Lesser suppression of response to bright visual stimuli and visual abnormality in children with autism spectrum disorder: a magnetoencephalographic study

Abstract Background Visual abnormality is a common sensory impairment in autism spectrum disorder (ASD), which may cause behavioral problems. However, only a few studies exist on the neural features corresponding to the visual symptoms in ASD. The purpose of this study was to investigate the relatio...

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Main Authors: Sho Aoki, Kuriko Kagitani-Shimono, Junko Matsuzaki, Ryuzo Hanaie, Mariko Nakanishi, Koji Tominaga, Yukie Nagai, Ikuko Mohri, Masako Taniike
Format: Article
Language:English
Published: BMC 2019-06-01
Series:Journal of Neurodevelopmental Disorders
Subjects:
Online Access:http://link.springer.com/article/10.1186/s11689-019-9266-0
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author Sho Aoki
Kuriko Kagitani-Shimono
Junko Matsuzaki
Ryuzo Hanaie
Mariko Nakanishi
Koji Tominaga
Yukie Nagai
Ikuko Mohri
Masako Taniike
author_facet Sho Aoki
Kuriko Kagitani-Shimono
Junko Matsuzaki
Ryuzo Hanaie
Mariko Nakanishi
Koji Tominaga
Yukie Nagai
Ikuko Mohri
Masako Taniike
author_sort Sho Aoki
collection DOAJ
description Abstract Background Visual abnormality is a common sensory impairment in autism spectrum disorder (ASD), which may cause behavioral problems. However, only a few studies exist on the neural features corresponding to the visual symptoms in ASD. The purpose of this study was to investigate the relationship between cortical responses to visual stimuli and visual abnormality to examine the neurophysiological mechanisms of the visual abnormality in ASD. Methods Twenty-two high-functioning children with ASD (10.95 ± 2.01 years old) and 23 age-matched typically developing (TD) children (10.13 ± 2.80 years old) participated in this study. We measured the cortical responses (i.e., activated intensity and attenuation ratio) elicited by the Original visual image and other two types of bright images (the Dot noise or Blind image, which includes overlapped particles onto the Original image or the enhanced-brightness version of the Original image, respectively) using magnetoencephalography. Results The severity of visual abnormalities was significantly associated with behavioral problems in children with ASD. In addition, we found the increased cortical activation in response to the Original image in the left supramarginal gyrus (SMG) and middle temporal gyrus in children with ASD. However, there were no inter-group differences in the primary visual and medial orbitofrontal cortices. Furthermore, when we compared cortical responses according to the type of images, children with ASD showed lesser attenuation of the activated intensities than children with TD in response to the bright images compared with the Original image in the right SMG. These attenuation ratios (Dot noise/Original and Blind/Original) were also associated with the severity of visual abnormalities. Conclusions Our results show that dysfunction of stimulus-driven neural suppression plays a crucial role in the neural mechanism of visual abnormality in children with ASD. To the best of our knowledge, this is the first magnetoencephalography study to demonstrate the association between the severity of visual abnormality and lower attenuation ratios in children with ASD. Our results contribute to the knowledge of the mechanisms underlying visual abnormality in children with ASD, and may therefore lead to more effective diagnosis and earlier intervention.
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spelling doaj.art-86e28a6e5a734457bcff980a81b066e82022-12-22T00:36:39ZengBMCJournal of Neurodevelopmental Disorders1866-19471866-19552019-06-0111111310.1186/s11689-019-9266-0Lesser suppression of response to bright visual stimuli and visual abnormality in children with autism spectrum disorder: a magnetoencephalographic studySho Aoki0Kuriko Kagitani-Shimono1Junko Matsuzaki2Ryuzo Hanaie3Mariko Nakanishi4Koji Tominaga5Yukie Nagai6Ikuko Mohri7Masako Taniike8Division of Developmental Neuroscience, United Graduate School of Child Development, Osaka UniversityDivision of Developmental Neuroscience, United Graduate School of Child Development, Osaka UniversityMolecular Research Center for Children’s Mental Development, United Graduate School of Child Development, Osaka UniversityMolecular Research Center for Children’s Mental Development, United Graduate School of Child Development, Osaka UniversityMolecular Research Center for Children’s Mental Development, United Graduate School of Child Development, Osaka UniversityDivision of Developmental Neuroscience, United Graduate School of Child Development, Osaka UniversityNational Institute of Information and Communications TechnologyDivision of Developmental Neuroscience, United Graduate School of Child Development, Osaka UniversityDivision of Developmental Neuroscience, United Graduate School of Child Development, Osaka UniversityAbstract Background Visual abnormality is a common sensory impairment in autism spectrum disorder (ASD), which may cause behavioral problems. However, only a few studies exist on the neural features corresponding to the visual symptoms in ASD. The purpose of this study was to investigate the relationship between cortical responses to visual stimuli and visual abnormality to examine the neurophysiological mechanisms of the visual abnormality in ASD. Methods Twenty-two high-functioning children with ASD (10.95 ± 2.01 years old) and 23 age-matched typically developing (TD) children (10.13 ± 2.80 years old) participated in this study. We measured the cortical responses (i.e., activated intensity and attenuation ratio) elicited by the Original visual image and other two types of bright images (the Dot noise or Blind image, which includes overlapped particles onto the Original image or the enhanced-brightness version of the Original image, respectively) using magnetoencephalography. Results The severity of visual abnormalities was significantly associated with behavioral problems in children with ASD. In addition, we found the increased cortical activation in response to the Original image in the left supramarginal gyrus (SMG) and middle temporal gyrus in children with ASD. However, there were no inter-group differences in the primary visual and medial orbitofrontal cortices. Furthermore, when we compared cortical responses according to the type of images, children with ASD showed lesser attenuation of the activated intensities than children with TD in response to the bright images compared with the Original image in the right SMG. These attenuation ratios (Dot noise/Original and Blind/Original) were also associated with the severity of visual abnormalities. Conclusions Our results show that dysfunction of stimulus-driven neural suppression plays a crucial role in the neural mechanism of visual abnormality in children with ASD. To the best of our knowledge, this is the first magnetoencephalography study to demonstrate the association between the severity of visual abnormality and lower attenuation ratios in children with ASD. Our results contribute to the knowledge of the mechanisms underlying visual abnormality in children with ASD, and may therefore lead to more effective diagnosis and earlier intervention.http://link.springer.com/article/10.1186/s11689-019-9266-0Autism spectrum disorders (ASD)Visual abnormalityNeural suppressionBright visual stimuliSupramarginal gyrus (SMG)Magnetoencephalography (MEG)
spellingShingle Sho Aoki
Kuriko Kagitani-Shimono
Junko Matsuzaki
Ryuzo Hanaie
Mariko Nakanishi
Koji Tominaga
Yukie Nagai
Ikuko Mohri
Masako Taniike
Lesser suppression of response to bright visual stimuli and visual abnormality in children with autism spectrum disorder: a magnetoencephalographic study
Journal of Neurodevelopmental Disorders
Autism spectrum disorders (ASD)
Visual abnormality
Neural suppression
Bright visual stimuli
Supramarginal gyrus (SMG)
Magnetoencephalography (MEG)
title Lesser suppression of response to bright visual stimuli and visual abnormality in children with autism spectrum disorder: a magnetoencephalographic study
title_full Lesser suppression of response to bright visual stimuli and visual abnormality in children with autism spectrum disorder: a magnetoencephalographic study
title_fullStr Lesser suppression of response to bright visual stimuli and visual abnormality in children with autism spectrum disorder: a magnetoencephalographic study
title_full_unstemmed Lesser suppression of response to bright visual stimuli and visual abnormality in children with autism spectrum disorder: a magnetoencephalographic study
title_short Lesser suppression of response to bright visual stimuli and visual abnormality in children with autism spectrum disorder: a magnetoencephalographic study
title_sort lesser suppression of response to bright visual stimuli and visual abnormality in children with autism spectrum disorder a magnetoencephalographic study
topic Autism spectrum disorders (ASD)
Visual abnormality
Neural suppression
Bright visual stimuli
Supramarginal gyrus (SMG)
Magnetoencephalography (MEG)
url http://link.springer.com/article/10.1186/s11689-019-9266-0
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