Cited by 49Neurobiology and Insect Physiology ResearchNeuroscience and Neuropharmacology ResearchVisual perception and processing mechanisms

ON selectivity in the Drosophila visual system is a multisynaptic process involving both glutamatergic and GABAergic inhibition

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Molina-Obando, Sebastian, Vargas-Fique, Juan Felipe, Henning, Miriam, Gür, Burak, Schladt, T Moritz, Akhtar, Junaid, Berger, Thomas K, Silies, Marion·2019·eLife

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.

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  • Within the fly brain, glutamate has largely been observed to be inhibitory.

    “Glutamate can be either excitatory or inhibitory, but within the brain of the fly, it has largely been observed to be inhibitory29,30.”

    From Network statistics of the whole-brain connectome of Drosophila (2024) · cites this paper as [30]

    The Discussion (page unavailable) says glutamatergic inhibition contributes to contrast selectivity in T4 neurons, and the Results describe inhibitory glutamate receptors in the fly visual system. These passages support inhibitory action in a specific visual circuit, but do not establish that glutamate has largely been observed to be inhibitory throughout the fly brain. (LLM, conf=0.86)

    Experimental — accuracy not yet measured
  • In the D. melanogaster central brain, most reported examples for glutamate are of inhibition via GluClAlpha channels.

    “In the D. melanogaster central brain, most reported examples for glutamate are of inhibition via GluClAlpha channels.89,90,91,92,115”

    From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [92]

    The Results section reports that GluClα is the fly’s only glutamate-gated chloride channel and documents its expression in the visual system. The paper supports glutamate-mediated inhibition via GluClα in that system, but it does not establish that most reported examples in the D. melanogaster central brain use this mechanism. The indexed passages provide no page numbers. (LLM, conf=0.85)

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Authors
Molina-Obando, S., Vargas-Fique, J. F., Henning, M., Gür, B., Schladt, T. M., Akhtar, J., Berger, T. K., & Silies, M.
Affiliations
  • Max Planck Society (DE)
  • Department of Molecular Sensory Systems, Center of Advanced European Studies and Research (caesar), Bonn, Germany
  • Johannes Gutenberg University Mainz (DE)
  • Philipps University of Marburg (DE)
Corresponding author
Silies, Marion
Venue
eLife
Published
2019-09-19
Volume
8
ISSN
2050-084X (ISSN-L)
OpenAlex
W2974015364
Cited by
49
References
87
Citations by year
2026: 5 · 2025: 5 · 2024: 11 · 2023: 5 · 2022: 8 · 2021: 7 · 2020: 7 · 2019: 1
FWCI
2.75
Type
journal article
Language
en
Open access
Locations
  • eLife (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
  • GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, other-oa)
Funders
Deutsche Forschungsgemeinschaft (Emmy Noether SI 1991/1-1, SFB889, Project C08)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
Keywords
Drosophila visual system, glutamatergic inhibition, GABAergic inhibition, RDL, sensory coding, pharmacogenetics
MeSH terms
Animals, Drosophila, Interneurons, Models, Neurological, Visual Pathways, Visual Perception, GABA Agents, Excitatory Amino Acid Agents

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