TL;DR
Evidence for asymmetric development across the fiber bundles studied is found, with the corticospinal tracts showing earlier maturation but slower volumetric growth compared to the callosal fibers.
The putamen is a major hub of the basal ganglia that emerges early in gestation. However, whether its mature organization is established before birth or emerges postnatally remains unknown. Using cross-sectional and longitudinal quantitative MRI (R1 and R2*, related to tissue density and iron, respectively), and diffusion MRI, we characterized the development of putamen’s microstructure and its white matter connectivity with cortex from birth to 12 months and compared their trajectories with those in adults. Despite its prenatal emergence, the putamen undergoes substantial postnatal development. R1 increases from birth to 12 months, producing a prominent anterior–posterior gradient, whereas R2* increases primarily between age one and adulthood, producing a medial– lateral gradient. Cortico-putamen white matter connectivity is diffuse in infants but becomes topographic in adults, with anterior putamen linked to frontal cortex and posterior putamen to sensorimotor cortex. In autism spectrum disorder, this organization is largely preserved and accompanied by increased anterior putamen–prefrontal connectivity. Our findings reveal distinct spatial developmental trajectories of putamen microstructure and cortical connectivity providing a developmental framework for understanding the organization of the putamen in infancy, which has implications for assessing neurodevelopmental disorders of the basal ganglia. Teaser From birth to one year, the putamen develops distinct microstructural gradients and increasingly topographic cortical connections.
Abstract Early childhood development is scaffolded by rapid maturation of brain white matter structure, believed to support the emergence of cognitive and socioemotional functions. Previous whole-tract studies have suggested patterns of white matter development occurring along posterior–anterior, deep–superficial, and inferior–superior axes. However, these have largely been cross-sectional and employed nonspecific metrics of white matter organization. Using longitudinal diffusion imaging data from 133 children (4 to 8 years; 76 females), the present work characterizes along-tract patterns of white matter development across association, commissural, and projection bundles using fixel-based analysis. Within long range association bundles, faster age-related changes were observed for segments adjacent to the visual cortices relative to segments located near association regions, supporting a sensorimotor-association axis of brain development. An inferior–superior pattern was found for projection tracts, with faster age-effects observed for segments near the brainstem. Lastly, while several association and commissural bundles exhibited faster maturation within central segments; indicative of a deep-superficial axis, effects were mixed between micro- and macrostructure, underscoring the unique developmental timing of these different fiber properties. Our findings provide evidence that within-tract white matter maturation unfolds along key spatiotemporal axes, and suggests that increased spatial precision can advance our understanding of early childhood brain development.
OBJECTIVE Nonsyndromic craniosynostosis (NSC) might disrupt normal white matter maturation, and infant surgical intervention remains the standard of care. The aim of this multisite study was to assess baseline differences in white matter tract development and compare white matter tract development following surgical correction in NSC patients relative to normally developing controls using diffusion tensor imaging (DTI). METHODS Pre- and postoperative DTI was obtained at three centers (Arkansas, Vanderbilt, and Yale) in children who underwent surgical correction for NSC (n = 16), and age-matched control scans (n = 47) were obtained from the Lifespan Baby Connectome Project. Analysis of diffusion parameters was performed for 48 white matter tracts defined by the Johns Hopkins University white matter tractography atlas. Descriptive analyses were used to compare diffusion parameters between the NSC and control cohorts at pre- and postoperative time points. Linear mixed-effects models were fit to assess whether tract development between pre- and postoperative scans differed between patients and controls. RESULTS Patients with NSC showed greater global mean, axial, and radial diffusivity at the preoperative time point compared with age-matched controls. Following surgical correction, the NSC cohort had greater decreases in mean, axial, and radial diffusivity across multiple association, commissural, and projection tracts (e.g., the inferior and superior longitudinal fasciculi, corpus callosum, corona radiata, cingulum, and internal and external capsules) between pre- and postoperative time points compared with controls. Changes in fractional anisotropy were comparable between patients and controls. CONCLUSIONS Patients with NSC exhibited greater decreases in diffusivity across major white matter tracts following surgery compared with normally developing controls. These decreases might represent accelerated maturation/normalization of white matter following surgical correction of NSC.
BACKGROUND Extensive neuroimaging abnormalities in multiple brain regions constitute the neural basis of preterm infants (PTIs). However, the function of the brain and its spatial coupling with brain structure remain unknown, leaving a considerable gap in understanding the neural mechanism underlying atypical neurodevelopment in PTIs. METHODS Combining structural magnetic resonance imaging (MRI) and resting-state functional magnetic resonance imaging (fMRI) data from 14 PTIs and 14 term infants (TEIs), we quantified gray matter volume (GMV) via voxel-based morphometry, estimated intrinsic timescales from fMRI signals via autocorrelation function (ACF) analysis, and further assessed spatial structure-function coupling across individuals. RESULTS PTIs exhibited GMV alterations in multiple brain regions encompassing high-order cortical and subcortical regions (p < 0.001, corrected by family-wise error (FWE)), which were significantly associated with clinical variables such as gestational age (R = 0.716, p < 0.0001), postnatal age (R = -0.698, p < 0.0001) and birth weight (R = 0.727, p < 0.0001). Alterations in intrinsic timescales were revealed at both the spatial distribution (voxel-level p < 0.001, Gaussian random field (GRF)-corrected p < 0.05) and local regional levels, highlighting functional alterations of the medial frontal gyrus in PTIs (voxel-level p < 0.001, GRF-corrected p < 0.05). Furthermore, alterations in spatial structure-function coupling were also found in both high-order cortical and subcortical regions, with ACF decay in these regions significantly correlated with serum iron levels (R = -0.664, p = 0.0096) in PTIs. CONCLUSIONS These findings suggest that preterm birth-related neurodevelopmental alterations may be associated with differences in the coordination between brain structure and function, which could be related to variations in neurobehavioral outcomes, and indicate that neuroimaging may provide useful insights into early neurodevelopmental differences in PTIs.
In-vivo examination of neurites to understand microstructural properties of white matter tissue utilizing neurite orientation dispersion and density imaging (NODDI) has shown sensitivity to healthy aging as well as disease biomarkers and status. Neurite density index (NDI), which is a proxy for the amount of neurites, in white matter tissue typically decreases with age. However, orientation dispersion index (ODI), which is a proxy for neurite dispersion or fanning, has been mixed with studies finding both increases and decreases with age. Furthermore, white matter tracts are not uniform and hold its own unique spatial pattern or gradient in microstructural properties. In addition to the spatial pattern of the microstructural property, age-related effects have also shown spatial patterns with stronger age effects in the medial, anterior, and dorsal portions of white matter tissue. However, spatial gradients along cardinal axes within an individual’s tract have yet to be examined with age in an adult lifespan sample. The current aim of the study was to examine whether average and spatial gradients of neurite microstructural properties within tracts related to the cortico-striato-pallido-thalamic (CSPT) loop were age-sensitive. An adult lifespan sample aged 20-90 years old was recruited from the Dallas-Fort Worth metroplex (N = 104, 62% females) as part of the Dallas Area Longitudinal Lifespan Area Study (DALLAS). Participants completed an MRI session that included a structural T1-weighted image as well as multi-shell diffusion weighted imaging (MS-DWI). MS-DWI were preprocessed and tracts of interest related to the CSPT loop were obtained using probabilistic tractography. For most tracts, a significant inverted-U association with age was found for both average NDI and ODI. Most tracts revealed a reliable spatial gradient of NDI and ODI in the medial-to-lateral, posterior-to-anterior, and ventral-to-dorsal direction. Tracts related to CSPT loop were age-sensitive such that the spatial gradient was becoming more homogenous with age. This loss of spatial gradients with age is analogous to network-level dedifferentiation observed in BOLD functional connectivity. These findings highlight that age effects in a fundamental circuit for both basic and higher-order function is significantly age sensitive and while organized into spatial gradients, these gradients are also vulnerable to aging.
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