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      High Angular Resolution Diffusion MRI Reveals Conserved and Deviant Programs in the Paths that Guide Human Cortical Circuitry

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          Abstract

          Diffusion magnetic resonance (MR) tractography represents a novel opportunity to investigate conserved and deviant developmental programs between humans and other species such as mice. To that end, we acquired high angular resolution diffusion MR scans of mice [embryonic day (E) 10.5 to postnatal week 4] and human brains [gestational week (GW) 17–30] at successive stages of fetal development to investigate potential evolutionary changes in radial organization and emerging pathways between humans and mice. We compare radial glial development as well as commissural development (e.g., corpus callosum), primarily because our findings can be integrated with previous work. We also compare corpus callosal growth trajectories across primates (i.e., humans and rhesus macaques) and rodents (i.e., mice). One major finding is that the developing cortex of humans is predominated by pathways likely associated with a radial glial organization at GW 17–20, which is not as evident in age-matched mice (E 16.5, 17.5). Another finding is that, early in development, the corpus callosum follows a similar developmental timetable in primates (i.e., macaques and humans) as in mice. However, the corpus callosum grows for an extended period of time in primates compared with rodents. Taken together, these findings highlight deviant developmental programs underlying the emergence of cortical pathways in the human brain.

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          Most cited references158

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          The delayed rise of present-day mammals.

          Did the end-Cretaceous mass extinction event, by eliminating non-avian dinosaurs and most of the existing fauna, trigger the evolutionary radiation of present-day mammals? Here we construct, date and analyse a species-level phylogeny of nearly all extant Mammalia to bring a new perspective to this question. Our analyses of how extant lineages accumulated through time show that net per-lineage diversification rates barely changed across the Cretaceous/Tertiary boundary. Instead, these rates spiked significantly with the origins of the currently recognized placental superorders and orders approximately 93 million years ago, before falling and remaining low until accelerating again throughout the Eocene and Oligocene epochs. Our results show that the phylogenetic 'fuses' leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today's mammals.
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            Inferring the historical patterns of biological evolution.

            M. Pagel (1999)
            Phylogenetic trees describe the pattern of descent amongst a group of species. With the rapid accumulation of DNA sequence data, more and more phylogenies are being constructed based upon sequence comparisons. The combination of these phylogenies with powerful new statistical approaches for the analysis of biological evolution is challenging widely held beliefs about the history and evolution of life on Earth.
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              Neurons derived from radial glial cells establish radial units in neocortex.

              The neocortex of the adult brain consists of neurons and glia that are generated by precursor cells of the embryonic ventricular zone. In general, glia are generated after neurons during development, but radial glia are an exception to this rule. Radial glia are generated before neurogenesis and guide neuronal migration. Radial glia are mitotically active throughout neurogenesis, and disappear or become astrocytes when neuronal migration is complete. Although the lineage relationships of cortical neurons and glia have been explored, the clonal relationship of radial glia to other cortical cells remains unknown. It has been suggested that radial glia may be neuronal precursors, but this has not been demonstrated in vivo. We have used a retroviral vector encoding enhanced green fluorescent protein to label precursor cells in vivo and have examined clones 1-3 days later using morphological, immunohistochemical and electrophysiological techniques. Here we show that clones consist of mitotic radial glia and postmitotic neurons, and that neurons migrate along clonally related radial glia. Time-lapse images show that proliferative radial glia generate neurons. Our results support the concept that a lineage relationship between neurons and proliferative radial glia may underlie the radial organization of neocortex.
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                Author and article information

                Journal
                Cerebral Cortex
                Oxford University Press (OUP)
                1047-3211
                1460-2199
                March 2020
                March 14 2020
                October 30 2019
                March 2020
                March 14 2020
                October 30 2019
                : 30
                : 3
                : 1447-1464
                Affiliations
                [1 ]Department of Psychology, Delaware State University, Dover, DE 19901, USA
                [2 ]Medical Sciences in the College of Arts and Sciences, Boston University, Boston, MA 02215, USA
                [3 ]Division of Newborn Medicine, Department of Medicine, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02215, USA
                [4 ]Fetal-Neonatal Brain Imaging and Developmental Science Center, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02215, USA
                [5 ]Division of Neuroradiology, Department of Radiology, Massachusetts General Hospital, Boston, MA 02114, USA
                [6 ]Department of Behavioral Neuroscience, Northeastern University, Boston, MA 02115, USA
                [7 ]Science Center, Wellesley College, Wellesley, MA 02481, USA
                [8 ]Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02129, USA
                Article
                10.1093/cercor/bhz178
                7132938
                31667494
                5946ccd8-e730-4810-9fd0-89a5a07b8a77
                © 2019

                https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model

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