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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

Microstructural abnormalities determined by template based VBM (A) and TBSS (B). Compared to the controls, the preterm children with PVL were found to have significantly reduced fractional anisotropy (FA) in large sectors of the central and posterior white matter, bilaterally, extending into the midbrain and brainstem. This included key regions within the visual system (i.e., posterior temporal–occipital white matter in region of the optic radiations, the inferior frontal–occipital fasciculus (IFOF), inferior longitudinal fasciculus, and the splenium of the corpus callosum), the limbic system (i.e., cingulum, fimbria, fornix) and the motor system (i.e., corona radiata, body of the corpus callosum, posterior limb of the internal capsule, crus pedunculi, middle cerebellar peduncles, and inferior cerebellar peduncles). Significant reductions in FA were also seen in frontal regions (either the deep white matter of the frontal lobe or in the region of the crossing of those fibers — the genu of the corpus callosum). When examining the regions of that contained longitudinal visual association fibers tract, including the ILF, IFOF and the SLF, there was no clear regional FA abnormality noted that was comparable to the along tract and spatial distribution analysis.
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f0010: Microstructural abnormalities determined by template based VBM (A) and TBSS (B). Compared to the controls, the preterm children with PVL were found to have significantly reduced fractional anisotropy (FA) in large sectors of the central and posterior white matter, bilaterally, extending into the midbrain and brainstem. This included key regions within the visual system (i.e., posterior temporal–occipital white matter in region of the optic radiations, the inferior frontal–occipital fasciculus (IFOF), inferior longitudinal fasciculus, and the splenium of the corpus callosum), the limbic system (i.e., cingulum, fimbria, fornix) and the motor system (i.e., corona radiata, body of the corpus callosum, posterior limb of the internal capsule, crus pedunculi, middle cerebellar peduncles, and inferior cerebellar peduncles). Significant reductions in FA were also seen in frontal regions (either the deep white matter of the frontal lobe or in the region of the crossing of those fibers — the genu of the corpus callosum). When examining the regions of that contained longitudinal visual association fibers tract, including the ILF, IFOF and the SLF, there was no clear regional FA abnormality noted that was comparable to the along tract and spatial distribution analysis.

Mentions: The VBM maps of the preterm children with PVL were concordant with the TBSS results, showing diffuse decreased diffusivity in white matter throughout (Fig. 1). Compared to the controls, the preterm children with PVL were found to have significantly reduced fractional anisotropy (FA) in large sectors of the central and posterior white matter, bilaterally, extending into the midbrain and brainstem (Fig. 2). This included key regions within the visual system (i.e., posterior temporal–occipital white matter in region of the optic radiations, the inferior frontal–occipital fasciculus (IFOF), inferior longitudinal fasciculus, and the splenium of the corpus callosum), the limbic system (i.e., cingulum, fimbria, fornix) and the motor system (i.e., corona radiata, body of the corpus callosum, posterior limb of the internal capsule, crus pedunculi, middle cerebellar peduncles, and inferior cerebellar peduncles). Significant reductions in FA were also seen in frontal regions (either the deep white matter of the frontal lobe or in the region of the crossing of those fibers — the genu of the corpus callosum). However, when examining the regions that contained longitudinal visual association fibers, including the ILF, IFOF and the SLF, there was no clear regional FA abnormality noted.


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)

Microstructural abnormalities determined by template based VBM (A) and TBSS (B). Compared to the controls, the preterm children with PVL were found to have significantly reduced fractional anisotropy (FA) in large sectors of the central and posterior white matter, bilaterally, extending into the midbrain and brainstem. This included key regions within the visual system (i.e., posterior temporal–occipital white matter in region of the optic radiations, the inferior frontal–occipital fasciculus (IFOF), inferior longitudinal fasciculus, and the splenium of the corpus callosum), the limbic system (i.e., cingulum, fimbria, fornix) and the motor system (i.e., corona radiata, body of the corpus callosum, posterior limb of the internal capsule, crus pedunculi, middle cerebellar peduncles, and inferior cerebellar peduncles). Significant reductions in FA were also seen in frontal regions (either the deep white matter of the frontal lobe or in the region of the crossing of those fibers — the genu of the corpus callosum). When examining the regions of that contained longitudinal visual association fibers tract, including the ILF, IFOF and the SLF, there was no clear regional FA abnormality noted that was comparable to the along tract and spatial distribution analysis.
© Copyright Policy - CC BY-NC-ND
Related In: Results  -  Collection

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

f0010: Microstructural abnormalities determined by template based VBM (A) and TBSS (B). Compared to the controls, the preterm children with PVL were found to have significantly reduced fractional anisotropy (FA) in large sectors of the central and posterior white matter, bilaterally, extending into the midbrain and brainstem. This included key regions within the visual system (i.e., posterior temporal–occipital white matter in region of the optic radiations, the inferior frontal–occipital fasciculus (IFOF), inferior longitudinal fasciculus, and the splenium of the corpus callosum), the limbic system (i.e., cingulum, fimbria, fornix) and the motor system (i.e., corona radiata, body of the corpus callosum, posterior limb of the internal capsule, crus pedunculi, middle cerebellar peduncles, and inferior cerebellar peduncles). Significant reductions in FA were also seen in frontal regions (either the deep white matter of the frontal lobe or in the region of the crossing of those fibers — the genu of the corpus callosum). When examining the regions of that contained longitudinal visual association fibers tract, including the ILF, IFOF and the SLF, there was no clear regional FA abnormality noted that was comparable to the along tract and spatial distribution analysis.
Mentions: The VBM maps of the preterm children with PVL were concordant with the TBSS results, showing diffuse decreased diffusivity in white matter throughout (Fig. 1). Compared to the controls, the preterm children with PVL were found to have significantly reduced fractional anisotropy (FA) in large sectors of the central and posterior white matter, bilaterally, extending into the midbrain and brainstem (Fig. 2). This included key regions within the visual system (i.e., posterior temporal–occipital white matter in region of the optic radiations, the inferior frontal–occipital fasciculus (IFOF), inferior longitudinal fasciculus, and the splenium of the corpus callosum), the limbic system (i.e., cingulum, fimbria, fornix) and the motor system (i.e., corona radiata, body of the corpus callosum, posterior limb of the internal capsule, crus pedunculi, middle cerebellar peduncles, and inferior cerebellar peduncles). Significant reductions in FA were also seen in frontal regions (either the deep white matter of the frontal lobe or in the region of the crossing of those fibers — the genu of the corpus callosum). However, when examining the regions that contained longitudinal visual association fibers, including the ILF, IFOF and the SLF, there was no clear regional FA abnormality noted.

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