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

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.

Fig. 1

White matter language and reading network. White matter regions (red) on the FA-skeleton (green), overlaid on axial slices of mean FA image (grayscale), associated with at least one behavioral measure, p < .05, in the preterm group (n=23). Regions located on 15 tracts: corpus callosum (z=4–34), forceps major (z=4–16), forceps minor (z=7–22), bilateral anterior thalamic radiation (z=4–19), bilateral corticospinal tract (z=4–37), bilateral inferior fronto-occipital fasciculus (z=4–22), bilateral inferior longitudinal fasciculus (z=4–7), bilateral superior longitudinal fasciculus (z=16–37), and bilateral uncinate fasciculus (z= − 25 to − 7). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

A region of interest (left panel) on the right inferior fronto-occipital fasciculus (red circled in yellow) shown on sagittal (x=26), coronal (y=21), and axial (z=14) slices of FA-skeleton (green) overlaid on the mean FA image (grayscale). Though the FA of 14 tracts correlated with verbal IQ, the FA of this region was the only significant predictor in the regression model predicting verbal IQ, β=.66, p<.01, R²=.44, (top right panel); and though the FA of 15 tracts correlated with syntactic comprehension, the FA of this region was the only significant predictor in the regression model predicting syntactic comprehension, β=− .65, p<.01, R²=.42, (bottom right panel) in children born preterm. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 3

A region of interest (left panel) on the forceps minor (red circled in yellow) shown on sagittal (x=18), coronal (y=26), and axial (z=21) slices of FA-skeleton (green) overlaid on the mean FA image (grayscale). Though the FA of 13 tracts correlated with verbal memory, the FA of this region was the only significant predictor in the regression model predicting verbal memory, β=.61, p <.01, R²=.38, (top right panel); and though the FA of 12 tracts correlated with receptive vocabulary, the FA of this region was the only significant predictor in the regression model predicting receptive vocabulary, β= −.56, p < .01, R² =.31 (bottom right panel) in children born preterm. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 4

A region of interest (left panel) on the right anterior thalamic radiation (red circled in yellow) shown on sagittal (x=11), coronal (y = −5), and axial (z = − 7) slices of FA-skeleton (green) overlaid on the mean FA image (grayscale). Though the FA of 9 tracts correlated with linguistic processing speed, the FA of this region was the only significant predictor in the regression model predicting linguistic processing speed, β= − .53, p <.01, R²=.28 (right panel) in children born preterm. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 5

A region of interest (left panel) on the genu of the corpus callosum (red circled in yellow) shown on sagittal (x=17), coronal (y=26), and axial (z=20) slices of FA-skeleton (green) overlaid on the mean FA image (gray scale). Though the FA of 15 tracts correlated with decoding, the FA of this region was the only significant predictor in the regression model predicting decoding, β=.67, p<.001, R²=.45 (right panel) in children born preterm. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 6

A region of interest (left panel) on the left uncinate fasciculus (red circled in yellow) shown on sagittal (x = −36), coronal (y = −6), and axial (z= −21) slices of FA-skeleton (green) overlaid on the mean FA image (grayscale). Though the FA of 9 tracts correlated with reading comprehension, the FA of this region was the only significant predictor in the regression model predicting reading comprehension, β=.52, p < .05, R²=.27 (right panel) in children born preterm. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)