Common and Distinct Disruptions of Cortical Surface Morphology Between Autism Spectrum Disorder Children With and Without SHANK3 Deficiency
SH3 and Multiple Ankyrin Repeat Domains 3 (SHANK3)-caused autism spectrum disorder (ASD) may present a unique opportunity to clarify the heterogeneous neuropathological mechanisms of ASD. However, the specificity and commonality of disrupted large-scale brain organization in SHANK3-deficient childre...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-10-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2021.751364/full |
| _version_ | 1818719344620732416 |
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| author | Dongyun Li Chunxue Liu Ziyi Huang Ziyi Huang Huiping Li Qiong Xu Bingrui Zhou Chunchun Hu Ying Zhang Yi Wang Jingxin Nie Zhongwei Qiao Dazhi Yin Xiu Xu |
| author_facet | Dongyun Li Chunxue Liu Ziyi Huang Ziyi Huang Huiping Li Qiong Xu Bingrui Zhou Chunchun Hu Ying Zhang Yi Wang Jingxin Nie Zhongwei Qiao Dazhi Yin Xiu Xu |
| author_sort | Dongyun Li |
| collection | DOAJ |
| description | SH3 and Multiple Ankyrin Repeat Domains 3 (SHANK3)-caused autism spectrum disorder (ASD) may present a unique opportunity to clarify the heterogeneous neuropathological mechanisms of ASD. However, the specificity and commonality of disrupted large-scale brain organization in SHANK3-deficient children remain largely unknown. The present study combined genetic tests, neurobehavioral evaluations, and magnetic resonance imaging, aiming to explore the disruptions of both local and networked cortical structural organization in ASD children with and without SHANK3 deficiency. Multiple surface morphological parameters such as cortical thickness (CT) and sulcus depth were estimated, and the graph theory was adopted to characterize the topological properties of structural covariance networks (SCNs). Finally, a correlation analysis between the alterations in brain morphological features and the neurobehavioral evaluations was performed. Compared with typically developed children, increased CT and reduced nodal degree were found in both ASD children with and without SHANK3 defects mainly in the lateral temporal cortex, prefrontal cortex (PFC), temporo-parietal junction (TPJ), superior temporal gyrus (STG), and limbic/paralimbic regions. Besides commonality, our findings showed some distinct abnormalities in ASD children with SHANK3 defects compared to those without. Locally, more changes in the STG and orbitofrontal cortex were exhibited in ASD children with SHANK3 defects, while more changes in the TPJ and inferior parietal lobe (IPL) in those without SHANK3 defects were observed. For the SCNs, a trend toward regular network topology was observed in ASD children with SHANK3 defects, but not in those without. In addition, ASD children with SHANK3 defects showed more alterations of nodal degrees in the anterior and posterior cingulate cortices and right insular, while there were more disruptions in the sensorimotor areas and the left insular and dorsomedial PFC in ASD without SHANK3 defects. Our findings indicate dissociable disruptions of local and networked brain morphological features in ASD children with and without SHANK3 deficiency. Moreover, this monogenic study may provide a valuable path for parsing the heterogeneity of brain disturbances in ASD. |
| first_indexed | 2024-12-17T20:05:27Z |
| format | Article |
| id | doaj.art-95bcdd2cce6c47ec994c5f20748986fc |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-12-17T20:05:27Z |
| publishDate | 2021-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj.art-95bcdd2cce6c47ec994c5f20748986fc2022-12-21T21:34:21ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2021-10-011510.3389/fnins.2021.751364751364Common and Distinct Disruptions of Cortical Surface Morphology Between Autism Spectrum Disorder Children With and Without SHANK3 DeficiencyDongyun Li0Chunxue Liu1Ziyi Huang2Ziyi Huang3Huiping Li4Qiong Xu5Bingrui Zhou6Chunchun Hu7Ying Zhang8Yi Wang9Jingxin Nie10Zhongwei Qiao11Dazhi Yin12Xiu Xu13Department of Child Health Care, Children’s Hospital of Fudan University, Shanghai, ChinaDepartment of Child Health Care, Children’s Hospital of Fudan University, Shanghai, ChinaShanghai Key Laboratory of Brain Functional Genomics (Ministry of Education), School of Psychology and Cognitive Science, Affiliated Mental Health Center, East China Normal University, Shanghai, ChinaSchool of Psychology, South China Normal University, Guangzhou, ChinaDepartment of Child Health Care, Children’s Hospital of Fudan University, Shanghai, ChinaDepartment of Child Health Care, Children’s Hospital of Fudan University, Shanghai, ChinaDepartment of Child Health Care, Children’s Hospital of Fudan University, Shanghai, ChinaDepartment of Child Health Care, Children’s Hospital of Fudan University, Shanghai, ChinaDepartment of Child Health Care, Children’s Hospital of Fudan University, Shanghai, ChinaDepartment of Child Health Care, Children’s Hospital of Fudan University, Shanghai, ChinaSchool of Psychology, South China Normal University, Guangzhou, ChinaDepartment of Radiology, Children’s Hospital of Fudan University, Shanghai, ChinaShanghai Key Laboratory of Brain Functional Genomics (Ministry of Education), School of Psychology and Cognitive Science, Affiliated Mental Health Center, East China Normal University, Shanghai, ChinaDepartment of Child Health Care, Children’s Hospital of Fudan University, Shanghai, ChinaSH3 and Multiple Ankyrin Repeat Domains 3 (SHANK3)-caused autism spectrum disorder (ASD) may present a unique opportunity to clarify the heterogeneous neuropathological mechanisms of ASD. However, the specificity and commonality of disrupted large-scale brain organization in SHANK3-deficient children remain largely unknown. The present study combined genetic tests, neurobehavioral evaluations, and magnetic resonance imaging, aiming to explore the disruptions of both local and networked cortical structural organization in ASD children with and without SHANK3 deficiency. Multiple surface morphological parameters such as cortical thickness (CT) and sulcus depth were estimated, and the graph theory was adopted to characterize the topological properties of structural covariance networks (SCNs). Finally, a correlation analysis between the alterations in brain morphological features and the neurobehavioral evaluations was performed. Compared with typically developed children, increased CT and reduced nodal degree were found in both ASD children with and without SHANK3 defects mainly in the lateral temporal cortex, prefrontal cortex (PFC), temporo-parietal junction (TPJ), superior temporal gyrus (STG), and limbic/paralimbic regions. Besides commonality, our findings showed some distinct abnormalities in ASD children with SHANK3 defects compared to those without. Locally, more changes in the STG and orbitofrontal cortex were exhibited in ASD children with SHANK3 defects, while more changes in the TPJ and inferior parietal lobe (IPL) in those without SHANK3 defects were observed. For the SCNs, a trend toward regular network topology was observed in ASD children with SHANK3 defects, but not in those without. In addition, ASD children with SHANK3 defects showed more alterations of nodal degrees in the anterior and posterior cingulate cortices and right insular, while there were more disruptions in the sensorimotor areas and the left insular and dorsomedial PFC in ASD without SHANK3 defects. Our findings indicate dissociable disruptions of local and networked brain morphological features in ASD children with and without SHANK3 deficiency. Moreover, this monogenic study may provide a valuable path for parsing the heterogeneity of brain disturbances in ASD.https://www.frontiersin.org/articles/10.3389/fnins.2021.751364/fullsurface-based morphometrystructural covariance networksautism spectrum disorderSHANK3children |
| spellingShingle | Dongyun Li Chunxue Liu Ziyi Huang Ziyi Huang Huiping Li Qiong Xu Bingrui Zhou Chunchun Hu Ying Zhang Yi Wang Jingxin Nie Zhongwei Qiao Dazhi Yin Xiu Xu Common and Distinct Disruptions of Cortical Surface Morphology Between Autism Spectrum Disorder Children With and Without SHANK3 Deficiency Frontiers in Neuroscience surface-based morphometry structural covariance networks autism spectrum disorder SHANK3 children |
| title | Common and Distinct Disruptions of Cortical Surface Morphology Between Autism Spectrum Disorder Children With and Without SHANK3 Deficiency |
| title_full | Common and Distinct Disruptions of Cortical Surface Morphology Between Autism Spectrum Disorder Children With and Without SHANK3 Deficiency |
| title_fullStr | Common and Distinct Disruptions of Cortical Surface Morphology Between Autism Spectrum Disorder Children With and Without SHANK3 Deficiency |
| title_full_unstemmed | Common and Distinct Disruptions of Cortical Surface Morphology Between Autism Spectrum Disorder Children With and Without SHANK3 Deficiency |
| title_short | Common and Distinct Disruptions of Cortical Surface Morphology Between Autism Spectrum Disorder Children With and Without SHANK3 Deficiency |
| title_sort | common and distinct disruptions of cortical surface morphology between autism spectrum disorder children with and without shank3 deficiency |
| topic | surface-based morphometry structural covariance networks autism spectrum disorder SHANK3 children |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2021.751364/full |
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