Cited by 17Neurobiology and Insect Physiology ResearchVisual perception and processing mechanismsNeuroscience and Neuropharmacology Research

Multilevel visual motion opponency in Drosophila

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Ammer, Georg, Serbe-Kamp, Etienne, Mauss, Alex S., Richter, Florian G., Fendl, Sandra, Borst, Alexander·2023·Nature Neuroscience

Abstract

Inhibitory interactions between opponent neuronal pathways constitute a common circuit motif across brain areas and species. However, in most cases, synaptic wiring and biophysical, cellular and network mechanisms generating opponency are unknown. Here, we combine optogenetics, voltage and calcium imaging, connectomics, electrophysiology and modeling to reveal multilevel opponent inhibition in the fly visual system. We uncover a circuit architecture in which a single cell type implements direction-selective, motion-opponent inhibition at all three network levels. This inhibition, mediated by GluClα receptors, is balanced with excitation in strength, despite tenfold fewer synapses. The different opponent network levels constitute a nested, hierarchical structure operating at increasing spatiotemporal scales. Electrophysiology and modeling suggest that distributing this computation over consecutive network levels counteracts a reduction in gain, which would result from integrating large opposing conductances at a single instance. We propose that this neural architecture provides resilience to noise while enabling high selectivity for relevant sensory information.

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  • Inhibition can be shunting rather than subtractive in some fly neurons, and the conductance of an inhibitory synapse can be ten times higher than that of an excitatory synapse.

    “For example, inhibition can be shunting rather than subtractive in some fly neurons100, and the conductance of an inhibitory synapse can be ten times higher than that of an excitatory synapse101.”

    From Neuronal wiring diagram of an adult brain (2024) · cites this paper as [101]

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Research works printed but not linked: 2

  1. [4]Shepherd, G. M. in The Synaptic Organization of the Brain (ed. Shepherd, G. M.) 1–38 (Oxford Univ. Press, 2004).
  2. [41]Koch, C. Biophysics of Computation: Information Processing in Single Neurons (Oxford Univ. Press, 2004).

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Authors
Ammer, G., Serbe-Kamp, E., Mauss, A. S., Richter, F. G., Fendl, S., & Borst, A.
Affiliations
Max Planck Institute for Biological Intelligence (DE)
Corresponding author
Ammer, Georg
Venue
Nature Neuroscience
Published
2023-10-02
Volume
26
Issue
11
Pages
1894-1905
ISSN
  • 1097-6256 (ISSN-L)
  • 1546-1726
OpenAlex
W4387252283
Cited by
17
References
59
Citations by year
2026: 7 · 2025: 4 · 2024: 5 · 2023: 1
FWCI
2.06
Type
journal article
Language
en
Open access
Locations
  • Nature Neuroscience (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
Max-Planck-Gesellschaft
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
visual motion processing, direction selectivity, Drosophila visual system, inhibitory interneurons, noise robustness
MeSH terms
Animals, Drosophila, Motion Perception, Neurons, Synapses, Visual Pathways

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