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Random convergence of olfactory inputs in the Drosophila mushroom body

Nature volume 497, pages 113–117 (2013)Cite this article

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Abstract

The mushroom body in the fruitfly Drosophila melanogaster is an associative brain centre that translates odour representations into learned behavioural responses1. Kenyon cells, the intrinsic neurons of the mushroom body, integrate input from olfactory glomeruli to encode odours as sparse distributed patterns of neural activity2,3. We have developed anatomic tracing techniques to identify the glomerular origin of the inputs that converge onto 200 individual Kenyon cells. Here we show that each Kenyon cell integrates input from a different and apparently random combination of glomeruli. The glomerular inputs to individual Kenyon cells show no discernible organization with respect to their odour tuning, anatomic features or developmental origins. Moreover, different classes of Kenyon cells do not seem to preferentially integrate inputs from specific combinations of glomeruli. This organization of glomerular connections to the mushroom body could allow the fly to contextualize novel sensory experiences, a feature consistent with the role of this brain centre in mediating learned olfactory associations and behaviours.

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Figure 1: Dye electroporation labels the PN connected to a KC claw.
Figure 2: Dye labelling identifies functional connections between PNs and KCs.
Figure 3: The connectivity matrix between AL glomeruli and KCs.
Figure 4: KCs do not receive structured input.

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Acknowledgements

We thank C. Bargmann, T. Jessell, F. Maderspacher, L. Paninski and members of the Axel laboratory for comments on the manuscript; C. Franqui for assistance with fly work; and P. Kisloff, M. Gutierrez and A. Nemes for assistance with general laboratory concerns and the preparation of this manuscript. This work was funded in part by a grant from the Foundation for the National Institutes of Health through the Grand Challenges in Global Health Initiative (R.A.). Further financial support was provided by the Howard Hughes Medical Institute (R.A.), by the Swartz and Gatsby Foundations (L.F.A.) and by the Pew Charitable Trusts, McKnight Foundation, and New York Stem Cell Foundation (V.R.).

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Authors and Affiliations

  1. Department of Neuroscience, College of Physicians and Surgeons, Columbia University, New York, 10032, New York, USA

    Sophie J. C. Caron, L. F. Abbott & Richard Axel

  2. Laboratory of Neurophysiology and Behavior, The Rockefeller University, New York, 10065, New York, USA

    Vanessa Ruta

  3. Department of Physiology and Cellular Biophysics, College of Physicians and Surgeons, Columbia University, New York, 10032, New York, USA

    L. F. Abbott

  4. Department of Biochemistry and Molecular Biophysics, College of Physicians and Surgeons, Columbia University, New York, 10032, New York, USA

    Richard Axel

  5. Howard Hughes Medical Institute, Columbia University, New York, 10032, New York, USA

    Richard Axel

Authors
  1. Sophie J. C. Caron
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  2. Vanessa Ruta
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  4. Richard Axel
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Contributions

S.J.C.C., V.R., L.F.A. and R.A. planned the research and wrote the paper; S.J.C.C. and V.R. performed the experiments; L.F.A. performed all statistical analyses.

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Correspondence to Richard Axel.

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The authors declare no competing financial interests.

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Caron, S., Ruta, V., Abbott, L. et al. Random convergence of olfactory inputs in the Drosophila mushroom body. Nature 497, 113–117 (2013). https://doi.org/10.1038/nature12063

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