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Early childhood is an important period for cognitive and brain development, though white matter changes specific to this period remain understudied. Here we utilize a novel analytic approach to quantify and track developmental changes in white matter micro- and macro-structure, calculated from individually oriented fiber-bundle populations, termed “fixels”. Fixel-based analysis and mixed-effects models were used to assess tract-wise changes in fiber density and bundle morphology in 73 girls scanned at baseline (ages 4.09–7.02, mean ​= ​5.47, SD ​= ​0.81), 6-month (N ​= ​7), and one-year follow-up (N ​= ​42). For comparison, we also assessed changes in commonly utilized diffusion tensor metrics: fractional anisotropy (FA), and mean, radial and axial diffusivity (MD, RD, AD). Maturational increases in fixel-metrics were seen in most major white matter tracts, with the most rapid increases in the corticospinal tract and slowest or non-significant increases in the genu of the corpus callosum and uncinate fasciculi. As expected, we observed developmental increases in FA and decreases in MD, RD and AD, though percent changes were smaller relative to fixel-metrics. The majority of tracts showed more substantial morphological than microstructural changes. These findings highlight early childhood as a period of dynamic white matter maturation, characterized by large increases in macroscopic fiber bundle size, mild changes in axonal density, and parallel, albeit less substantial, changes in diffusion tensor metrics. •White matter fiber density and bundle size increase with age in early childhood.•Increases in fiber density and bundle size occur in most major white matter tracts.•Rate of change is fastest in the corticospinal tract and slowest in frontal tracts.•Increases in fiber bundle size are more substantial than increases in fiber density.•These changes are more substantial than changes in diffusion tensor metrics.

ABSTRACTThe ascending reticular activating system (ARAS) mediates arousal, an essential component of human consciousness. Lesions of the ARAS cause coma, the most severe disorder of consciousness. Because of current methodological limitations, including of postmortem tissue analysis, the neuroanatomic connectivity of the human ARAS is poorly understood. We applied the advanced imaging technique of high angular resolution diffusion imaging (HARDI) to elucidate the structural connectivity of the ARAS in 3 adult human brains, 2 of which were imaged postmortem. High angular resolution diffusion imaging tractography identified the ARAS connectivity previously described in animals and also revealed novel human pathways connecting the brainstem to the thalamus, the hypothalamus, and the basal forebrain. Each pathway contained different distributions of fiber tracts from known neurotransmitter-specific ARAS nuclei in the brainstem. The histologically guided tractography findings reported here provide initial evidence for human-specific pathways of the ARAS. The unique composition of neurotransmitter-specific fiber tracts within each ARAS pathway suggests structural specializations that subserve the different functional characteristics of human arousal. This ARAS connectivity analysis provides proof of principle that HARDI tractography may affect the study of human consciousness and its disorders, including in neuropathologic studies of patients dying in coma and the persistent vegetative state.

Very preterm-born infants are at risk of adverse neurodevelopmental outcomes. Brain magnetic resonance imaging (MRI) at term equivalent age (TEA) can probe tissue microstructure and morphology, and demonstrates potential in the early prediction of outcomes. In this study, we use the recently introduced fixel-based analysis method for diffusion MRI to investigate the association between microstructure and morphology at TEA, and motor and cognitive development at 1 and 2 years corrected age (CA). Eighty infants born <31 weeks’ gestation successfully underwent diffusion MRI (3T; 64 directions; b ​= ​2000s/mm2) at term equivalent age, and had neurodevelopmental follow-up using the Bayley-III motor and cognitive assessments at 1 year (n ​= ​78) and/or 2 years (n ​= ​76) CA. Diffusion MRI data were processed using constrained spherical deconvolution (CSD) and aligned to a study-specific fibre orientation distribution template, yielding measures of fibre density (FD), fibre-bundle cross-section (FC), and fibre density and bundle cross-section (FDC). The association between FD, FC, and FDC at TEA, and motor and cognitive composite scores at 1 and 2 years CA, and change in composite scores from 1 to 2 years, was assessed using whole-brain fixel-based analysis. Additionally, the association between diffusion tensor imaging (DTI) metrics (fractional anisotropy FA, mean diffusivity MD, axial diffusivity AD, radial diffusivity RD) and outcomes was investigated. Motor function at 1 and 2 years CA was associated with CSD-based measures of the bilateral corticospinal tracts and corpus callosum. Cognitive function was associated with CSD-based measures of the midbody (1-year outcomes only) and splenium of the corpus callosum, as well as the bilateral corticospinal tracts. The change in motor/cognitive outcomes from 1 to 2 years was associated with CSD-based measures of the splenium of the corpus callosum. Analysis of DTI-based measures showed overall less extensive associations. Post-hoc analysis showed that associations were weaker for 2-year outcomes than they were for 1-year outcomes. Infants with better neurodevelopmental outcomes demonstrated higher FD, FC, and FDC at TEA, indicating better information transfer capacity which may be related to increased number of neurons, increased myelination, thicker bundles, and/or combinations thereof. The fibre bundles identified here may serve as the basis for future studies investigating the predictive ability of these metrics. •Brain measures at term are associated with outcomes at 1 and 2 years.•Infants with higher FD, FC and FDC at term perform better on Bayley-III.•DTI measures (FA, MD, AD, RD) show limited associations with outcomes.•Associations are stronger for 1-year outcomes than for 2-year outcomes.

Neural language development involves the maturation of both frontal and temporal language centers and their white matter connections. Leftward asymmetry of white matter tracts has been seen at 5 years of age, and the maintenance of laterality into adulthood likely supports mature language functioning and cortical lateralization. However, it is not known if this laterality is present in infancy or how it relates to early language acquisition. We examined longitudinal changes in white matter microstructure and macrostructure in language (arcuate fasciculus [AF], uncinate fasciculus [UF]) and motor (corticospinal tract [CST]) white matter pathways in typically developing infants. We hypothesized that left hemisphere language tracts would demonstrate more rapid maturation in infancy compared to their right hemisphere counterparts, supporting an early left hemisphere bias for language in the left hemisphere, and we hypothesized that nonmotor tracts would demonstrate concurrent bilateral maturation. We characterized the development of hemispheric asymmetry in the bilateral AF, UF, and CST in 114 typically developing infants from 0 to 24 months of age using data from the HCP Baby Connectome Project. We measured longitudinal changes in fractional anisotropy (FA), mean diffusivity (MD), radial diffusivity (RD), axial diffusivity (AD), probabilistic streamlines, and tract volume. We used linear mixed‐effects modeling to estimate the developmental trajectories in micro‐ and macrostructure in the left and right hemisphere tracts. We additionally reconstructed these tracts in a cohort of healthy adults from the 100 Unrelated Subjects Cohort of the Human Connectome Project. We successfully reconstructed these tracts in the adult brain and demonstrated broad left‐lateralization, replicating prior findings. For infants, all tracts demonstrated rapid age‐related changes in microstructure, but there were no age‐related increases in tract volume or number of streamlines. There were no main effects of sex in any measure. In contrast to adults, while we did see a difference between hemispheres in the number of streamlines in the UF, which was greater in the right hemisphere, we did not find other differences or any asymmetries in rates of maturation between left and right hemisphere tracts. Our methods are capable of identifying laterality differences between left and right hemisphere white matter tracts in adults. However, the picture was quite different in infants. We found that both the left and right AF and UF demonstrated rapid microstructural maturation over the first 2 years of life. However, left lateralization of these tracts was not present in infancy. This may indicate that strong laterality develops as more language skills are acquired or perhaps not until strong cortical lateralization emerges in childhood. Future studies should add to this work by including other language tracts and including data from infancy through childhood, when functional language lateralization begins to emerge and core language acquisition is complete. We examined white matter pathways within the infant language network in order to assess the development of structural language lateralization. We find that white matter pathways that support language functions—and are typically left‐lateralized in adults—are bilaterally symmetric in infants from birth to 24 months.

Tractography based on diffusion tensor imaging (DTI) allows visualization of white matter tracts. In this study, protocols to reconstruct eleven major white matter tracts are described. The protocols were refined by several iterations of intra- and inter-rater measurements and identification of sources of variability. Reproducibility of the established protocols was then tested by raters who did not have previous experience in tractography. The protocols were applied to a DTI database of adult normal subjects to study size, fractional anisotropy (FA), and T2 of individual white matter tracts. Distinctive features in FA and T2 were found for the corticospinal tract and callosal fibers. Hemispheric asymmetry was observed for the size of white matter tracts projecting to the temporal lobe. This protocol provides guidelines for reproducible DTI-based tract-specific quantification.

Local circuit connectivity patterns have been described as being either layer specific or projection class specific. Here, Anderson et al . find that the main excitatory pathway in mouse motor cortex, from layer 2/3 to layer 5, is fractionated on the basis of both neuronal sublayer position and projection class. The mammalian motor system is organized around distinct subcortical subsystems, suggesting that the intracortical circuits immediately upstream of spinal cord and basal ganglia might be functionally differentiated as well. We found that the main excitatory pathway in mouse motor cortex, layer 2/3→5, is fractionated into distinct pathways targeting corticospinal and corticostriatal neurons, which are involved in motor control. However, connections were selective for neurons in certain sublayers: corticospinal neurons in upper layer 5B and corticostriatal neurons in lower 5A. A simple structural combinatorial principle accounts for this highly specific functional circuit architecture: potential connectivity is established by neuronal sublayer positioning and actual connectivity in this framework is determined by long-range axonal projection targets. Thus, intracortical circuits of these pyramidal neurons are specified not only by their long-range axonal targets or their layer or sublayer positions, but by both, in specific combinations.

With the advent of diffusion tensor imaging (DTI), the study of plastic changes in white matter architecture due to long-term practice has attracted increasing interest. Professional musicians provide an ideal model for investigating white matter plasticity because of their early onset of extensive auditory and sensorimotor training. We performed fiber tractography and subsequent voxelwise analysis, region of interest (ROI) analysis, and detailed slicewise analysis of diffusion parameters in the corticospinal tract (CST) on 26 professional musicians and a control group of 13 participants. All analyses resulted in significantly lower fractional anisotropy (FA) values in both the left and the right CST in the musician group. Furthermore, a right-greater-than-left asymmetry of FA was observed regardless of group. In the musician group, diffusivity was negatively correlated with the onset of musical training in childhood. A subsequent median split into an early and a late onset musician group (median=7 years) revealed increased diffusivity in the CST of the early onset group as compared to both the late onset group and the controls. In conclusion, these DTI-based findings might indicate plastic changes in white matter architecture of the CST in professional musicians. Our results imply that training-induced changes in diffusion characteristics of the axonal membrane may lead to increased radial diffusivity as reflected in decreased FA values.

Abstract BACKGROUND The brainstem is one of the most challenging areas for the neurosurgeon because of the limited space between gray matter nuclei and white matter pathways. Diffusion tensor imaging-based tractography has been used to study the brainstem structure, but the angular and spatial resolution could be improved further with advanced diffusion magnetic resonance imaging (MRI). OBJECTIVE To construct a high-angular/spatial resolution, wide-population-based, comprehensive tractography atlas that presents an anatomical review of the surgical approaches to the brainstem. METHODS We applied advanced diffusion MRI fiber tractography to a population-based atlas constructed with data from a total of 488 subjects from the Human Connectome Project-488. Five formalin-fixed brains were studied for surgical landmarks. Luxol Fast Blue-stained histological sections were used to validate the results of tractography RESULTS We acquired the tractography of the major brainstem pathways and validated them with histological analysis. The pathways included the cerebellar peduncles, corticospinal tract, corticopontine tracts, medial lemniscus, lateral lemniscus, spinothalamic tract, rubrospinal tract, central tegmental tract, medial longitudinal fasciculus, and dorsal longitudinal fasciculus. Then, the reconstructed 3-dimensional brainstem structure was sectioned at the level of classic surgical approaches, namely supracollicular, infracollicular, lateral mesencephalic, perioculomotor, peritrigeminal, anterolateral (to the medulla), and retro-olivary approaches. CONCLUSION The advanced diffusion MRI fiber tracking is a powerful tool to explore the brainstem neuroanatomy and to achieve a better understanding of surgical approaches.

Brain development continues actively during adolescence. Previous MRI studies have shown complex patterns of apparent loss of grey matter (GM) volume and increases in white matter (WM) volume and fractional anisotropy (FA), an index of WM microstructure. In this longitudinal study (mean follow-up=2.5±0.5 years) of 24 adolescents, we used a voxel-based morphometry (VBM)-style analysis with conventional T1-weighted images to test for age-related changes in GM and WM volumes. We also performed tract-based spatial statistics (TBSS) analysis of diffusion tensor imaging (DTI) data to test for age-related WM changes across the whole brain. Probabilistic tractography was used to carry out quantitative comparisons across subjects in measures of WM microstructure in two fiber tracts important for supporting speech and motor functions (arcuate fasciculus [AF] and corticospinal tract [CST]). The whole-brain analyses identified age-related increases in WM volume and FA bilaterally in many fiber tracts, including AF and many parts of the CST. FA changes were mainly driven by increases in parallel diffusivity, probably reflecting increases in the diameter of the axons forming the fiber tracts. FA values of both left and right AF (but not of the CST) were significantly higher at the end of the follow-up than at baseline. Over the same period, widespread reductions in the cortical GM volume were found. These findings provide imaging-based anatomical data suggesting that brain maturation in adolescence is associated with structural changes enhancing long-distance connectivities in different WM tracts, specifically in the AF and CST, at the same time that cortical GM exhibits synaptic “pruning”.

Long-term motor training, such as dance or gymnastics, has been associated with increased diffusivity and reduced fiber coherence in regions including the corticospinal tract. Comparisons between different types of motor experts suggest that experience might result in specific structural changes related to the trained effectors (e.g., hands or feet). However, previous studies have not segregated the descending motor pathways from different body-part representations in motor cortex (M1). Further, most previous diffusion tensor imaging studies used whole-brain analyses based on a single tensor, which provide poor information about regions where multiple white matter (WM) tracts cross. Here, we used multi-tensor probabilistic tractography to investigate the specific components of the descending motor pathways in well-matched groups of dancers, musicians and controls. To this aim, we developed a procedure to identify the WM regions below the motor representations of the head, hand, trunk and leg that served as seeds for tractography. Dancers showed increased radial diffusivity (RD) in comparison with musicians, in descending motor pathways from all the regions, particularly in the right hemisphere, whereas musicians had increased fractional anisotropy (FA) in the hand and the trunk/arm motor tracts. Further, dancers showed larger volumes compared to both other groups. Finally, we found negative correlations between RD and FA with the age of start of dance or music training, respectively, and between RD and performance on a melody task, and positive correlations between RD and volume with performance on a whole-body dance task. These findings suggest that different types of training might have different effects on brain structure, likely because dancers must coordinate movements of the entire body, whereas musicians focus on fewer effectors.