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Altered Structural and Functional Connectivity in Late Preterm Preadolescence: An Anatomic Seed-Based Study of Resting State Networks Related to the Posteromedial and Lateral Parietal Cortex.

Degnan AJ, Wisnowski JL, Choi S, Ceschin R, Bhushan C, Leahy RM, Corby P, Schmithorst VJ, Panigrahy A - PLoS ONE (2015)

Bottom Line: Late preterm preadolescence is associated with altered functional connectivity from the PMC and lateral parietal cortex to known distributed functional cortical networks despite no significant executive neurocognitive differences.Selective increased structural connectivity was observed in the setting of decreased posterior interhemispheric connections.Future work is needed to determine if these findings represent a compensatory adaptation employing alternate neural circuitry or could reflect subtle pathology resulting in emotional processing deficits not seen with neurocognitive testing.

View Article: PubMed Central - PubMed

Affiliation: Department of Pediatric Radiology, Children's Hospital of Pittsburgh of UPMC, 4401 Penn Avenue, Floor 2, Pittsburgh, PA, 15224, United States of America; Department of Radiology, University of Pittsburgh Medical Center (UPMC), 3950 Presby South Tower, 200 Lothrop Street, Pittsburgh, PA 15213, United States of America.

ABSTRACT

Objective: Late preterm birth confers increased risk of developmental delay, academic difficulties and social deficits. The late third trimester may represent a critical period of development of neural networks including the default mode network (DMN), which is essential to normal cognition. Our objective is to identify functional and structural connectivity differences in the posteromedial cortex related to late preterm birth.

Methods: Thirty-eight preadolescents (ages 9-13; 19 born in the late preterm period (≥32 weeks gestational age) and 19 at term) without access to advanced neonatal care were recruited from a low socioeconomic status community in Brazil. Participants underwent neurocognitive testing, 3-dimensional T1-weighted imaging, diffusion-weighted imaging and resting state functional MRI (RS-fMRI). Seed-based probabilistic diffusion tractography and RS-fMRI analyses were performed using unilateral seeds within the posterior DMN (posterior cingulate cortex, precuneus) and lateral parietal DMN (superior marginal and angular gyri).

Results: Late preterm children demonstrated increased functional connectivity within the posterior default mode networks and increased anti-correlation with the central-executive network when seeded from the posteromedial cortex (PMC). Key differences were demonstrated between PMC components with increased anti-correlation with the salience network seen only with posterior cingulate cortex seeding but not with precuneus seeding. Probabilistic tractography showed increased streamlines within the right inferior longitudinal fasciculus and inferior fronto-occipital fasciculus within late preterm children while decreased intrahemispheric streamlines were also observed. No significant differences in neurocognitive testing were demonstrated between groups.

Conclusion: Late preterm preadolescence is associated with altered functional connectivity from the PMC and lateral parietal cortex to known distributed functional cortical networks despite no significant executive neurocognitive differences. Selective increased structural connectivity was observed in the setting of decreased posterior interhemispheric connections. Future work is needed to determine if these findings represent a compensatory adaptation employing alternate neural circuitry or could reflect subtle pathology resulting in emotional processing deficits not seen with neurocognitive testing.

No MeSH data available.


Related in: MedlinePlus

Summary of Tractography Methods.Probabilistic tractography comparison between groups was performed as summarized above [33, 87, 88].
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pone.0130686.g001: Summary of Tractography Methods.Probabilistic tractography comparison between groups was performed as summarized above [33, 87, 88].

Mentions: Between-group probabilistic tractography analysis was carried out in a similar manner as a previously published method [31]. Diffusion tensors were estimated from diffusion scans after distortion correction and co-registration with segmented 3D-T1-weighted images using BrainSuite (http://brainsuite.usc.edu) including the SVReg atlas [32–34]. Seed regions were generated from anatomical labels for individual subjects and manually edited for each study to ensure precise correspondence with anatomical landmarks on a participant-specific basis. The posterior DMN seeds included the posterior cingulate and precuneus, both collectively and separately. Lateral inferior parietal cortex was also used as a seed related to the posterior DMN. These regions of interest were then applied as seed points for probabilistic tractography analysis using FSL ProbTrackx (FDT Toolbox, version 2.0; http://fsl.fmrib.ox.ac.uk/fsl/fsl-4.1.9/fdt/fdt_probtrackx.html). This process is depicted graphically in Fig 1. Following seed placement, streamlines representing tracts to and from these regions were reconstructed. 1000 streamlines were initiated from each seed voxel; the stopping criterion was a curvature threshold of 80 degrees. The number of streamlines through each voxel was divided by the total number of streamlines. These maps were spatially normalized into MNI space using routines in SPM8 (Wellcome Institute of Cognitive Neurology, London, UK). A white matter map was segmented from an anatomical T1-weighted image and then spatially normalized into MNI space using a pediatric white matter template; the same transformation was then used for the streamline maps. A GLM was used with preterm status the variable of interest; and sex and age as covariates of no interest. A clustered wild bootstrap (5000 repetitions, Rademacher distribution) was used [35] in order to appropriately handle the different sources of variance (e.g. within-family, between-family). For each bootstrap replication, the residual multipliers were kept the same for each voxel in order to accurately account for the effects of spatial autocorrelation. T-scores were determined as the mean over the bootstrap repetitions divided by the standard deviation. T-scores were then converted into Z-scores. A Monte-Carlo simulation [36] which estimates intrinsic spatial autocorrelation via “noise” maps obtained from the fit residuals was used to determine family-wise-error (FWE) statistical significance. FWE corrected p < 0.05 was determined to be at Z > 2.75, spatial filtering at σ = 3 mm, spatial extent threshold at 200 voxels (= 1600 mm3).


Altered Structural and Functional Connectivity in Late Preterm Preadolescence: An Anatomic Seed-Based Study of Resting State Networks Related to the Posteromedial and Lateral Parietal Cortex.

Degnan AJ, Wisnowski JL, Choi S, Ceschin R, Bhushan C, Leahy RM, Corby P, Schmithorst VJ, Panigrahy A - PLoS ONE (2015)

Summary of Tractography Methods.Probabilistic tractography comparison between groups was performed as summarized above [33, 87, 88].
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4476681&req=5

pone.0130686.g001: Summary of Tractography Methods.Probabilistic tractography comparison between groups was performed as summarized above [33, 87, 88].
Mentions: Between-group probabilistic tractography analysis was carried out in a similar manner as a previously published method [31]. Diffusion tensors were estimated from diffusion scans after distortion correction and co-registration with segmented 3D-T1-weighted images using BrainSuite (http://brainsuite.usc.edu) including the SVReg atlas [32–34]. Seed regions were generated from anatomical labels for individual subjects and manually edited for each study to ensure precise correspondence with anatomical landmarks on a participant-specific basis. The posterior DMN seeds included the posterior cingulate and precuneus, both collectively and separately. Lateral inferior parietal cortex was also used as a seed related to the posterior DMN. These regions of interest were then applied as seed points for probabilistic tractography analysis using FSL ProbTrackx (FDT Toolbox, version 2.0; http://fsl.fmrib.ox.ac.uk/fsl/fsl-4.1.9/fdt/fdt_probtrackx.html). This process is depicted graphically in Fig 1. Following seed placement, streamlines representing tracts to and from these regions were reconstructed. 1000 streamlines were initiated from each seed voxel; the stopping criterion was a curvature threshold of 80 degrees. The number of streamlines through each voxel was divided by the total number of streamlines. These maps were spatially normalized into MNI space using routines in SPM8 (Wellcome Institute of Cognitive Neurology, London, UK). A white matter map was segmented from an anatomical T1-weighted image and then spatially normalized into MNI space using a pediatric white matter template; the same transformation was then used for the streamline maps. A GLM was used with preterm status the variable of interest; and sex and age as covariates of no interest. A clustered wild bootstrap (5000 repetitions, Rademacher distribution) was used [35] in order to appropriately handle the different sources of variance (e.g. within-family, between-family). For each bootstrap replication, the residual multipliers were kept the same for each voxel in order to accurately account for the effects of spatial autocorrelation. T-scores were determined as the mean over the bootstrap repetitions divided by the standard deviation. T-scores were then converted into Z-scores. A Monte-Carlo simulation [36] which estimates intrinsic spatial autocorrelation via “noise” maps obtained from the fit residuals was used to determine family-wise-error (FWE) statistical significance. FWE corrected p < 0.05 was determined to be at Z > 2.75, spatial filtering at σ = 3 mm, spatial extent threshold at 200 voxels (= 1600 mm3).

Bottom Line: Late preterm preadolescence is associated with altered functional connectivity from the PMC and lateral parietal cortex to known distributed functional cortical networks despite no significant executive neurocognitive differences.Selective increased structural connectivity was observed in the setting of decreased posterior interhemispheric connections.Future work is needed to determine if these findings represent a compensatory adaptation employing alternate neural circuitry or could reflect subtle pathology resulting in emotional processing deficits not seen with neurocognitive testing.

View Article: PubMed Central - PubMed

Affiliation: Department of Pediatric Radiology, Children's Hospital of Pittsburgh of UPMC, 4401 Penn Avenue, Floor 2, Pittsburgh, PA, 15224, United States of America; Department of Radiology, University of Pittsburgh Medical Center (UPMC), 3950 Presby South Tower, 200 Lothrop Street, Pittsburgh, PA 15213, United States of America.

ABSTRACT

Objective: Late preterm birth confers increased risk of developmental delay, academic difficulties and social deficits. The late third trimester may represent a critical period of development of neural networks including the default mode network (DMN), which is essential to normal cognition. Our objective is to identify functional and structural connectivity differences in the posteromedial cortex related to late preterm birth.

Methods: Thirty-eight preadolescents (ages 9-13; 19 born in the late preterm period (≥32 weeks gestational age) and 19 at term) without access to advanced neonatal care were recruited from a low socioeconomic status community in Brazil. Participants underwent neurocognitive testing, 3-dimensional T1-weighted imaging, diffusion-weighted imaging and resting state functional MRI (RS-fMRI). Seed-based probabilistic diffusion tractography and RS-fMRI analyses were performed using unilateral seeds within the posterior DMN (posterior cingulate cortex, precuneus) and lateral parietal DMN (superior marginal and angular gyri).

Results: Late preterm children demonstrated increased functional connectivity within the posterior default mode networks and increased anti-correlation with the central-executive network when seeded from the posteromedial cortex (PMC). Key differences were demonstrated between PMC components with increased anti-correlation with the salience network seen only with posterior cingulate cortex seeding but not with precuneus seeding. Probabilistic tractography showed increased streamlines within the right inferior longitudinal fasciculus and inferior fronto-occipital fasciculus within late preterm children while decreased intrahemispheric streamlines were also observed. No significant differences in neurocognitive testing were demonstrated between groups.

Conclusion: Late preterm preadolescence is associated with altered functional connectivity from the PMC and lateral parietal cortex to known distributed functional cortical networks despite no significant executive neurocognitive differences. Selective increased structural connectivity was observed in the setting of decreased posterior interhemispheric connections. Future work is needed to determine if these findings represent a compensatory adaptation employing alternate neural circuitry or could reflect subtle pathology resulting in emotional processing deficits not seen with neurocognitive testing.

No MeSH data available.


Related in: MedlinePlus