Delayed convergence between brain network structure and function in rolandic epilepsy

R.M.H. Besseling, J.F.A. Jansen, G.M. Overvliet, S.J.M. van der Kruijs, S.C.M. Ebus, A.J.A. de Louw, P.A.M. Hofman, A.P. Aldenkamp, W.H. Backes

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    INTRODUCTION: Rolandic epilepsy (RE) manifests during a critical phase of brain development, and has been associated with language impairments. Concordant abnormalities in structural and functional connectivity (SC and FC) have been described before. As SC and FC are under mutual influence, the current study investigates abnormalities in the SC-FC synergy in RE.

    METHODS: Twenty-two children with RE (age, mean ± SD: 11.3 ± 2.0 y) and 22 healthy controls (age 10.5 ± 1.6 y) underwent structural, diffusion weighted, and resting-state functional magnetic resonance imaging (MRI) at 3T. The probabilistic anatomical landmarks atlas was used to parcellate the (sub)cortical gray matter. Constrained spherical deconvolution tractography and correlation of time series were used to assess SC and FC, respectively. The SC-FC correlation was assessed as a function of age for the non-zero structural connections over a range of sparsity values (0.01-0.75). A modularity analysis was performed on the mean SC network of the controls to localize potential global effects to subnetworks. SC and FC were also assessed separately using graph analysis.

    RESULTS: The SC-FC correlation was significantly reduced in children with RE compared to healthy controls, especially for the youngest participants. This effect was most pronounced in a left and a right centro-temporal network, as well as in a medial parietal network. Graph analysis revealed no prominent abnormalities in SC or FC network organization.

    CONCLUSION: Since SC and FC converge during normal maturation, our finding of reduced SC-FC correlation illustrates impaired synergy between brain structure and function. More specifically, since this effect was most pronounced in the youngest participants, RE may represent a developmental disorder of delayed brain network maturation. The observed effects seem especially attributable to medial parietal connections, which forms an intermediate between bilateral centro-temporal modules of epileptiform activity, and bear relevance for language function.

    TaalEngels
    Pagina's704
    TijdschriftFrontiers in Human Neuroscience
    Volume8
    DOI's
    StatusGepubliceerd - 2014

    Vingerafdruk

    Rolandic Epilepsy
    Brain
    Language
    Atlases
    Brain Diseases
    Magnetic Resonance Imaging

    Trefwoorden

      Citeer dit

      Besseling, R. M. H., Jansen, J. F. A., Overvliet, G. M., van der Kruijs, S. J. M., Ebus, S. C. M., de Louw, A. J. A., ... Backes, W. H. (2014). Delayed convergence between brain network structure and function in rolandic epilepsy. Frontiers in Human Neuroscience, 8, 704. DOI: 10.3389/fnhum.2014.00704
      Besseling, R.M.H. ; Jansen, J.F.A. ; Overvliet, G.M. ; van der Kruijs, S.J.M. ; Ebus, S.C.M. ; de Louw, A.J.A. ; Hofman, P.A.M. ; Aldenkamp, A.P. ; Backes, W.H./ Delayed convergence between brain network structure and function in rolandic epilepsy. In: Frontiers in Human Neuroscience. 2014 ; Vol. 8. blz. 704
      @article{fa9077bb9ca74252b556844e706aae97,
      title = "Delayed convergence between brain network structure and function in rolandic epilepsy",
      abstract = "INTRODUCTION: Rolandic epilepsy (RE) manifests during a critical phase of brain development, and has been associated with language impairments. Concordant abnormalities in structural and functional connectivity (SC and FC) have been described before. As SC and FC are under mutual influence, the current study investigates abnormalities in the SC-FC synergy in RE.METHODS: Twenty-two children with RE (age, mean ± SD: 11.3 ± 2.0 y) and 22 healthy controls (age 10.5 ± 1.6 y) underwent structural, diffusion weighted, and resting-state functional magnetic resonance imaging (MRI) at 3T. The probabilistic anatomical landmarks atlas was used to parcellate the (sub)cortical gray matter. Constrained spherical deconvolution tractography and correlation of time series were used to assess SC and FC, respectively. The SC-FC correlation was assessed as a function of age for the non-zero structural connections over a range of sparsity values (0.01-0.75). A modularity analysis was performed on the mean SC network of the controls to localize potential global effects to subnetworks. SC and FC were also assessed separately using graph analysis.RESULTS: The SC-FC correlation was significantly reduced in children with RE compared to healthy controls, especially for the youngest participants. This effect was most pronounced in a left and a right centro-temporal network, as well as in a medial parietal network. Graph analysis revealed no prominent abnormalities in SC or FC network organization.CONCLUSION: Since SC and FC converge during normal maturation, our finding of reduced SC-FC correlation illustrates impaired synergy between brain structure and function. More specifically, since this effect was most pronounced in the youngest participants, RE may represent a developmental disorder of delayed brain network maturation. The observed effects seem especially attributable to medial parietal connections, which forms an intermediate between bilateral centro-temporal modules of epileptiform activity, and bear relevance for language function.",
      keywords = "Journal Article",
      author = "R.M.H. Besseling and J.F.A. Jansen and G.M. Overvliet and {van der Kruijs}, S.J.M. and S.C.M. Ebus and {de Louw}, A.J.A. and P.A.M. Hofman and A.P. Aldenkamp and W.H. Backes",
      year = "2014",
      doi = "10.3389/fnhum.2014.00704",
      language = "English",
      volume = "8",
      pages = "704",
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      Besseling, RMH, Jansen, JFA, Overvliet, GM, van der Kruijs, SJM, Ebus, SCM, de Louw, AJA, Hofman, PAM, Aldenkamp, AP & Backes, WH 2014, 'Delayed convergence between brain network structure and function in rolandic epilepsy' Frontiers in Human Neuroscience, vol. 8, blz. 704. DOI: 10.3389/fnhum.2014.00704

      Delayed convergence between brain network structure and function in rolandic epilepsy. / Besseling, R.M.H.; Jansen, J.F.A.; Overvliet, G.M.; van der Kruijs, S.J.M.; Ebus, S.C.M.; de Louw, A.J.A.; Hofman, P.A.M.; Aldenkamp, A.P.; Backes, W.H.

      In: Frontiers in Human Neuroscience, Vol. 8, 2014, blz. 704.

      Onderzoeksoutput: Bijdrage aan tijdschriftTijdschriftartikelAcademicpeer review

      TY - JOUR

      T1 - Delayed convergence between brain network structure and function in rolandic epilepsy

      AU - Besseling,R.M.H.

      AU - Jansen,J.F.A.

      AU - Overvliet,G.M.

      AU - van der Kruijs,S.J.M.

      AU - Ebus,S.C.M.

      AU - de Louw,A.J.A.

      AU - Hofman,P.A.M.

      AU - Aldenkamp,A.P.

      AU - Backes,W.H.

      PY - 2014

      Y1 - 2014

      N2 - INTRODUCTION: Rolandic epilepsy (RE) manifests during a critical phase of brain development, and has been associated with language impairments. Concordant abnormalities in structural and functional connectivity (SC and FC) have been described before. As SC and FC are under mutual influence, the current study investigates abnormalities in the SC-FC synergy in RE.METHODS: Twenty-two children with RE (age, mean ± SD: 11.3 ± 2.0 y) and 22 healthy controls (age 10.5 ± 1.6 y) underwent structural, diffusion weighted, and resting-state functional magnetic resonance imaging (MRI) at 3T. The probabilistic anatomical landmarks atlas was used to parcellate the (sub)cortical gray matter. Constrained spherical deconvolution tractography and correlation of time series were used to assess SC and FC, respectively. The SC-FC correlation was assessed as a function of age for the non-zero structural connections over a range of sparsity values (0.01-0.75). A modularity analysis was performed on the mean SC network of the controls to localize potential global effects to subnetworks. SC and FC were also assessed separately using graph analysis.RESULTS: The SC-FC correlation was significantly reduced in children with RE compared to healthy controls, especially for the youngest participants. This effect was most pronounced in a left and a right centro-temporal network, as well as in a medial parietal network. Graph analysis revealed no prominent abnormalities in SC or FC network organization.CONCLUSION: Since SC and FC converge during normal maturation, our finding of reduced SC-FC correlation illustrates impaired synergy between brain structure and function. More specifically, since this effect was most pronounced in the youngest participants, RE may represent a developmental disorder of delayed brain network maturation. The observed effects seem especially attributable to medial parietal connections, which forms an intermediate between bilateral centro-temporal modules of epileptiform activity, and bear relevance for language function.

      AB - INTRODUCTION: Rolandic epilepsy (RE) manifests during a critical phase of brain development, and has been associated with language impairments. Concordant abnormalities in structural and functional connectivity (SC and FC) have been described before. As SC and FC are under mutual influence, the current study investigates abnormalities in the SC-FC synergy in RE.METHODS: Twenty-two children with RE (age, mean ± SD: 11.3 ± 2.0 y) and 22 healthy controls (age 10.5 ± 1.6 y) underwent structural, diffusion weighted, and resting-state functional magnetic resonance imaging (MRI) at 3T. The probabilistic anatomical landmarks atlas was used to parcellate the (sub)cortical gray matter. Constrained spherical deconvolution tractography and correlation of time series were used to assess SC and FC, respectively. The SC-FC correlation was assessed as a function of age for the non-zero structural connections over a range of sparsity values (0.01-0.75). A modularity analysis was performed on the mean SC network of the controls to localize potential global effects to subnetworks. SC and FC were also assessed separately using graph analysis.RESULTS: The SC-FC correlation was significantly reduced in children with RE compared to healthy controls, especially for the youngest participants. This effect was most pronounced in a left and a right centro-temporal network, as well as in a medial parietal network. Graph analysis revealed no prominent abnormalities in SC or FC network organization.CONCLUSION: Since SC and FC converge during normal maturation, our finding of reduced SC-FC correlation illustrates impaired synergy between brain structure and function. More specifically, since this effect was most pronounced in the youngest participants, RE may represent a developmental disorder of delayed brain network maturation. The observed effects seem especially attributable to medial parietal connections, which forms an intermediate between bilateral centro-temporal modules of epileptiform activity, and bear relevance for language function.

      KW - Journal Article

      U2 - 10.3389/fnhum.2014.00704

      DO - 10.3389/fnhum.2014.00704

      M3 - Article

      VL - 8

      SP - 704

      JO - Frontiers in Human Neuroscience

      T2 - Frontiers in Human Neuroscience

      JF - Frontiers in Human Neuroscience

      SN - 1662-5161

      ER -