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The Journal of Neuroscience, April 15, 2009, 29(15):4756-4767; doi:10.1523/JNEUROSCI.0118-09.2009

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Cellular/Molecular
From the Olfactory Bulb to Higher Brain Centers: Genetic Visualization of Secondary Olfactory Pathways in Zebrafish

Nobuhiko Miyasaka,¹ Kozo Morimoto,¹ Tatsuya Tsubokawa,³ Shin-ichi Higashijima,⁴ Hitoshi Okamoto,² and Yoshihiro Yoshihara¹

Laboratories for ¹Neurobiology of Synapse and ²Developmental Gene Regulation, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan, ³Department of Biology, Keio University, Yokohama, Kanagawa 223-8521, Japan, and ⁴National Institute of Natural Sciences, Okazaki Institute for Integrative Bioscience, National Institute for Physiological Sciences, Okazaki, Aichi 444-8787, Japan

Correspondence should be addressed to Dr. Yoshihiro Yoshihara, Laboratory for Neurobiology of Synapse, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan. Email: yoshihara{at}brain.riken.jp

In the vertebrate olfactory system, odor information is represented as a topographic map in the olfactory bulb (OB). However, it remains unknown how this odor map is transferred from the OB to higher olfactory centers. Using genetic labeling techniques in zebrafish, we found that the OB output neurons, mitral cells (MCs), are heterogeneous with respect to transgene expression profiles and spatial distributions. Tracing MC axons at single-cell resolution revealed that (1) individual MCs send axons to multiple target regions in the forebrain; (2) MCs innervating the same glomerulus do not necessarily display the same axon trajectory; (3) MCs innervating distinct glomerular clusters tend to project axons to different, but partly overlapping, target regions; (4) MCs innervating the medial glomerular cluster directly and asymmetrically send axons to the right habenula. We propose that the topographic odor map in the OB is not maintained intact, but reorganized in higher olfactory centers. Moreover, our finding of asymmetric bulbo-habenular projection renders the olfactory system an attractive model for the studies of brain asymmetry and lateralized behaviors.

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Received Jan. 9, 2009; revised Feb. 25, 2009; accepted March 9, 2009.

Correspondence should be addressed to Dr. Yoshihiro Yoshihara, Laboratory for Neurobiology of Synapse, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan. Email: yoshihara{at}brain.riken.jp

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