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The habenula is crucial for experience-dependent modification of fear responses in zebrafish

Nature Neuroscience volume 13, pages 1354–1356 (2010)Cite this article

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Abstract

The zebrafish dorsal habenula (dHb) shows conspicuous asymmetry in its connection with the interpeduncular nucleus (IPN) and is equivalent to the mammalian medial habenula. Genetic inactivation of the lateral subnucleus of dHb (dHbL) biased fish towards freezing rather than the normal flight response to a conditioned fear stimulus, suggesting that the dHbL-IPN pathway is important for controlling experience-dependent modification of fear responses.

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Figure 1: The habenula-IPN projection pattern and the genetic manipulation of dHbL-d/iIPN transmission.
Figure 2: The dHbL-silenced fish showed enhanced freezing responses to the conditioned stimulus instead of flight behaviors.

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  • 17 October 2010

    In the version of this article initially published online, there was an error on page 2, right column, second paragraph, 14th line. Here, ‘Mtz’ should read ‘metronidazole’. The supplementary material file was also missing some information from the images. Both errors have been corrected for the print, PDF and HTML versions of this article.

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Acknowledgements

We thank Y. Yoshihara, T. Koide and other members of the Yoshihara laboratory for transgenic fish and advice on the behavioral experiments, S. Watanabe for help in setting up the behavioral experiments, N. Copeland for the BAC homologous recombination system, S. Fraser for GAL4VP16 and UAS plasmids, M. Parsons for the UAS:nfsB-mCherry plasmid, A. Thomson for correction of the manuscript and S. Jesuthasan for communication of unpublished data. We are grateful to all of the members of the Okamoto laboratory for support and advice, the Research Resource Center of RIKEN BSI for animal care and the National BioResource Project of Japan for fish strains. This work was supported by Grant-in-Aids from the Ministry of Education, Culture, Sports, Science and Technology of Japan to H.O. and H.A. and by the Core Research for Evolutional Science and Technology of Japan Science and Technology Agency to H.O.

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Author notes

  1. Takayuki Sassa

    Present address: Present address: Laboratory of Biochemistry, Faculty of Pharmaceutical Sciences, Hokkaido University, Higashi, Kita-ku, Sapporo, Japan.,

Authors and Affiliations

  1. RIKEN Brain Science Institute, Wako, Saitama, Japan

    Masakazu Agetsuma, Hidenori Aizawa, Tazu Aoki, Ryoko Nakayama, Mikako Takahoko, Midori Goto, Takayuki Sassa, Ryunosuke Amo, Toshiyuki Shiraki, Toshihiko Hosoya & Hitoshi Okamoto

  2. Research Resource Center, RIKEN Brain Science Institute, Wako, Saitama, Japan

    Ryoko Nakayama, Mikako Takahoko & Toshiyuki Shiraki

  3. Department of Life Science and Medical Bioscience, Graduate School of Advanced Science and Engineering, Waseda University, Shinjuku-ku, Tokyo, Japan

    Ryunosuke Amo

  4. Division of Molecular and Developmental Biology, and Department of Genetics, National Institute of Genetics, the Graduate University for Advanced Studies, Mishima, Shizuoka, Japan

    Koichi Kawakami

  5. National Institutes of Natural Sciences, Okazaki Institute for Integrative Bioscience, National Institute for Physiological Sciences, Okazaki, Aichi, Japan

    Shin-ichi Higashijima

  6. Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, Sanbancho, Chiyoda-ku, Tokyo, Japan

    Hitoshi Okamoto

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  1. Masakazu Agetsuma
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Contributions

M.A., H.A. and H.O. designed the experiments and wrote the manuscript. H.O. supervised the research project. M.A. performed most of the experiments using transgenic fish with T.A., R.N., M.T., T. Sassa, T. Shiraki, K.K., T.H. and S.H. H.A. performed the neural tracing study with M.G., M.T. and R.A.

Corresponding author

Correspondence to Hitoshi Okamoto.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–24, Supplementary Table 1, Supplementary Methods and Supplementary Data (PDF 4168 kb)

Supplementary Movie 1

Response of the control fish at the first trial of the retrieval session. (MOV 494 kb)

Supplementary Movie 2

Response of the dHbl-silenced fish at the first trial of the retrieval session. (MOV 1138 kb)

Supplementary Movie 3

Persistent rotation of the dHbl-silenced fish at the first trial of the retrieval session. (MOV 581 kb)

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Agetsuma, M., Aizawa, H., Aoki, T. et al. The habenula is crucial for experience-dependent modification of fear responses in zebrafish. Nat Neurosci 13, 1354–1356 (2010). https://doi.org/10.1038/nn.2654

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