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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

Spatial distribution of inferior fronto-occipital fasciculus (IFOF). Comparison of spatial distribution of the IFOF after normalization to MNI space, between control and PVL groups. At each voxel, the color map indicates the proportion of subjects in each cohort that had the IFOF pass through it.
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figS1: Spatial distribution of inferior fronto-occipital fasciculus (IFOF). Comparison of spatial distribution of the IFOF after normalization to MNI space, between control and PVL groups. At each voxel, the color map indicates the proportion of subjects in each cohort that had the IFOF pass through it.

Mentions: In the controls, there were three distinct segments of the IFOF identified within the fractional anisotropy tract profile (Fig. 3) which corresponded to the trajectory of the fiber tract extending from the occipital/temporal lobe (Segment 1), coursing through the external capsule (Segment 2), towards the inferior frontal lobe (Segmental 3). The highest peak of FA values was in in the occipital–temporal segmental and the lowest peak of FA values was in the external capsule segment. There was a small distinct peak in FA values in the region where the uncinate fasiculus joins with the IFOF and a relatively higher peak adjacent to the areas of the cross fibers within inferior frontal lobes. When comparing this FA tract profiles to the preterm PVL cases, the greatest reduction in FA occurred in Segment 1 and Segment 2, with a greater reduction noted within the occipital portion of the tract. The right and left IFOF did show similar distribution of both normal FA variance along the tract in the controls and the pattern of regional FA reduction in the preterm PVL cases, demonstrating no evidence of lateralization. The probabilistic spatial distribution maps did confirm both the anatomic and pathological regional variations (described above) of the IFOF in both the controls and preterm PVL cases (Supplementary Fig. 1).


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)

Spatial distribution of inferior fronto-occipital fasciculus (IFOF). Comparison of spatial distribution of the IFOF after normalization to MNI space, between control and PVL groups. At each voxel, the color map indicates the proportion of subjects in each cohort that had the IFOF pass through it.
© Copyright Policy - CC BY-NC-ND
Related In: Results  -  Collection

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

figS1: Spatial distribution of inferior fronto-occipital fasciculus (IFOF). Comparison of spatial distribution of the IFOF after normalization to MNI space, between control and PVL groups. At each voxel, the color map indicates the proportion of subjects in each cohort that had the IFOF pass through it.
Mentions: In the controls, there were three distinct segments of the IFOF identified within the fractional anisotropy tract profile (Fig. 3) which corresponded to the trajectory of the fiber tract extending from the occipital/temporal lobe (Segment 1), coursing through the external capsule (Segment 2), towards the inferior frontal lobe (Segmental 3). The highest peak of FA values was in in the occipital–temporal segmental and the lowest peak of FA values was in the external capsule segment. There was a small distinct peak in FA values in the region where the uncinate fasiculus joins with the IFOF and a relatively higher peak adjacent to the areas of the cross fibers within inferior frontal lobes. When comparing this FA tract profiles to the preterm PVL cases, the greatest reduction in FA occurred in Segment 1 and Segment 2, with a greater reduction noted within the occipital portion of the tract. The right and left IFOF did show similar distribution of both normal FA variance along the tract in the controls and the pattern of regional FA reduction in the preterm PVL cases, demonstrating no evidence of lateralization. The probabilistic spatial distribution maps did confirm both the anatomic and pathological regional variations (described above) of the IFOF in both the controls and preterm PVL cases (Supplementary Fig. 1).

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