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WIREs Dev Biol
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How is it that some cells become neurons? And how is it that neurons become organized in the spinal cord and brain to allow us to walk and talk, to see, recall events in our lives, feel pain, keep our balance, and think? The cells that are specified to form the brain and spinal cord are originally located on the outside surface of the embryo. They loop inward to form the neural tube in a process called neurulation. Structures that are nearby send signals to the posterior neural tube to form and pattern the spinal cord so that the dorsal side receives sensory input and the ventral side sends motor signals from neurons to muscles. In the brain, stem cells near the center of the neural tube migrate out to form a mantel zone, and a set of dividing cells from the mantle zone migrate further to produce a second set of neurons at the outer surface of the brain. These neurons will form the cerebral cortex, which contains six discrete layers. Each layer has different connections and different functions. WIREs Dev Biol 2017, 6:e215. doi: 10.1002/wdev.215 This article is categorized under: Early Embryonic Development > Gastrulation and Neurulation Early Embryonic Development > Development to the Basic Body Plan
Gastrulation in the chicken embryo as a model for early human development. Cell movements of gastrulation begin very early (6–19 h for chicken and 14–16 days for human). (a) The primitive streak forms in the central portion of the embryo. (b and c) The first cells migrating through the primitive streak migrate underneath the covering layer (epiblast) and become the anterior endoderm and the notochord. The anterior endoderm and notochord instruct the epiblast cells above them to become neural tube rather than skin epidermis (19–23 h/16–21 days). Photographs of RNA accumulation during these stages of development: (a, MIR130B, a micro RNA expressed in the primitive streak; b, ARHGAP8, encodes an enzyme found in the primitive streak and notochord; c, SNX30, encodes a cytoplasmic protein found in the notochord and anterior endoderm) courtesy of the GEISHA database, University of Arizona, Tucson, AZ, URL: http://geisha.arizona.edu.
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‘Birthdays’ of neurons. The neural stem cells are located in the lowest layer of the neural tube, the inside layer, bordering the fluid‐filled lumen, which will become the ventricles. As neurons are generated (‘born’) from the stem cells, they migrate through the already‐existing neurons to join their age‐appropriate peers. In the cerebral cortex in human and mouse (shown), there are six major layers. The connections of some of these nerves are shown in the figure at the right. (Reprinted with permission from Ref . Copyright 2012 Oxford University Press)
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Specification of the dorsal (upper) and ventral (lower) portion of the neural tube. In the trunk of the embryo, the epidermis instructs the uppermost cells at the neural tube to secrete compounds that turn the nearby cells into sensory neurons. These neurons will receive touch, pain, and temperature input from the skin and other peripheral organs. In the lower portion of the neural tube, the notochord secretes proteins that instruct the ventral‐most cells of the neural tube to secrete proteins that instruct the nearby cells to become motor neurons. The motor neurons innervate the muscles. (Reprinted with permission from Ref . Copyright 2001 Macmillan Publishers Ltd.)
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Formation of the first chambers of the chick brain. (a) At about 28 h in the chick (~21 days in human) the neural tube closes in the head. (b) The neural tube begins to expand into the early brain vesicles, forebrain, midbrain, and hindbrain anterior to the spinal cord. By 40 h in chick (~24 days in human) the neural vesicles become further specialized; the forebrain into the telencephalon and diencephalon (which includes the two bulging regions that will become the eyes), the midbrain or mesencephalon, and the hindbrain into the met‐ and myelencephalon. (c) In the human the three primary brain vesicles become similarly subdivided as development continues and become functionally different from each other. Photographs courtesy of Gary Schoenwolf, University of Utah.
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Closing the neural tube demands coordination among nuclear genes, cytoplasmic proteins, and extracellular matrix proteins. (a) The neural plate cells fold as a result of cell shape changes. The nuclei are stained blue; the cytoplasmic contractile proteins are stained red; and the extracellular matrix proteins connecting the cells are stained green. The rod‐like notochord can be readily identified beneath the folding neural plate cells by its round cross‐section. It serves as an anchor, giving a pivot upon which the folding takes place. The clumps of cells to the side of the neural tube and notochord are the somites, which will form structures including the back muscles, dermis of the skin, and the vertebral bones that will surround the neural tube. (b) The moment of neural tube closure. In this part of the embryo, the tips of the neural folds reach out toward each other and form a tube, as the prospective epidermis covers it. Photographs courtesy of Drs. M. Angeles Rabadán and Elisa Martí Gorostiza, Institute of Molecular Biology of Barcelona, Spain.
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Neurulation in the chick embryo. (a–d) Three‐dimensional photographs taken by a scanning electron microscope, which allows one to see individual cells. (a) Cells of the neural plate (NP) elongate, becoming taller than the more lateral cells that are going to become the skin epidermis (SE). (b) The bending of the neural tube (NT) begins. (c) Prospective skin epidermal cells from the sides migrate toward the center of the embryo, causing the neural plate to start forming a NT. (d) The epidermal cells come together over the top of the NT. (e) An over‐view, looking down at a chick embryo (33 h) labeling a gene product (OLFM1 in blue) expressed in the neural plate and tube. The neural tube has started closing, beginning in the head region. Because the embryo develops in a head to tail progression, all phases of neural plate and tube closure can be seen at different axial levels in an embryo of this stage. Labels a–d on this embryo correspond approximately with the neural development shown in panels a–d. (a–d) Courtesy of Dr. Kathryn Tosney, University of Miami, USA, E (OLFM1) courtesy of the GEISHA database, University of Arizona, Tucson, AZ.
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