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Olfactory processing and behavior downstream from highly selective receptor neurons

Nature Neuroscience volume 10, pages 623–630 (2007)Cite this article

Abstract

In both the vertebrate nose and the insect antenna, most olfactory receptor neurons (ORNs) respond to multiple odors. However, some ORNs respond to just a single odor, or at most to a few highly related odors. It has been hypothesized that narrowly tuned ORNs project to narrowly tuned neurons in the brain, and that these dedicated circuits mediate innate behavioral responses to a particular ligand. Here we have investigated neural activity and behavior downstream from two narrowly tuned ORN types in Drosophila melanogaster. We found that genetically ablating either of these ORN types impairs innate behavioral attraction to their cognate ligand. Neurons in the antennal lobe postsynaptic to one of these ORN types are, like their presynaptic ORNs, narrowly tuned to a pheromone. However, neurons postsynaptic to the second ORN type are broadly tuned. These results demonstrate that some narrowly tuned ORNs project to dedicated central circuits, ensuring a tight connection between stimulus and behavior, whereas others project to central neurons that participate in the ensemble representations of many odors.

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Figure 1: Two narrowly tuned ORN types.
Figure 2: DA1 ORNs are required for behavioral attraction to cis-vaccenyl acetate.
Figure 3: VA6 ORNs are required for behavioral attraction to geranyl acetate.
Figure 4: DA1 projection neurons are narrowly tuned to cis-vaccenyl acetate.
Figure 5: VA6 projection neurons are more broadly tuned to odors than their presynaptic ORNs.
Figure 6: There is a significant transformation of odor tuning in glomerulus VA6, but not in DA1.

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Acknowledgements

We are grateful to L. Vosshall, B. Dickson, L. Stevens and L. Luo for gifts of fly stocks, and to V. Bhandawat for help with single-sensillum recordings. C. Dulac and members of the Wilson lab provided feedback on earlier versions of the manuscript. Funding was provided by a Pew Scholarship in the Biomedical Sciences, a New Investigator Award from the Smith Family Foundation, an Armenise-Harvard Junior Faculty Grant, a Loreen Arbus Scholarship in Neuroscience and a grant from the US National Institutes of Health (RO1 1R01DC008174-01).

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Authors and Affiliations

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

    Michelle L Schlief & Rachel I Wilson

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  1. Michelle L Schlief
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  2. Rachel I Wilson
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Contributions

This study was jointly designed by M.L.S. and R.I.W. The experiments and data analysis were performed by M.L.S., and M.L.S. and R.I.W. jointly wrote the paper.

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Correspondence to Rachel I Wilson.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

In Or67d-Gal4 flies, Gal4 is expressed ectopically in ab5A ORNs. (PDF 398 kb)

Supplementary Fig. 2

VA6 ORNs respond more strongly to geranyl acetate than to other highly related odors. (PDF 156 kb)

Supplementary Table 1 (PDF 90 kb)

Supplementary Methods (PDF 18 kb)

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Schlief, M., Wilson, R. Olfactory processing and behavior downstream from highly selective receptor neurons. Nat Neurosci 10, 623–630 (2007). https://doi.org/10.1038/nn1881

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