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Cerebral Cortex Advance Access published online on September 2, 2009
Cerebral Cortex, doi:10.1093/cercor/bhp168
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© The Author 2009. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

The Subventricular Zone Is the Developmental Milestone of a 6-Layered Neocortex: Comparisons in Metatherian and Eutherian Mammals

Amanda F. P. Cheung1, Shinichi Kondo1, Omar Abdel-Mannan1, Rebecca A. Chodroff1, Tamara M. Sirey1, Lisa E. Bluy1, Natalie Webber1, Jamin DeProto1, Sarah J. Karlen2, Leah Krubitzer2, Helen B. Stolp1,3, Norman R. Saunders3 and Zoltán Molnár1

1 Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3QX, UK, 2 University of California Davis, Center for Neuroscience, Davis, CA 95618, USA, 3 Department of Pharmacology, University of Melbourne, Parkville VIC 3010, Australia

Address correspondence to Zoltán Molnár, Department of Physiology, Anatomy and Genetics, University of Oxford, Le Gros Clark Building, South Parks Road, Oxford OX1 3QX, UK. Email: zoltan.molnar{at}dpag.ox.ac.uk.

The major lineages of mammals (Eutheria, Metatheria, and Monotremata) diverged more than 100 million years ago and have undergone independent changes in the neocortex. We found that adult South American gray short-tailed opossum (Monodelphis domestica) and tammar wallaby (Macropus eugenii) possess a significantly lower number of cerebral cortical neurons compared with the mouse (Mus musculus). To determine whether the difference is reflected in the development of the cortical germinal zones, the location of progenitor cell divisions was examined in opossum, tammar wallaby, and rat. The basic pattern of the cell divisions was conserved, but the emergence of a distinctive band of dividing cells in the subventricular zone (SVZ) occurred relatively later in the opossum (postnatal day [P14]) and the tammar wallaby (P40) than in rodents. The planes of cell divisions in the ventricular zone (VZ) were similar in all species, with comparable mRNA expression patterns of Brn2, Cux2, NeuroD6, Tbr2, and Pax6 in opossum (P12 and P20) and mouse (embryonic day 15 and P0). In conclusion, the marsupial neurodevelopmental program utilizes an organized SVZ, as indicated by the presence of intermediate (or basal) progenitor cell divisions and gene expression patterns, suggesting that the SVZ emerged prior to the Eutherian–Metatherian split.

Key Words: basal progenitors • cortical neurogenesis • cortical unit column • evolutionary biology of cerebral cortex • intermediate progenitors • Monodelphis domestica

Amanda F. P. Cheung and Shinichi Kondo have contributed equally to this work.


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