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The Journal of Neuroscience, December 1, 1999, 19(23):10357-10371
Sequence of Neuron Origin and Neocortical Laminar Fate: Relation to Cell Cycle of Origin in the Developing Murine Cerebral Wall
T. Takahashi1, 2, T. Goto1, 2, S. Miyama1, 2, R. S. Nowakowski3, and V. S. Caviness Jr1 1 Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts 02114, 2 Department of Pediatrics, Keio University School of Medicine, Tokyo 160, Japan, and 3 Department of Neuroscience and Cell Biology, University of Medicine and Dentistry of New Jersey-Robert Wood Johnson Medical School, Piscataway, New Jersey 08854
Neurons destined for each region of the neocortex are known to arise approximately in an "inside-to-outside" sequence from a pseudostratified ventricular epithelium (PVE). This sequence is initiated rostrolaterally and propagates caudomedially. Moreover, independently of location in the PVE, the neuronogenetic sequence in mouse is divisible into 11 cell cycles that occur over a 6 d period. Here we use a novel "birth hour" method that identifies small cohorts of neurons born during a single 2 hr period, i.e., 10-20% of a single cell cycle, which corresponds to ~1.5% of the 6 d neuronogenetic period. This method shows that neurons arising with the same cycle of the 11 cycle sequence in mouse have common laminar fates even if they arise from widely separated positions on the PVE (neurons of fields 1 and 40) and therefore arise at different embryonic times. Even at this high level of temporal resolution, simultaneously arising cells occupy more than one cortical layer, and there is substantial overlap in the distributions of cells arising with successive cycles. We demonstrate additionally that the laminar representation of cells arising with a given cycle is little if at all modified over the early postnatal interval of histogenetic cell death. We infer from these findings that cell cycle is a neuronogenetic counting mechanism and that this counting mechanism is integral to subsequent processes that determine cortical laminar fate.
Key words: neocortical histogenesis; neuronogenesis; pseudostratified ventricular epithelium (PVE); cell cycle; neuronogenetic sequence; transverse neuronogenetic gradient
Copyright © 1999 Society for Neuroscience 0270-6474/99/192310357-15$05.00/0
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