motor control and motor coordination, in addition to core symptoms. However, the neural mechanisms underlying motor dysfunction in ASD are poorly understood. To elucidate this issue, we focused on brain oscillations and their coupling in the primary motor cortex (M1). We recorded magnetoencephalography in 18 children with ASD, aged 5 to 7 years, and 19 age- and IQ-matched typically-developing children while they pressed a button during a video-game-like motor task. The motor-related gamma (70 to 90 Hz) and pre-movement beta oscillations (15 to 25 Hz) were analyzed in the primary motor cortex using an inverse method. To determine the coupling between beta and gamma oscillations, we applied phase-amplitude coupling to calculate the statistical dependence between the amplitude of fast oscillations and the phase of slow oscillations. We observed a motor-related gamma increase and a pre-movement beta decrease in both groups. The ASD group exhibited a reduced motor-related gamma increase and enhanced pre-movement beta decrease in the ipsilateral primary motor cortex. We found phase-amplitude coupling, in which high-gamma activity was modulated by the beta rhythm in the primary motor cortex. Phase-amplitude coupling in the ipsilateral primary motor cortex was reduced in the ASD group compared with the control group. Using oscillatory changes and their couplings, linear discriminant analysis classified the ASD and control groups with high accuracy (area under the receiver operating characteristic curve: 97.1%). The current findings revealed alterations in oscillations and oscillatory coupling, reflecting the dysregulation of motor gating mechanisms in ASD. These results may be helpful for elucidating the neural mechanisms underlying motor dysfunction in ASD, suggesting the possibility of developing a biomarker for ASD diagnosis.
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spelling pubmed-78387652021-02-02 Aberrant brain oscillatory coupling from the primary motor cortex in children with autism spectrum disorders An, Kyung-min Ikeda, Takashi Hasegawa, Chiaki Yoshimura, Yuko Tanaka, Sanae Saito, Daisuke N. Yaoi, Ken Iwasaki, Sumie Hirosawa, Tetsu Jensen, Ole Kikuchi, Mitsuru Neuroimage Clin Regular Article Autism spectrum disorder (ASD) often involves dysfunction in general motor control and motor coordination, in addition to core symptoms. However, the neural mechanisms underlying motor dysfunction in ASD are poorly understood. To elucidate this issue, we focused on brain oscillations and their coupling in the primary motor cortex (M1). We recorded magnetoencephalography in 18 children with ASD, aged 5 to 7 years, and 19 age- and IQ-matched typically-developing children while they pressed a button during a video-game-like motor task. The motor-related gamma (70 to 90 Hz) and pre-movement beta oscillations (15 to 25 Hz) were analyzed in the primary motor cortex using an inverse method. To determine the coupling between beta and gamma oscillations, we applied phase-amplitude coupling to calculate the statistical dependence between the amplitude of fast oscillations and the phase of slow oscillations. We observed a motor-related gamma increase and a pre-movement beta decrease in both groups. The ASD group exhibited a reduced motor-related gamma increase and enhanced pre-movement beta decrease in the ipsilateral primary motor cortex. We found phase-amplitude coupling, in which high-gamma activity was modulated by the beta rhythm in the primary motor cortex. Phase-amplitude coupling in the ipsilateral primary motor cortex was reduced in the ASD group compared with the control group. Using oscillatory changes and their couplings, linear discriminant analysis classified the ASD and control groups with high accuracy (area under the receiver operating characteristic curve: 97.1%). The current findings revealed alterations in oscillations and oscillatory coupling, reflecting the dysregulation of motor gating mechanisms in ASD. These results may be helpful for elucidating the neural mechanisms underlying motor dysfunction in ASD, suggesting the possibility of developing a biomarker for ASD diagnosis. Elsevier 2021-01-14 /pmc/articles/PMC7838765/ /pubmed/33494029 http://dx.doi.org/10.1016/j.nicl.2021.102560 Text en © 2021 The Author(s) http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Regular Article
An, Kyung-min
Ikeda, Takashi
Hasegawa, Chiaki
Yoshimura, Yuko
Tanaka, Sanae
Saito, Daisuke N.
Yaoi, Ken
Iwasaki, Sumie
Hirosawa, Tetsu
Jensen, Ole
Kikuchi, Mitsuru
Aberrant brain oscillatory coupling from the primary motor cortex in children with autism spectrum disorders
title Aberrant brain oscillatory coupling from the primary motor cortex in children with autism spectrum disorders
title_full Aberrant brain oscillatory coupling from the primary motor cortex in children with autism spectrum disorders
title_fullStr Aberrant brain oscillatory coupling from the primary motor cortex in children with autism spectrum disorders
title_full_unstemmed Aberrant brain oscillatory coupling from the primary motor cortex in children with autism spectrum disorders
title_short Aberrant brain oscillatory coupling from the primary motor cortex in children with autism spectrum disorders
title_sort aberrant brain oscillatory coupling from the primary motor cortex in children with autism spectrum disorders
topic Regular Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7838765/
https://www.ncbi.nlm.nih.gov/pubmed/33494029
http://dx.doi.org/10.1016/j.nicl.2021.102560
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