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The Journal of Neuroscience, September 30, 2009, 29(39):12343-12354; doi:10.1523/JNEUROSCI.6108-08.2009

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Development/Plasticity/Repair
Novel Subtype-Specific Genes Identify Distinct Subpopulations of Callosal Projection Neurons

Bradley J. Molyneaux, ^* Paola Arlotta, ^* Ryann M. Fame,  Jessica L. MacDonald,  Kyle L. MacQuarrie, and Jeffrey D. Macklis

Massachusetts General Hospital–Harvard Medical School Center for Nervous System Repair, Departments of Neurosurgery and Neurology, and Program in Neuroscience, Harvard Medical School, Nayef Al-Rodhan Laboratories, Massachusetts General Hospital, and Department of Stem Cell and Regenerative Biology, and Harvard Stem Cell Institute, Harvard University, Boston, Massachusetts 02114

Correspondence should be addressed to Jeffrey Macklis, Massachusetts General Hospital–Harvard Medical School Center for Nervous System Repair, Edwards Research Building, EDR-410, 50 Blossom Street, Boston, MA 02114. Email: jeffrey_macklis{at}hms.harvard.edu

Little is known about the molecular development and heterogeneity of callosal projection neurons (CPN), cortical commissural neurons that connect homotopic regions of the two cerebral hemispheres via the corpus callosum and that are critical for bilateral integration of cortical information. Here we report on the identification of a series of genes that individually and in combination define CPN and novel CPN subpopulations during embryonic and postnatal development. We used in situ hybridization analysis, immunocytochemistry, and retrograde labeling to define the layer-specific and neuron-type-specific distribution of these newly identified CPN genes across different stages of maturation. We demonstrate that a subset of these genes (e.g., Hspb3 and Lpl) appear specific to all CPN (in layers II/III and V–VI), whereas others (e.g., Nectin-3, Plexin-D1, and Dkk3) discriminate between CPN of the deep layers and those of the upper layers. Furthermore, the data show that several genes finely subdivide CPN within individual layers and appear to label CPN subpopulations that have not been described previously using anatomical or morphological criteria. The genes identified here likely reflect the existence of distinct programs of gene expression governing the development, maturation, and function of the newly identified subpopulations of CPN. Together, these data define the first set of genes that identify and molecularly subcategorize distinct populations of callosal projection neurons, often located in distinct subdivisions of the canonical cortical laminae.

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Received Dec. 22, 2008; revised July 27, 2009; accepted Aug. 22, 2009.

Correspondence should be addressed to Jeffrey Macklis, Massachusetts General Hospital–Harvard Medical School Center for Nervous System Repair, Edwards Research Building, EDR-410, 50 Blossom Street, Boston, MA 02114. Email: jeffrey_macklis{at}hms.harvard.edu

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