Cited by 10Neurobiology and Insect Physiology ResearchVisual perception and processing mechanismsCell Image Analysis Techniques

Identifying Inputs to Visual Projection Neurons in Drosophila Lobula by Analyzing Connectomic Data

Open access
Tanaka (田中涼介), Ryosuke, Clark, Damon A.·2022·eneuro

Published version of a preprint

Abstract

Abstract Electron microscopy-based connectomes provide important insights into how visual circuitry of fruit fly Drosophila computes various visual features, guiding and complementing behavioral and physiological studies. However, connectomic analyses of lobula, a putative center of object-like feature detection, remains underdeveloped, largely because of incomplete data on the inputs to the brain region. Here, we attempted to map the columnar inputs into the Drosophila lobula neuropil by performing connectivity- and morphology-based clustering on a densely reconstructed connectome dataset. While the dataset mostly lacked visual neuropils other than lobula, which would normally help identify inputs to lobula, our clustering analysis successfully extracted clusters of cells with homogeneous connectivity and morphology, likely representing genuine cell types. We were able to draw a correspondence between the resulting clusters and previously identified cell types, revealing previously undocumented connectivity between lobula input and output neurons. While future, more complete connectomic reconstructions are necessary to verify the results presented here, they can serve as a useful basis for formulating hypotheses on mechanisms of visual feature detection in lobula.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1523/eneuro.0053-22.2022

Cites

15 of 15 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • 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 [39]

    The Discussion (page unavailable) says LC6, LPLC1 and LPLC2 are sensitive to looming stimuli, supporting the citation’s characterization of those types as involved in non-social visual processing. The cited passages discuss LC4’s morphology but do not establish its non-social behavioral role or explicitly link these four types to escape. The statement about encoding female movements and driving male courtship appears to be the citing authors’ conclusion, not the part this citation supports. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 55

  1. Agrochao M, Tanaka R, Salazar-Gatzimas E, Clark DA (2020) Mechanism for analogous illusory motion perception in flies and humans. Proc Natl Acad Sci U S A 117: 23044– 23053. 10.1073/pnas.2002937117 32839324 PMC7502748 · DOI
  2. Bausenwein B, Dittrich APM, Fischbach KF (1992) The optic lobe of Drosophila melanogaster - II. Sorting of retinotopic pathways in the medulla. Cell Tissue Res 267: 17– 28. 10.1007/BF00318687 1735111 · DOI
  3. Behnia R, Clark DA, Carter AG, Clandinin TR, Desplan C (2014) Processing properties of ON and OFF pathways for Drosophila motion detection. Nature 512: 427– 430. 10.1038/nature13427 25043016 PMC4243710 · DOI · Paper page
  4. Borst A (2018) A biophysical mechanism for preferred direction enhancement in fly motion vision. PLoS Comput Biol 14: e1006240. 10.1371/journal.pcbi.1006240 29897917 PMC6016951 · DOI
  5. Cheong H, Siwanowicz I, Card GM (2020) Multi-regional circuits underlying visually guided decision-making in Drosophila. Curr Opin Neurobiol 65: 77– 87. 10.1016/j.conb.2020.10.010 33217639 · DOI · Paper page
  6. Clements J, Dolafi T, Umayam L, Neubarth NL, Berg S, Scheffer LK, Plaza SM (2020a) neuPrint: analysis tools for EM connectomics. bioRxiv 2020.01.16.909465. PMC9350508 35935535
  7. Davis FP, Nern A, Picard S, Reiser MB, Rubin GM, Eddy SR, Henry GL (2020) A genetic, genomic, and computational resource for exploring neural circuit function. Elife 9: e50901. 10.7554/eLife.50901 31939737 PMC7034979 · DOI · Paper page
  8. de Andres-Bragado L, Sprecher SG (2019) Mechanisms of vision in the fruit fly. Curr Opin Insect Sci 36: 25– 32. 10.1016/j.cois.2019.06.005 31325739 · DOI
  9. Dorkenwald S, et al. (2021) FlyWire: online community for whole-brain connectomics. Nat Methods 19: 119– 128. 34949809 PMC8903166
  10. Douglass JK, Strausfeld NJ (1998) Functionally and anatomically segregated visual pathways in the lobula complex of a calliphorid fly. J Comp Neurol 396: 84– 104. 10.1002/(SICI)1096-9861(19980622)396:1<84::AID-CNE7>3.0.CO;2-E 9623889 · DOI
  11. Feinberg EH, VanHoven MK, Bendesky A, Wang G, Fetter RD, Shen K, Bargmann CI (2008) GFP reconstitution across synaptic partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 57: 353– 363. 10.1016/j.neuron.2007.11.030 18255029 · DOI
  12. Karuppudurai T, Lin TY, Ting CY, Pursley R, Melnattur KV, Diao F, White BH, Macpherson LJ, Gallio M, Pohida T, Lee CH (2014) A hard-wired glutamatergic circuit pools and relays UV signals to mediate spectral preference in Drosophila. Neuron 81: 603– 615. 10.1016/j.neuron.2013.12.010 24507194 PMC3920195 · DOI · Paper page
  13. Kazama H (2015) Systems neuroscience in Drosophila: conceptual and technical advantages. Neuroscience 296: 3– 14. 10.1016/j.neuroscience.2014.06.035 24973655 · DOI
  14. Keleş MF, Frye MA (2017) Object-detecting neurons in Drosophila. Curr Biol 27: 1– 8. 28190726 PMC5340600
  15. Keleş MF, Hardcastle BJ, Städele C, Qi X, Frye MA (2020) Inhibitory interactions and columnar inputs to an object motion detector in Drosophila. Cell Rep 30: 2115– 2124. 10.1016/j.celrep.2020.01.061 32075756 PMC7210872 · DOI · Paper page
  16. Kitamoto T (2001) Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol 47: 81– 92. 10.1002/neu.1018 11291099 · DOI
  17. Klapoetke NC, Nern A, Peek MY, Rogers EM, Breads P, Rubin GM, Reiser MB, Card GM (2017) Ultra-selective looming detection from radial motion opponency. Nature 551: 237– 241. 10.1038/nature24626 29120418 PMC7457385 · DOI · Paper page
  18. Kohn JR, Portes JP, Christenson MP, Abbott LF, Behnia R (2021) Flexible filtering by neural inputs supports motion computation across states and stimuli. Curr Biol 31: 5249– 5260.e5. 34670114 PMC8725177
  19. Lin TY, Luo J, Shinomiya K, Ting CY, Lu Z, Meinertzhagen IA, Lee CH (2016) Mapping chromatic pathways in the Drosophila visual system. J Comp Neurol 524: 213– 227. 10.1002/cne.23857 26179639 PMC4678965 · DOI
  20. Meier M, Borst A (2019) Extreme compartmentalization in a Drosophila amacrine cell. Curr Biol 29: 1545– 1550.e2. 10.1016/j.cub.2019.03.070 31031119 · DOI · Paper page
  21. Meinertzhagen IA (2016) Connectome studies on Drosophila: a short perspective on a tiny brain. J Neurogenet 30: 62– 68. 10.3109/01677063.2016.1166224 27328842 · DOI
  22. Meinertzhagen IA (2018) Of what use is connectomics? A personal perspective on the Drosophila connectome. J Exp Biol 221: jeb164954. 29784759
  23. Melnattur KV, Pursley R, Lin TY, Ting CY, Smith PD, Pohida T, Lee CH (2014) Multiple redundant medulla projection neurons mediate color vision in Drosophila. J Neurogenet 28: 374– 388. 10.3109/01677063.2014.891590 24766346 PMC4245076 · DOI
  24. Morimoto MM, Nern A, Zhao A, Rogers EM, Wong AM, Isaacson MD, Bock DD, Rubin GM, Reiser MB (2020) Spatial readout of visual looming in the central brain of Drosophila. Elife 9: e57685. 10.7554/eLife.57685 33205753 PMC7744102 · DOI
  25. Mu L, Ito K, Bacon JP, Strausfeld NJ (2012) Optic glomeruli and their inputs in Drosophila share an organizational ground pattern with the antennal lobes. J Neurosci 32: 6061– 6071. 10.1523/JNEUROSCI.0221-12.2012 22553013 PMC3358351 · DOI
  26. Otsuna H, Ito K (2006) Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula-specific pathways. J Comp Neurol 497: 928– 958. 10.1002/cne.21015 16802334 · DOI · Paper page
  27. Otsuna H, Shinomiya K, Ito K (2014) Parallel neural pathways in higher visual centers of the Drosophila brain that mediate wavelength-specific behavior. Front Neural Circuits 8: 8– 12. 24574974 PMC3918591
  28. Otsuna H, Ito M, Kawase T (2018) Color depth MIP mask search: a new tool to expedite Split-GAL4 creation. bioRxiv 4: 318006.
  29. Özel MN, Simon F, Jafari S, Holguera I, Chen Y-C, Benhra N, El-Danaf RN, Kapuralin K, Malin JA, Konstantinides N, Desplan C (2021) Neuronal diversity and convergence in a visual system developmental atlas. Nature 589: 88– 95. 10.1038/s41586-020-2879-3 33149298 PMC7790857 · DOI · Paper page
  30. Panser K, Tirian L, Schulze F, Villalba S, Jefferis GSXE, Bühler K, Straw AD (2016) Automatic segmentation of Drosophila neural compartments using GAL4 expression data reveals novel visual pathways. Curr Biol 26: 1943– 1954. 10.1016/j.cub.2016.05.052 27426516 PMC4985560 · DOI
  31. Pfeiffer BD, Ngo TTB, Hibbard KL, Murphy C, Jenett A, Truman JW, Rubin GM (2010) Refinement of tools for targeted gene expression in Drosophila. Genetics 186: 735– 755. 10.1534/genetics.110.119917 20697123 PMC2942869 · DOI · Paper page
  32. Raji JI, Potter CJ (2021) The number of neurons in Drosophila and mosquito brains. PLoS One 16: e0250381. 10.1371/journal.pone.0250381 33989293 PMC8121336 · DOI
  33. Ramos-Traslosheros G, Silies M (2021) The physiological basis for contrast opponency in motion computation in Drosophila. Nat Commun 12: 4987. 10.1038/s41467-021-24986-w 34404776 PMC8371135 · DOI
  34. Ribeiro IMA, Drews M, Bahl A, Machacek C, Borst A, Dickson BJ (2018) Visual projection neurons mediating directed courtship in Drosophila. Cell 174: 607– 621.e18. 10.1016/j.cell.2018.06.020 30033367 · DOI · Paper page
  35. Schnaitmann C, Haikala V, Abraham E, Oberhauser V, Thestrup T, Griesbeck O, Reiff DF (2018) Color processing in the early visual system of Drosophila. Cell 172: 318– 330.e18. 10.1016/j.cell.2017.12.018 29328919 · DOI
  36. Serbe E, Meier M, Leonhardt A, Borst A, Serbe E, Meier M, Leonhardt A, Borst A (2016) Comprehensive characterization of the major presynaptic elements to the Drosophila OFF motion detector. Neuron 89: 829– 841. 10.1016/j.neuron.2016.01.006 26853306 · DOI
  37. Shearin HK, Quinn CD, Mackin RD, Macdonald IS, Stowers RS (2018) t-GRASP, a targeted GRASP for assessing neuronal connectivity. J Neurosci Methods 306: 94– 102. 10.1016/j.jneumeth.2018.05.014 29792886 PMC6689385 · DOI
  38. Shinomiya K, Karuppudurai T, Lin TY, Lu Z, Lee CH, Meinertzhagen IA (2014) Candidate neural substrates for off-edge motion detection in Drosophila. Curr Biol 24: 1062– 1070. 10.1016/j.cub.2014.03.051 24768048 PMC4031294 · DOI
  39. Shinomiya K, Takemura SY, Rivlin PK, Plaza SM, Scheffer LK, Meinertzhagen IA (2015) A common evolutionary origin for the ON- and OFF-edge motion detection pathways of the Drosophila visual system. Front Neural Circuits 9: 1– 12. 26217193 PMC4496578
  40. Shinomiya K, et al. (2019) Comparisons between the ON- and OFF-edge motion pathways in the Drosophila brain. Elife 8: e40025. 10.7554/eLife.40025 30624205 PMC6338461 · DOI · Paper page
  41. Simpson JH, Looger LL (2018) Functional imaging and optogenetics in Drosophila. Genetics 208: 1291– 1309. 10.1534/genetics.117.300228 29618589 PMC5887132 · DOI
  42. Strother JA, Wu S, Wong AM, Nern A, Rogers EM, Le JQ, Rubin GM, Reiser MB (2017) The emergence of directional selectivity in the visual motion pathway of Drosophila. Neuron 94: 168– 182.e10. 10.1016/j.neuron.2017.03.010 28384470 · DOI
  43. Takemura S, Lu Z, Meinertzhagen IA (2008) Synaptic circuits of the Drosophila optic lobe: the input terminals to the medulla. J Comp Neurol 509: 493– 513. 10.1002/cne.21757 18537121 PMC2481516 · DOI · Paper page
  44. Takemura SY, et al. (2015) Synaptic circuits and their variations within different columns in the visual system of Drosophila. Proc Natl Acad Sci U S A 112: 13711– 13716. 26483464 PMC4640747
  45. Tanaka R, Clark DA (2020) Object-displacement-sensitive visual neurons drive freezing in Drosophila. Curr Biol 30: 1– 19. 32442466 PMC8716191
  46. Tanaka R, Clark DA (2021) Neural mechanisms to exploit positional geometry for collision avoidance. bioRxiv 1– 15. PMC9177691 35508172
  47. Tirian L, Dickson BJ (2017) The VT GAL4, LexA, and split-GAL4 driver line collections for targeted expression in the Drosophila nervous system. bioRxiv 198648. doi: 10.1101/198648. 10.1101/198648 · DOI
  48. Virtanen P, et al. (2020) SciPy 1.0: fundamental algorithms for scientific computing in Python. Nat Methods 17: 261– 272. 10.1038/s41592-019-0686-2 32015543 PMC7056644 · DOI · Paper page
  49. von Reyn CR, Breads P, Peek MY, Zheng GZ, Williamson WR, Yee AL, Leonardo A, Card GM (2014) A spike-timing mechanism for action selection. Nat Neurosci 17: 962– 970. 10.1038/nn.3741 24908103 · DOI · Paper page
  50. Ward JH (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58: 236– 244. 10.1080/01621459.1963.10500845 · DOI
  51. Wu M, Nern A, Williamson WR, Morimoto MM, Reiser MB, Card GM, Rubin GM (2016) Visual projection neurons in the Drosophila lobula link feature detection to distinct behavioral programs. Elife 5: e21022. 10.7554/eLife.21022 28029094 PMC5293491 · DOI · Paper page
  52. Yang HH, Clandinin TR (2018) Elementary motion detection in Drosophila: algorithms and mechanisms. Annu Rev Vis Sci 4: 143– 163. 10.1146/annurev-vision-091517-034153 29949723 PMC8097889 · DOI
  53. Zavatone-Veth JA, Badwan BA, Clark DA (2020) A minimal synaptic model for direction selective neurons in Drosophila. J Vis 20: 2– 22. 10.1167/jov.20.2.2 32040161 PMC7343402 · DOI
  54. Zhao T, Plaza SM (2014) Automatic Neuron Type Identification by Neurite Localization in the Drosophila Medulla. arXiv: 1409. 1892.
  55. Zheng Z, et al. (2018) A complete electron microscopy volume of the brain of adult Drosophila melanogaster. Cell 174: 730– 714. 10.1016/j.cell.2018.06.019 30033368 PMC6063995 · DOI · Paper page

Cited by

Sorted by citations

Authors
Tanaka (田中涼介), R., & Clark, D. A.
Affiliations
Yale University (US)
Corresponding author
Clark, Damon A.
Venue
eneuro
Published
2022-03
Volume
9
Issue
2
Pages
ENEURO.0053-22.2022
ISSN
2373-2822 (ISSN-L)
OpenAlex
W4226018478
Cited by
10
References
15
Citations by year
2026: 1 · 2025: 2 · 2024: 2 · 2023: 4 · 2022: 1
FWCI
0.99
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • eNeuro (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • Gruber Foundation
  • National Institutes of Health
  • National Eye Institute (R01EY026555, P30EY026878)
  • National Institute of Neurological Disorders and Stroke (R01NS121773)
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 › Biochemistry, Genetics and Molecular Biology › Biophysics › Cell Image Analysis Techniques
Keywords
connectome, cell type annotation, visual feature detection
MeSH terms
Animals, Drosophila, Drosophila melanogaster, Neurons, Visual Pathways, Neuropil, Connectome

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review