The proliferative ventricular zone in adult vertebrates: a comparative study using reptiles, birds, and mammals

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Abstract

Although evidence accumulated during the last decades has advanced our understanding of adult neurogenesis in the vertebrate brain, many aspects of this intriguing phenomenon remain controversial. Here we review the organization and cellular composition of the ventricular wall of reptiles, birds, and mammals in an effort to identify differences and commonalities among these vertebrate classes. Three major cell types have been identified in the ventricular zone of reptiles and birds: migrating (Type A) cells, radial glial (Type B) cells, and ependymal (Type E) cells. Cells similar anatomically and functionally to Types A, B, and E have also been described in the ventricular wall of mammals, which contains an additional cell type (Type C) not found in reptiles or birds. The bulk of the evidence points to a role of Type B cells as primary neural precursors (stem cells) in the three classes of living amniotic vertebrates. This finding may have implications for the development of strategies for the possible treatment of human neurological disorders.

Introduction

During embryonic development of the vertebrate brain, the vast majority of cells arise from multipotent stem cells located in the germinal layer of the telencephalic ventricles. The ventricles are formed by the folding of the epithelial ectoderm during the first stages of embryonic development. The cell layer surrounding the ventricles has been termed ventricular zone (VZ) [16]. The VZ consists of a pseudostratified columnar epithelium of proliferating radial cells adjacent to the brain ventricles. These radial cells give rise to almost all the neurons of the brain. The new neurons migrate both radially and tangentially to reach their final destinations. During radial migration, radial glial processes, which extend from the VZ to the pial surface, form a scaffolding used by migrating cells to reach their final destination in the brain parenchyma 18, 30, 38, 67. In contrast, in tangential migration cells disperse without following the radial pathways [62]. The mechanisms responsible for the new neurons’ commitment to one of these two migrating modes remain unknown. Both tangential and radial migration persist in all adult vertebrates for which data are available 23, 50, 73.

Until recently it was generally believed that the VZ disappeared as brain histogenesis came to an end and was transformed into the ependymal layer, which is composed of cells that do not divide 16, 40. However, it is now well established that in all major groups of vertebrates the VZ persists into adulthood albeit with a reduction in volume 1, 4, 65. Moreover, the actively proliferating zones responsible for adult neurogenesis in all vertebrate taxa studied to date are located, with few exceptions, in the VZ 5, 7, 49 (Fig. 1). While in reptiles and birds the area in contact with the ventricle is known as the VZ, in mammals a distinction is made between two regions: (1) the VZ, which is directly in contact with the ventricular lumen; and (2) the subventricular zone (SVZ), adjacent to the VZ, where the proliferating population of cells is found.

We present here a brief review of what is known about the organization and cellular composition of the walls of the lateral ventricles in the three living classes of amniotic vertebrates: reptiles, birds, and mammals. The identity of the primary neural precursors (stem cells) in the adult vertebrate brain is currently a much debated topic 13, 78. The comparative study of this structure might yield important clues about the morphology of the stem cells. These precursors are of interest not only for their role in adult neurogenesis, but also because of their potential use in therapeutic neuronal replacement [45].

Section snippets

Adult neurogenesis in vertebrates

Over the last decades, reports of abundant neurogenesis in all major vertebrate taxa have contributed to the demise of the long-held dogma that the brain is incapable of cell renewal during adulthood 5, 7, 37. In addition to the evidence for adult neurogenesis in a few areas of the mammalian brain 26, 35, 63, numerous studies have documented widespread neurogenesis in non-mammals, such as fish, 15, 69, 82, amphibians [70], reptiles 51, 52, and birds 33, 56, 57, 59, 74. Unfortunately, research

Reptiles

Data on the cellular composition and organization of the VZ in reptiles are available for three species of lizards and one turtle species 51, 52, 64, 65. The lizard VZ has been analyzed at the electron microscopic level using proliferation and immunocytochemical markers. Recently, serial ultrathin sections have also been used to reconstruct the composition and three-dimensional organization of the ventricular wall in the lizard Podarcis hispanica. The VZ ependyma displays regional variation and

Concluding remarks

The evidence reviewed above confirms that the epithelium lining the ventricular walls retains the functional and anatomical characteristics of a VZ in representatives of all major groups of amniotic vertebrates. The fact that ependymal cells (Type E) and neural stem cells (Type B) are present in the same epithelium suggests that neurogenic and ependymal functions can coexist. Our results suggest that these two functions may be segregated among two different kinds of cells within the same

Acknowledgements

This work has been supported by a grant from the Generalitat Valenciana (GV01-229).

References (82)

  • D.A Lim et al.

    Noggin antagonizes BMP signaling to create a niche for adult neurogenesis

    Neuron

    (2000)
  • C López-Garcı́a et al.

    Delayed postnatal neurogenesis in the cerebral cortex of lizards

    Dev. Brain Res.

    (1988)
  • F Nottebohm

    Reassessing the mechanisms and origins of vocal learning in birds

    Trends Neurosci.

    (1991)
  • F Nottebohm et al.

    Neurogenesis and neuronal replacement in adult birds

  • J Parnavelas

    The origin and migration of cortical neuronesNew vistas

    Trends Neurosci.

    (2000)
  • P Peretto et al.

    The subependymal layer in rodentsA site of structural plasticity and cell migration in the adult mammalian brain

    Brain Res. Bull.

    (1999)
  • M.M Pérez-Cañellas et al.

    Postnatal neurogenesis in the telencephalon of turtlesEvidence for nonradial migration of new neurons from distant proliferative ventricular zones to the olfactory bulbs

    Dev. Brain Res.

    (1997)
  • M.M Pérez-Cañellas et al.

    Adult neurogenesis in the telencephalon of a lizardA [3H]thymidine autoradiographic and bromodeoxyuridine immunocytochemical study

    Dev. Brain Res.

    (1996)
  • C Scharff

    Chasing fate and function of new neurons in adult brains

    Curr. Opin. Neurobiol.

    (2000)
  • C Scharff et al.

    Targeted neuronal death affects neuronal replacement and vocal behavior in adult songbirds

    Neuron

    (2000)
  • S Temple et al.

    Stem cells in the adult mammalian central nervous system

    Curr. Opin. Neurobiol.

    (1999)
  • A.D Tramontin et al.

    Seasonal plasticity in the adult brain

    Trends Neurosci.

    (2000)
  • J Altman

    Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb

    J. Comp. Neurol.

    (1969)
  • J Altman et al.

    Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats

    J. Comp. Neurol.

    (1965)
  • A Alvarez-Buylla

    Mechanism of neurogenesis in adult avian brain

    Experientia

    (1990)
  • A Alvarez-Buylla et al.

    Primary neural precursors and intermitotic nuclear migration in the ventricular zone of adult canaries

    J. Neurosci.

    (1998)
  • A Alvarez-Buylla et al.

    A unified hypothesis on the lineage of neural stem cells

    Nat. Rev. Neurosci.

    (2001)
  • A Alvarez-Buylla et al.

    Contribution of neurons born during embryonic juvenile and adult life to the brain of adult canariesRegional specificity and delayed birth of neurons in the song control nuclei

    J. Comp. Neurol.

    (1994)
  • A Alvarez-Buylla et al.

    Neuronal stem cells in the brain of adult vertebrates

    Stem Cells

    (1995)
  • A Alvarez-Buylla et al.

    Migration of young neurons in adult avian brain

    Nature

    (1988)
  • A Alvarez-Buylla et al.

    Mapping of radial glia and of a new cell type in adult canary brain

    J. Neurosci.

    (1988)
  • A Barnea et al.

    Recruitment and replacement of hippocampal neurons in young and adult chickadeesAn addition to the theory of hippocampal learning

    Proc. Natl. Acad. Sci. USA

    (1996)
  • A Barnea et al.

    Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees

    Proc. Natl. Acad. Sci. USA

    (1994)
  • S.A Bayer et al.

    Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life

    Science

    (1982)
  • C.S Birse et al.

    Neural increase in various areas of the nervous system of the guppy, Lebistes

    J. Comp. Neurol.

    (1980)
  • Embryonic vertebrate central nervous systemRevised terminology

    Anat. Rec.

    (1970)
  • G Chanas-Sacre et al.

    Radial glia phenotypeOrigin, regulation, and transdifferentiation

    J. Neurosci. Res.

    (2000)
  • V.K Chetverukhin et al.

    Ultrastructural radioautographic analysis of neurogenesis in the hypothalamus of the adult frog, Rana temporaria, with special reference to physiological regeneration of the preoptic nucleus. I. Ventricular zone cell proliferation

    Cell Tissue Res.

    (1993)
  • B.J Chiasson et al.

    Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics

    J. Neurosci.

    (1999)
  • J.C Conover et al.

    Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone

    Nat. Neurosci.

    (2000)
  • F Doetsch et al.

    Network of tangential pathways for neuronal migration in adult mammalian brain

    Proc. Natl. Acad. Sci. USA

    (1996)
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