ON selectivity in Drosophila vision is a multisynaptic process involving both glutamatergic and GABAergic inhibition

  1. Sebastian Molina-Obando
  2. Juan Felipe Vargas-Fique
  3. Miriam Henning
  4. Burak Gür
  5. T Moritz Schladt
  6. Junaid Akhtar
  7. Thomas K Berger
  8. Marion Silies  Is a corresponding author
  1. Johannes Gutenberg Universität Mainz, Germany
  2. Center of Advanced European Research (Caesar), Germany

Abstract

Sensory systems sequentially extract increasingly complex features. ON and OFF pathways, for example, encode increases or decreases of a stimulus from a common input. This ON/OFF pathway split is thought to occur at individual synaptic connections through a sign-inverting synapse in one of the pathways. Here, we show that ON selectivity is a multisynaptic process in the Drosophila visual system. A pharmacogenetics approach demonstrates that both glutamatergic inhibition through GluClα and GABAergic inhibition through Rdl mediate ON responses. Although neurons postsynaptic to the glutamatergic ON pathway input L1 lose all responses in GluClα mutants, they are resistant to a cell-type-specific loss of GluClα. This shows that ON selectivity is distributed across multiple synapses, and raises the possibility that cell-type-specific manipulations might reveal similar strategies in other sensory systems. Thus, sensory coding is more distributed than predicted by simple circuit motifs, allowing for robust neural processing.

Data availability

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

The following previously published data sets were used

Article and author information

Author details

  1. Sebastian Molina-Obando

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg Universität Mainz, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1222-723X
  2. Juan Felipe Vargas-Fique

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg Universität Mainz, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Miriam Henning

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg Universität Mainz, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Burak Gür

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg Universität Mainz, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8221-9767
  5. T Moritz Schladt

    Center of Advanced European Research (Caesar), Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Junaid Akhtar

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg Universität Mainz, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Thomas K Berger

    Center of Advanced European Research (Caesar), Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Marion Silies

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg Universität Mainz, Mainz, Germany
    For correspondence
    msilies@uni-mainz.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2810-9828

Funding

Deutsche Forschungsgemeinschaft (Emmy Noether SI 1991/1-1)

  • Miriam Henning
  • Burak Gür
  • Junaid Akhtar
  • Marion Silies

Deutsche Forschungsgemeinschaft (SFB889)

  • Sebastian Molina-Obando
  • Juan Felipe Vargas-Fique

Deutsche Forschungsgemeinschaft (Project C08)

  • Sebastian Molina-Obando
  • Juan Felipe Vargas-Fique

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

Copyright

© 2019, Molina-Obando 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.

Metrics

  • 3,873
    views
  • 533
    downloads
  • 35
    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. Sebastian Molina-Obando
  2. Juan Felipe Vargas-Fique
  3. Miriam Henning
  4. Burak Gür
  5. T Moritz Schladt
  6. Junaid Akhtar
  7. Thomas K Berger
  8. Marion Silies
(2019)
ON selectivity in Drosophila vision is a multisynaptic process involving both glutamatergic and GABAergic inhibition
eLife 8:e49373.
https://doi.org/10.7554/eLife.49373

Share this article

https://doi.org/10.7554/eLife.49373

Further reading

    1. Neuroscience
    Lian Hollander-Cohen, Omer Cohen ... Berta Levavi-Sivan
    Research Article

    Life histories of oviparous species dictate high metabolic investment in the process of gonadal development leading to ovulation. In vertebrates, these two distinct processes are controlled by the gonadotropins follicle-stimulating hormone (FSH) and luteinizing hormone (LH), respectively. While it was suggested that a common secretagogue, gonadotropin-releasing hormone (GnRH), oversees both functions, the generation of loss-of-function fish challenged this view. Here, we reveal that the satiety hormone cholecystokinin (CCK) is the primary regulator of this axis in zebrafish. We found that FSH cells express a CCK receptor, and our findings demonstrate that mutating this receptor results in a severe hindrance to ovarian development. Additionally, it causes a complete shutdown of both gonadotropins secretion. Using in-vivo and ex-vivo calcium imaging of gonadotrophs, we show that GnRH predominantly activates LH cells, whereas FSH cells respond to CCK stimulation, designating CCK as the bona fide FSH secretagogue. These findings indicate that the control of gametogenesis in fish was placed under different neural circuits, that are gated by CCK.

    1. Neuroscience
    Mina Mišić, Noah Lee ... Herta Flor
    Research Article

    Chronic back pain (CBP) is a global health concern with significant societal and economic burden. While various predictors of back pain chronicity have been proposed, including demographic and psychosocial factors, neuroimaging studies have pointed to brain characteristics as predictors of CBP. However, large-scale, multisite validation of these predictors is currently lacking. In two independent longitudinal studies, we examined white matter diffusion imaging data and pain characteristics in patients with subacute back pain (SBP) over 6- and 12-month periods. Diffusion data from individuals with CBP and healthy controls (HC) were analyzed for comparison. Whole-brain tract-based spatial statistics analyses revealed that a cluster in the right superior longitudinal fasciculus (SLF) tract had larger fractional anisotropy (FA) values in patients who recovered (SBPr) compared to those with persistent pain (SBPp), and predicted changes in pain severity. The SLF FA values accurately classified patients at baseline and follow-up in a third publicly available dataset (Area under the Receiver Operating Curve ~0.70). Notably, patients who recovered had FA values larger than those of HC suggesting a potential role of SLF integrity in resilience to CBP. Structural connectivity-based models also classified SBPp and SBPr patients from the three data sets (validation accuracy 67%). Our results validate the right SLF as a robust predictor of CBP development, with potential for clinical translation. Cognitive and behavioral processes dependent on the right SLF, such as proprioception and visuospatial attention, should be analyzed in subacute stages as they could prove important for back pain chronicity.