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Structured sampling of olfactory input by the fly mushroom body

View ORCID ProfileZhihao Zheng, Feng Li, Corey Fisher, Iqbal J. Ali, Nadiya Sharifi, Steven Calle-Schuler, Joseph Hsu, Najla Masoodpanah, Lucia Kmecova, Tom Kazimiers, View ORCID ProfileEric Perlman, Matthew Nichols, View ORCID ProfilePeter H. Li, View ORCID ProfileViren Jain, View ORCID ProfileDavi D. Bock
doi: https://doi.org/10.1101/2020.04.17.047167
Zhihao Zheng
1Princeton Neuroscience Institute, Princeton, New Jersey 08544, USA
2Howard Hughes Medical Institute Janelia Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA
3The Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University, Baltimore, MD, USA
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  • ORCID record for Zhihao Zheng
Feng Li
2Howard Hughes Medical Institute Janelia Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA
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Corey Fisher
2Howard Hughes Medical Institute Janelia Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA
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Iqbal J. Ali
2Howard Hughes Medical Institute Janelia Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA
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Nadiya Sharifi
2Howard Hughes Medical Institute Janelia Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA
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Steven Calle-Schuler
2Howard Hughes Medical Institute Janelia Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA
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Joseph Hsu
2Howard Hughes Medical Institute Janelia Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA
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Najla Masoodpanah
2Howard Hughes Medical Institute Janelia Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA
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Lucia Kmecova
2Howard Hughes Medical Institute Janelia Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA
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Tom Kazimiers
2Howard Hughes Medical Institute Janelia Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA
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Eric Perlman
2Howard Hughes Medical Institute Janelia Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA
4Yikes LLC, Baltimore, MD, USA
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Matthew Nichols
2Howard Hughes Medical Institute Janelia Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA
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Peter H. Li
5Google Research, Mountain View, CA, USA
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Viren Jain
5Google Research, Mountain View, CA, USA
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Davi D. Bock
2Howard Hughes Medical Institute Janelia Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA
6Department of Neurological Sciences, University of Vermont, Burlington, VT, USA
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  • For correspondence: dbock@uvm.edu
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Abstract

Associative memory formation and recall in the adult fruit fly Drosophila melanogaster is subserved by the mushroom body (MB). Upon arrival in the MB, sensory information undergoes a profound transformation. Olfactory projection neurons (PNs), the main MB input, exhibit broadly tuned, sustained, and stereotyped responses to odorants; in contrast, their postsynaptic targets in the MB, the Kenyon cells (KCs), are nonstereotyped, narrowly tuned, and only briefly responsive to odorants. Theory and experiment have suggested that this transformation is implemented by random connectivity between KCs and PNs. However, this hypothesis has been challenging to test, given the difficulty of mapping synaptic connections between large numbers of neurons to achieve a unified view of neuronal network structure. Here we used a recent whole-brain electron microscopy (EM) volume of the adult fruit fly to map large numbers of PN- to-KC connections at synaptic resolution. Comparison of the observed connectome to precisely defined null models revealed unexpected network structure, in which a subset of food-responsive PN types converge on individual downstream KCs more frequently than expected. The connectivity bias is consistent with the neurogeometry: axons of the overconvergent PNs tend to arborize near one another in the MB main calyx, making local KC dendrites more likely to receive input from those types. Computational modeling of the observed PN-to-KC network showed that input from the overconvergent PN types is better discriminated than input from other types. These results suggest an ‘associative fovea’ for olfaction, in that the MB is wired to better discriminate more frequently occurring and ethologically relevant combinations of food-related odors.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • corrected author affiliation & added orcid IDs

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted April 21, 2020.
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Structured sampling of olfactory input by the fly mushroom body
Zhihao Zheng, Feng Li, Corey Fisher, Iqbal J. Ali, Nadiya Sharifi, Steven Calle-Schuler, Joseph Hsu, Najla Masoodpanah, Lucia Kmecova, Tom Kazimiers, Eric Perlman, Matthew Nichols, Peter H. Li, Viren Jain, Davi D. Bock
bioRxiv 2020.04.17.047167; doi: https://doi.org/10.1101/2020.04.17.047167
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Structured sampling of olfactory input by the fly mushroom body
Zhihao Zheng, Feng Li, Corey Fisher, Iqbal J. Ali, Nadiya Sharifi, Steven Calle-Schuler, Joseph Hsu, Najla Masoodpanah, Lucia Kmecova, Tom Kazimiers, Eric Perlman, Matthew Nichols, Peter H. Li, Viren Jain, Davi D. Bock
bioRxiv 2020.04.17.047167; doi: https://doi.org/10.1101/2020.04.17.047167

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