Longitudinal changes in resting-state fMRI from age 5 to age 6years covary with language development

Abstract

Resting-state functional magnetic resonance imaging is a powerful technique to study the whole-brain neural connectivity that underlies cognitive systems. The present study aimed to define the changes in neural connectivity in their relation to language development. Longitudinal resting-state functional data were acquired from a cohort of preschool children at age 5 and one year later, and changes in functional connectivity were correlated with language performance in sentence comprehension. For this, degree centrality, a voxel-based network measure, was used to assess age-related differences in connectivity at the whole-brain level. Increases in connectivity with age were found selectively in a cluster within the left posterior superior temporal gyrus and sulcus (STG/STS). In order to further specify the connection changes, a secondary seed-based functional connectivity analysis on this very cluster was performed. The correlations between resting-state functional connectivity (RSFC) and language performance revealed developmental effects with age and, importantly, also dependent on the advancement in sentence comprehension ability over time. In children with greater advancement in language abilities, the behavioral improvement was positively correlated with RSFC increase between left posterior STG/STS and other regions of the language network, i.e., left and right inferior frontal cortex. The age-related changes observed in this study provide evidence for alterations in the language network as language develops and demonstrates the viability of this approach for the investigation of normal and aberrant language development.

Keywords: Frontal-to-temporal connection; Intrinsic connectivity; Language development; Preschool children; Resting-state fMRI.

Fig. 1

Mean accuracy of sentence comprehension performance (TSVK) at age 5 and 6 years. Error bars represent standard error of the mean (*** P < .001).

Fig. 2

Voxel-wise degree centrality maps at age 5 (2A) and age 6 (2B). Red–yellow colors indicate positive connectivity, whereas blue colors indicate negative connectivity. Z value is the scale of degree centrality. Multiple comparisons were corrected at the cluster-level using Gaussian random field theory (| Z | > 3.5, cluster-wise p < .001, GRF corrected). L, left hemisphere; R, right hemisphere.

Fig. 3

Comparison of degree centrality maps between age 5 and age 6 years (3A). Red–yellow colors indicates stronger degree centrality at age 6 compared to age 5 in the left posterior STG/STS. Multiple comparisons were corrected at the cluster level using Gaussian random field theory (Z > 2.3, cluster-wise p < .05, GRF corrected). Figure B illustrates individual variation in degree centrality of left posterior STG/STS and also includes the mean values of the cluster in posterior STG/STS at age 5 and age 6 years, as well as error bars representing standard error of the mean (3B). L, left hemisphere; R, right hemisphere. STG/STS, superior temporal gyrus and sulcus.

Fig. 4

Average functional connectivity maps seeded in the left posterior STG/STS shown for children at age 5 (4A) and age 6 (4B). Significant correlations to left inferior frontal cortex are only found for age 6 (Z = 0.3 with minimal cluster size of 60 voxels). Fig. C depicts the direct contrast between the two time points (4C), with red–yellow colors indicating stronger connections at age 6 (Z > 2.3, cluster-wise p < .05, GRF corrected). In addition, the individual variation in correlations between left posterior STG/STS and left IFS (4D), as well as between posterior STG/STS and left angular gyrus (4E) are depicted including the mean correlation coefficients at age 5 and age 6. Error bars represent standard error of the mean. L, left hemisphere; R, right hemisphere. IFS, inferior frontal sulcus.

Fig. 5

Correlations between changes in functional connectivity seeded in the left posterior STG/STS cluster (green circle) and changes in language comprehension performance from age 5 to age 6 in children with greater advancement in language abilities (5A) and children with less advancement in language abilities (5B). While for the former, significant correlations to the bilateral inferior frontal cortex were found, for the latter, no such correlations to other parts of the language network were observed and rather correlations to regions within the DMN exist. Multiple comparisons were corrected at the cluster level using Gaussian random field theory (Z > 2.3, cluster-wise p < .05, GRF corrected). L, left hemisphere; R, right hemisphere. IFG, inferior frontal gyrus; IFS, inferior frontal sulcus; PCC, posterior cingulate cortex/precuneus; VMPFC/ACC, ventromedial prefrontal cortex/anterior cingulate cortex.