Feature Integration Drives Probabilistic Behavior in the Drosophila Escape Response
Open accessAbstract
Animals rely on dedicated sensory circuits to extract and encode environmental features. How individual neurons integrate and translate these features into behavioral responses remains a major question. Here, we identify a visual projection neuron type that conveys predator approach information to the Drosophila giant fiber (GF) escape circuit. Genetic removal of this input during looming stimuli reveals that it encodes angular expansion velocity, whereas other input cell type(s) encode angular size. Motor program selection and timing emerge from linear integration of these two features within the GF. Linear integration improves size detection invariance over prior models and appropriately biases motor selection to rapid, GF-mediated escapes during fast looms. Our findings suggest feature integration, and motor control may occur as simultaneous operations within the same neuron and establish the Drosophila escape circuit as a model system in which these computations may be further dissected at the circuit level. VIDEO ABSTRACT.
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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.”
From Mapping model units to visual neurons reveals population code for social behaviour (2024) · cites this paper as [21]
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Syed, D. S., Ravbar, P., & Simpson, J. (2026) · eLife · doi:10.7554/elife.106446 · Cited by 6 · see citing works
McFarland, B. W., Jang, H., Smolin, N., Hina, B. W., Parisi, M. J., Davis, K. C., Mosca, T. J., Godenschwege, T. A., Nern, A., Kurmangaliyev, Y. Z., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.08.20.504653 · Cited by 5 · see citing works
Self-citationGabbiani, F., Preuss, T., & Dewell, R. B. (2023) · Biological cybernetics · doi:10.1007/s00422-023-00961-0 · Cited by 6 · see citing works
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Action selection based on multiple-stimulus aspects in wind-elicited escape behavior of crickets
Sato, N., Shidara, H., & Ogawa, H. (2022) · Heliyon · doi:10.1016/j.heliyon.2022.e08800 · Cited by 6 · see citing works
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Fly visual evolutionary neural network solving large‐scale global optimization
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On analogies in vertebrate and insect visual systems
Tanaka, R., & Portugues, R. (2025) · Nature Reviews Neuroscience · doi:10.1038/s41583-025-00932-3 · Cited by 5 · see citing works
“Similar to tectal neurons, different LC types were found to be selective for visual features such as looming 166,229–232 , small moving objects 97,166,233,234 and oriented bars 235,236 .”
Cognitive control and consciousness in open biological systems
Kriete, A. (2025) · Biosystems · doi:10.1016/j.biosystems.2025.105457 · Cited by 6 · see citing works
Moreno-Sánchez, A., Vasserman, A. N., Jang, H., Hina, B. W., von Reyn, C. R., & Ausborn, J. (2024) · bioRxiv · doi:10.1101/2024.04.24.591016 · Cited by 5 · see citing works
“…VPN information is organized on DN dendrites, we selected five representative DNs demonstrated or predicted to be looming responsive for our analyses: DNp01, DNp02, DNp03, DNp04, and DNp06 (Dombrovski et al., 2023; Jang et al., 2023; Namiki et al., 2018; Peek, 2018; von Reyn et al., 2017, 2017).”
InfluentialMoulin, T. C., Dey, S., Dashi, G., Li, L., Sridhar, V., Safa, T., Berkins, S., Williams, M. J., & Schiöth, H. (2022) · BMC Biology · doi:10.1186/s12915-022-01476-z · Cited by 5 · see citing works
“Current methods measure the flies’ escape reaction by the presentation of a transient shadow or looming stimuli, evoking a jump response, especially in white-eyed flies [11, 12].”
BackgroundMethodShoenhard, H., Jain, R. A., & Granato, M. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111790 · Cited by 5 · see citing works
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“Data from [Von Reyn et al., 2017, Ache et al., 2019]).”
InfluentialA Neuronal Pathway that Commands Deceleration in Drosophila Larval Light-Avoidance
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“Feature integration of these two types in giant fibres appropriately biases rapid escapes from predators (von Reyn et al., 2014, 2017).”
BackgroundShorter-duration escapes driven by Drosophila giant interneurons promote survival during predation
Chai, C. M., Morrow, C. M., Parikh, D. D., von Reyn, C. R., Leonardo, A., & Card, G. (2025) · Proceedings. Biological sciences · doi:10.1098/rspb.2024.1724 · Cited by 4 · see citing works
Self-citationHoney bee foraging behaviour can be influenced by preferencesfor oscillating flowers
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“Interestingly, a different phenomenological model for the membrane potential of the Drosophila giant fibre (GF) in response to looming stimuli has been developed (Ache et al., 2019; von Reyn et al., 2017).”
BackgroundEvidence for Prepulse Inhibition of Visually Evoked Motor Response in Drosophila melanogaster
Schiöth, H. B., Donzelli, L., Arvidsson, N., Williams, M. J., & Moulin, T. C. (2023) · Biology · doi:10.3390/biology12040635 · Cited by 5 · see citing works
“The stereotypic movements of the fly jumping–landing response to looming shadows or lights-off stimuli have been extensively studied [29]; however, more complex behavioral protocols based on this paradigm are still limited in Drosophila.”
Blagburn, J. M. (2019) · bioRxiv · doi:10.1371/journal.pone.0224057 · Cited by 4 · see citing works
Courtship behavior induced by appetitive olfactory memory
Onodera, Y., Ichikawa, R., Terao, K., Tanimoto, H., & Yamagata, N. (2019) · Journal of Neurogenetics · doi:10.1080/01677063.2019.1593978 · Cited by 4 · see citing works
“…2014; Branson, Robie, Bender, Perona, & Dickinson, 2009; Kabra, Robie, RiveraAlba, Branson, & Branson, 2013; Kain et al., 2013; Lihoreau, Clarke, Buhl, Sumpter, & Simpson, 2016; Qiao, Li, Allen, Shirasu-Hiza, & Syed, 2018; Ramdya, et al., 2015; van Breugel & Dickinson, 2014; von Reyn et al., 2017).”
Khakhalin, A. S. (2019) · bioRxiv · doi:10.1101/589887 · Cited by 4 · see citing works
“And yet, while our understanding of looming detection in insects has recently improved (Rind et al., 2016; von Reyn et al., 2017), the mechanisms that underlie collision avoidance in vertebrates are still unclear.”
BackgroundThe Mechanisms of Insect Cognition
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Dynamical modeling of individual sensory reactivity and habituation learning
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“The startle response relies on the giant fiber (GF) and its efferent motor neurons (47), with LC4 and LPLC2 neurons as candidate inputs (48, 49).”
The organization of visual pathways in the Drosophila brainPreprint
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“Recent anatomical studies have revealed this full repertoire 11,16,52,53 , although the response properties and behavioral roles of some VPNs have been characterized in detail and intensively studied in recent years 45,52,54–56 , most remain functionally untested.”
Self-citationPerception of aerodynamical looming stimuli.
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“Indeed, these threat-evoked responses are found in lizards 1 , squirrels 2 , crayfishes 3 , fish 4,5 , Drosophila 6,7 , birds 8,9 , mice 10 and in humans 11,12 .”
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Dewell, R. B., Carroll-Mikhail, T., Eisenbrandt, M. R., Preuss, T., & Gabbiani, F. (2022) · bioRxiv · doi:10.1101/2022.10.26.513903 · Cited by 3
“Interestingly, a different phenomenological model for the membrane potential of the Drosophila giant fiber (GF) in response to looming stimuli has been developed (von Reyn et al. , 2017; Ache et al. , 2019).”
BackgroundAction selection based on multiple-stimulus aspects in the wind-elicited escape behavior of crickets
Sato, N., Shidara, H., & Ogawa, H. (2021) · bioRxiv · doi:10.1101/2021.04.23.441064 · Cited by 3
“Previously, the choice of escape response has been reported to depend on stimulus velocity (Bhattacharyya et al., 2017; von Reyn et al., 2014, 2017).”
BackgroundSerotonin selectively modulates visual responses of object motion detectors in Drosophila
Bertsch, D. J., Castillo, L. M. P., & Frye, M. A. (2025) · bioRxiv · doi:10.1101/2025.03.21.644681 · Cited by 2
“Angular velocity information about an expanding loom and its functional relevance to takeoff behavior has been shown in the looming-sensitive LC4 (74,75).”
- Authors
- von Reyn, C. R., Nern, A., Williamson, W. R., Breads, P., Wu, M., Namiki, S., & Card, G. M.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Card, Gwyneth M.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2017-06
- Volume
- 94
- Issue
- 6
- Pages
- 1190-1204.e6
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2699457337
- Cited by
- 156
- References
- 0
- Citations by year
- 2026: 16 · 2025: 19 · 2024: 29 · 2023: 19 · 2022: 20 · 2021: 8 · 2020: 13 · 2019: 16 · 2018: 15 · 2017: 1
- FWCI
- 6.04
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Japan Society for the Promotion of Science (17H05011)
- 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
- feature integration, giant fiber, looming stimuli, angular size, linear integration, escape behavior
- MeSH terms
- Animals, Behavior, Animal, Brain, Drosophila melanogaster, Escape Reaction, Immunohistochemistry, Neurons, Probability, Visual Perception, Patch-Clamp Techniques, Microscopy, Confocal, Optogenetics
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