Letter | Published:

Plasticity-driven individualization of olfactory coding in mushroom body output neurons

Nature volume 526, pages 258262 (08 October 2015) | Download Citation

Abstract

Although all sensory circuits ascend to higher brain areas where stimuli are represented in sparse, stimulus-specific activity patterns, relatively little is known about sensory coding on the descending side of neural circuits, as a network converges. In insects, mushroom bodies have been an important model system for studying sparse coding in the olfactory system1,2,3, where this format is important for accurate memory formation4,5,6. In Drosophila, it has recently been shown that the 2,000 Kenyon cells of the mushroom body converge onto a population of only 34 mushroom body output neurons (MBONs), which fall into 21 anatomically distinct cell types7,8. Here we provide the first, to our knowledge, comprehensive view of olfactory representations at the fourth layer of the circuit, where we find a clear transition in the principles of sensory coding. We show that MBON tuning curves are highly correlated with one another. This is in sharp contrast to the process of progressive decorrelation of tuning in the earlier layers of the circuit2,9. Instead, at the population level, odour representations are reformatted so that positive and negative correlations arise between representations of different odours. At the single-cell level, we show that uniquely identifiable MBONs display profoundly different tuning across different animals, but that tuning of the same neuron across the two hemispheres of an individual fly was nearly identical. Thus, individualized coordination of tuning arises at this level of the olfactory circuit. Furthermore, we find that this individualization is an active process that requires a learning-related gene, rutabaga. Ultimately, neural circuits have to flexibly map highly stimulus-specific information in sparse layers onto a limited number of different motor outputs. The reformatting of sensory representations we observe here may mark the beginning of this sensory-motor transition in the olfactory system.

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Acknowledgements

We would like to thank V. Jayaraman, J. Dubnau and K. Ito for fly strains. We are grateful to H. Kazama, W. Li and J. Dubnau for helpful advice, and to V. Jayaraman, G. Otazu and the members of the Turner laboratory for valuable comments on the manuscript. This work was supported by NIH grant R01 DC010403-01A1 to G.C.T.; T.H. was partially supported by a Postdoctoral Fellowship for Research Abroad from Japan Society for the Promotion of Science and a Postdoctoral Fellowship from the Uehara Memorial Foundation.

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Author notes

    • Toshihide Hige

    Present address: Janelia Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA

Affiliations

  1. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, USA

    • Toshihide Hige
    •  & Glenn C. Turner
  2. Janelia Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA

    • Yoshinori Aso
    •  & Gerald M. Rubin

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Contributions

T.H. and G.C.T. designed the experiments with help from Y.A. and G.M.R.; T.H. performed all imaging and electrophysiology experiments and data analyses. Y.A. and G.M.R created fly strains and collected anatomical data for MBONs. T.H. and G.C.T. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Glenn C. Turner.

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https://doi.org/10.1038/nature15396

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