Elsevier

Neuropsychologia

Volume 50, Issue 14, December 2012, Pages 3348-3362
Neuropsychologia

Language and reading skills in school-aged children and adolescents born preterm are associated with white matter properties on diffusion tensor imaging

https://doi.org/10.1016/j.neuropsychologia.2012.10.014Get rights and content

Abstract

Children born preterm are at risk for deficits in language and reading. They are also at risk for injury to the white matter of the brain. The goal of this study was to determine whether performance in language and reading skills would be associated with white matter properties in children born preterm and full-term. Children born before 36 weeks gestation (n=23, mean±SD age 12.5±2.0 years, gestational age 28.7±2.5 weeks, birth weight 1184±431 g) and controls born after 37 weeks gestation (n=19, 13.1±2.1 years, 39.3±1.0 weeks, 3178±413 g) underwent a battery of language and reading tests. Diffusion Tensor Imaging (DTI) scans were processed using Tract-Based Spatial Statistics to generate a core white matter skeleton that was anatomically comparable across participants. Fractional anisotropy (FA) was the diffusion property used in analyses. In the full-term group, no regions of the whole FA-skeleton were associated with language and reading. In the preterm group, regions of the FA-skeleton were significantly associated with verbal IQ, linguistic processing speed, syntactic comprehension, and decoding. Combined, the regions formed a composite map of 22 clusters on 15 tracts in both hemispheres and in the ventral and dorsal streams. ROI analyses in the preterm group found that several of these regions also showed positive associations with receptive vocabulary, verbal memory, and reading comprehension. Some of the same regions showed weak negative correlations within the full-term group. Exploratory multiple regression in the preterm group found that specific white matter pathways were related to different aspects of language processing and reading, accounting for 27–44% of the variance. The findings suggest that higher performance in language and reading in a group of preterm but not full-term children is associated with higher fractional anisotropy of a bilateral and distributed white matter network.

Highlights

► Language and reading measures are associated with white matter properties in children born preterm. ► The white matter network for language and reading was bilateral and widely distributed. ► Decoding skills were most strongly associated with fractional anisotropy in the corpus callosum. ► Verbal IQ and syntactic comprehension were most strongly associated with a right ventral pathway.

Section snippets

Background

Approximately 13% of the children in the United States are born prematurely (Allen, 2008), and these children are at elevated risk of neurodevelopmental disability (Fletcher et al., 1997, Hack, 2006, Msall and Tremont, 2002, Ornstein et al., 1991, Rose and Feldman, 1996, Rose et al., 2009, Strang-Karlsson et al., 2010). Among those born before 32 weeks gestation or weighing less than 1500 g, major disabilities, including cerebral palsy, sensory impairments, and/or intellectual disability affect

Participants

Participants were 9–16 years old and enrolled in the Palo Alto CA site of a larger multi-site study of prematurity outcomes (N=100) (Lee et al., 2011b, Loe et al., 2011, Loe et al., 2012). This study reports on participants who underwent MRI scanning at Stanford University. The Stanford University institutional review board approved this study. A parent provided informed consent; participants provided assent.

Preterm subjects were born at<36 weeks gestation with birth weight<2500 g. Controls were

Behavioral results and overall DTI results

There were no statistically significant group differences in the language and reading scores in this sample of children by independent t-tests (Table 1).

Associations between the FA-skeleton and language and reading scores

In the preterm group only, voxelwise analysis of the entire FA-skeleton with scores from language and reading tasks showed positive associations with FA for four measures: verbal IQ, linguistic processing speed, syntactic comprehension, and decoding. The regions of significant positive correlation for the different measures overlapped. There

Summary of results

Four language and reading measures—verbal IQ, linguistic processing speed, syntactic comprehension, and decoding—were associated with areas of the FA-skeleton in the preterm group in the voxelwise analysis. Contrary to the hypotheses, we found that language and reading measures were not associated with FA in the full-term group in the voxelwise analysis. A bilateral and widely distributed network of tracts was associated with the measures in the preterm group. The network included 22 clusters

Acknowledgements

This work was supported by a grant from the National Institutes of Health, Eunice Kennedy Shriver National Institute of Child Health and Human Development, RO1 HD046500 to Heidi M. Feldman; and by the Clinical and Translational Science Award 1UL1 RR025744 for the Stanford Center for Clinical and Translational Education and Research (Spectrum) from the National Center for Research Resources, National Institutes of Health. We thank the children and families who participated in our study. We thank

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