The wiring diagram of a glomerular olfactory system

  1. Matthew E Berck
  2. Avinash Khandelwal
  3. Lindsey Claus
  4. Luis Hernandez-Nunez
  5. Guangwei Si
  6. Christopher J Tabone
  7. Feng Li
  8. James W Truman
  9. Richard D Fetter
  10. Matthieu Louis
  11. Aravinthan DT Samuel
  12. Albert Cardona  Is a corresponding author
  1. Harvard University, United States
  2. The Barcelona Institute of Science and Technology, Spain
  3. Fly Base, United States
  4. Janelia Research Campus, Howard Hughes Medical Institute, United States

Abstract

The sense of smell enables animals to react to long-distance cues according to learned and innate valences. Here, we have mapped with electron microscopy the complete wiring diagram of the Drosophila larval antennal lobe, an olfactory neuropil similar to the vertebrate olfactory bulb. We found a canonical circuit with uniglomerular projection neurons (uPNs) relaying gain-controlled ORN activity to the mushroom body and the lateral horn. A second, parallel circuit with multiglomerular projection neurons (mPNs) and hierarchically connected local neurons (LNs) selectively integrates multiple ORN signals already at the first synapse. LN-LN synaptic connections putatively implement a bistable gain control mechanism that either computes odor saliency through panglomerular inhibition, or allows some glomeruli to respond to faint aversive odors in the presence of strong appetitive odors. This complete wiring diagram will support experimental and theoretical studies towards bridging the gap between circuits and behavior.

Article and author information

Author details

  1. Matthew E Berck

    Department of Physics and Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Avinash Khandelwal

    EMBL-CRG Systems Biology Program, Centre for Genomic Regulation, The Barcelona Institute of Science and Technology, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Lindsey Claus

    Department of Physics and Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Luis Hernandez-Nunez

    Department of Physics and Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Guangwei Si

    Department of Physics and Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Christopher J Tabone

    Fly Base, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Feng Li

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. James W Truman

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Richard D Fetter

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Matthieu Louis

    EMBL-CRG Systems Biology Program, Centre for Genomic Regulation, The Barcelona Institute of Science and Technology, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  11. Aravinthan DT Samuel

    Department of Physics and Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Albert Cardona

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    cardonaa@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

Publication history

  1. Received: January 30, 2016
  2. Accepted: May 6, 2016
  3. Accepted Manuscript published: May 13, 2016 (version 1)
  4. Version of Record published: July 1, 2016 (version 2)

Copyright

© 2016, Berck 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. Matthew E Berck
  2. Avinash Khandelwal
  3. Lindsey Claus
  4. Luis Hernandez-Nunez
  5. Guangwei Si
  6. Christopher J Tabone
  7. Feng Li
  8. James W Truman
  9. Richard D Fetter
  10. Matthieu Louis
  11. Aravinthan DT Samuel
  12. Albert Cardona
(2016)
The wiring diagram of a glomerular olfactory system
eLife 5:e14859.
https://doi.org/10.7554/eLife.14859
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