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Research Article

Functional diversity among sensory receptors in a Drosophila olfactory circuit

Dennis Mathew, Carlotta Martelli, Elizabeth Kelley-Swift, Christopher Brusalis, Marc Gershow, Aravinthan D. T. Samuel, Thierry Emonet, and John R. Carlson
PNAS June 4, 2013 110 (23) E2134-E2143; https://doi.org/10.1073/pnas.1306976110
Dennis Mathew
aDepartment of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06511;
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Carlotta Martelli
aDepartment of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06511;
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Elizabeth Kelley-Swift
aDepartment of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06511;
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Christopher Brusalis
aDepartment of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06511;
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Marc Gershow
bDepartment of Physics and Center for Brain Science, Harvard University, Cambridge, MA 02138; and
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Aravinthan D. T. Samuel
bDepartment of Physics and Center for Brain Science, Harvard University, Cambridge, MA 02138; and
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Thierry Emonet
aDepartment of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06511;
cDepartment of Physics, Yale University, New Haven, CT 06511
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John R. Carlson
aDepartment of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06511;
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  • For correspondence: john.carlson@yale.edu
  1. Contributed by John R. Carlson, April 16, 2013 (sent for review March 28, 2013)

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Significance

The coding of olfactory information is based on the activity of odor receptors. The larval olfactory system of Drosophila contains 21 olfactory receptor neurons and a comparable number of odor receptors. Through a screen of >10,000 receptor–odorant combinations, we identify for each of 19 receptors an odorant that excites it strongly. These odorants elicited little cross-activation of other receptors under test conditions. Systematic analysis reveals dramatic diversity in the sensitivity and temporal dynamics of responses to cognate odorants. The odorants elicited diverse behavioral responses. The analysis provides a foundation for elucidating the circuitry that translates receptor responses into behavior.

Abstract

The ability of an animal to detect, discriminate, and respond to odors depends on the function of its olfactory receptor neurons (ORNs), which in turn depends ultimately on odorant receptors. To understand the diverse mechanisms used by an animal in olfactory coding and computation, it is essential to understand the functional diversity of its odor receptors. The larval olfactory system of Drosophila melanogaster contains 21 ORNs and a comparable number of odorant receptors whose properties have been examined in only a limited way. We systematically screened them with a panel of ∼500 odorants, yielding >10,000 receptor–odorant combinations. We identify for each of 19 receptors an odorant that excites it strongly. The responses elicited by each of these odorants are analyzed in detail. The odorants elicited little cross-activation of other receptors at the test concentration; thus, low concentrations of many of these odorants in nature may be signaled by a single ORN. The receptors differed dramatically in sensitivity to their cognate odorants. The responses showed diverse temporal dynamics, with some odorants eliciting supersustained responses. An intriguing question in the field concerns the roles of different ORNs and receptors in driving behavior. We found that the cognate odorants elicited behavioral responses that varied across a broad range. Some odorants elicited strong physiological responses but weak behavioral responses or weak physiological responses but strong behavioral responses.

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: john.carlson{at}yale.edu.
  • Author contributions: D.M. and J.R.C. designed research; D.M., E.K.-S., and C.B. performed research; D.M., C.M., E.K.-S., C.B., M.G., A.D.T.S., T.E., and J.R.C. analyzed data; and D.M. and J.R.C. wrote the paper.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1306976110/-/DCSupplemental.

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Diversity of receptors in an olfactory circuit
Dennis Mathew, Carlotta Martelli, Elizabeth Kelley-Swift, Christopher Brusalis, Marc Gershow, Aravinthan D. T. Samuel, Thierry Emonet, John R. Carlson
Proceedings of the National Academy of Sciences Jun 2013, 110 (23) E2134-E2143; DOI: 10.1073/pnas.1306976110

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Diversity of receptors in an olfactory circuit
Dennis Mathew, Carlotta Martelli, Elizabeth Kelley-Swift, Christopher Brusalis, Marc Gershow, Aravinthan D. T. Samuel, Thierry Emonet, John R. Carlson
Proceedings of the National Academy of Sciences Jun 2013, 110 (23) E2134-E2143; DOI: 10.1073/pnas.1306976110
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