Asynchrony of the early maturation of white matter bundles in healthy infants: Quantitative landmarks revealed noninvasively by diffusion tensor imaging

Abstract

Normal cognitive development in infants follows a well-known temporal sequence, which is assumed to be correlated with the structural maturation of underlying functional networks. Postmortem studies and, more recently, structural MR imaging studies have described qualitatively the heterogeneous spatiotemporal progression of white matter myelination. However, in vivo quantification of the maturation phases of fiber bundles is still lacking. We used noninvasive diffusion tensor MR imaging and tractography in twenty-three 1-4-month-old healthy infants to quantify the early maturation of the main cerebral fascicles. A specific maturation model, based on the respective roles of different maturational processes on the diffusion phenomena, was designed to highlight asynchronous maturation across bundles by evaluating the time-course of mean diffusivity and anisotropy changes over the considered developmental period. Using an original approach, a progression of maturation in four relative stages was determined in each tract by estimating the maturation state and speed, from the diffusion indices over the infants group compared with an adults group on one hand, and in each tract compared with the average over bundles on the other hand. Results were coherent with, and extended previous findings in 8 of 11 bundles, showing the anterior limb of the internal capsule and cingulum as the most immature, followed by the optic radiations, arcuate and inferior longitudinal fascicles, then the spinothalamic tract and fornix, and finally the corticospinal tract as the most mature bundle. Thus, this approach provides new quantitative landmarks for further noninvasive research on brain-behavior relationships during normal and abnormal development.

Resting-state networks in the infant brain

“…This discrepancy in the spatial configuration of resting-state patterns may be related to recent findings regarding white matter (WM) fiber tracts in infants. A diffusion tensor MR imaging investigation revealed a significantly lower anisotropy index in the inferior longitudinal fasciculus, inferior frontooccipital fasciculus, and superior longitudinal fasciculus compared with the detected degree of anisotrophy in the interhemispheric callosal fibers (21), which suggests that the WM tracts that support functional connectivity in the anterior-posterior direction are less well developed in the infant brain compared with the tracts that support transcallosal functional connectivity (50).…”

Long‐term white matter tract reorganization following prolonged febrile seizures

“…A possible mechanism for AD increase is greater coherence and alignment of the axons 21, 25, 28, 29. Alongside this, increases in MD suggest disruption of WM microstructure perhaps as a result of decreased axonal or myelin content.…”

“…Therefore, myelination occurs in brainstem WM before cerebral WM, in central WM before peripheral WM, and in projection and commissural pathways before association pathways. The rate of maturation of WM tracts, however, is not linear, with a steep increase in the first year after birth and a slower rate in the following years 19, 20, 23, 24, 25. In addition, WM tracts less mature at birth (e.g.…”

Neonatal brain microstructure correlates of neurodevelopment and gait in preterm children 18–22 mo of age: an MRI and DTI study

“…As the brain develops, cellular microstructures become more complex and organized, water content decreases, and extracellular spaces diminish, changes that can be quantified with DTI (12,13). Scalars obtained from DTI, such as fractional anisotropy (FA) and MD, can assess brain development and maturation (14).…”