Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations

Nature Neuroscience volume 10, pages 1474–1482 (2007)Cite this article

Abstract

Here we describe several fundamental principles of olfactory processing in the Drosophila melanogaster antennal lobe (the analog of the vertebrate olfactory bulb), through the systematic analysis of input and output spike trains of seven identified glomeruli. Repeated presentations of the same odor elicit more reproducible responses in second-order projection neurons (PNs) than in their presynaptic olfactory receptor neurons (ORNs). PN responses rise and accommodate rapidly, emphasizing odor onset. Furthermore, weak ORN inputs are amplified in the PN layer but strong inputs are not. This nonlinear transformation broadens PN tuning and produces more uniform distances between odor representations in PN coding space. In addition, portions of the odor response profile of a PN are not systematically related to their direct ORN inputs, which probably indicates the presence of lateral connections between glomeruli. Finally, we show that a linear discriminator classifies odors more accurately using PN spike trains than using an equivalent number of ORN spike trains.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Odor responses are more reliable in PNs than in ORNs.
Figure 2: PNs preferentially transmit the rising phase of ORN signals.
Figure 3: ORNs and PNs differ in their odor selectivity.
Figure 4: ORNs and PNs differ in their odor selectivity even at low stimulus intensities.
Figure 5: The rank order of ORN and PN odor preferences is different.
Figure 6: PN odor responses are partly explained by a highly nonlinear transformation of their direct ORN inputs.
Figure 7: Odors are distributed more uniformly in ensemble PN coding space than in ensemble ORN coding space.
Figure 8: Correlations between different glomeruli are similar for ORNs and PNs.
Figure 9: A linear discriminator can classify odors more accurately with responses from multiple PNs than with responses from the same number of ORNs.

Similar content being viewed by others

References

  1. Bargmann, C.I. Comparative chemosensation from receptors to ecology. Nature 444, 295–301 (2006).

    Article  CAS  PubMed  Google Scholar 

  2. Mombaerts, P. Genes and ligands for odorant, vomeronasal and taste receptors. Nat. Rev. Neurosci. 5, 263–278 (2004).

    Article  CAS  PubMed  Google Scholar 

  3. Laissue, P.P. et al. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J. Comp. Neurol. 405, 543–552 (1999).

    Article  CAS  PubMed  Google Scholar 

  4. Hallem, E.A. & Carlson, J.R. The odor coding system of Drosophila. Trends Genet. 20, 453–459 (2004).

    Article  CAS  PubMed  Google Scholar 

  5. Couto, A., Alenius, M. & Dickson, B.J. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15, 1535–1547 (2005).

    Article  CAS  PubMed  Google Scholar 

  6. Fishilevich, E. & Vosshall, L.B. Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15, 1548–1553 (2005).

    Article  CAS  PubMed  Google Scholar 

  7. Stopfer, M. & Laurent, G. Short-term memory in olfactory network dynamics. Nature 402, 664–668 (1999).

    Article  CAS  PubMed  Google Scholar 

  8. Bazhenov, M., Stopfer, M., Sejnowski, T.J. & Laurent, G. Fast odor learning improves reliability of odor responses in the locust antennal lobe. Neuron 46, 483–492 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Derby, C.D. & Ache, B.W. Quality coding of a complex odorant in an invertebrate. J. Neurophysiol. 51, 906–924 (1984).

    Article  CAS  PubMed  Google Scholar 

  10. Mathews, D.F. Response patterns of single neurons in the tortoise olfactory epithelium and olfactory bulb. J. Gen. Physiol. 60, 166–180 (1972).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Duchamp, A. Electrophysiological responses of olfactory bulb interneurons to odor stimuli in the frog. A comparison with receptor cells. Chem. Senses 7, 191–210 (1982).

    Article  CAS  Google Scholar 

  12. 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 

  13. 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 

  14. Wilson, R.I., Turner, G.C. & Laurent, G. Transformation of olfactory representations in the Drosophila antennal lobe. Science 303, 366–370 (2004).

    Article  CAS  PubMed  Google Scholar 

  15. Pologruto, T.A., Yasuda, R. & Svoboda, K. Monitoring neural activity and [Ca2+] with genetically encoded Ca2+ indicators. J. Neurosci. 24, 9572–9579 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Sankaranarayanan, S. & Ryan, T.A. Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nat. Cell Biol. 2, 197–204 (2000).

    Article  CAS  PubMed  Google Scholar 

  17. Shadlen, M.N. & Newsome, W.T. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J. Neurosci. 18, 3870–3896 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kara, P., Reinagel, P. & Reid, R.C. Low response variability in simultaneously recorded retinal, thalamic, and cortical neurons. Neuron 27, 635–646 (2000).

    Article  CAS  PubMed  Google Scholar 

  19. Vogel, A., Hennig, R.M. & Ronacher, B. Increase of neuronal response variability at higher processing levels as revealed by simultaneous recordings. J. Neurophysiol. 93, 3548–3559 (2005).

    Article  CAS  PubMed  Google Scholar 

  20. 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 

  21. de Bruyne, M., Clyne, P.J. & Carlson, J.R. Odor coding in a model olfactory organ: the Drosophila maxillary palp. J. Neurosci. 19, 4520–4532 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. de Bruyne, M., Foster, K. & Carlson, J.R. Odor coding in the Drosophila antenna. Neuron 30, 537–552 (2001).

    Article  CAS  PubMed  Google Scholar 

  23. Budick, S.A. & Dickinson, M.H. Free-flight responses of Drosophila melanogaster to attractive odors. J. Exp. Biol. 209, 3001–3017 (2006).

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  25. Hallem, E.A., Ho, M.G. & Carlson, J.R. The molecular basis of odor coding in the Drosophila antenna. Cell 117, 965–979 (2004).

    Article  CAS  PubMed  Google Scholar 

  26. Olsen, S.R., Bhandawat, V. & Wilson, R.I. Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54, 89–103 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Shang, Y., Claridge-Chang, A., Sjulson, L., Pypaert, M. & Miesenbock, G. Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128, 601–612 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Laughlin, S. A simple coding procedure enhances a neuron's information capacity. Z. Naturforsch. [C] 36, 910–912 (1981).

    Article  CAS  Google Scholar 

  29. Perez-Orive, J. et al. Oscillations and sparsening of odor representations in the mushroom body. Science 297, 359–365 (2002).

    Article  CAS  PubMed  Google Scholar 

  30. 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 

  31. 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 

  32. Tanaka, N.K., Awasaki, T., Shimada, T. & Ito, K. Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr. Biol. 14, 449–457 (2004).

    Article  CAS  PubMed  Google Scholar 

  33. Simoncelli, E.P. Vision and the statistics of the visual environment. Curr. Opin. Neurobiol. 13, 144–149 (2003).

    Article  CAS  PubMed  Google Scholar 

  34. Shadlen, M.N. & Newsome, W.T. Noise, neural codes and cortical organization. Curr. Opin. Neurobiol. 4, 569–579 (1994).

    Article  CAS  PubMed  Google Scholar 

  35. Berry, M.J., Warland, D.K. & Meister, M. The structure and precision of retinal spike trains. Proc. Natl. Acad. Sci. USA 94, 5411–5416 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Alonso, J.M., Usrey, W.M. & Reid, R.C. Rules of connectivity between geniculate cells and simple cells in cat primary visual cortex. J. Neurosci. 21, 4002–4015 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Berry, M.J. II & Meister, M. Refractoriness and neural precision. J. Neurosci. 18, 2200–2211 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Shanbhag, S.R., Muller, B. & Steinbrecht, R.A. Atlas of olfactory organs of Drosophila melanogaster. 1. Types, external organization, innervation, and distribution of olfactory sensilla. Int. J. Insect Morphol. Embryol. 28, 377–397 (1999).

    Article  Google Scholar 

  39. Armstrong-Gold, C.E. & Rieke, F. Bandpass filtering at the rod to second-order cell synapse in salamander (Ambystoma tigrinum) retina. J. Neurosci. 23, 3796–3806 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Stopfer, M., Jayaraman, V. & Laurent, G. Intensity versus identity coding in an olfactory system. Neuron 39, 991–1004 (2003).

    Article  CAS  PubMed  Google Scholar 

  41. Mazor, O. & Laurent, G. Transient dynamics vs. fixed points in odor representations by locust antennal lobe projection neurons. Neuron 48, 661–673 (2005).

    Article  CAS  PubMed  Google Scholar 

  42. Laughlin, S.B., Howard, J. & Blakeslee, B. Synaptic limitations to contrast coding in the retina of the blowfly Calliphora. Proc. R. Soc. Lond. B 231, 437–467 (1987).

    Article  CAS  PubMed  Google Scholar 

  43. Laurent, G. Olfactory network dynamics and the coding of multidimensional signals. Nat. Rev. Neurosci. 3, 884–895 (2002).

    Article  CAS  PubMed  Google Scholar 

  44. Schlief, M.L. & Wilson, R.I. Olfactory processing and behavior downstream from highly selective receptor neurons. Nat. Neurosci. 10, 623–630 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Nozawa, M. & Nei, M. Evolutionary dynamics of olfactory receptor genes in Drosophila species. Proc. Natl. Acad. Sci. USA 104, 7122–7127 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Wilson, R.I. & Laurent, G. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J. Neurosci. 25, 9069–9079 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Wachowiak, M. et al. Inhibition of olfactory receptor neuron input to olfactory bulb glomeruli mediated by suppression of presynaptic calcium influx. J. Neurophysiol. 94, 2700–2712 (2005).

    Article  CAS  PubMed  Google Scholar 

  48. Vinje, W.E. & Gallant, J.L. Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287, 1273–1276 (2000).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank K. Ito, L. Luo, L.B. Vosshall and L.M. Stevens for gifts of fly stocks. We benefited from helpful conversations with S.A. Baccus, V. Jayaraman, H. Kazama, A.W. Liu, J.H.R. Maunsell, O. Mazor, M. Meister, R.C. Reid, H. Sompolinsky, G.C. Turner and Y. Zhou. This work was funded by a grant from the US National Institutes of Health (1R01DC008174-01), a Pew Scholar Award, a McKnight Scholar Award, a Smith Family Foundation New Investigators Award and an Armenise-Harvard Junior Faculty Award (to R.I.W.). S.R.O. is supported by a US National Science Foundation Predoctoral Fellowship. N.W.G. is supported by a Howard Hughes Medical Institute Predoctoral Fellowship. M.L.S. is supported by a National Institutes of Health Postdoctoral Fellowship (1F32DC008741-01A1).

Author information

Author notes

  1. Shawn R Olsen, Nathan W Gouwens and Michelle L Schlief: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, 02115, Massachusetts, USA

    Vikas Bhandawat, Shawn R Olsen, Nathan W Gouwens, Michelle L Schlief & Rachel I Wilson

Authors
  1. Vikas Bhandawat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shawn R Olsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nathan W Gouwens
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michelle L Schlief
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rachel I Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rachel I Wilson.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–6, Tables 1–4 and Methods (PDF 1846 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bhandawat, V., Olsen, S., Gouwens, N. et al. Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations. Nat Neurosci 10, 1474–1482 (2007). https://doi.org/10.1038/nn1976

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1976

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing