Migration of neuronal precursors from the telencephalic ventricular zone into the olfactory bulb in adult zebrafish

Authors

  • Norihito Kishimoto,

    1. Department of Developmental and Regenerative Biology, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Japan
    2. Center for Integrated Medical Research, Keio University, 35 Shinanomachi Shinjuku-ku, Tokyo 160-8582, Japan
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  • Clara Alfaro-Cervello,

    1. Laboratorio de Morfología Celular, Centro de Investigación Príncipe Felipe, CIBERNED, 46013 Valencia, Spain
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  • Kohei Shimizu,

    1. Department of Developmental and Regenerative Biology, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Japan
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  • Kazuhide Asakawa,

    1. Division of Molecular and Developmental Biology, National Institute of Genetics, and Department of Genetics, Graduate University for Advanced Studies (SOKENDAI), Mishima, Shizuoka 411-8540, Japan
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  • Akihiro Urasaki,

    1. Division of Molecular and Developmental Biology, National Institute of Genetics, and Department of Genetics, Graduate University for Advanced Studies (SOKENDAI), Mishima, Shizuoka 411-8540, Japan
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  • Shigenori Nonaka,

    1. Laboratory for Spatiotemporal Regulation, National Institute for Basic Biology, Okazaki 444-8585, Japan
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  • Koichi Kawakami,

    1. Division of Molecular and Developmental Biology, National Institute of Genetics, and Department of Genetics, Graduate University for Advanced Studies (SOKENDAI), Mishima, Shizuoka 411-8540, Japan
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  • Jose Manuel Garcia-Verdugo,

    1. Laboratorio de Morfología Celular, Centro de Investigación Príncipe Felipe, CIBERNED, 46013 Valencia, Spain
    2. Laboratorio de Neurobiología Comparada, Instituto Cavanilles, Universidad de Valencia, 46980 Valencia, Spain
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  • Kazunobu Sawamoto

    Corresponding author
    1. Department of Developmental and Regenerative Biology, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Japan
    • Department of Developmental and Regenerative Biology, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Japan
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Abstract

In the brain of adult mammals, neuronal precursors are generated in the subventricular zone in the lateral wall of the lateral ventricles and migrate into the olfactory bulbs (OBs) through a well-studied route called the rostral migratory stream (RMS). Recent studies have revealed that a comparable neural stem cell niche is widely conserved at the ventricular wall of adult vertebrates. However, little is known about the migration route of neuronal precursors in nonmammalian adult brains. Here, we show that, in the adult zebrafish, a cluster of neuronal precursors generated in the telencephalic ventricular zone migrates into the OB via a route equivalent to the mammalian RMS. Unlike the mammalian RMS, these neuronal precursors are not surrounded by glial tubes, although radial glial cells with a single cilium lined the telencephalic ventricular wall, much as in embryonic and neonatal mammals. To observe the migrating neuronal precursors in living brain tissue, we established a brain hemisphere culture using a zebrafish line carrying a GFP transgene driven by the neurogenin1 (ngn1) promoter. In these fish, GFP was observed in the neuronal precursors migrating in the RMS, some of which were aligned with blood vessels. Numerous ngn1:gfp-positive cells were observed migrating tangentially in the RMS-like route medial to the OB. Taken together, our results suggest that the RMS in the adult zebrafish telencephalon is a functional migratory pathway. This is the first evidence for the tangential migration of neuronal precursors in a nonmammalian adult telencephalon. J. Comp. Neurol. 519:3549–3565, 2011. © 2011 Wiley-Liss, Inc.

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