Slow presynaptic mechanisms that mediate adaptation in the olfactory pathway of Drosophila

  1. Carlotta Martelli  Is a corresponding author
  2. André Fiala
  1. University of Konstanz, Germany
  2. Georg-August-Universität Göttingen, Germany

Abstract

The olfactory system encodes odor stimuli as combinatorial activity of populations of neurons whose response depends on stimulus history. How and on which timescales previous stimuli affect these combinatorial representations remains unclear. We use in vivo optical imaging in Drosophila to analyze sensory adaptation at the first synaptic step along the olfactory pathway. We show that calcium signals in the axon terminals of olfactory receptor neurons (ORNs) do not follow the same adaptive properties as the firing activity measured at the antenna. While ORNs calcium responses are sustained on long timescales, calcium signals in the postsynaptic projection neurons (PNs) adapt within tens of seconds. We propose that this slow component of the postsynaptic response is mediated by a slow presynaptic depression of vesicle release and enables the combinatorial population activity of PNs to adjust to the mean and variance of fluctuating odor stimuli.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Carlotta Martelli

    Department of Biology, Neurobiology, University of Konstanz, Konstanz, Germany
    For correspondence
    carlotta.martelli@uni-konstanz.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5663-6580
  2. André Fiala

    Department of Molecular Neurobiology of Behavior, Georg-August-Universität Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

Funding

Alexander von Humboldt-Stiftung (Postdoctoral Fellowship)

  • Carlotta Martelli

Deutsche Forschungsgemeinschaft (SFB 889/B4)

  • André Fiala

University of Konstanz

  • Carlotta Martelli

Zukunftskolleg of the University of Konstanz

  • Carlotta Martelli

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

Copyright

© 2019, Martelli & Fiala

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.

Metrics

  • 2,548
    views
  • 420
    downloads
  • 37
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Carlotta Martelli
  2. André Fiala
(2019)
Slow presynaptic mechanisms that mediate adaptation in the olfactory pathway of Drosophila
eLife 8:e43735.
https://doi.org/10.7554/eLife.43735

Share this article

https://doi.org/10.7554/eLife.43735

Further reading

    1. Neuroscience
    Aneri Soni, Michael J Frank
    Research Article

    How and why is working memory (WM) capacity limited? Traditional cognitive accounts focus either on limitations on the number or items that can be stored (slots models), or loss of precision with increasing load (resource models). Here, we show that a neural network model of prefrontal cortex and basal ganglia can learn to reuse the same prefrontal populations to store multiple items, leading to resource-like constraints within a slot-like system, and inducing a trade-off between quantity and precision of information. Such ‘chunking’ strategies are adapted as a function of reinforcement learning and WM task demands, mimicking human performance and normative models. Moreover, adaptive performance requires a dynamic range of dopaminergic signals to adjust striatal gating policies, providing a new interpretation of WM difficulties in patient populations such as Parkinson’s disease, ADHD, and schizophrenia. These simulations also suggest a computational rather than anatomical limit to WM capacity.

    1. Neuroscience
    Sergio Plaza-Alonso, Nicolas Cano-Astorga ... Lidia Alonso-Nanclares
    Research Article Updated

    The entorhinal cortex (EC) plays a pivotal role in memory function and spatial navigation, connecting the hippocampus with the neocortex. The EC integrates a wide range of cortical and subcortical inputs, but its synaptic organization in the human brain is largely unknown. We used volume electron microscopy to perform a 3D analysis of the microanatomical features of synapses in all layers of the medial EC (MEC) from the human brain. Using this technology, 12,974 synapses were fully 3D reconstructed at the ultrastructural level. The MEC presented a distinct set of synaptic features, differentiating this region from other human cortical areas. Furthermore, ultrastructural synaptic characteristics within the MEC was predominantly similar, although layers I and VI exhibited several synaptic characteristics that were distinct from other layers. The present study constitutes an extensive description of the synaptic characteristics of the neuropil of all layers of the EC, a crucial step to better understand the connectivity of this cortical region, in both health and disease.