White matter development and early cognition in babies and toddlers

Abstract

The normal myelination of neuronal axons is essential to neurodevelopment, allowing fast inter-neuronal communication. The most dynamic period of myelination occurs in the first few years of life, in concert with a dramatic increase in cognitive abilities. How these processes relate, however, is still unclear. Here we aimed to use a data-driven technique to parcellate developing white matter into regions with consistent white matter growth trajectories and investigate how these regions related to cognitive development. In a large sample of 183 children aged 3 months to 4 years, we calculated whole brain myelin volume fraction (VFM ) maps using quantitative multicomponent relaxometry. We used spatial independent component analysis (ICA) to blindly segment these quantitative VFM images into anatomically meaningful parcels with distinct developmental trajectories. We further investigated the relationship of these trajectories with standardized cognitive scores in the same children. The resulting components represented a mix of unilateral and bilateral white matter regions (e.g., cortico-spinal tract, genu and splenium of the corpus callosum, white matter underlying the inferior frontal gyrus) as well as structured noise (misregistration, image artifact). The trajectories of these regions were associated with individual differences in cognitive abilities. Specifically, components in white matter underlying frontal and temporal cortices showed significant relationships to expressive and receptive language abilities. Many of these relationships had a significant interaction with age, with VFM becoming more strongly associated with language skills with age. These data provide evidence for a changing coupling between developing myelin and cognitive development.

Keywords: cognitive development; language; multicomponent relaxometry; myelin volume fraction; neurodevelopment; white matter.

Figure 1

The average myelin map with the white matter mask overlaid as a blue outline. All analyses took place within this white matter mask. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 2

Example independent components grouped by anatomical profile. Group (a) demonstrates components that are bilaterally symmetric. Group (b) demonstrates components that are lateralized but have a symmetrical counterpart. Group (c) shows three aspects of the corpus callosum. Groups (d) and (e) show regions in the cerebellum, thalamus and basal ganglia respectively. Images here and throughout are presented in radiological format (left is right).

Figure 3

Correspondence between independent component loadings and VF_M in two components. The left component represents the anterior corpus callosum and shows a near 1:1 correspondence between the independent component loading and the underlying VF_M values. The right component's signal is predominantly in the inferior temporal lobe susceptibility area and demonstrates a less clear relationship with VF_M.

Figure 4

Trajectories of VF_M against age in the first three components. Developmental trajectories have highly nonlinear trajectory. The corticospinal tracts demonstrate a logarithmic profile and the anterior corpus callosum and left frontal white matter show a sigmoidal shape.

Figure 5

Components showing a significant relationship with receptive and expressive language scores. Red circles indicate a significant relationship with receptive language, blue with expressive language. Dashed lines indicate a significant interaction in the relationship between a component and language with age.

Figure 6

Three example regions and their linear correlations to cognitive scores. The first component in the anterior corpus callosum shows a significant relationship to both expressive and receptive language and this relationship an linear interaction with age. The second component in white matter underlying left premotor cortex shows a relationship, and interaction with age, with receptive language scores only. The third component in white matter underlying right premotor cortex shows a relationship, and interaction with age, with expressive language scores only. Note these figures are illustrative only, the statistical significance of the relationships occurs in the context of the full general linear model described in the text. Grey lines indicate the 95% confidence intervals of the correlation coefficients. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]