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Longitudinal white matter development in children is associated with puberty, attentional difficulties, and mental health

By Sila Genc, Charles B Malpas, Alisha Gulenc, Emma Sciberras, Daryl Efron, Tim Silk, Marc L Seal

Posted 12 Apr 2019
bioRxiv DOI: 10.1101/607671

Purpose: The pubertal period involves dynamic white matter development. This period also corresponds with rapid gains in higher cognitive functions including attention, as well as increased risk of developing mental health difficulties. We performed a longitudinal investigation of the relationship between white matter fibre properties and pubertal stage, attentional difficulties, and internalising problems. Methods: This study reports on a community-based sample of children aged 9-13 years (n=130, 47 female). Diffusion magnetic resonance imaging (dMRI) data were acquired on a 3.0T Siemens Tim Trio (b=2800 s/mm2, 60 directions) at two time-points approximately 16 months apart: time-point 1 (age: M = 10.4, SD = .44 years old), time-point 2 (age: M = 11.7, SD = .51 years old). We leverage the fixel-based analysis (FBA) framework, to derive measures of: fibre density (FD), fibre cross-section (FC), and fibre density and cross-section (FDC), in 17 manually delineated white matter tracts. We apply a longitudinal mixed-effects modelling analysis: to understand how specific fibre properties vary with age, sex, and pubertal stage; and as a function of the development of internalising behaviours and attentional difficulties. Results: We observed significant increases in FD, FC, and FDC across a large number of white matter pathways, with protracted development of frontal pathways such as the inferior fronto-occipital fasciculus (IFOF) and uncinate fasciculus (UF). We observed a linear relationship between FBA metrics and pubertal stage, in the right superior longitudinal fasciculus (SLF). Increases in FD were associated with greater attentional dysfunction, particularly in older males. Lastly, we found evidence for an association between lower FD and greater internalising problems in the right UF, a region known to be implicated in psychiatric disorders. Discussion: These longitudinal results shed light on regional fibre developmental profiles in early puberty. The development of fibre density and morphology across ages 9-13 years involved the expansion of key white matter tracts, excluding regions known to have protracted development over adolescence. The associations between mental health and attentional problems with fibre density in the UF suggests that this region may be sensitive to adopting a different neurodevelopmental course in the presence of such symptoms. Overall, our findings highlight the interrelated nature of fibre development with puberty, mental health problems, and attentional difficulties.

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