Functional and anatomical specificity in a higher olfactory centre

  1. Shahar Frechter  Is a corresponding author
  2. Alexander Shakeel Bates
  3. Sina Tootoonian
  4. Michael-John Dolan
  5. James D Manton
  6. Arian Rokkum Jamasb
  7. Johannes Kohl
  8. Davi Bock
  9. Gregory SXE Jefferis  Is a corresponding author
  1. MRC Laboratory of Molecular Biology, United Kingdom
  2. The Francis Crick Institute, United Kingdom
  3. University of Cambridge, United Kingdom
  4. Janelia Research Campus, Howard Hughes Medical Institute, United States

Abstract

Most sensory systems are organized into parallel neuronal pathways that process distinct aspects of incoming stimuli. In the insect olfactory system, second order projection neurons target both the mushroom body, required for learning, and the lateral horn (LH), proposed to mediate innate olfactory behavior. Mushroom body neurons form a sparse olfactory population code, which is not stereotyped across animals. In contrast, odor coding in the LH remains poorly understood. We combine genetic driver lines, anatomical and functional criteria to show that the Drosophila LH has ~1400 neurons and >165 cell types. Genetically labeled LHNs have stereotyped odor responses across animals and on average respond to three times more odors than single projection neurons. LHNs are better odor categorizers than projection neurons, likely due to stereotyped pooling of related inputs. Our results reveal some of the principles by which a higher processing area can extract innate behavioral significance from sensory stimuli.

Data availability

Digital skeletons for neuronal morphology and summary electrophysiological data have been provided as supplemental zip files. An interactive version of these data is available as online supplement linked from the paper. Full source data and source code are available on GitHub.

Article and author information

Author details

  1. Shahar Frechter

    Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    For correspondence
    frechter@mrc-lmb.cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0431-5849
  2. Alexander Shakeel Bates

    Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1195-0445
  3. Sina Tootoonian

    Neurophysiology of Behaviour Laboratory, The Francis Crick Institute, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Michael-John Dolan

    Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9666-3682
  5. James D Manton

    Neurobiology Divison, MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9260-3156
  6. Arian Rokkum Jamasb

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6727-7579
  7. Johannes Kohl

    Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Davi Bock

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8218-7926
  9. Gregory SXE Jefferis

    Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    For correspondence
    jefferis@mrc-lmb.cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0587-9355

Funding

European Commission (ERC CoG 649111)

  • Shahar Frechter
  • Alexander Shakeel Bates
  • Sina Tootoonian
  • Michael-John Dolan
  • James D Manton
  • Gregory SXE Jefferis

Medical Research Council (U105188491)

  • Shahar Frechter
  • Alexander Shakeel Bates
  • Michael-John Dolan
  • James D Manton
  • Johannes Kohl
  • Gregory SXE Jefferis

Wellcome (203261/Z/16/Z)

  • Arian Rokkum Jamasb
  • Davi Bock
  • Gregory SXE Jefferis

European Commission (ERC StG 211089)

  • Shahar Frechter
  • Alexander Shakeel Bates
  • Sina Tootoonian
  • Michael-John Dolan
  • James D Manton
  • Gregory SXE Jefferis

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Publication history

  1. Received: December 20, 2018
  2. Accepted: April 12, 2019
  3. Accepted Manuscript published: May 21, 2019 (version 1)
  4. Version of Record published: June 5, 2019 (version 2)

Copyright

© 2019, Frechter et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Shahar Frechter
  2. Alexander Shakeel Bates
  3. Sina Tootoonian
  4. Michael-John Dolan
  5. James D Manton
  6. Arian Rokkum Jamasb
  7. Johannes Kohl
  8. Davi Bock
  9. Gregory SXE Jefferis
(2019)
Functional and anatomical specificity in a higher olfactory centre
eLife 8:e44590.
https://doi.org/10.7554/eLife.44590

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