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      Distinct developmental growth patterns account for the disproportionate expansion of the rostral and caudal isocortex in evolution

      research-article
      Frontiers in Human Neuroscience
      Frontiers Media S.A.
      cortex, gradient, neurogenesis, development, evolution

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          Abstract

          In adulthood, the isocortex of several species is characterized by a gradient in neurons per unit of cortical surface area with fewer neurons per unit of cortical surface area in the rostral pole relative to the caudal pole. A gradient in neurogenesis timing predicts differences in neurons across the isocortex: neurons per unit of cortical surface area are fewer rostrally, where neurogenesis duration is short, and higher caudally where neurogenesis duration is longer. How species differences in neurogenesis duration impact cortical progenitor cells across its axis is not known. I estimated progenitor cells per unit of ventricular area across the rostro-caudal axis of the isocortex in cats ( Felis catus) and in dogs ( Canis familiaris) mostly before layers VI-II neurons are generated. I also estimated the ventricular length across the rostro-caudal axis at various stages of development in both species. These two species were chosen because neurogenesis duration in dogs is extended compared with cats. Caudally, cortical progenitors expand more tangentially and in numbers in dogs compared with cats. Rostrally, the cortical proliferative zone expands more tangentially in dogs compared with cats. However, the tangential expansion in the rostral cortical proliferative zone occurs without a concomitant increase in progenitor cell numbers. The tangential expansion of the ventricular surface in the rostral cortex is mediated by a reduction in cell density. These different developmental growth patterns account for the disproportionate expansion of the rostral (i.e., frontal cortex) and caudal cortex (e.g., primary visual cortex) when neurogenesis duration lengthens in evolution.

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          Most cited references63

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          Modeling transformations of neurodevelopmental sequences across mammalian species.

          A general model of neural development is derived to fit 18 mammalian species, including humans, macaques, several rodent species, and six metatherian (marsupial) mammals. The goal of this work is to describe heterochronic changes in brain evolution within its basic developmental allometry, and provide an empirical basis to recognize equivalent maturational states across animals. The empirical data generating the model comprises 271 developmental events, including measures of initial neurogenesis, axon extension, establishment, and refinement of connectivity, as well as later events such as myelin formation, growth of brain volume, and early behavioral milestones, to the third year of human postnatal life. The progress of neural events across species is sufficiently predictable that a single model can be used to predict the timing of all events in all species, with a correlation of modeled values to empirical data of 0.9929. Each species' rate of progress through the event scale, described by a regression equation predicting duration of development in days, is highly correlated with adult brain size. Neural heterochrony can be seen in selective delay of retinogenesis in the cat, associated with greater numbers of rods in its retina, and delay of corticogenesis in all species but rodents and the rabbit, associated with relatively larger cortices in species with delay. Unexpectedly, precocial mammals (those unusually mature at birth) delay the onset of first neurogenesis but then progress rapidly through remaining developmental events.
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            A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution.

            The more than 1000-fold increase in the cortical surface without a comparable increase in its thickness during mammalian evolution is explained in the context of the radial-unit hypothesis of cortical development. According to the proposed model, cortical expansion is the result of changes in proliferation kinetics that increase the number of radial columnar units without changing the number of neurons within each unit significantly. Thus, mutation of a regulatory gene(s) that controls the timing and ratio of symmetric and asymmetric modes of cell divisions in the proliferative zone, coupled with radial constraints in the distribution of migrating neurons, could create an expanded cortical plate with enhanced capacity for establishing new patterns of connectivity that are validated through natural selection.
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              Development of the human cerebral cortex: Boulder Committee revisited.

              In 1970 the Boulder Committee described the basic principles of the development of the CNS, derived from observations on the human embryonic cerebrum. Since then, numerous studies have significantly advanced our knowledge of the timing, sequence and complexity of developmental events, and revealed important inter-species differences. We review current data on the development of the human cerebral cortex and update the classical model of how the structure that makes us human is formed.
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                Author and article information

                Contributors
                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                08 April 2014
                2014
                : 8
                : 190
                Affiliations
                Department of Psychology, Cornell University Ithaca, NY, USA
                Author notes

                Edited by: Chet C. Sherwood, George Washington University, USA

                Reviewed by: Francisco Aboitiz, Pontificia Universidad Catolica de Chile, Chile; Michel A. Hofman, Royal Netherlands Academy of Arts and Sciences, Netherlands

                *Correspondence: Christine J. Charvet, Department of Psychology, Cornell University, 229 Uris Hall, Ithaca, NY 14853, USA e-mail: charvetcj@ 123456gmail.com

                This article was submitted to the journal Frontiers in Human Neuroscience.

                Article
                10.3389/fnhum.2014.00190
                3986531
                24782736
                21a0390c-44e8-43eb-aeda-e3bd02fd92c5
                Copyright © 2014 Charvet.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 26 January 2014
                : 14 March 2014
                Page count
                Figures: 9, Tables: 5, Equations: 0, References: 67, Pages: 11, Words: 8782
                Categories
                Neuroscience
                Original Research Article

                Neurosciences
                cortex,gradient,neurogenesis,development,evolution
                Neurosciences
                cortex, gradient, neurogenesis, development, evolution

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