Delineation of early brain development from fetuses to infants with diffusion MRI and beyond

Abstract

Dynamic macrostructural and microstructural changes take place from the mid-fetal stage to 2 years after birth. Delineating structural changes of the brain during early development provides new insights into the complicated processes of both typical development and the pathological mechanisms underlying various psychiatric and neurological disorders including autism, attention deficit hyperactivity disorder and schizophrenia. Decades of histological studies have identified strong spatial and functional maturation gradients in human brain gray and white matter. The recent improvements in magnetic resonance imaging (MRI) techniques, especially diffusion MRI (dMRI), relaxometry imaging, and magnetization transfer imaging (MTI) have provided unprecedented opportunities to non-invasively quantify and map the early developmental changes at whole brain and regional levels. Here, we review the recent advances in understanding early brain structural development during the second half of gestation and the first two postnatal years using modern MR techniques. Specifically, we review studies that delineate the emergence and microstructural maturation of white matter tracts, as well as dynamic mapping of inhomogeneous cortical microstructural organization unique to fetuses and infants. These imaging studies converge into maturational curves of MRI measurements that are distinctive across different white matter tracts and cortical regions. Furthermore, contemporary models offering biophysical interpretations of the dMRI-derived measurements are illustrated to infer the underlying microstructural changes. Collectively, this review summarizes findings that contribute to charting spatiotemporally heterogeneous gray and white matter structural development, offering MRI-based biomarkers of typical brain development and setting the stage for understanding aberrant brain development in neurodevelopmental disorders.

Diffusion-MRI-based regional cortical microstructure at birth for predicting neurodevelopmental outcomes of 2-year-olds

“…During emergence of brain circuits, increasing dendritic arborization (Bystron et al, 2008;Sidman and Rakic, 1973), synapses formation (Huttenlocher and Dabholkar, 1997), and myelination of intracortical axons (Yakovlev and Lecours, 1967) disrupt the highly organized radial glia in the immature cortex and result in cortical FA decreases. Such reproducible cortical FA change patterns were documented in many studies of perinatal human brain development (Ball et al, 2013;Huang et al, 2006;Huang et al, 2009;Huang et al, 2013;Kroenke et al, 2007;McKinstry et al, 2002;Neil et al, 1998;Ouyang et al, 2019a;Ouyang et al, 2019b;Yu et al, 2016), suggesting sensitivity of cortical FA measures to maturational processes of cortical microstructure. Diffusion-MRI-based regional cortical microstructure at birth, encoding rich "footage" of regional cellular and molecular processes, may provide novel information regarding typical cortical development and biomarkers for neuropsychiatric disorders.…”

“…2) is probably due to sensitivity of cortical microstructural changes to maturational processes involving synaptic formation, dendritic arborization and axonal growth. Distinctive maturation processes manifested by differentiated cortical FA changes across cortical regions in fetal and infant brains were reproducibly reported development (Ball et al, 2013;Huang et al, 2006;Huang et al, 2009;Huang et al, 2013;Kroenke et al, 2007;McKinstry et al, 2002;Neil et al, 1998;Ouyang et al, 2019a;Ouyang et al, 2019b;Yu et al, 2016). Although cortical thickness, volume or surface area from structural MRI scans (i.e.…”

“…The first 2 years of life is a critical period for behavioral development, with brain development in this period most rapid across lifespan. In parallel to rapid maturation of cortical architecture and establishment of complex neuronal connections (Hüppi et al, 1998;Ouyang et al, 2019a;Pfefferbaum et al, 1994), babies learn to walk, talk, and build the core capacities for lifetime. Infant behaviors including cognition, language and motor emerge during this time and become measurable at around 2 years of age.…”

Anatomo-functional correlates of auditory development in infancy

“…including the development of dendritic arborization (Ball et al, 2013), the increase in synaptic density, the myelination of intra-cortical fibers (Lebenberg, Labit, et al, 2019) or the changes in intracellular organelle density (for a review see (Ouyang, Dubois, Yu, Mukherjee, & Huang, 2019)). A recent study using another diffusion-based method (neurite orientation dispersion and density imaging: NODDI) also pointed to the increasing cellular and organelle densities around the term period as sources of developmental changes in diffusion parameters (Batalle et al, 2019).…”

Automated Brain Masking of Fetal Functional MRI

“…Image acquisition improvements have occurred mainly with respect to fetal structural MRI, particularly in anatomical (primarily T2 HASTE; Half-Fourier Acquisition Single-shot Turbo spin Echo imaging) and diffusion tensor imaging (DTI) [5,6]. Advances have been made in inter-slice motion correction and volume reconstruction [7,8], mapping structural connectivity [9,10,11,12,13], comparing different MRI signals [14]. These strategies have made it possible to use sparse acquisition sequences, which alleviate movement concerns [15,16], and enable more sophisticated analytic approaches, such as morphometric [7,17,18,19], cortical folding [20], and cytoarchitectural examinations [21].…”