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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

Diagram of spatial distribution map technique/along tract analysis methodology using the cortical spinal tract. A) Comparison of spatial distribution of corticospinal tract (CST) after normalization to MNI space, between control and PVL groups. B) Example tract profile generation using the right CST for all controls. Valleys correspond to known regions of crossing fibers. C) Statistical comparison of bilateral tract profiles between control (blue) and PVL (red) groups. Along-tract statistics were performed using the Welch t-test and family-wise error was controlled for by permutation test.
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f0005: Diagram of spatial distribution map technique/along tract analysis methodology using the cortical spinal tract. A) Comparison of spatial distribution of corticospinal tract (CST) after normalization to MNI space, between control and PVL groups. B) Example tract profile generation using the right CST for all controls. Valleys correspond to known regions of crossing fibers. C) Statistical comparison of bilateral tract profiles between control (blue) and PVL (red) groups. Along-tract statistics were performed using the Welch t-test and family-wise error was controlled for by permutation test.

Mentions: In order to purely compare general tract distribution among the cohorts, right and left spatially normalized tracts were averaged on each population by flipping the left side tracts over the mid-sagittal plane and averaging with their contralateral counterparts. The spatial distribution maps were generated by overlaying each cohort's averaged bilateral tracts onto standard space and thresholding to only include voxels containing at least 10% of all subject tracts. Fig. 1A shows an example spatial distribution map comparing the corticospinal tract (CST) between controls and PVL groups. This map gives a visual representation of each tract's anatomical variability within each population using a standard space reference point.


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)

Diagram of spatial distribution map technique/along tract analysis methodology using the cortical spinal tract. A) Comparison of spatial distribution of corticospinal tract (CST) after normalization to MNI space, between control and PVL groups. B) Example tract profile generation using the right CST for all controls. Valleys correspond to known regions of crossing fibers. C) Statistical comparison of bilateral tract profiles between control (blue) and PVL (red) groups. Along-tract statistics were performed using the Welch t-test and family-wise error was controlled for by permutation test.
© Copyright Policy - CC BY-NC-ND
Related In: Results  -  Collection

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

f0005: Diagram of spatial distribution map technique/along tract analysis methodology using the cortical spinal tract. A) Comparison of spatial distribution of corticospinal tract (CST) after normalization to MNI space, between control and PVL groups. B) Example tract profile generation using the right CST for all controls. Valleys correspond to known regions of crossing fibers. C) Statistical comparison of bilateral tract profiles between control (blue) and PVL (red) groups. Along-tract statistics were performed using the Welch t-test and family-wise error was controlled for by permutation test.
Mentions: In order to purely compare general tract distribution among the cohorts, right and left spatially normalized tracts were averaged on each population by flipping the left side tracts over the mid-sagittal plane and averaging with their contralateral counterparts. The spatial distribution maps were generated by overlaying each cohort's averaged bilateral tracts onto standard space and thresholding to only include voxels containing at least 10% of all subject tracts. Fig. 1A shows an example spatial distribution map comparing the corticospinal tract (CST) between controls and PVL groups. This map gives a visual representation of each tract's anatomical variability within each population using a standard space reference point.

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