Ultra-selective looming detection from radial motion opponency
Open accessAbstract
Nervous systems combine lower-level sensory signals to detect higher-order stimulus features critical to survival, such as the visual looming motion created by an imminent collision or approaching predator. Looming-sensitive neurons have been identified in diverse animal species. Different large-scale visual features such as looming often share local cues, which means loom-detecting neurons face the challenge of rejecting confounding stimuli. Here we report the discovery of an ultra-selective looming detecting neuron, lobula plate/lobula columnar, type II (LPLC2) in Drosophila, and show how its selectivity is established by radial motion opponency. In the fly visual system, directionally selective small-field neurons called T4 and T5 form a spatial map in the lobula plate, where they each terminate in one of four retinotopic layers, such that each layer responds to motion in a different cardinal direction. Single-cell anatomical analysis reveals that each arm of the LPLC2 cross-shaped primary dendrites ramifies in one of these layers and extends along that layer's preferred motion direction. In vivo calcium imaging demonstrates that, as their shape predicts, individual LPLC2 neurons respond strongly to outward motion emanating from the centre of the neuron's receptive field. Each dendritic arm also receives local inhibitory inputs directionally selective for inward motion opposing the excitation. This radial motion opponency generates a balance of excitation and inhibition that makes LPLC2 non-responsive to related patterns of motion such as contraction, wide-field rotation or luminance change. As a population, LPLC2 neurons densely cover visual space and terminate onto the giant fibre descending neurons, which drive the jump muscle motor neuron to trigger an escape take off. Our findings provide a mechanistic description of the selective feature detection that flies use to discern and escape looming threats.
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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.”
From Mapping model units to visual neurons reveals population code for social behaviour (2024) · cites this paper as [25]
LPLC2 neurons respond to a looming object and synapse onto the giant fibre neuron to drive an escape take-off.
“LPLC2 neurons respond to a looming object and synapse onto the giant fibre neuron to drive an escape take-off25.”
From Mapping model units to visual neurons reveals population code for social behaviour (2024) · cites this paper as [25]
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Independent optical excitation of distinct neural populations
Klapoetke, N. C., Murata, Y., Kim, S. S., Pulver, S. R., Birdsey-Benson, A., Cho, Y. K., Morimoto, T. K., Chuong, A. S., Carpenter, E. J., Tian, Z., et al. (2014) · Nature Methods · doi:10.1038/nmeth.2836 · Cited by 2,344 · see citing works
Self-citationA GAL4-Driver Line Resource for Drosophila Neurobiology
Jenett, A., Rubin, G. M., Ngo, T.-T. B., Shepherd, D., Murphy, C., Dionne, H., Pfeiffer, B. D., Cavallaro, A., Hall, D., Jeter, J., et al. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.09.011 · Cited by 1,449 · see citing works
Self-citationA visual motion detection circuit suggested by Drosophila connectomics
Takemura, S.-Y., Bharioke, A., Lu, Z., Nern, A., Vitaladevuni, S., Rivlin, P. K., Katz, W. T., Olbris, D. J., Plaza, S. M., Winston, P., et al. (2013) · Nature · doi:10.1038/nature12450 · Cited by 686 · see citing works
Self-citationNern, A., Pfeiffer, B. D., & Rubin, G. M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1506763112 · Cited by 584 · see citing works
Self-citationNeural circuits underlying visually evoked escapes in larval zebrafish
Dunn, T. W., Gebhardt, C., Naumann, E. A., Riegler, C., Ahrens, M. B., Engert, F., & Del Bene, F. (2016) · Neuron · doi:10.1016/j.neuron.2015.12.021 · Cited by 347 · see citing works
A neural command circuit for grooming movement control
Hampel, S., Franconville, R., Simpson, J. H., & Seeds, A. M. (2015) · eLife · doi:10.7554/elife.08758 · Cited by 177 · see citing works
Feature Integration Drives Probabilistic Behavior in the Drosophila Escape Response
von Reyn, C. R., Nern, A., Williamson, W. R., Breads, P., Wu, M., Namiki, S., & Card, G. M. (2017) · Neuron · doi:10.1016/j.neuron.2017.05.036 · Cited by 156 · see citing works
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Flagged first, then by citations
Research works printed but not linked: 36
- [1]Barlow HB Summation and inhibition in the frog’s retina. The Journal of physiology 119, 69– 88 (1953). 13035718 PMC1393035
- [2]Lettvin JY, Maturana HR, McCulloch WS & Pitts WH What the frog’s eye tells the frog’s brain. Proceedings of the IRE 47, 1940– 1951 (1959).
- [3]Hubel DH & Wiesel TN Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. The Journal of physiology 160, 106– 154 (1962). 14449617 PMC1359523
- [4]Gibson JJ Visually controlled locomotion and visual orientation in animals. British journal of psychology 49, 182– 194 (1958). 13572790
- [5]O’Shea M & Williams J The anatomy and output connection of a locust visual interneurone; the lobular giant movement detector (LGMD) neurone. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 91, 257– 266 (1974).
- [6]Wang Y & Frost BJ Time to collision is signalled by neurons in the nucleus rotundus of pigeons. Nature 356, 236– 238, doi: 10.1038/356236a0 (1992). 1552942 · DOI
- [7]de Vries SE & Clandinin TR Loom-sensitive neurons link computation to action in the Drosophila visual system. Current biology: CB 22, 353– 362, doi: 10.1016/j.cub.2012.01.007 (2012). 22305754 PMC3298569 · DOI
- [9]Peek MY & Card GM Comparative approaches to escape. Current opinion in neurobiology 41, 167– 173, doi: 10.1016/j.conb.2016.09.012 (2016). 27710794 · DOI
- [10]Wu M Visual projection neurons in the Drosophila lobula link feature detection to distinct behavioral programs. eLife 5, doi: 10.7554/eLife.21022 (2016). PMC5293491 28029094 · DOI · Paper page
- [11]Maisak MS A directional tuning map of Drosophila elementary motion detectors. Nature 500, 212– 216, doi: 10.1038/nature12320 (2013). 23925246 · DOI · Paper page
- [14]von Reyn CR A spike-timing mechanism for action selection. Nature neuroscience 17, 962– 970, doi: 10.1038/nn.3741 (2014). 24908103 · DOI · Paper page
- [17]Schilling T & Borst A Local motion detectors are required for the computation of expansion flow-fields. Biology open 4, 1105– 1108, doi: 10.1242/bio.012690 (2015). 26231626 PMC4582123 · DOI
- [18]Seelig JD Two-photon calcium imaging from head-fixed Drosophila during optomotor walking behavior. Nature methods 7, 535– 540, doi: 10.1038/nmeth.1468 (2010). 20526346 PMC2945246 · DOI
- [19]Chen TW Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295– 300, doi: 10.1038/nature12354 (2013). 23868258 PMC3777791 · DOI · Paper page
- [20]Strother JA The Emergence of Directional Selectivity in the Visual Motion Pathway of Drosophila. Neuron 94, 168– 182 e110, doi: 10.1016/j.neuron.2017.03.010 (2017). 28384470 · DOI
- [21]Mauss AS Neural Circuit to Integrate Opposing Motions in the Visual Field. Cell 162, 351– 362, doi: 10.1016/j.cell.2015.06.035 (2015). 26186189 · DOI
- [22]Fraser Rowell CH, O’Shea M & Williams JL The neuronal basis of a sensory analyser, the acridid movement detector system. IV. The preference for small field stimuli. The Journal of experimental biology 68, 157– 185 (1977). 894184
- [23]Ishikane H, Kawana A & Tachibana M Short- and long-range synchronous activities in dimming detectors of the frog retina. Visual neuroscience 16, 1001– 1014 (1999). 10614583
- [24]Munch TA Approach sensitivity in the retina processed by a multifunctional neural circuit. Nature neuroscience 12, 1308– 1316, doi: 10.1038/nn.2389 (2009). 19734895 · DOI
- [25]Gabbiani F, Krapp HG, Koch C & Laurent G Multiplicative computation in a visual neuron sensitive to looming. Nature 420, 320– 324, doi: 10.1038/nature01190 (2002). 12447440 · DOI
- [26]Peron S & Gabbiani F Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron. Nature neuroscience 12, 318– 326, doi: 10.1038/nn.2259 (2009). 19198607 PMC2662764 · DOI
- [27]Jones PW & Gabbiani F Synchronized neural input shapes stimulus selectivity in a collision-detecting neuron. Current biology: CB 20, 2052– 2057, doi: 10.1016/j.cub.2010.10.025 (2010). 21055939 PMC2998055 · DOI
- [28]Woolsey TA & Van der Loos H The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain research 17, 205– 242 (1970). 4904874
- [31]Kvon EZ Genome-scale functional characterization of Drosophila developmental enhancers in vivo. Nature 512, 91– 95, doi: 10.1038/nature13395 (2014). 24896182 · DOI
- [32]Pfeiffer BD Refinement of tools for targeted gene expression in Drosophila. Genetics 186, 735– 755, doi: 10.1534/genetics.110.119917 (2010). 20697123 PMC2942869 · DOI · Paper page
- [34]Aso Y The neuronal architecture of the mushroom body provides a logic for associative learning. eLife 3, e04577, doi: 10.7554/eLife.04577 (2014). PMC4273437 25535793 · DOI · Paper page
- [35]Wagh DA Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49, 833– 844, doi: 10.1016/j.neuron.2006.02.008 (2006). 16543132 · DOI · Paper page
- [36]Iwai Y Axon patterning requires DN-cadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS. Neuron 19, 77– 89 (1997). 9247265
- [37]Peng H, Ruan Z, Long F, Simpson JH & Myers EW V3D enables real-time 3D visualization and quantitative analysis of large-scale biological image data sets. Nature biotechnology 28, 348– 353, doi: 10.1038/nbt.1612 (2010). PMC2857929 20231818 · DOI · Paper page
- [38]Wan Y, Otsuna H, Chien CB & Hansen C FluoRender: An Application of 2D Image Space Methods for 3D and 4D Confocal Microscopy Data Visualization in Neurobiology Research. IEEE Pacific Visualization Symposium: [proceedings]. IEEE Pacific Visualisation Symposium, 201– 208 (2012). PMC3622106 23584131
- [39]Strother JA, Nern A & Reiser MB Direct observation of ON and OFF pathways in the Drosophila visual system. Current biology: CB 24, 976– 983, doi: 10.1016/j.cub.2014.03.017 (2014). 24704075 · DOI · Paper page
- [40]Franceschini N & Kirschfeld K Les phénomènes de pseudopupille dans l’oeil composé deDrosophila. Kybernetik 9, 159– 182 (1971). 5134358
- [41]Pologruto TA, Sabatini BL & Svoboda K ScanImage: flexible software for operating laser scanning microscopes. Biomedical engineering online 2, 13, doi: 10.1186/1475-925X-2-13 (2003). 12801419 PMC161784 · DOI
- [42]Wilson RI, Turner GC & Laurent G Transformation of olfactory representations in the Drosophila antennal lobe. Science 303, 366– 370, doi: 10.1126/science.1090782 (2004). 14684826 · DOI
- [43]Gabbiani F, Krapp HG & Laurent G Computation of object approach by a wide-field, motion-sensitive neuron. The Journal of neuroscience: the official journal of the Society for Neuroscience 19, 1122– 1141 (1999). 9920674 PMC6782150
- [44]Schneider CA, Rasband WS & Eliceiri KW NIH Image to ImageJ: 25 years of image analysis. Nature methods 9, 671– 675 (2012). 22930834 PMC5554542
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- Authors
- Klapoetke, N. C., Nern, A., Peek, M. Y., Rogers, E. M., Breads, P., Rubin, G. M., Reiser, M. B., & Card, G. M.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Reiser, Michael B.
- Card, Gwyneth M.
- ORCID
- Venue
- Nature
- Published
- 2017-11-09
- Volume
- 551
- Issue
- 7679
- Pages
- 237-241
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC7457385
- OpenAlex
- W2767680158
- Cited by
- 173
- References
- 7
- Citations by year
- 2026: 16 · 2025: 22 · 2024: 36 · 2023: 16 · 2022: 20 · 2021: 14 · 2020: 23 · 2019: 11 · 2018: 14 · 2014: 1
- FWCI
- 6.43
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- 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
- looming detection, directionally selective neurons, lobula plate, dendritic morphology, excitation-inhibition balance, calcium imaging
- MeSH terms
- Animals, Calcium, Dendrites, Drosophila melanogaster, Female, Motion Perception, Motor Neurons, Neural Inhibition, Single-Cell Analysis
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