Cited by 153Neurobiology and Insect Physiology ResearchVisual perception and processing mechanismsNeuroscience and Neuropharmacology Research

Neural Basis for Looming Size and Velocity Encoding in the Drosophila Giant Fiber Escape Pathway

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Ache, Jan M., Polsky, Jason, Alghailani, Shada, Parekh, Ruchi, Breads, Patrick, Peek, Martin Y., Bock, Davi D., von Reyn, Catherine R. +1 more·2019·Current Biology

Abstract

Identified neuron classes in vertebrate cortical [1-4] and subcortical [5-8] areas and invertebrate peripheral [9-11] and central [12-14] brain neuropils encode specific visual features of a panorama. How downstream neurons integrate these features to control vital behaviors, like escape, is unclear [15]. In Drosophila, the timing of a single spike in the giant fiber (GF) descending neuron [16-18] determines whether a fly uses a short or long takeoff when escaping a looming predator [13]. We previously proposed that GF spike timing results from summation of two visual features whose detection is highly conserved across animals [19]: an object's subtended angular size and its angular velocity [5-8, 11, 20, 21]. We attributed velocity encoding to input from lobula columnar type 4 (LC4) visual projection neurons, but the size-encoding source remained unknown. Here, we show that lobula plate/lobula columnar, type 2 (LPLC2) visual projection neurons anatomically specialized to detect looming [22] provide the entire GF size component. We find LPLC2 neurons to be necessary for GF-mediated escape and show that LPLC2 and LC4 synapse directly onto the GF via reconstruction in a fly brain electron microscopy (EM) volume [23]. LPLC2 silencing eliminates the size component of the GF looming response in patch-clamp recordings, leaving only the velocity component. A model summing a linear function of angular velocity (provided by LC4) and a Gaussian function of angular size (provided by LPLC2) replicates GF looming response dynamics and predicts the peak response time. We thus present an identified circuit in which information from looming feature-detecting neurons is combined by a common post-synaptic target to determine behavioral output.

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Crossref · 10.1016/j.cub.2019.01.079

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  • Model LPLC2 was driven by large female sizes.

    “other model LC units, such as LPLC2, were driven by large female sizes, consistent with its known response to looming stimuli17,24,25,31.”
  • The results were consistent with previous studies, such as LC11 encoding the position of a small moving spot and LPLC2 encoding loom.

    “Our results were consistent with previous studies, such as LC11 encoding the position of a small moving spot27,28 (Fig. 3g, LC11 has highest R2 for ‘position’ in ‘vary female position’ than in other stimulus sequences) and LPLC2 encoding loom24 (Fig. 3g, LPLC2 has highest R2 for ‘size’ in ‘vary female size’).”
  • LC types involved in non-social behaviours (LC4, LC6, LPLC1 and LPLC2) participate in encoding the movements of the female and driving the courtship actions of the male.

    “Even LC types involved in non-social behaviours (for example, escape), such as LC4, LC6, LPLC1 and LPLC221,24,26,38–40, participate in encoding the movements of the female and driving the courtship actions of the male.”
  • For behaviours that rely on quick and robust processing, such as escape from a predator, the arrangement of LC types into optic glomeruli may facilitate the fast readout of specific channels.

    “for behaviours that rely on quick and robust processing, such as escape from a predator, the arrangement of LC types into optic glomeruli may facilitate the fast readout of specific channels24.”

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Authors
Ache, J. M., Polsky, J., Alghailani, S., Parekh, R., Breads, P., Peek, M. Y., Bock, D. D., von Reyn, C. R., & Card, G. M.
Affiliations
  • Howard Hughes Medical Institute (US)
  • University of Vermont (US)
Corresponding author
Card, Gwyneth M.
Venue
Current Biology
Publisher
Elsevier BV
Published
2019-03
Volume
29
Issue
6
Pages
1073-1081.e4
ISSN
0960-9822 (ISSN-L)
OpenAlex
W2919639595
Cited by
153
References
50
Citations by year
2026: 18 · 2025: 25 · 2024: 25 · 2023: 25 · 2022: 22 · 2021: 9 · 2020: 20 · 2019: 9
FWCI
7.19
Type
journal article
Language
en
Open access
Locations
  • Current Biology (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
Howard Hughes Medical Institute
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
giant fiber, Drosophila, neural circuits, behavioral decision making
MeSH terms
Animals, Brain, Drosophila melanogaster, Escape Reaction, Female, Neurons, Visual Perception

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