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First published online 16 February 2005
doi: 10.1242/dev.01698

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Robo2 is required for establishment of a precise glomerular map in the zebrafish olfactory system

Nobuhiko Miyasaka¹, Yuki Sato¹, Sang-Yeob Yeo^2,*, Lara D. Hutson^3,, Chi-Bin Chien³, Hitoshi Okamoto^2,4 and Yoshihiro Yoshihara^1,

¹ Laboratory for Neurobiology of Synapse, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan
² Laboratory for Developmental Gene Regulation, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan
³ Department of Neurobiology and Anatomy, University of Utah Medical Center, Salt Lake City, UT 84132, USA
⁴ Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Corporation (JST), 3-4-5 Nihonbashi, Chuo-ku, Tokyo 103-0027, Japan

Author for correspondence (e-mail: yoshihara{at}brain.riken.go.jp)

Accepted 14 January 2005

Olfactory sensory neurons (OSNs) expressing a given odorant receptor project their axons to specific glomeruli, creating a topographic odor map in the olfactory bulb (OB). The mechanisms underlying axonal pathfinding of OSNs to their precise targets are not fully understood. Here, we demonstrate that Robo2/Slit signaling functions to guide nascent olfactory axons to the OB primordium in zebrafish. robo2 is transiently expressed in the olfactory placode during the initial phase of olfactory axon pathfinding. In the robo2 mutant, astray (ast), early growing olfactory axons misroute ventromedially or posteriorly, and often penetrate into the diencephalon without reaching the OB primordium. Four zebrafish Slit homologs are expressed in regions adjacent to the olfactory axon trajectory, consistent with their role as repulsive ligands for Robo2. Masking of endogenous Slit gradients by ubiquitous misexpression of Slit2 in transgenic fish causes posterior pathfinding errors that resemble the ast phenotype. We also found that the spatial arrangement of glomeruli in OB is perturbed in ast adults, suggesting an essential role for the initial olfactory axon scaffold in determining a topographic glomerular map. These data provide functional evidence for Robo2/Slit signaling in the establishment of olfactory neural circuitry in zebrafish.

Key words: Axon guidance, Pioneer neurons, Glomerulus, Transgenic zebrafish

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