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      MRI of the Neonatal Brain: A Review of Methodological Challenges and Neuroscientific Advances

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          Abstract

          In recent years, exploration of the developing brain has become a major focus for researchers and clinicians in an attempt to understand what allows children to acquire amazing and unique abilities, as well as the impact of early disruptions (eg, prematurity, neonatal insults) that can lead to a wide range of neurodevelopmental disorders. Noninvasive neuroimaging methods such as MRI are essential to establish links between the brain and behavioral changes in newborns and infants. In this review article, we aim to highlight recent and representative studies using the various techniques available: anatomical MRI, quantitative MRI (relaxometry, diffusion MRI), multiparametric approaches, and functional MRI. Today, protocols use 1.5 or 3T MRI scanners, and specialized methodologies have been put in place for data acquisition and processing to address the methodological challenges specific to this population, such as sensitivity to motion. MR sequences must be adapted to the brains of newborns and infants to obtain relevant good soft‐tissue contrast, given the small size of the cerebral structures and the incomplete maturation of tissues. The use of age‐specific image postprocessing tools is also essential, as signal and contrast differ from the adult brain. Appropriate methodologies then make it possible to explore multiple neurodevelopmental mechanisms in a precise way, and assess changes with age or differences between groups of subjects, particularly through large‐scale projects. Although MRI measurements only indirectly reflect the complex series of dynamic processes observed throughout development at the molecular and cellular levels, this technique can provide information on brain morphology, structural connectivity, microstructural properties of gray and white matter, and on the functional architecture. Finally, MRI measures related to clinical, behavioral, and electrophysiological markers have a key role to play from a diagnostic and prognostic perspective in the implementation of early interventions to avoid long‐term disabilities in children.

          Evidence Level

          2

          Technical Efficacy Stage

          1

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          Most cited references201

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          NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain.

          This paper introduces neurite orientation dispersion and density imaging (NODDI), a practical diffusion MRI technique for estimating the microstructural complexity of dendrites and axons in vivo on clinical MRI scanners. Such indices of neurites relate more directly to and provide more specific markers of brain tissue microstructure than standard indices from diffusion tensor imaging, such as fractional anisotropy (FA). Mapping these indices over the whole brain on clinical scanners presents new opportunities for understanding brain development and disorders. The proposed technique enables such mapping by combining a three-compartment tissue model with a two-shell high-angular-resolution diffusion imaging (HARDI) protocol optimized for clinical feasibility. An index of orientation dispersion is defined to characterize angular variation of neurites. We evaluate the method both in simulation and on a live human brain using a clinical 3T scanner. Results demonstrate that NODDI provides sensible neurite density and orientation dispersion estimates, thereby disentangling two key contributing factors to FA and enabling the analysis of each factor individually. We additionally show that while orientation dispersion can be estimated with just a single HARDI shell, neurite density requires at least two shells and can be estimated more accurately with the optimized two-shell protocol than with alternative two-shell protocols. The optimized protocol takes about 30 min to acquire, making it feasible for inclusion in a typical clinical setting. We further show that sampling fewer orientations in each shell can reduce the acquisition time to just 10 min with minimal impact on the accuracy of the estimates. This demonstrates the feasibility of NODDI even for the most time-sensitive clinical applications, such as neonatal and dementia imaging. Copyright © 2012 Elsevier Inc. All rights reserved.
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            Biology of oligodendrocyte and myelin in the mammalian central nervous system.

            Oligodendrocytes, the myelin-forming cells of the central nervous system (CNS), and astrocytes constitute macroglia. This review deals with the recent progress related to the origin and differentiation of the oligodendrocytes, their relationships to other neural cells, and functional neuroglial interactions under physiological conditions and in demyelinating diseases. One of the problems in studies of the CNS is to find components, i.e., markers, for the identification of the different cells, in intact tissues or cultures. In recent years, specific biochemical, immunological, and molecular markers have been identified. Many components specific to differentiating oligodendrocytes and to myelin are now available to aid their study. Transgenic mice and spontaneous mutants have led to a better understanding of the targets of specific dys- or demyelinating diseases. The best examples are the studies concerning the effects of the mutations affecting the most abundant protein in the central nervous myelin, the proteolipid protein, which lead to dysmyelinating diseases in animals and human (jimpy mutation and Pelizaeus-Merzbacher disease or spastic paraplegia, respectively). Oligodendrocytes, as astrocytes, are able to respond to changes in the cellular and extracellular environment, possibly in relation to a glial network. There is also a remarkable plasticity of the oligodendrocyte lineage, even in the adult with a certain potentiality for myelin repair after experimental demyelination or human diseases.
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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

                Contributors
                jessica.dubois@centraliens.net
                Journal
                J Magn Reson Imaging
                J Magn Reson Imaging
                10.1002/(ISSN)1522-2586
                JMRI
                Journal of Magnetic Resonance Imaging
                John Wiley & Sons, Inc. (Hoboken, USA )
                1053-1807
                1522-2586
                18 May 2020
                May 2021
                : 53
                : 5 ( doiID: 10.1002/jmri.v53.5 )
                : 1318-1343
                Affiliations
                [ 1 ] University of Paris NeuroDiderot, INSERM,Paris France
                [ 2 ] UNIACT, NeuroSpin, CEA; Paris‐Saclay University Gif‐sur‐Yvette France
                [ 3 ] Department of Pediatric Radiology APHP, Robert‐Debré Hospital Paris France
                [ 4 ] Centre for the Developing Brain School of Biomedical Engineering & Imaging Sciences, King's College London London UK
                [ 5 ] Division of Development and Growth, Department of Woman, Child and Adolescent University Hospitals of Geneva Geneva Switzerland
                [ 6 ] Department of Neonatology University Medical Center Utrecht, Utrecht University Utrecht the Netherlands
                Author notes
                [*] [* ]Address reprint requests to: J.D., CEA/SAC/ NeuroSpin, Bât 145, point courrier 156, 91191 Gif‐Sur‐Yvette, France. E‐mail: jessica.dubois@ 123456centraliens.net
                Author information
                https://orcid.org/0000-0003-4865-8111
                Article
                JMRI27192
                10.1002/jmri.27192
                8247362
                32420684
                33f95763-a5d8-49bf-8f14-8e9b66bba71f
                © 2020 The Authors. Journal of Magnetic Resonance Imaging published by Wiley Periodicals, Inc. on behalf of International Society for Magnetic Resonance in Medicine.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 24 April 2020
                : 23 December 2019
                : 24 April 2020
                Page count
                Figures: 12, Tables: 0, Pages: 26, Words: 20533
                Funding
                Funded by: Fondation de France , open-funder-registry 10.13039/501100004431;
                Award ID: Call Neurodevelopment 2012
                Funded by: Fondation Fyssen , open-funder-registry 10.13039/501100003135;
                Award ID: Research grant 2009
                Funded by: Fondation Médisite
                Award ID: Prize for Clinical Research in Neurosciences 2018
                Funded by: IdEx University of Paris
                Award ID: ANR‐18‐IDEX‐0001
                Funded by: Seventh Framework Programme , open-funder-registry 10.13039/100011102;
                Award ID: Human Brain Project 2013
                Categories
                Review Article
                Review Articles
                Custom metadata
                2.0
                May 2021
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.0.2 mode:remove_FC converted:01.07.2021

                Radiology & Imaging
                brain development,newborns,infants,anatomical mri,diffusion mri,quantitative mri,functional mri

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