Comparative analysis of the subventricular zone in rat, ferret and macaque: Evidence for an outer subventricular zone in rodents

Veronica Martinez-Cerdeno, Christopher L. Cunningham, Jasmin Camacho, Jared L. Antczak, Anish N. Prakash, Matthew E. Cziep, Anita I. Walker, Stephen C Noctor

Research output: Contribution to journalArticle

112 Citations (Scopus)

Abstract

The mammalian cerebral cortex arises from precursor cells that reside in a proliferative region surrounding the lateral ventricles of the developing brain. Recent work has shown that precursor cells in the subventricular zone (SVZ) provide a major contribution to prenatal cortical neurogenesis, and that the SVZ is significantly thicker in gyrencephalic mammals such as primates than it is in lissencephalic mammals including rodents. Identifying characteristics that are shared by or that distinguish cortical precursor cells across mammalian species will shed light on factors that regulate cortical neurogenesis and may point toward mechanisms that underlie the evolutionary expansion of the neocortex in gyrencephalic mammals. We immunostained sections of the developing cerebral cortex from lissencephalic rats, and from gyrencephalic ferrets and macaques to compare the distribution of precursor cell types in each species. We also performed time-lapse imaging of precursor cells in the developing rat neocortex. We show that the distribution of Pax6+ and Tbr2+ precursor cells is similar in lissencephalic rat and gyrencephalic ferret, and different in the gyrencephalic cortex of macaque. We show that mitotic Pax6+ translocating radial glial cells (tRG) are present in the cerebral cortex of each species during and after neurogenesis, demonstrating that the function of Pax6+ tRG cells is not restricted to neurogenesis. Furthermore, we show that Olig2 expression distinguishes two distinct subtypes of Pax6+ tRG cells. Finally we present a novel method for discriminating the inner and outer SVZ across mammalian species and show that the key cytoarchitectural features and cell types that define the outer SVZ in developing primates are present in the developing rat neocortex. Our data demonstrate that the developing rat cerebral cortex possesses an outer subventricular zone during late stages of cortical neurogenesis and that the developing rodent cortex shares important features with that of primates.

Original languageEnglish (US)
Article numbere30178
JournalPLoS One
Volume7
Issue number1
DOIs
StatePublished - Jan 17 2012

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Ferrets
Lateral Ventricles
ferrets
Macaca
Rats
Rodentia
rodents
Mammals
neurogenesis
Neurogenesis
rats
cerebral cortex
Ependymoglial Cells
neocortex
Cerebral Cortex
Neocortex
neuroglia
cells
Primates
mammals

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Comparative analysis of the subventricular zone in rat, ferret and macaque : Evidence for an outer subventricular zone in rodents. / Martinez-Cerdeno, Veronica; Cunningham, Christopher L.; Camacho, Jasmin; Antczak, Jared L.; Prakash, Anish N.; Cziep, Matthew E.; Walker, Anita I.; Noctor, Stephen C.

In: PLoS One, Vol. 7, No. 1, e30178, 17.01.2012.

Research output: Contribution to journalArticle

Martinez-Cerdeno, Veronica ; Cunningham, Christopher L. ; Camacho, Jasmin ; Antczak, Jared L. ; Prakash, Anish N. ; Cziep, Matthew E. ; Walker, Anita I. ; Noctor, Stephen C. / Comparative analysis of the subventricular zone in rat, ferret and macaque : Evidence for an outer subventricular zone in rodents. In: PLoS One. 2012 ; Vol. 7, No. 1.
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