Quantitative in vivo evidence for broad regional gradients in the timing of white matter maturation during adolescence

Abstract

A fundamental tenet in the field of developmental neuroscience is that brain maturation generally proceeds from posterior/inferior to anterior/superior. This pattern is thought to underlie the similar timing of cognitive development in related domains, with the dorsal frontal cortices – important for decision making and cognitive control – the last to fully mature. While this caudal to rostral wave of structural development was first qualitatively described for white matter in classical postmortem studies, and has been discussed frequently in the developmental neuroimaging literature and in the popular press, it has never been formally demonstrated continuously and quantitatively across the whole brain with magnetic resonance imaging (MRI). Here we use diffusion imaging to map developmental changes in the white matter in 32 typically-developing individuals age 5-28 years. We then employ a novel meta-statistic that is sensitive to the timing of this developmental trajectory, and use this integrated strategy to both confirm these long-postulated broad regional gradients in the timing of white matter maturation in vivo, and demonstrate a surprisingly smooth transition in the timing of white matter maturational peaks along a caudal-rostral arc in this cross-sectional sample. These results provide further support for the notion of continued plasticity in these regions well into adulthood, and may provide a new approach for the investigation of neurodevelopmental disorders that could alter the timing of this typical developmental sequence.

Becoming Consistent: Developmental Reductions in Intraindividual Variability in Reaction Time Are Related to White Matter Integrity

“…The frontal lobe hypothesis has also been partly supported by a functional MRI study that found an association between IIV and task-related brain activation within a network consisting of middle frontal, inferior parietal, and thalamic regions (Bellgrove et al, 2004). An association between IIV and frontal WM integrity could be expected in adolescence, as regional differences observed in developmental curves indicate a pattern of maturation in which fronto-temporal networks show a relatively protracted development (Tamnes et al, 2010a;Colby et al, 2011;Lebel and Beaulieu, 2011). However, as discussed below, the majority of effects found in the current study were in central brain regions.…”

Developmental improvements in dynamic control of fingertip forces last throughout childhood and into adolescence

“…This domain of sensorimotor function is of particular interest because it has been shown to engage the cortical sensory-motor networks for manipulation more intensely than during manipulation with larger forces (Ehrsson et al 2001). Moreover, the development of manipulation has largely been attributed to the neuroanatomical development in projection and association white matter tracts [such as the corticospinal tracts (CSTs)] that undergo significant changes in microstructure, myelination, and synaptogenesis throughout childhood and continuing into adolescence (Asato et al 2010;Colby et al 2011;Giedd et al 1999;Lebel and Beaulieu 2011;Lebel et al 2008;Paus et al 1999;Sowell et al 1999b). Thus we hypothesize that behavioral improvements in dynamic dexterous manipulation at low forces will follow a timeline similar to those neurodevelopmental changes that last into adolescence.…”

White matter microstructure in boys with persistent depressive disorder

“…However, regional differences have been observed with fibres connecting frontal and temporal cortices (Colby, Van Horn, & Sowell, 2011;Lebel & Beaulieu, 2011;Tamnes et al, 2010) including the cingulum and uncinate fasciculi, which develop at a slower rate than some of the other fibres Olson, Von Der Heide, Alm, & Vyas, 2015;Westlye et al, 2010). Environmental stressor or genetic predisposition may differentially affect the development of white matter pathways and concomitant changes may relate to the development of depressive symptoms (Ladouceur, Peper, Crone, & Dahl, 2012).…”