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      Differential cortical microstructural maturation in the preterm human brain with diffusion kurtosis and tensor imaging

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          Significance

          Delineating cortical microstructure differentiation is important for understanding complicated yet precisely organized patterns in early developing brain. Knowledge of cortical differentiation predominantly from histological studies is limited in localized and discrete cortical regions. We quantified the preterm brain cerebral cortical profile with microstructural complexity [indexed by mean kurtosis (MK)] and microstructural organization [indexed by fractional anisotropy (FA)] from advanced diffusion MRI. Cortical MK and FA maps revealed a heterogeneous maturation signature. Spatiotemporally distinctive disruption of radial glia and decrease of neuronal density among cortical regions were inferred by FA and MK decreases, respectively. These findings suggest that diffusion kurtosis metrics are significant imaging markers for microstructural differentiation of the developmental brain in health and disease.

          Abstract

          During the third trimester, the human brain undergoes rapid cellular and molecular processes that reshape the structural architecture of the cerebral cortex. Knowledge of cortical differentiation obtained predominantly from histological studies is limited in localized and small cortical regions. How cortical microstructure is differentiated across cortical regions in this critical period is unknown. In this study, the cortical microstructural architecture across the entire cortex was delineated with non-Gaussian diffusion kurtosis imaging as well as conventional diffusion tensor imaging of 89 preterm neonates aged 31–42 postmenstrual weeks. The temporal changes of cortical mean kurtosis (MK) or fractional anisotropy (FA) were heterogeneous across the cortical regions. Cortical MK decreases were observed throughout the studied age period, while cortical FA decrease reached its plateau around 37 weeks. More rapid decreases in MK were found in the primary visual region, while faster FA declines were observed in the prefrontal cortex. We found that distinctive cortical microstructural changes were coupled with microstructural maturation of associated white matter tracts. Both cortical MK and FA measurements predicted the postmenstrual age of preterm infants accurately. This study revealed a differential 4D spatiotemporal cytoarchitectural signature inferred by non-Gaussian diffusion barriers inside the cortical plate during the third trimester. The cytoarchitectural processes, including dendritic arborization and neuronal density decreases, were inferred by regional cortical FA and MK measurements. The presented findings suggest that cortical MK and FA measurements could be used as effective imaging markers for cortical microstructural changes in typical and potentially atypical brain development.

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          Most cited references 46

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          Specification of cerebral cortical areas.

           P Rakic (1988)
          How the immense population of neurons that constitute the human cerebral neocortex is generated from progenitors lining the cerebral ventricle and then distributed to appropriate layers of distinctive cytoarchitectonic areas can be explained by the radial unit hypothesis. According to this hypothesis, the ependymal layer of the embryonic cerebral ventricle consists of proliferative units that provide a proto-map of prospective cytoarchitectonic areas. The output of the proliferative units is translated via glial guides to the expanding cortex in the form of ontogenetic columns, whose final number for each area can be modified through interaction with afferent input. Data obtained through various advanced neurobiological techniques, including electron microscopy, immunocytochemistry, [3H]thymidine and receptor autoradiography, retrovirus gene transfer, neural transplants, and surgical or genetic manipulation of cortical development, furnish new details about the kinetics of cell proliferation, their lineage relationships, and phenotypic expression that favor this hypothesis. The radial unit model provides a framework for understanding cerebral evolution, epigenetic regulation of the parcellation of cytoarchitectonic areas, and insight into the pathogenesis of certain cortical disorders in humans.
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            Regional differences in synaptogenesis in human cerebral cortex.

            The formation of synaptic contacts in human cerebral cortex was compared in two cortical regions: auditory cortex (Heschl's gyrus) and prefrontal cortex (middle frontal gyrus). Synapse formation in both cortical regions begins in the fetus, before conceptual age 27 weeks. Synaptic density increases more rapidly in auditory cortex, where the maximum is reached near postnatal age 3 months. Maximum synaptic density in middle frontal gyrus is not reached until after age 15 months. Synaptogenesis occurs concurrently with dendritic and axonal growth and with myelination of the subcortical white matter. A phase of net synapse elimination occurs late in childhood, earlier in auditory cortex, where it has ended by age 12 years, than in prefrontal cortex, where it extends to midadolescence. Synaptogenesis and synapse elimination in humans appear to be heterochronous in different cortical regions and, in that respect, appears to differ from the rhesus monkey, where they are concurrent. In other respects, including overproduction of synaptic contacts in infancy, persistence of high levels of synaptic density to late childhood or adolescence, the absolute values of maximum and adult synaptic density, and layer specific differences, findings in the human resemble those in rhesus monkeys.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                5 March 2019
                19 February 2019
                19 February 2019
                : 116
                : 10
                : 4681-4688
                Affiliations
                aRadiology Research, Children’s Hospital of Philadelphia , Philadelphia, PA 19104;
                bAdvanced Imaging Research Center, University of Texas Southwestern Medical Center , Dallas, TX 75390;
                cDepartment of Radiology, Perelman School of Medicine, University of Pennsylvania , Philadelphia, PA 19106;
                dLou Ruvo Center for Brain Health, Cleveland Clinic , Las Vegas, NV 89106;
                eDepartment of Radiology, University of Texas Southwestern Medical Center , Dallas, TX 75390;
                fDepartment of Mathematical Sciences, University of Texas at Dallas , Richardson, TX 75080;
                gDepartment of Pediatrics, University of Texas Southwestern Medical Center , Dallas, TX 75390
                Author notes
                2To whom correspondence should be addressed. Email: huangh6@ 123456email.chop.edu .

                Edited by Marcus E. Raichle, Washington University in St. Louis, St. Louis, MO, and approved January 22, 2019 (received for review July 16, 2018)

                Author contributions: H.H. designed research; M.O., T.J., A.S., Q.P., V.M., C.H., L.C., N.R., T.P.L.R., C.D., and H.H. performed research; H.H. contributed new reagents/analytic tools; M.O., T.J., A.S., Q.P., V.M., M.C., and H.H. analyzed data; and M.O., T.J., A.S., and H.H. wrote the paper.

                1M.O. and T.J. contributed equally to this work.

                Article
                201812156
                10.1073/pnas.1812156116
                6410816
                30782802
                Copyright © 2019 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                Page count
                Pages: 8
                Product
                Funding
                Funded by: HHS | NIH | National Institute of Mental Health (NIMH) 100000025
                Award ID: R01MH092535
                Award Recipient : Hao Huang
                Funded by: HHS | NIH | Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) 100009633
                Award ID: U54HD086984
                Award Recipient : Timothy PL Roberts Award Recipient : Hao Huang
                Funded by: HHS | NIH | National Institute of Mental Health (NIMH) 100000025
                Award ID: R01MH092535-S1
                Award Recipient : Hao Huang
                Categories
                PNAS Plus
                Biological Sciences
                Neuroscience
                PNAS Plus

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