Diffusion tensor tractography reveals disrupted structural connectivity in childhood absence epilepsy

Summary Purpose The structural connection patterns of the human brain are the underlying bases for functional connectivity. Although abnormal functional connectivity has been uncovered in childhood absence epilepsy (CAE) in previous electroencephalography and functional magnetic resonance imaging st...

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Veröffentlicht in:Epilepsy research 2014-01, Vol.108 (1), p.125-138
Hauptverfasser: Xue, Kaiqing, Luo, Cheng, Zhang, Dan, Yang, Tianhua, Li, Jianfu, Gong, Diankun, Chen, Long, Medina, Yasser Iturria, Gotman, Jean, Zhou, Dong, Yao, Dezhong
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container_end_page 138
container_issue 1
container_start_page 125
container_title Epilepsy research
container_volume 108
creator Xue, Kaiqing
Luo, Cheng
Zhang, Dan
Yang, Tianhua
Li, Jianfu
Gong, Diankun
Chen, Long
Medina, Yasser Iturria
Gotman, Jean
Zhou, Dong
Yao, Dezhong
description Summary Purpose The structural connection patterns of the human brain are the underlying bases for functional connectivity. Although abnormal functional connectivity has been uncovered in childhood absence epilepsy (CAE) in previous electroencephalography and functional magnetic resonance imaging studies, little is known regarding the structural connectivity in CAE. We hypothesized that the structural connectivity would be disrupted in response to the decreased brain function in CAE. Methods Diffusion tensor imaging tractography was utilized to map the white matter (WM) structural network, composed of 90 cortical and sub-cortical regions, in 18 CAE and 18 age- and gender-matched healthy controls. Graph theoretical methods were applied to investigate the alterations in the topological and nodal properties of the networks in these patients. Results Both the CAE and the controls showed small-world properties in their WM networks. However, the network connection strength, absolute clustering coefficient, and global/local efficiency were significantly decreased, but characteristic path length was significantly increased in the CAE compared with the controls. Significantly decreased WM connections, nodal properties, and impaired sub-networks were found in the sub-cortical structures, orbitofrontal area, and limbic cortex in the CAE. Moreover, network connection strength, local efficiency, and nodal features in some regions were significantly negatively correlated with the duration of epilepsy. Conclusions The present study demonstrated, for the first time, the disrupted topological organization of WM networks in CAE. The decreased connectivity and efficiency in the orbitofrontal and sub-cortical regions may serve as anatomical evidence to support the functional abnormalities related to the epileptic discharges observed in CAE. Moreover, the orbitofrontal sub-network may play a key role in CAE. These findings open up new avenues toward the understanding of absence epilepsy.
doi_str_mv 10.1016/j.eplepsyres.2013.10.002
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Although abnormal functional connectivity has been uncovered in childhood absence epilepsy (CAE) in previous electroencephalography and functional magnetic resonance imaging studies, little is known regarding the structural connectivity in CAE. We hypothesized that the structural connectivity would be disrupted in response to the decreased brain function in CAE. Methods Diffusion tensor imaging tractography was utilized to map the white matter (WM) structural network, composed of 90 cortical and sub-cortical regions, in 18 CAE and 18 age- and gender-matched healthy controls. Graph theoretical methods were applied to investigate the alterations in the topological and nodal properties of the networks in these patients. Results Both the CAE and the controls showed small-world properties in their WM networks. However, the network connection strength, absolute clustering coefficient, and global/local efficiency were significantly decreased, but characteristic path length was significantly increased in the CAE compared with the controls. Significantly decreased WM connections, nodal properties, and impaired sub-networks were found in the sub-cortical structures, orbitofrontal area, and limbic cortex in the CAE. Moreover, network connection strength, local efficiency, and nodal features in some regions were significantly negatively correlated with the duration of epilepsy. Conclusions The present study demonstrated, for the first time, the disrupted topological organization of WM networks in CAE. The decreased connectivity and efficiency in the orbitofrontal and sub-cortical regions may serve as anatomical evidence to support the functional abnormalities related to the epileptic discharges observed in CAE. Moreover, the orbitofrontal sub-network may play a key role in CAE. These findings open up new avenues toward the understanding of absence epilepsy.</description><identifier>ISSN: 0920-1211</identifier><identifier>EISSN: 1872-6844</identifier><identifier>DOI: 10.1016/j.eplepsyres.2013.10.002</identifier><identifier>PMID: 24246142</identifier><identifier>CODEN: EPIRE8</identifier><language>eng</language><publisher>Kidlington: Elsevier B.V</publisher><subject>Absence epilepsy ; Biological and medical sciences ; Brain - pathology ; Brain - physiopathology ; Child ; Child, Preschool ; Diffusion Tensor Imaging - methods ; Diffusion tensor tractography ; Epilepsy, Absence - diagnosis ; Epilepsy, Absence - physiopathology ; Female ; Graph theory ; Headache. Facial pains. Syncopes. Epilepsia. Intracranial hypertension. Brain oedema. Cerebral palsy ; Humans ; Male ; Medical sciences ; Nerve Fibers, Myelinated - pathology ; Nerve Net - pathology ; Nerve Net - physiopathology ; Nervous system (semeiology, syndromes) ; Neural Pathways - pathology ; Neural Pathways - physiopathology ; Neurology ; Structural connectivity</subject><ispartof>Epilepsy research, 2014-01, Vol.108 (1), p.125-138</ispartof><rights>Elsevier B.V.</rights><rights>2013 Elsevier B.V.</rights><rights>2015 INIST-CNRS</rights><rights>Copyright © 2013 Elsevier B.V. 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Although abnormal functional connectivity has been uncovered in childhood absence epilepsy (CAE) in previous electroencephalography and functional magnetic resonance imaging studies, little is known regarding the structural connectivity in CAE. We hypothesized that the structural connectivity would be disrupted in response to the decreased brain function in CAE. Methods Diffusion tensor imaging tractography was utilized to map the white matter (WM) structural network, composed of 90 cortical and sub-cortical regions, in 18 CAE and 18 age- and gender-matched healthy controls. Graph theoretical methods were applied to investigate the alterations in the topological and nodal properties of the networks in these patients. Results Both the CAE and the controls showed small-world properties in their WM networks. However, the network connection strength, absolute clustering coefficient, and global/local efficiency were significantly decreased, but characteristic path length was significantly increased in the CAE compared with the controls. Significantly decreased WM connections, nodal properties, and impaired sub-networks were found in the sub-cortical structures, orbitofrontal area, and limbic cortex in the CAE. Moreover, network connection strength, local efficiency, and nodal features in some regions were significantly negatively correlated with the duration of epilepsy. Conclusions The present study demonstrated, for the first time, the disrupted topological organization of WM networks in CAE. The decreased connectivity and efficiency in the orbitofrontal and sub-cortical regions may serve as anatomical evidence to support the functional abnormalities related to the epileptic discharges observed in CAE. Moreover, the orbitofrontal sub-network may play a key role in CAE. These findings open up new avenues toward the understanding of absence epilepsy.</description><subject>Absence epilepsy</subject><subject>Biological and medical sciences</subject><subject>Brain - pathology</subject><subject>Brain - physiopathology</subject><subject>Child</subject><subject>Child, Preschool</subject><subject>Diffusion Tensor Imaging - methods</subject><subject>Diffusion tensor tractography</subject><subject>Epilepsy, Absence - diagnosis</subject><subject>Epilepsy, Absence - physiopathology</subject><subject>Female</subject><subject>Graph theory</subject><subject>Headache. Facial pains. Syncopes. Epilepsia. Intracranial hypertension. Brain oedema. Cerebral palsy</subject><subject>Humans</subject><subject>Male</subject><subject>Medical sciences</subject><subject>Nerve Fibers, Myelinated - pathology</subject><subject>Nerve Net - pathology</subject><subject>Nerve Net - physiopathology</subject><subject>Nervous system (semeiology, syndromes)</subject><subject>Neural Pathways - pathology</subject><subject>Neural Pathways - physiopathology</subject><subject>Neurology</subject><subject>Structural connectivity</subject><issn>0920-1211</issn><issn>1872-6844</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkk2P0zAQhiMEYsvCX0C-IHFJGTu2m1yQYJcvaSUOwNlynDF1Se1gO5Xy73FoYSVOnCyNn3ln9GiqilDYUqDy1WGL04hTWiKmLQPalPIWgD2oNrTdsVq2nD-sNtAxqCmj9Kp6ktIBAHbA-ePqinHGJeVsU-Gts3ZOLniS0acQSY7a5PA96mm_kIgn1GMig0txnjIOJOU4mzxHPRITvEeT3cnlhThPzN6Nwz6Egeg-oTdIcHK_13xaPbIlBp9d3uvq2_t3X28-1nefP3y6eXNXG8FEro1kVMuubXnfdkz2bYODQM4tp43tRW_NgEIwMJpp4FYKYzsUFCyl1Oxk11xXL8-5Uww_Z0xZHV0yOI7aY5iToryDHQMJK9qeURNDShGtmqI76rgoCmqVrA7qXrJaJa8_RXJpfX6ZMvdHHP42_rFagBcXQCejRxu1Ny7dcy10IIUs3Nszh8XJyWFUybhV3OBiEauG4P5nm9f_hJjReVfm_sAF0yHM0RfniqrEFKgv61GsN0Gb0i1k2_wCsG23dA</recordid><startdate>20140101</startdate><enddate>20140101</enddate><creator>Xue, Kaiqing</creator><creator>Luo, Cheng</creator><creator>Zhang, Dan</creator><creator>Yang, Tianhua</creator><creator>Li, Jianfu</creator><creator>Gong, Diankun</creator><creator>Chen, Long</creator><creator>Medina, Yasser Iturria</creator><creator>Gotman, Jean</creator><creator>Zhou, Dong</creator><creator>Yao, Dezhong</creator><general>Elsevier B.V</general><general>Elsevier</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20140101</creationdate><title>Diffusion tensor tractography reveals disrupted structural connectivity in childhood absence epilepsy</title><author>Xue, Kaiqing ; Luo, Cheng ; Zhang, Dan ; Yang, Tianhua ; Li, Jianfu ; Gong, Diankun ; Chen, Long ; Medina, Yasser Iturria ; Gotman, Jean ; Zhou, Dong ; Yao, Dezhong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c525t-c621a69884b8926b83ed5e44f413fb5bfcde5520ca2a04f65cf9e510f111c7693</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Absence epilepsy</topic><topic>Biological and medical sciences</topic><topic>Brain - pathology</topic><topic>Brain - physiopathology</topic><topic>Child</topic><topic>Child, Preschool</topic><topic>Diffusion Tensor Imaging - methods</topic><topic>Diffusion tensor tractography</topic><topic>Epilepsy, Absence - diagnosis</topic><topic>Epilepsy, Absence - physiopathology</topic><topic>Female</topic><topic>Graph theory</topic><topic>Headache. Facial pains. Syncopes. Epilepsia. Intracranial hypertension. Brain oedema. Cerebral palsy</topic><topic>Humans</topic><topic>Male</topic><topic>Medical sciences</topic><topic>Nerve Fibers, Myelinated - pathology</topic><topic>Nerve Net - pathology</topic><topic>Nerve Net - physiopathology</topic><topic>Nervous system (semeiology, syndromes)</topic><topic>Neural Pathways - pathology</topic><topic>Neural Pathways - physiopathology</topic><topic>Neurology</topic><topic>Structural connectivity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xue, Kaiqing</creatorcontrib><creatorcontrib>Luo, Cheng</creatorcontrib><creatorcontrib>Zhang, Dan</creatorcontrib><creatorcontrib>Yang, Tianhua</creatorcontrib><creatorcontrib>Li, Jianfu</creatorcontrib><creatorcontrib>Gong, Diankun</creatorcontrib><creatorcontrib>Chen, Long</creatorcontrib><creatorcontrib>Medina, Yasser Iturria</creatorcontrib><creatorcontrib>Gotman, Jean</creatorcontrib><creatorcontrib>Zhou, Dong</creatorcontrib><creatorcontrib>Yao, Dezhong</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Epilepsy research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xue, Kaiqing</au><au>Luo, Cheng</au><au>Zhang, Dan</au><au>Yang, Tianhua</au><au>Li, Jianfu</au><au>Gong, Diankun</au><au>Chen, Long</au><au>Medina, Yasser Iturria</au><au>Gotman, Jean</au><au>Zhou, Dong</au><au>Yao, Dezhong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Diffusion tensor tractography reveals disrupted structural connectivity in childhood absence epilepsy</atitle><jtitle>Epilepsy research</jtitle><addtitle>Epilepsy Res</addtitle><date>2014-01-01</date><risdate>2014</risdate><volume>108</volume><issue>1</issue><spage>125</spage><epage>138</epage><pages>125-138</pages><issn>0920-1211</issn><eissn>1872-6844</eissn><coden>EPIRE8</coden><abstract>Summary Purpose The structural connection patterns of the human brain are the underlying bases for functional connectivity. Although abnormal functional connectivity has been uncovered in childhood absence epilepsy (CAE) in previous electroencephalography and functional magnetic resonance imaging studies, little is known regarding the structural connectivity in CAE. We hypothesized that the structural connectivity would be disrupted in response to the decreased brain function in CAE. Methods Diffusion tensor imaging tractography was utilized to map the white matter (WM) structural network, composed of 90 cortical and sub-cortical regions, in 18 CAE and 18 age- and gender-matched healthy controls. Graph theoretical methods were applied to investigate the alterations in the topological and nodal properties of the networks in these patients. Results Both the CAE and the controls showed small-world properties in their WM networks. However, the network connection strength, absolute clustering coefficient, and global/local efficiency were significantly decreased, but characteristic path length was significantly increased in the CAE compared with the controls. Significantly decreased WM connections, nodal properties, and impaired sub-networks were found in the sub-cortical structures, orbitofrontal area, and limbic cortex in the CAE. Moreover, network connection strength, local efficiency, and nodal features in some regions were significantly negatively correlated with the duration of epilepsy. Conclusions The present study demonstrated, for the first time, the disrupted topological organization of WM networks in CAE. The decreased connectivity and efficiency in the orbitofrontal and sub-cortical regions may serve as anatomical evidence to support the functional abnormalities related to the epileptic discharges observed in CAE. Moreover, the orbitofrontal sub-network may play a key role in CAE. These findings open up new avenues toward the understanding of absence epilepsy.</abstract><cop>Kidlington</cop><pub>Elsevier B.V</pub><pmid>24246142</pmid><doi>10.1016/j.eplepsyres.2013.10.002</doi><tpages>14</tpages></addata></record>
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subjects Absence epilepsy
Biological and medical sciences
Brain - pathology
Brain - physiopathology
Child
Child, Preschool
Diffusion Tensor Imaging - methods
Diffusion tensor tractography
Epilepsy, Absence - diagnosis
Epilepsy, Absence - physiopathology
Female
Graph theory
Headache. Facial pains. Syncopes. Epilepsia. Intracranial hypertension. Brain oedema. Cerebral palsy
Humans
Male
Medical sciences
Nerve Fibers, Myelinated - pathology
Nerve Net - pathology
Nerve Net - physiopathology
Nervous system (semeiology, syndromes)
Neural Pathways - pathology
Neural Pathways - physiopathology
Neurology
Structural connectivity
title Diffusion tensor tractography reveals disrupted structural connectivity in childhood absence epilepsy
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