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Interhemispheric asymmetry of olfactory input-dependent neuronal specification in the adult brain

Nature Neuroscience volume 16, pages 884–888 (2013)Cite this article

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Abstract

The vertebrate brain is anatomically and functionally asymmetric. The left and right cerebral hemispheres harbor neural stem cell niches at the ventricular-subventricular zone (V-SVZ) of the ventricular walls, where new neurons are continuously generated throughout life. However, any interhemispheric asymmetry of neural stem cell niches remains unclear. We performed gene-trap screens in adult zebrafish to identify genes that are differentially expressed in the two hemispheres and found that adult-born neurons expressing the neural zinc-finger protein Myt1 exist predominantly in the left V-SVZ. This lateralization could be reversed by left olfactory sensory deprivation–induced inactivation of Notch signaling. The olfactory behavioral preference for attractive amino acids was also impaired by sensory deprivation of the left olfactory system, but not of the right olfactory system. Our findings suggest that olfactory input generates interhemispheric differences in the fate of adult-born neurons in the zebrafish brain.

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Figure 1: Age-dependent asymmetric GFP expression in new neurons in the olfactory system of SAGFF31B fish.
Figure 2: A functional asymmetry of neurons between the olfactory bulbs.
Figure 3: Alteration of the asymmetry in the distribution of a subpopulation of V-SVZ–RMS cells after olfactory deprivation.
Figure 4: Characterization of the SAGFF31B insertion.
Figure 5: Notch-mediated asymmetric Myt1 expression in the V-SVZ.
Figure 6: Neuronal activity in the habenula is reduced by the left olfactory deprivation.

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Change history

  • 11 June 2013

    In the version of this article initially published online, two images, a figure legend and an Online Methods heading were incorrect. In Figure 3a, the Left Occlusion panel was a mirror image of the Control panel. In Figure 5a, the Control panel was a mirror image of Figure 1e, center panel. (All quantitative analyses were performed on the correct images, so these errors do not affect the conclusions of the article.) Figure 6c was described as retrograde labeling from the olfactory bulb; it shows anterograde labeling from the left olfactory bulb. And an Online Methods section was entitled “Labeling of habenular efferent projections”; the correct title is “Anterograde DiI labeling from the olfactory bulb.” The errors have been corrected for the print, PDF and HTML versions of this article.

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Acknowledgements

We thank T. Seki (Tokyo Medical University) for the antibody to PSA-NCAM, U. Strähle (Karlsruhe Institute of Technology) for the Tg(neurog1:gfp) fish, A. Alvarez-Buylla and Y. Yoshihara for helpful comments on the manuscript, and members of the Sawamoto laboratory for discussions. This work was supported by the Funding Program for Next Generation World-Leading Researchers from the Japan Society for the Promotion of Science (LS104 to K.S.), the National BioResource Project (K.K.), a Grant-in-Aid for Scientific Research (C) (20509005 to N.K.) and a Grant-in-Aid for Scientific Research (A) (23241063 to K.K.) from the Ministry of Education, Culture, Sports, Science and Technology.

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Authors and Affiliations

  1. Department of Developmental and Regenerative Biology, Nagoya City University Graduate School of Medical Sciences, Nagoya, Japan

    Norihito Kishimoto & Kazunobu Sawamoto

  2. Division of Molecular and Developmental Biology, and Department of Genetics, National Institute of Genetics, Graduate University for Advanced Studies (SOKENDAI), Mishima, Shizuoka, Japan

    Kazuhide Asakawa & Koichi Kawakami

  3. Université de Toulouse, UPS, Centre de Biologie du Développement, Toulouse, France

    Romain Madelaine & Patrick Blader

  4. Centre National de la Recherche Scientifique, Centre de Biologie du Développement, UMR 5547, Toulouse, France

    Romain Madelaine & Patrick Blader

Authors
  1. Norihito Kishimoto
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  2. Kazuhide Asakawa
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  3. Romain Madelaine
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  4. Patrick Blader
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  5. Koichi Kawakami
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  6. Kazunobu Sawamoto
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Contributions

N.K. collected most of the data. N.K. and K.S. wrote the manuscript. K.A., R.M., P.B. and K.K. generated transgenic fish.

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Correspondence to Kazunobu Sawamoto.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–6 (PDF 2987 kb)

Supplementary Movie 1

GFP-expressing cells migrate toward the olfactory bulb in the adult SAGFF31B brain. Time-lapse video imaging of the GFP+ cells moving in the RMS, recorded at 15-minute intervals for 20 hours. GFP+ cells migrated toward the olfactory bulb at 35 ± 3 μm/h (n=30 cells from 3 animals, P<0.001). (AVI 1044 kb)

Supplementary Movie 2

The attraction response to amino acids of adult wild-type zebrafish. (AVI 4919 kb)

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Kishimoto, N., Asakawa, K., Madelaine, R. et al. Interhemispheric asymmetry of olfactory input-dependent neuronal specification in the adult brain. Nat Neurosci 16, 884–888 (2013). https://doi.org/10.1038/nn.3409

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