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Cerebral Cortex Advance Access originally published online on January 23, 2009
Cerebral Cortex 2009 19(10):2439-2450; doi:10.1093/cercor/bhn260
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Published by Oxford University Press 2009.

Intermediate Neuronal Progenitors (Basal Progenitors) Produce Pyramidal–Projection Neurons for All Layers of Cerebral Cortex

Tom Kowalczyk1, Adria Pontious1, Chris Englund1, Ray A. M. Daza1, Francesco Bedogni1, Rebecca Hodge1, Alessio Attardo2, Chris Bell1, Wieland B. Huttner2 and Robert F. Hevner1

1 Departments of Neurological Surgery and Pathology, University of Washington and Center for Neuroscience, Seattle Children's Hospital Research Institute, Seattle, WA 98101, USA, 2 Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, D-01307 Dresden, Germany

Address correspondence to Dr Robert Hevner, Seattle Children's Hospital Research Institute, Room 828, 1900 Ninth Avenue, Seattle, WA 98101-1304, USA. Email: rhevner{at}u.washington.edu.

The developing cerebral cortex contains apical and basal types of neurogenic progenitor cells. Here, we investigated the cellular properties and neurogenic output of basal progenitors, also called intermediate neuronal progenitors (INPs). We found that basal mitoses expressing transcription factor Tbr2 (an INP marker) were present throughout corticogenesis, from embryonic day 10.5 through birth. Postnatally, Tbr2+ progenitors were present in the dentate gyrus, subventricular zone (SVZ), and posterior periventricle (pPV). Two morphological subtypes of INPs were distinguished in the embryonic cortex, "short radial" in the ventricular zone (VZ) and multipolar in the SVZ, probably corresponding to molecularly defined INP subtypes. Unexpectedly, many short radial INPs appeared to contact the apical (ventricular) surface and some divided there. Time-lapse video microscopy suggested that apical INP divisions produced daughter INPs. Analysis of neurogenic divisions (Tis21-green fluorescent protein [GFP]+) indicated that INPs may produce the majority of projection neurons for preplate, deep, and superficial layers. Conversely, proliferative INP divisions (Tis21-GFP–) increased from early to middle corticogenesis, concomitant with SVZ growth. Our findings support the hypothesis that regulated amplification of INPs may be an important factor controlling the balance of neurogenesis among different cortical layers.

Key Words: Eomes • intermediate progenitor cells • Pax6 • radial glia • Tbr2

Tom Kowalczyk and Adria Pontious contributed equally to this work


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