Evolutionary origin of Tbr2-expressing precursor cells and the subventricular zone in the developing cortex

Veronica Martinez-Cerdeno, Christopher L. Cunningham, Jasmin Camacho, Janet A. Keiter, Jeanelle Ariza, Matthew Lovern, Stephen C Noctor

Research output: Contribution to journalArticle

25 Citations (Scopus)

Abstract

The subventricular zone (SVZ) is greatly expanded in primates with gyrencephalic cortices and is thought to be absent from vertebrates with three-layered, lissencephalic cortices, such as the turtle. Recent work in rodents has shown that Tbr2-expressing neural precursor cells in the SVZ produce excitatory neurons for each cortical layer in the neocortex. Many excitatory neurons are generated through a two-step process in which Pax6-expressing radial glial cells divide in the VZ to produce Tbr2-expressing intermediate progenitor cells, which divide in the SVZ to produce cortical neurons. We investigated the evolutionary origin of SVZ neural precursor cells in the prenatal cerebral cortex by testing for the presence and distribution of Tbr2-expressing cells in the prenatal cortex of reptilian and avian species. We found that mitotic Tbr2+ cells are present in the prenatal cortex of lizard, turtle, chicken, and dove. Furthermore, Tbr2+ cells are organized into a distinct SVZ in the dorsal ventricular ridge (DVR) of turtle forebrain and in the cortices of chicken and dove. Our results are consistent with the concept that Tbr2+ neural precursor cells were present in the common ancestor of mammals and reptiles. Our data also suggest that the organizing principle guiding the assembly of Tbr2+ cells into an anatomically distinct SVZ, both developmentally and evolutionarily, may be shared across vertebrates. Finally, our results indicate that Tbr2 expression can be used to test for the presence of a distinct SVZ and to define the boundaries of the SVZ in developing cortices.

Original languageEnglish (US)
Pages (from-to)433-447
Number of pages15
JournalJournal of Comparative Neurology
Volume524
Issue number3
DOIs
StatePublished - Feb 15 2016

Fingerprint

Lateral Ventricles
Turtles
Neurons
Vertebrates
Chickens
Ependymoglial Cells
Reptiles
Lizards
Neocortex
Prosencephalon
Cerebral Cortex
Primates
Mammals
Rodentia
Stem Cells

Keywords

  • Cortical neurons
  • Neural precursor cell types
  • Pax6
  • Subventricular zone
  • Tbr2

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Evolutionary origin of Tbr2-expressing precursor cells and the subventricular zone in the developing cortex. / Martinez-Cerdeno, Veronica; Cunningham, Christopher L.; Camacho, Jasmin; Keiter, Janet A.; Ariza, Jeanelle; Lovern, Matthew; Noctor, Stephen C.

In: Journal of Comparative Neurology, Vol. 524, No. 3, 15.02.2016, p. 433-447.

Research output: Contribution to journalArticle

Martinez-Cerdeno, Veronica ; Cunningham, Christopher L. ; Camacho, Jasmin ; Keiter, Janet A. ; Ariza, Jeanelle ; Lovern, Matthew ; Noctor, Stephen C. / Evolutionary origin of Tbr2-expressing precursor cells and the subventricular zone in the developing cortex. In: Journal of Comparative Neurology. 2016 ; Vol. 524, No. 3. pp. 433-447.
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