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The Journal of Neuroscience, January 17, 2007, 27(3):657-664; doi:10.1523/JNEUROSCI.2870-06.2007

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Development/Plasticity/Repair
Generation of Distinct Types of Periglomerular Olfactory Bulb Interneurons during Development and in Adult Mice: Implication for Intrinsic Properties of the Subventricular Zone Progenitor Population

Silvia De Marchis,¹ Serena Bovetti,^1,2 * Barbara Carletti,^3 * Yi-Chun Hsieh,² Donatella Garzotto,¹ Paolo Peretto,¹ Aldo Fasolo,¹ Adam C. Puche,² and Ferdinando Rossi³

¹Department of Animal and Human Biology, University of Turin, I-10123 Turin, Italy, ²Department of Anatomy and Neurobiology, University of Maryland School of Medicine, Baltimore, Maryland 21201, and ³Department of Neuroscience, University of Turin, I-10125 Turin, Italy

Correspondence should be addressed to Dr. Silvia De Marchis, Department of Animal and Human Biology, University of Turin, Via Accademia Albertina 13, I-10123 Turin, Italy. Email: silvia.demarchis{at}unito.it

The subventricular zone (SVZ) of the lateral ventricle develops from residual progenitors of the embryonic lateral ganglionic eminence (LGE) and maintains neurogenic activity throughout life. Precursors from LGE/SVZ migrate to the olfactory bulb (OB) where they differentiate into local interneurons, principally in the granule layer and glomerular layer (GL). By in situ dye labeling, we show that neonatal and adult SVZ progenitors differentially contribute to neurochemically distinct types of periglomerular interneurons in the GL. Namely, calbindin-positive periglomerular cells are preferentially generated during early life, whereas calretinin- and tyrosine hydroxylase-expressing neurons are mainly produced at later ages. Furthermore, homochronic/heterochronic transplantation demonstrates that progenitor cells isolated from the LGE or SVZ at different stages (embryonic day 15 and postnatal days 2 and 30) engraft into the SVZ of neonatal or adult mice, migrate to the OB, and differentiate into local interneurons, including granule and periglomerular cells as well as other types of interneurons. The total number of integrated cells and the relative proportion of granule or periglomerular neurons change, according to the donor age, whereas they are weakly influenced by the recipient age. Analysis of the neurochemical phenotypes acquired by transplanted cells in the GL shows that donor cells of different ages also differentiate according to their origin, regardless of the host age. This suggests that progenitor cells at different ontogenetic stages are intrinsically directed toward specific lineages. Neurogenic processes occurring during development and in adult OB are not equivalent and produce different types of periglomerular interneurons as a consequence of intrinsic properties of the SVZ progenitors.

Key words: olfactory bulb; subventricular zone; transplantation; periglomerular cell; specification; neurogenesis

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Received July 6, 2006; revised Nov. 28, 2006; accepted Dec. 4, 2006.

Correspondence should be addressed to Dr. Silvia De Marchis, Department of Animal and Human Biology, University of Turin, Via Accademia Albertina 13, I-10123 Turin, Italy. Email: silvia.demarchis{at}unito.it

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