The anterior paired lateral neuron normalizes odour-evoked activity in the Drosophila mushroom body calyx

  1. Luigi Prisco
  2. Stephan Hubertus Deimel
  3. Hanna Yeliseyeva
  4. André Fiala
  5. Gaia Tavosanis  Is a corresponding author
  1. German Center for Neurodegenerative Diseases, Germany
  2. University of Göttingen, Germany

Abstract

To identify and memorize discrete but similar environmental inputs, the brain needs to distinguish between subtle differences of activity patterns in defined neuronal populations. The Kenyon cells of the Drosophila adult mushroom body (MB) respond sparsely to complex olfactory input, a property that is thought to support stimuli discrimination in the MB. To understand how this property emerges, we investigated the role of the inhibitory anterior paired lateral neuron (APL) in the input circuit of the MB, the calyx. Within the calyx, presynaptic boutons of projection neurons (PNs) form large synaptic microglomeruli (MGs) with dendrites of postsynaptic Kenyon cells (KCs). Combining EM data analysis and in vivo calcium imaging, we show that APL, via inhibitory and reciprocal synapses targeting both PN boutons and KC dendrites, normalizes odour-evoked representations in MGs of the calyx. APL response scales with the PN input strength and is regionalized around PN input distribution. Our data indicate that the formation of a sparse code by the Kenyon cells requires APL-driven normalization of their MG postsynaptic responses. This work provides experimental insights on how inhibition shapes sensory information representation in a higher brain centre, thereby supporting stimuli discrimination and allowing for efficient associative memory formation.

Data availability

All source data used to generate figures are available at: https://doi.org/10.5061/dryad.bk3j9kdd1

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Luigi Prisco

    Dynamics of neuronal circuits, German Center for Neurodegenerative Diseases, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Stephan Hubertus Deimel

    Department of Molecular Neurobiology of Behavior, University of Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4678-4926
  3. Hanna Yeliseyeva

    Dynamics of neuronal circuits, German Center for Neurodegenerative Diseases, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. André Fiala

    Department of Molecular Neurobiology of Behavior, University of Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9745-5145
  5. Gaia Tavosanis

    Dynamics of neuronal circuits, German Center for Neurodegenerative Diseases, Bonn, Germany
    For correspondence
    Gaia.Tavosanis@dzne.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8679-5515

Funding

Deutsche Forschungsgemeinschaft (FOR 2705)

  • André Fiala
  • Gaia Tavosanis

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

Reviewing Editor

  1. Mani Ramaswami, Trinity College Dublin, Ireland

Version history

  1. Preprint posted: September 22, 2021 (view preprint)
  2. Received: September 23, 2021
  3. Accepted: December 28, 2021
  4. Accepted Manuscript published: December 29, 2021 (version 1)
  5. Version of Record published: January 7, 2022 (version 2)

Copyright

© 2021, Prisco 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. Luigi Prisco
  2. Stephan Hubertus Deimel
  3. Hanna Yeliseyeva
  4. André Fiala
  5. Gaia Tavosanis
(2021)
The anterior paired lateral neuron normalizes odour-evoked activity in the Drosophila mushroom body calyx
eLife 10:e74172.
https://doi.org/10.7554/eLife.74172

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https://doi.org/10.7554/eLife.74172

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