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Regional vulnerability of longitudinal cortical association connectivity: Associated with structural network topology alterations in preterm children with cerebral palsy.

Ceschin R, Lee VK, Schmithorst V, Panigrahy A - Neuroimage Clin (2015)

Bottom Line: Despite mean tract analysis, Tract-Based Spatial Statistics (TBSS) and voxel-based morphometry (VBM) demonstrating diffusely reduced fractional anisotropy (FA) reduction in all white matter tracts, the along-tract analysis improved the detection of regional tract vulnerability.The along-tract map-structural network topology correlates revealed two associations: (1) reduced regional posterior-anterior gradient in FA of the longitudinal visual cortical association tracts (inferior fronto-occipital fasciculus, inferior longitudinal fasciculus, optic radiation, posterior thalamic radiation) correlated with reduced posterior-anterior gradient of intra-regional (nodal efficiency) metrics with relative sparing of frontal and temporal regions; and (2) reduced regional FA within frontal-thalamic-striatal white matter pathways (anterior limb/anterior thalamic radiation, superior longitudinal fasciculus and cortical spinal tract) correlated with alteration in eigenvector centrality, clustering coefficient (inter-regional) and participation co-efficient (inter-modular) alterations of frontal-striatal and fronto-limbic nodes suggesting re-organization of these pathways.Both along tract and structural topology network measurements correlated strongly with motor and visual clinical outcome scores.

View Article: PubMed Central - PubMed

Affiliation: Department of Pediatric Radiology, Children's Hospital of Pittsburgh of UPMC, Pittsburgh, PA, USA ; Department of Biomedical Informatics, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

ABSTRACT
Preterm born children with spastic diplegia type of cerebral palsy and white matter injury or periventricular leukomalacia (PVL), are known to have motor, visual and cognitive impairments. Most diffusion tensor imaging (DTI) studies performed in this group have demonstrated widespread abnormalities using averaged deterministic tractography and voxel-based DTI measurements. Little is known about structural network correlates of white matter topography and reorganization in preterm cerebral palsy, despite the availability of new therapies and the need for brain imaging biomarkers. Here, we combined novel post-processing methodology of probabilistic tractography data in this preterm cohort to improve spatial and regional delineation of longitudinal cortical association tract abnormalities using an along-tract approach, and compared these data to structural DTI cortical network topology analysis. DTI images were acquired on 16 preterm children with cerebral palsy (mean age 5.6 ± 4) and 75 healthy controls (mean age 5.7 ± 3.4). Despite mean tract analysis, Tract-Based Spatial Statistics (TBSS) and voxel-based morphometry (VBM) demonstrating diffusely reduced fractional anisotropy (FA) reduction in all white matter tracts, the along-tract analysis improved the detection of regional tract vulnerability. The along-tract map-structural network topology correlates revealed two associations: (1) reduced regional posterior-anterior gradient in FA of the longitudinal visual cortical association tracts (inferior fronto-occipital fasciculus, inferior longitudinal fasciculus, optic radiation, posterior thalamic radiation) correlated with reduced posterior-anterior gradient of intra-regional (nodal efficiency) metrics with relative sparing of frontal and temporal regions; and (2) reduced regional FA within frontal-thalamic-striatal white matter pathways (anterior limb/anterior thalamic radiation, superior longitudinal fasciculus and cortical spinal tract) correlated with alteration in eigenvector centrality, clustering coefficient (inter-regional) and participation co-efficient (inter-modular) alterations of frontal-striatal and fronto-limbic nodes suggesting re-organization of these pathways. Both along tract and structural topology network measurements correlated strongly with motor and visual clinical outcome scores. This study shows the value of combining along-tract analysis and structural network topology in depicting not only selective parietal occipital regional vulnerability but also reorganization of frontal-striatal and frontal-limbic pathways in preterm children with cerebral palsy. These finding also support the concept that widespread, but selective posterior-anterior neural network connectivity alterations in preterm children with cerebral palsy likely contribute to the pathogenesis of neurosensory and cognitive impairment in this group.

No MeSH data available.


Related in: MedlinePlus

Small-world architecture. Visualization of the small-world architecture using a circle diagram demonstrated a tendency towards less short-range connections (i.e., smaller “arcs”, suggesting localized processing) in the frontal, temporal and subcortical regions as well as differences in the number and spatial localization of long-range connections in the frontal, temporal and subcortical regions (i.e., with long-range connections appearing more numerous and clustered in the preterm cerebral palsy cohort rather than uniformly distributed as in the term control cohort) in the frontal, temporal and subcortical regional compared to the parietal–occipital region.
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f0050: Small-world architecture. Visualization of the small-world architecture using a circle diagram demonstrated a tendency towards less short-range connections (i.e., smaller “arcs”, suggesting localized processing) in the frontal, temporal and subcortical regions as well as differences in the number and spatial localization of long-range connections in the frontal, temporal and subcortical regions (i.e., with long-range connections appearing more numerous and clustered in the preterm cerebral palsy cohort rather than uniformly distributed as in the term control cohort) in the frontal, temporal and subcortical regional compared to the parietal–occipital region.

Mentions: To better understand the basis of these topological differences, we visualized the network topology of the preterm cerebral palsy group and the controls with regard to community structure (Fig. 9) and then to small-world architecture (Fig. 10). Utilizing the spring-loaded technique, which maps the nodes of a network in accordance with their connection strength rather than anatomical proximity, Fig. 9 demonstrated that, in the preterm cerebral palsy cohort, the global network topology was clustered into four separate modules or subnetworks similar to the term controls (right/left interhemispheric and anterior/posterior medial interhemispheric). We noted that while the overall number of modules was similar between preterm and term cohort, there were alterations in the anterior aspect of bilateral intrahemispheric modules relative to clusters of frontal, temporal and subcortical (striatal) nodes with regard to the spatial distribution of the intrahemispheric modules related to the medial interhemispheric regions.


Regional vulnerability of longitudinal cortical association connectivity: Associated with structural network topology alterations in preterm children with cerebral palsy.

Ceschin R, Lee VK, Schmithorst V, Panigrahy A - Neuroimage Clin (2015)

Small-world architecture. Visualization of the small-world architecture using a circle diagram demonstrated a tendency towards less short-range connections (i.e., smaller “arcs”, suggesting localized processing) in the frontal, temporal and subcortical regions as well as differences in the number and spatial localization of long-range connections in the frontal, temporal and subcortical regions (i.e., with long-range connections appearing more numerous and clustered in the preterm cerebral palsy cohort rather than uniformly distributed as in the term control cohort) in the frontal, temporal and subcortical regional compared to the parietal–occipital region.
© Copyright Policy - CC BY-NC-ND
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4588423&req=5

f0050: Small-world architecture. Visualization of the small-world architecture using a circle diagram demonstrated a tendency towards less short-range connections (i.e., smaller “arcs”, suggesting localized processing) in the frontal, temporal and subcortical regions as well as differences in the number and spatial localization of long-range connections in the frontal, temporal and subcortical regions (i.e., with long-range connections appearing more numerous and clustered in the preterm cerebral palsy cohort rather than uniformly distributed as in the term control cohort) in the frontal, temporal and subcortical regional compared to the parietal–occipital region.
Mentions: To better understand the basis of these topological differences, we visualized the network topology of the preterm cerebral palsy group and the controls with regard to community structure (Fig. 9) and then to small-world architecture (Fig. 10). Utilizing the spring-loaded technique, which maps the nodes of a network in accordance with their connection strength rather than anatomical proximity, Fig. 9 demonstrated that, in the preterm cerebral palsy cohort, the global network topology was clustered into four separate modules or subnetworks similar to the term controls (right/left interhemispheric and anterior/posterior medial interhemispheric). We noted that while the overall number of modules was similar between preterm and term cohort, there were alterations in the anterior aspect of bilateral intrahemispheric modules relative to clusters of frontal, temporal and subcortical (striatal) nodes with regard to the spatial distribution of the intrahemispheric modules related to the medial interhemispheric regions.

Bottom Line: Despite mean tract analysis, Tract-Based Spatial Statistics (TBSS) and voxel-based morphometry (VBM) demonstrating diffusely reduced fractional anisotropy (FA) reduction in all white matter tracts, the along-tract analysis improved the detection of regional tract vulnerability.The along-tract map-structural network topology correlates revealed two associations: (1) reduced regional posterior-anterior gradient in FA of the longitudinal visual cortical association tracts (inferior fronto-occipital fasciculus, inferior longitudinal fasciculus, optic radiation, posterior thalamic radiation) correlated with reduced posterior-anterior gradient of intra-regional (nodal efficiency) metrics with relative sparing of frontal and temporal regions; and (2) reduced regional FA within frontal-thalamic-striatal white matter pathways (anterior limb/anterior thalamic radiation, superior longitudinal fasciculus and cortical spinal tract) correlated with alteration in eigenvector centrality, clustering coefficient (inter-regional) and participation co-efficient (inter-modular) alterations of frontal-striatal and fronto-limbic nodes suggesting re-organization of these pathways.Both along tract and structural topology network measurements correlated strongly with motor and visual clinical outcome scores.

View Article: PubMed Central - PubMed

Affiliation: Department of Pediatric Radiology, Children's Hospital of Pittsburgh of UPMC, Pittsburgh, PA, USA ; Department of Biomedical Informatics, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

ABSTRACT
Preterm born children with spastic diplegia type of cerebral palsy and white matter injury or periventricular leukomalacia (PVL), are known to have motor, visual and cognitive impairments. Most diffusion tensor imaging (DTI) studies performed in this group have demonstrated widespread abnormalities using averaged deterministic tractography and voxel-based DTI measurements. Little is known about structural network correlates of white matter topography and reorganization in preterm cerebral palsy, despite the availability of new therapies and the need for brain imaging biomarkers. Here, we combined novel post-processing methodology of probabilistic tractography data in this preterm cohort to improve spatial and regional delineation of longitudinal cortical association tract abnormalities using an along-tract approach, and compared these data to structural DTI cortical network topology analysis. DTI images were acquired on 16 preterm children with cerebral palsy (mean age 5.6 ± 4) and 75 healthy controls (mean age 5.7 ± 3.4). Despite mean tract analysis, Tract-Based Spatial Statistics (TBSS) and voxel-based morphometry (VBM) demonstrating diffusely reduced fractional anisotropy (FA) reduction in all white matter tracts, the along-tract analysis improved the detection of regional tract vulnerability. The along-tract map-structural network topology correlates revealed two associations: (1) reduced regional posterior-anterior gradient in FA of the longitudinal visual cortical association tracts (inferior fronto-occipital fasciculus, inferior longitudinal fasciculus, optic radiation, posterior thalamic radiation) correlated with reduced posterior-anterior gradient of intra-regional (nodal efficiency) metrics with relative sparing of frontal and temporal regions; and (2) reduced regional FA within frontal-thalamic-striatal white matter pathways (anterior limb/anterior thalamic radiation, superior longitudinal fasciculus and cortical spinal tract) correlated with alteration in eigenvector centrality, clustering coefficient (inter-regional) and participation co-efficient (inter-modular) alterations of frontal-striatal and fronto-limbic nodes suggesting re-organization of these pathways. Both along tract and structural topology network measurements correlated strongly with motor and visual clinical outcome scores. This study shows the value of combining along-tract analysis and structural network topology in depicting not only selective parietal occipital regional vulnerability but also reorganization of frontal-striatal and frontal-limbic pathways in preterm children with cerebral palsy. These finding also support the concept that widespread, but selective posterior-anterior neural network connectivity alterations in preterm children with cerebral palsy likely contribute to the pathogenesis of neurosensory and cognitive impairment in this group.

No MeSH data available.


Related in: MedlinePlus