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The Journal of Neuroscience, June 27, 2007, 27(26):6878-6891; doi:10.1523/JNEUROSCI.0254-07.2007

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Development/Plasticity/Repair
A Subpopulation of Olfactory Bulb GABAergic Interneurons Is Derived from Emx1- and Dlx5/6-Expressing Progenitors

Minoree Kohwi,^1 * Magdalena A. Petryniak,^2 * Jason E. Long,³ Marc Ekker,⁴ Kunihiko Obata,⁵ Yuchio Yanagawa,⁶ John L. R. Rubenstein,³ and Arturo Alvarez-Buylla¹

¹Department of Neurosurgery and Developmental and Stem Cell Biology Program, University of California at San Francisco, San Francisco, California 94143, ²Department of Pediatrics, University of California at San Francisco, San Francisco, California 94143-0748, ³Nina Ireland Laboratory of Developmental Neurobiology, Department of Psychiatry, University of California at San Francisco, San Francisco, California 94158-2611, ⁴Department of Biology, University of Ottawa, Ottawa, Ontario, Canada K1N 6N5, ⁵Obata Research Unit, RIKEN Brain Science Institute, Wako 351-0198, Japan, and ⁶Department of Genetic and Behavioral Neuroscience, Gunma University Graduate School of Medicine and Solution-Oriented Research for Science and Technology, Japan Science and Technology Agency, Maebashi 371-8511, Japan

Correspondence should be addressed to either of the following: John L. R. Rubenstein, Nina Ireland Laboratory of Developmental Neurobiology, Department of Psychiatry, University of California at San Francisco, San Francisco, CA 94158-2611, Email: john.rubenstein{at}ucsf.edu; or Arturo Alvarez-Buylla, Department of Neurosurgery and Developmental and Stem Cell Biology Program, University of California at San Francisco, San Francisco, CA 94143, Email: abuylla{at}stemcell.ucsf.edu

The subventricular zone (SVZ) of the postnatal brain continuously generates olfactory bulb (OB) interneurons. We show that calretinin⁺, calbindin⁺, and dopaminergic (TH⁺) periglomerular OB interneurons correspond to distinct subtypes of GABAergic cells; all were produced in the postnatal mouse brain, but they matured and were eliminated at different rates. The embryonic lateral ganglionic eminence (LGE) is thought to be the site of origin of postnatal SVZ neural progenitors. Consistently, grafts of the embryonic LGE into the adult brain SVZ generated many OB interneurons, including TH⁺ and calbindin⁺ periglomerular interneurons. However, calretinin⁺ cells were not produced from these LGE grafts. Surprisingly, pallial and septal embryonic progenitors transplanted into the adult brain SVZ also resulted in the generation of OB interneurons, including calretinin⁺ cells. A subset of Dlx2⁺ OB interneurons was derived from cells expressing Emx1, a transcription factor largely restricted to the pallium during development. Emx1 lineage-derived cells contributed a substantial portion of GABAergic cells in the OB, including calretinin⁺ interneurons. This is in contrast to cortex, in which Emx1 lineage-derived cells do not differentiate into GABAergic neurons. Our results suggest that some OB interneurons are derived from progenitors outside the LGE and that precursors expressing what has classically been considered a pallial transcription factor generate GABAergic interneurons.

Key words: pallial; Dlx2; Emx1; SVZ; GABAergic neuron; neurogenesis; olfactory bulb

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Received Jan. 19, 2007; revised May 17, 2007; accepted May 19, 2007.

Correspondence should be addressed to either of the following: John L. R. Rubenstein, Nina Ireland Laboratory of Developmental Neurobiology, Department of Psychiatry, University of California at San Francisco, San Francisco, CA 94158-2611, Email: john.rubenstein{at}ucsf.edu; or Arturo Alvarez-Buylla, Department of Neurosurgery and Developmental and Stem Cell Biology Program, University of California at San Francisco, San Francisco, CA 94143, Email: abuylla{at}stemcell.ucsf.edu

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