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Random convergence of olfactory inputs in the Drosophila mushroom body

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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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References

  1. Heisenberg, M. Mushroom body memoir: from maps to models. Nature Rev. Neurosci. 4, 266–275 (2003)

    Article  CAS  Google Scholar 

  2. Turner, G. C., Bazhenov, M. & Laurent, G. Olfactory representations by Drosophila mushroom body neurons. J. Neurophysiol. 99, 734–746 (2008)

    Article  PubMed  Google Scholar 

  3. Honegger, K. S., Campbell, R. A. & Turner, G. C. Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body. J. Neurosci. 31, 11772–11785 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Wang, J. W., Wong, A. M., Flores, J., Vosshall, L. B. & Axel, R. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112, 271–282 (2003)

    Article  CAS  PubMed  Google Scholar 

  5. Ng, M. et al. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36, 463–474 (2002)

    Article  CAS  PubMed  Google Scholar 

  6. Wong, A. M., Wang, J. W. & Axel, R. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109, 229–241 (2002)

    Article  CAS  PubMed  Google Scholar 

  7. Marin, E. C., Jefferis, G. S., Komiyama, T., Zhu, H. & Luo, L. Representation of the glomerular olfactory map in the Drosophila brain. Cell 109, 243–255 (2002)

    Article  CAS  PubMed  Google Scholar 

  8. de Belle, J. S. & Heisenberg, M. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263, 692–695 (1994)

    Article  ADS  CAS  PubMed  Google Scholar 

  9. Jefferis, G. S. et al. Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128, 1187–1203 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Butcher, N. J., Friedrich, A. B., Lu, Z., Tanimoto, H. & Meinertzhagen, I. A. Different classes of input and output neurons reveal new features in microglomeruli of the adult Drosophila mushroom body calyx. J. Comp. Neurol. 520, 2185–2201 (2012)

    Article  PubMed  Google Scholar 

  11. Leiss, F., Groh, C., Butcher, N. J., Meinertzhagen, I. A. & Tavosanis, G. Synaptic organization in the adult Drosophila mushroom body calyx. J. Comp. Neurol. 517, 808–824 (2009)

    Article  PubMed  Google Scholar 

  12. Yasuyama, K., Meinertzhagen, I. A. & Schurmann, F. W. Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J. Comp. Neurol. 445, 211–226 (2002)

    Article  PubMed  Google Scholar 

  13. Tanaka, N. K., Tanimoto, H. & Ito, K. Neuronal assemblies of the Drosophila mushroom body. J. Comp. Neurol. 508, 711–755 (2008)

    Article  PubMed  Google Scholar 

  14. Séjourné, J. et al. Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila. Nature Neurosci. 14, 903–910 (2011)

    Article  PubMed  Google Scholar 

  15. Aso, Y. et al. The mushroom body of adult Drosophila characterized by GAL4 drivers. J. Neurogenet. 23, 156–172 (2009)

    Article  CAS  PubMed  Google Scholar 

  16. Manoli, D. S. et al. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436, 395–400 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  17. Stockinger, P., Kvitsiani, D., Rotkopf, S., Tirian, L. & Dickson, B. J. Neural circuitry that governs Drosophila male courtship behavior. Cell 121, 795–807 (2005)

    Article  CAS  PubMed  Google Scholar 

  18. Keleman, K. et al. Dopamine neurons modulate pheromone responses in Drosophila courtship learning. Nature 489, 145–149 (2012)

    Article  ADS  CAS  PubMed  Google Scholar 

  19. Gallio, M., Ofstad, T. A., Macpherson, L. J., Wang, J. W. & Zuker, C. S. The coding of temperature in the Drosophila brain. Cell 144, 614–624 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Vosshall, L. B. & Stocker, R. F. Molecular architecture of smell and taste in Drosophila. Annu. Rev. Neurosci. 30, 505–533 (2007)

    Article  CAS  PubMed  Google Scholar 

  21. Hallem, E. A. & Carlson, J. R. Coding of odors by a receptor repertoire. Cell 125, 143–160 (2006)

    Article  CAS  PubMed  Google Scholar 

  22. Yu, H. H. et al. A complete developmental sequence of a Drosophila neuronal lineage as revealed by twin-spot MARCM. PLoS Biol. 8, e1000461 (2010)

    Article  PubMed  PubMed Central  Google Scholar 

  23. Lin, H. H., Lai, J. S., Chin, A. L., Chen, Y. C. & Chiang, A. S. A map of olfactory representation in the Drosophila mushroom body. Cell 128, 1205–1217 (2007)

    Article  CAS  PubMed  Google Scholar 

  24. Murthy, M., Fiete, I. & Laurent, G. Testing odor response stereotypy in the Drosophila mushroom body. Neuron 59, 1009–1023 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Ruta, V. et al. A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature 468, 686–690 (2010)

    Article  ADS  CAS  PubMed  Google Scholar 

  26. Pauli, A. et al. Cell-type-specific TEV protease cleavage reveals cohesin functions in Drosophila neurons. Dev. Cell 14, 239–251 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Connolly, J. B. et al. Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274, 2104–2107 (1996)

    Article  ADS  CAS  PubMed  Google Scholar 

  28. Stocker, R. F., Heimbeck, G., Gendre, N. & de Belle, J. S. Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J. Neurobiol. 32, 443–456 (1997)

    Article  CAS  PubMed  Google Scholar 

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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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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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