Systematic analysis of the visual projection neurons ofDrosophila melanogaster. I. Lobula-specific pathways
Abstract
In insects, visual information is processed in the optic lobe and conveyed to the central brain. Although neural circuits within the optic lobe have been studied extensively, relatively little is known about the connection between the optic lobe and the central brain. To understand how visual information is read by the neurons of the central brain, and what kind of centrifugal neurons send the control signal from the central brain to the optic lobe, we performed a systematic analysis of the visual projection neurons that connect the optic lobe and the central brain of Drosophila melanogaster. By screening approximately 4,000 GAL4 enhancer-trap strains we identified 44 pathways. The overall morphology and the direction of information of each pathway were investigated by expressing cytoplasmic and presynapsis-targeted fluorescent reporters. A canonical nomenclature system was introduced to describe the area of projection in the central brain. As the first part of a series of articles, we here describe 14 visual projection neurons arising specifically from the lobula. Eight pathways form columnar arborization in the lobula, whereas the remaining six form tangential or tree-like arborization. Eleven are centripetal pathways, among which nine terminate in the ventrolateral protocerebrum. Terminals of each columnar pathway form glomerulus-like structures in different areas of the ventrolateral protocerebrum. The posterior lateral protocerebrum and the optic tubercle were each contributed by a single centripetal pathway. Another pathway connects the lobula on each side of the brain. Two centrifugal pathways convey signals from the posterior lateral protocerebrum to the lobula.
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VPNs target specific neuropils or optic glomeruli in the central brain.
“VPNs target specific neuropils (for example, anterior optic tubercle (AOTU), posterior lateral protocerebrum (PLP) and posterior ventrolateral protocerebrum (PVLP)) or optic glomeruli60,61 in the central brain.”
From Neuronal wiring diagram of an adult brain (2024) · cites this paper as [61]
There are 524 neurons that project from the central brain to the optic lobes, called visual centrifugal neurons (VCNs).
“There are 524 neurons that project from the central brain to the optic lobes. We call these visual centrifugal neurons61 (VCNs).”
From Neuronal wiring diagram of an adult brain (2024) · cites this paper as [61]
Cites
Targeted gene expression as a means of altering cell fates and generating dominant phenotypes
Brand, A. H., & Perrimon, N. (1993) · Development · doi:10.1242/dev.118.2.401 · Cited by 9,510 · see citing works
The development of Drosophila melanogaster
Ingham, P. W. (1994) · Trends in Genetics · doi:10.1016/0168-9525(90)90017-z · Cited by 3,158 · see citing works
(1909) · Cited by 2,575 · see citing works
A stable genomic source of P element transposase in Drosophila melanogaster.
Robertson, H. M., Preston, C. R., Phillis, R. W., Johnson-Schlitz, D. M., Benz, W. K., & Engels, W. R. (1988) · Genetics · doi:10.1093/genetics/118.3.461 · Cited by 1,333 · see citing works
Strausfeld, N. (1976) · Springer Berlin Heidelberg · doi:10.1007/978-3-642-66179-2 · Cited by 1,178 · see citing works
Renn, S. C. P., Park, J. H., Rosbash, M., Hall, J. C., & Taghert, P. H. (1999) · Cell · doi:10.1016/s0092-8674(00)81676-1 · Cited by 1,117 · see citing works
Strausfeld, N. J. (1976) · Medical Entomology and Zoology · Cited by 967 · see citing works
Ito, K., Awano, W., Suzuki, K., Hiromi, Y., & Yamamoto, D. (1997) · Development · doi:10.1242/dev.124.4.761 · Cited by 757 · see citing works
Self-citationThe optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure
Fischbach, K.-F., & Dittrich, A. P. M. (1989) · Cell and Tissue Research · doi:10.1007/bf00218858 · Cited by 709 · see citing works
Spatial Representation of the Glomerular Map in the Drosophila Protocerebrum
Wong, A. M., Wang, J. W., & Axel, R. (2002) · Cell · doi:10.1016/s0092-8674(02)00707-9 · Cited by 560 · see citing works
Neuronal architecture of the antennal lobe in Drosophila melanogaster
Stocker, R. F., Lienhard, M. C., Borst, A., & Fischbach, K. F. (1990) · Cell and Tissue Research · doi:10.1007/bf00327741 · Cited by 457 · see citing works
Estimation of self-motion by optic flow processing in single visual interneurons
Krapp, H. G., & Hengstenberg, R. (1996) · Nature · doi:10.1038/384463a0 · Cited by 409 · see citing works
Neural Mechanisms of Visual Course Control in Insects
Hausen, K., & Egelhaaf, M. (1989) · Springer eBooks · doi:10.1007/978-3-642-74082-4_18 · Cited by 365 · see citing works
Ito, K., Urban, J., & Technau, G. M. (1995) · Development Genes and Evolution · doi:10.1007/bf02179499 · Cited by 353 · see citing works
Self-citationIto, K., Suzuki, K., Estes, P. S., Ramaswami, M., Yamamoto, D., & Strausfeld, N. J. (1998) · Learning & Memory · doi:10.1101/lm.5.1.52 · Cited by 337 · see citing works
Self-citationFruitless specifies sexually dimorphic neural circuitry in the Drosophila brain
Kimura, K.-I., Oté, M., Tazawa, T., & Yamamoto, D. (2005) · Nature · doi:10.1038/nature04229 · Cited by 314 · see citing works
Hayashi, S., Ito, K., Sado, Y., Taniguchi, M., Akimoto, A., Takeuchi, H., Aigaki, T., Matsuzaki, F., Nakagoshi, H., Tanimura, T., et al. (2002) · genesis · doi:10.1002/gene.10137 · Cited by 301 · see citing works
Self-citationIntegration of Chemosensory Pathways in the Drosophila Second-Order Olfactory Centers
Tanaka, N. K., Awasaki, T., Shimada, T., & Ito, K. (2004) · Current Biology · doi:10.1016/j.cub.2004.03.006 · Cited by 280 · see citing works
Self-citationThe optic lobe of Drosophila melanogaster
Bausenwein, B., Dittrich, A. P. M., & Fischbach, K. F. (1992) · Cell and Tissue Research · doi:10.1007/bf00318687 · Cited by 271 · see citing works
Salcedo, E. E., Huber, A., Henrich, S., Chadwell, L. V., Chou, W., Paulsen, R., & Britt, S. G. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-24-10716.1999 · Cited by 247 · see citing works
Serotonin and serotonin-immunoreactive neurons in the nervous system of insects
Nässel, D. R. (1988) · Progress in Neurobiology · doi:10.1016/0301-0082(88)90002-0 · Cited by 244 · see citing works
Drosophila Fragile X Protein, DFXR, Regulates Neuronal Morphology and Function in the Brain
Morales, J., Hiesinger, P. R., Schroeder, A. J., Kume, K., Verstreken, P., Jackson, F. R., Nelson, D. L., & Hassan, B. A. (2002) · Neuron · doi:10.1016/s0896-6273(02)00731-6 · Cited by 238 · see citing works
Strausfeld, N. J., & Gronenberg, W. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.903020419 · Cited by 210 · see citing works
Dendritic Integration and Its Role in Computing Image Velocity
Single, S., & Borst, A. (1998) · Science · doi:10.1126/science.281.5384.1848 · Cited by 194 · see citing works
The brain of Drosophila melanogaster
Power, M. E. (1943) · Journal of Morphology · doi:10.1002/jmor.1050720306 · Cited by 184 · see citing works
Local-feature assembling in visual pattern recognition and generalization in honeybees
Stach, S., Benard, J., & Giurfa, M. (2004) · Nature · doi:10.1038/nature02594 · Cited by 181 · see citing works
The Brain of Drosophila Melanogaster
(1943) · Annals of the Entomological Society of America · doi:10.1093/aesa/36.3.431 · Cited by 177 · see citing works
Binocular Contributions to Optic Flow Processing in the Fly Visual System
Krapp, H. G., Hengstenberg, R., & Egelhaaf, M. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.2.724 · Cited by 161 · see citing works
Neuronal basis for parallel visual processing in the fly
Strausfeld, N. J., & Lee, J.-K. (1991) · Visual Neuroscience · doi:10.1017/s0952523800010919 · Cited by 157 · see citing works
Feiler, R., Bjornson, R. D., Kirschfeld, K., Mismer, D., Rubin, G. M., Smith, D., Socolich, M., & Zuker, C. S. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-10-03862.1992 · Cited by 135 · see citing works
Kempf, S. C., Page, L. R., & Pires, A. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970929)386:3 · Cited by 130 · see citing works
Conti, F., Melone, M., Biasi, S. D., Minelli, A., Brecha, N. C., & Ducati, A. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980622)396:1 · Cited by 130 · see citing works
Sinakevitch, I. G., Douglass, J. K., Scholtz, G., Loesel, R., & Strausfeld, N. J. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10925 · Cited by 129 · see citing works
Estes, P. S., Ho, G. L. Y., Narayanan, R., & Ramaswami, M. (2000) · Journal of Neurogenetics · doi:10.3109/01677060009084496 · Cited by 123 · see citing works
Global perception in small brains: Topological pattern recognition in honey bees
Chen, L., Zhang, S., & Srinivasan, M. V. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0732090100 · Cited by 120 · see citing works
Neural mechanism underlying complex receptive field properties of motion-sensitive interneurons
Haag, J., & Borst, A. (2004) · Nature Neuroscience · doi:10.1038/nn1245 · Cited by 116 · see citing works
Homberg, U., Hofer, S., Pfeiffer, K., & Gebhardt, S. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10771 · Cited by 110 · see citing works
Verkhusha, V. V., Otsuna, H., Awasaki, T., Oda, H., Tsukita, S., & Ito, K. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.c100200200 · Cited by 110 · see citing works
Self-citationDouglass, J. K., & Strausfeld, N. J. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-15-04551.1996 · Cited by 105 · see citing works
Cell-specific immuno-probes for the brain of normal and mutant Drosophila melanogaster
Buchner, E., Bader, R., Buchner, S., Cox, J. A., Emson, P. C., Flory, E., Heizmann, C. W., Hemm, S., Hofbauer, A., & Oertel, W. (1988) · Cell and Tissue Research · doi:10.1007/bf00222292 · Cited by 103 · see citing works
The functional organization of male-specific visual neurons in flies
Gilbert, C., & Strausfeld, N. (1991) · Journal of Comparative Physiology A · doi:10.1007/bf00197653 · Cited by 101 · see citing works
Disabled-1 is expressed in type AII amacrine cells in the mouse retina
Rice, D. S., & Curran, T. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20000821)424:2 · Cited by 98 · see citing works
Fischbach, K. F. (1983) · Developmental Biology · doi:10.1016/0012-1606(83)90002-7 · Cited by 93 · see citing works
Activity labeling patterns in the medulla of Drosophila melanogaster caused by motion stimuli
Bausenwein, B., & Fischbach, K. F. (1992) · Cell and Tissue Research · doi:10.1007/bf00381876 · Cited by 88 · see citing works
Visual Pattern Recognition in Drosophila Is Invariant for Retinal Position
Tang, S., Wolf, R., Xu, S., & Heisenberg, M. (2004) · Science · doi:10.1126/science.1099839 · Cited by 85 · see citing works
Recurrent Network Interactions Underlying Flow-Field Selectivity of Visual Interneurons
Haag, J., & Borst, A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-15-05685.2001 · Cited by 78 · see citing works
Loesel, R., & Homberg, U. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1342 · Cited by 77 · see citing works
Harrison, J. B., Chen, H. H., Sattelle, E., Barker, P. J., Huskisson, N. S., Rauh, J. J., Bai, D., & Sattelle, D. B. (1996) · Cell and Tissue Research · doi:10.1007/s004410050587 · Cited by 76 · see citing works
Structural organization of male-specific visual neurons in calliphorid optic lobes
Strausfeld, N. (1991) · Journal of Comparative Physiology A · doi:10.1007/bf00197652 · Cited by 64 · see citing works
Visual Pattern Recognition in Drosophila Is Invariant for Retinal Position
Shi-Ming, Tang, Reinhard, Wolf, Shuping, Xu, & Martin, M. (2006) · 中国生物学文摘 · Cited by 60 · see citing works
Ito, K., Okada, R., Tanaka, N. K., & Awasaki, T. (2003) · Microscopy Research and Technique · doi:10.1002/jemt.10369 · Cited by 57 · see citing works
Self-citationAnatomical organization of retinotopic motion‐sensitive pathways in the optic lobes of flies
Douglass, J. K., & Strausfeld, N. J. (2003) · Microscopy Research and Technique · doi:10.1002/jemt.10367 · Cited by 57 · see citing works
Li, H. L., Roch, J., Sundsmo, M. P., Otero, D. A. C., Sisodia, S. S., Thomas, R. G., & Saitoh, T. (1997) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199705)32:5 · Cited by 56 · see citing works
The resolution of neuronal assemblies after cobalt injection into neuropil
Strausfeld, N. J., & Hausen, K. (1977) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1977.0154 · Cited by 55 · see citing works
The antennal centers and their connections within the brain of Drosophila melanogaster
Power, M. E. (1946) · The Journal of Comparative Neurology · doi:10.1002/cne.900850307 · Cited by 52 · see citing works
Encoding of motion in real time by the fly visual system
Egelhaaf, M., & Warzechat, A.-K. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)80068-3 · Cited by 41 · see citing works
Oculomotor control in calliphorid flies: GABAergic organization in heterolateral inhibitory pathways
Strausfeld, N. J., Kong, A., Milde, J. J., Gilbert, C., & Ramaiah, L. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903610208 · Cited by 38 · see citing works
Gilbert, C., & Strausfeld, N. J. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903160107 · Cited by 35 · see citing works
Genetic dissection of the anterior optic tract of Drosophila melanogaster
Fischbach, K. F., & Lyly-H�nerberg, I. (1983) · Cell and Tissue Research · doi:10.1007/bf00218113 · Cited by 30 · see citing works
Ibbotson, M. R., Maddess, T., & Dubois, R. (1991) · Journal of Comparative Physiology A · doi:10.1007/bf00207000 · Cited by 27 · see citing works
Strausfeld, N. J., & Gilbert, C. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903160106 · Cited by 25 · see citing works
Tangential medulla neurons in the mothManduca sexta. Structure and responses to optomotor stimuli
Milde, J. J. (1993) · Journal of Comparative Physiology A · doi:10.1007/bf02451909 · Cited by 19 · see citing works
Identification of [3H]deoxyglucose-labelled interneurons in the fly from serial autoradiographs
Buchner, E., Buchner, S., & Bülthoff, H. (1984) · Brain Research · doi:10.1016/0006-8993(84)90448-7 · Cited by 17 · see citing works
In vivo two-photon laser-scanning microscopy of Ca2+ dynamics in visual motion-sensitive neurons
Kalb, J., Tolker‐Nielsen, T., Fricke, M., Egelhaaf, M., & Kurtz, R. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.02.047 · Cited by 12 · see citing works
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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
A connectome and analysis of the adult Drosophila central brain
Scheffer, L. K., Xu, C. S., Januszewski, M., Lu, Z., Takemura, S.-Y., Hayworth, K. J., Huang, G. B., Shinomiya, K., Maitlin-Shepard, J., Berg, S., et al. (2020) · eLife · doi:10.7554/elife.57443 · Cited by 1,128 · see citing works
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Ito, K., Shinomiya, K., Ito, M., Armstrong, J. D., Boyan, G., Hartenstein, V., Harzsch, S., Heisenberg, M., Homberg, U., Jenett, A., et al. (2014) · Neuron · doi:10.1016/j.neuron.2013.12.017 · Cited by 611 · see citing works
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Dorkenwald, S., Matsliah, A., Sterling, A. R., Schlegel, P., Yu, S.-C., McKellar, C. E., Lin, A., Costa, M., Eichler, K., Yin, Y., et al. (2024) · Nature · doi:10.1038/s41586-024-07558-y · Cited by 570 · see citing works
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Sanes, J. R., & Zipursky, S. L. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.018 · Cited by 559 · see citing works
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Tanaka, N. K., Tanimoto, H., & Ito, K. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21692 · Cited by 470 · see citing works
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Kamikouchi, A., Inagaki, H. K., Effertz, T., Hendrich, O., Fiala, A., Göpfert, M. C., & Ito, K. (2009) · Nature · doi:10.1038/nature07810 · Cited by 406 · see citing works
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Li, F., Lindsey, J. W., Marin, E. C., Otto, N., Dreher, M., Dempsey, G., Stark, I., Bates, A. S., Pleijzier, M. W., Schlegel, P., et al. (2020) · eLife · doi:10.7554/elife.62576 · Cited by 403 · see citing works
Costa, M., Manton, J. D., Ostrovsky, A. D., Prohaska, S., & Jefferis, G. S. X. E. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.012 · Cited by 294 · see citing works
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Namiki, S., Dickinson, M. H., Wong, A. M., Korff, W., & Card, G. M. (2018) · eLife · doi:10.7554/elife.34272 · Cited by 337 · see citing works
Wu, M., Nern, A., Williamson, W. R., Morimoto, M. M., Reiser, M. B., Card, G. M., & Rubin, G. M. (2016) · eLife · doi:10.7554/elife.21022 · Cited by 304 · see citing works
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Kremer, M. C., Jung, C., Batelli, S., Rubin, G. M., & Gaul, U. (2017) · Glia · doi:10.1002/glia.23115 · Cited by 297 · see citing works
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Davis, F. P., Nern, A., Picard, S., Reiser, M. B., Rubin, G. M., Eddy, S. R., & Henry, G. L. (2020) · eLife · doi:10.7554/elife.50901 · Cited by 268 · see citing works
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Séjourné, J., Plaçais, P.-Y., Aso, Y., Siwanowicz, I., Trannoy, S., Thoma, V., Tedjakumala, S. R., Rubin, G. M., Tchénio, P., Ito, K., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2846 · Cited by 265 · see citing works
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Busch, S., Selcho, M., Ito, K., & Tanimoto, H. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21966 · Cited by 255 · see citing works
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Özel, M. N., Simon, F., Jafari, S., Holguera, I., Chen, Y.-C., Benhra, N., El-Danaf, R. N., Kapuralin, K., Malin, J. A., Konstantinides, N., et al. (2021) · Nature · doi:10.1038/s41586-020-2879-3 · Cited by 237 · see citing works
Kamikouchi, A., Shimada, T., & Ito, K. (2006) · Journal of Comparative Neurology · doi:10.1002/cne.21075 · Cited by 220 · see citing works
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Vogt, K., Schnaitmann, C., Dylla, K. V., Knapek, S., Aso, Y., Rubin, G. M., & Tanimoto, H. (2014) · eLife · doi:10.7554/elife.02395 · Cited by 219 · see citing works
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Villella, A., & Hall, J. C. (2008) · Advances in genetics · doi:10.1016/s0065-2660(08)00603-2 · Cited by 205 · see citing works
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Takemura, S., Lu, Z., & Meinertzhagen, I. A. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21757 · Cited by 199 · see citing works
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Heinze, S., Florman, J., Asokaraj, S., el Jundi, B., & Reppert, S. M. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23214 · Cited by 194 · see citing works
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Lai, S.-L., Awasaki, T., Ito, K., & Lee, T. (2008) · Development · doi:10.1242/dev.024380 · Cited by 171 · see citing works
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Dorkenwald, S., Matsliah, A., Sterling, A. R., Schlegel, P., Yu, S.-C., McKellar, C. E., Lin, A., Costa, M., Eichler, K., Yin, Y., et al. (2023) · doi:10.1101/2023.06.27.546656 · Cited by 149 · see citing works
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Anderson, J. R., Jones, B. W., Yang, J., Shaw, M. V., Watt, C. B., Koshevoy, P., Spaltenstein, J., Jurrus, E. R., Kannan, U. V., Whitaker, R., et al. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000074 · Cited by 146 · see citing works
Natalisin, a tachykinin-like signaling system, regulates sexual activity and fecundity in insects
Jiang, H., Lkhagva, A., Daubnerová, I., Chae, H.-S., Šimo, L., Jung, S.-H., Yoon, Y. K., Lee, N.-R., Seong, J. Y., Žitňan, D., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1310676110 · Cited by 144 · see citing works
Structure of the adult central complex in Drosophila: Organization of distinct neuronal subsets
Young, J. M., & Armstrong, J. D. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22284 · Cited by 142 · see citing works
Loom-Sensitive Neurons Link Computation to Action in the Drosophila Visual System
de Vries, S. E. J., & Clandinin, T. R. (2012) · Current Biology · doi:10.1016/j.cub.2012.01.007 · Cited by 142 · see citing works
Sexual arousal gates visual processing during Drosophila courtship
Hindmarsh Sten, T., Li, R., Otopalik, A., & Ruta, V. (2021) · Nature · doi:10.1038/s41586-021-03714-w · Cited by 140 · see citing works
Comparisons between the ON- and OFF-edge motion pathways in the Drosophila brain
Shinomiya, K., Huang, G., Lu, Z., Parag, T., Xu, C. S., Aniceto, R., Ansari, N., Cheatham, N., Lauchie, S., Neace, E., et al. (2019) · eLife · doi:10.7554/elife.40025 · Cited by 140 · see citing works
Anatomical basis of sun compass navigation I: The general layout of the monarch butterfly brain
Heinze, S., & Reppert, S. M. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23054 · Cited by 131 · see citing works
Object-Detecting Neurons in Drosophila
Keleş, M. F., & Frye, M. A. (2017) · Current Biology · doi:10.1016/j.cub.2017.01.012 · Cited by 130 · see citing works
Bayraktar, O. A., Boone, J. Q., Drummond, M. L., & Doe, C. Q. (2010) · Neural Development · doi:10.1186/1749-8104-5-26 · Cited by 125 · see citing works
Candidate Neural Substrates for Off-Edge Motion Detection in Drosophila
Shinomiya, K., Karuppudurai, T., Lin, T., Lu, Z., Lee, C., & Meinertzhagen, I. A. (2014) · Current Biology · doi:10.1016/j.cub.2014.03.051 · Cited by 119 · see citing works
Organization of descending neurons in Drosophila melanogaster
Hsu, C. T., & Bhandawat, V. (2016) · Scientific Reports · doi:10.1038/srep20259 · Cited by 112 · see citing works
Visual-Olfactory Integration in the Human Disease Vector Mosquito Aedes aegypti
Vinauger, C., van Breugel, F., Locke, L. T., Tobin, K. K. S., Dickinson, M. H., Fairhall, A. L., Akbari, O. S., & Riffell, J. A. (2019) · Current Biology · doi:10.1016/j.cub.2019.06.043 · Cited by 112 · see citing works
Visual Processing in the Central Bee Brain
Paulk, A. C., Dacks, A. M., Phillips‐Portillo, J., Fellous, J., & Gronenberg, W. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1325-09.2009 · Cited by 109 · see citing works
Topological and modality-specific representation of somatosensory information in the fly brain
Tsubouchi, A., Yano, T., Yokoyama, T. K., Murtin, C., Otsuna, H., & Ito, K. (2017) · Science · doi:10.1126/science.aan4428 · Cited by 108 · see citing works
Self-citationVisual circuits in flies: beginning to see the whole picture
Behnia, R., & Desplan, C. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.03.010 · Cited by 105 · see citing works
Single Serotonergic Neurons that Modulate Aggression in Drosophila
Alekseyenko, O. V., Chan, Y.-B., Fernandez, M. P., Bülow, T. R., Pankratz, M. J., & Kravitz, E. A. (2014) · Current Biology · doi:10.1016/j.cub.2014.09.051 · Cited by 102 · see citing works
Octopamine Neuromodulatory Effects on a Social Behavior Decision-Making Network in Drosophila Males
Certel, S. J., Leung, A. K.-W., Lin, C.-Y., Pérez, P. L., Chiang, A., & Kravitz, E. A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013248 · Cited by 104 · see citing works
Neuroarchitecture of Aminergic Systems in the Larval Ventral Ganglion of Drosophila melanogaster
Vömel, M., & Wegener, C. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001848 · Cited by 103 · see citing works
Nériec, N., & Desplan, C. (2016) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2015.11.032 · Cited by 101 · see citing works
Wan, Y., Otsuna, H., Chien, C.-B., & Hansen, C. D. (2009) · IEEE Transactions on Visualization and Computer Graphics · doi:10.1109/tvcg.2009.118 · Cited by 100 · see citing works
Self-citationA functionally ordered visual feature map in the Drosophila brain
Klapoetke, N. C., Nern, A., Rogers, E. M., Rubin, G. M., Reiser, M. B., & Card, G. M. (2022) · Neuron · doi:10.1016/j.neuron.2022.02.013 · Cited by 98 · see citing works
Connectome-driven neural inventory of a complete visual system
Nern, A., Loesche, F., Takemura, S.-Y., Burnett, L. E., Dreher, M., Gruntman, E., Hoeller, J., Huang, G. B., Januszewski, M., Klapoetke, N. C., et al. (2025) · Nature · doi:10.1038/s41586-025-08746-0 · Cited by 96 · see citing works
Color depth MIP mask search: a new tool to expedite Split-GAL4 creationPreprint
Otsuna, H., Ito, M., & Kawase, T. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/318006 · Cited by 93 · see citing works
Self-citationAuditory circuit in the <i>Drosophila</i> brain
Lai, J. S.-Y., Lo, S.-J., Dickson, B. J., & Chiang, A.-S. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1117307109 · Cited by 90 · see citing works
Mu, L., Ito, K., Bacon, J. P., & Strausfeld, N. J. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0221-12.2012 · Cited by 87 · see citing works
Self-citationColor vision in insects: insights from Drosophila
Schnaitmann, C., Pagni, M., & Reiff, D. F. (2020) · Journal of Comparative Physiology A · doi:10.1007/s00359-019-01397-3 · Cited by 83 · see citing works
Muscles that move the retina augment compound eye vision in Drosophila
Fenk, L. M., Avritzer, S. C., Weisman, J. L., Nair, A., Randt, L., Mohren, T. L., Siwanowicz, I., & Maimon, G. (2022) · Nature · doi:10.1038/s41586-022-05317-5 · Cited by 82 · see citing works
Panser, K., Tirián, L., Schulze, F., Villalba, S. D., Jefferis, G. S. X. E., Bühler, K., & Straw, A. D. (2016) · Current Biology · doi:10.1016/j.cub.2016.05.052 · Cited by 80 · see citing works
A Challenge of Numbers and Diversity: Neurogenesis in the Drosophila Optic Lobe
Apitz, H., & Salecker, I. (2014) · Journal of Neurogenetics · doi:10.3109/01677063.2014.922558 · Cited by 74 · see citing works
Drosophila as a genetic and cellular model for studies on axonal growth
Sánchez-Soriano, N., Tear, G., Whitington, P., & Prokop, A. (2007) · Neural Development · doi:10.1186/1749-8104-2-9 · Cited by 22 · see citing works
Clonal Unit Architecture of the Adult Fly Brain
Ito, K., & Awasaki, T. (2009) · Advances in experimental medicine and biology · doi:10.1007/978-0-387-78261-4_9 · Cited by 73 · see citing works
Self-citationSynaptic gradients transform object location to action
Dombrovski, M., Peek, M. Y., Park, J.-Y., Vaccari, A., Sumathipala, M., Morrow, C., Breads, P., Zhao, A., Kurmangaliyev, Y. Z., Sanfilippo, P., et al. (2023) · Nature · doi:10.1038/s41586-022-05562-8 · Cited by 67 · see citing works
Toward a Mechanistic Understanding of Color Vision in Insects
Song, B.-M., & Lee, C. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00016 · Cited by 70 · see citing works
Connecting neural codes with behavior in the auditory system of Drosophila
Clemens, J., Girardin, C. C., Coen, P., Guan, X.-J., Dickson, B. J., & Murthy, M. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.014 · Cited by 69 · see citing works
Conserved Role of the Vsx Genes Supports a Monophyletic Origin for Bilaterian Visual Systems
Erclik, T., Hartenstein, V., Lipshitz, H. D., & McInnes, R. R. (2008) · Current Biology · doi:10.1016/j.cub.2008.07.076 · Cited by 67 · see citing works
Neurons Forming Optic Glomeruli Compute Figure–Ground Discriminations inDrosophila
Aptekar, J. W., Keleş, M. F., Lu, P. M., Zolotova, N. M., & Frye, M. A. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0652-15.2015 · Cited by 66 · see citing works
Neuronal circuits integrating visual motion information in Drosophila melanogaster
Shinomiya, K., Nern, A., Meinertzhagen, I. A., Plaza, S. M., & Reiser, M. B. (2022) · Current Biology · doi:10.1016/j.cub.2022.06.061 · Cited by 64 · see citing works
Kind, E., Longden, K. D., Nern, A., Zhao, A., Sancer, G., Flynn, M. A., Laughland, C. W., Gezahegn, B., Ludwigh, H., Thomson, A., et al. (2021) · eLife · doi:10.7554/elife.71858 · Cited by 62 · see citing works
Deciphering the generating rules and functionalities of complex networks
Xiao, X., Chen, H., & Bogdan, P. (2021) · Scientific Reports · doi:10.1038/s41598-021-02203-4 · Cited by 63 · see citing works
Visual processing in the fly, from photoreceptors to behavior
Currier, T. A., Pang, M. M., & Clandinin, T. R. (2023) · GENETICS · doi:10.1093/genetics/iyad064 · Cited by 63 · see citing works
Intrinsic Activity in the Fly Brain Gates Visual Information during Behavioral ChoicesPreprint
Tang, S., & Juusola, M. (2010) · Nature Precedings · doi:10.1371/journal.pone.0014455 · Cited by 63 · see citing works
Eye evolution at high resolution: The neuron as a unit of homology
Erclik, T., Hartenstein, V., McInnes, R. R., & Lipshitz, H. D. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.05.565 · Cited by 61 · see citing works
Kinoshita, M., Shimohigasshi, M., Tominaga, Y., Arikawa, K., & Homberg, U. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23674 · Cited by 58 · see citing works
Neural network organization for courtship-song feature detection in Drosophila
Baker, C. A., McKellar, C., Pang, R., Nern, A., Dorkenwald, S., Pacheco, D. A., Eckstein, N., Funke, J., Dickson, B. J., & Murthy, M. (2022) · Current Biology · doi:10.1016/j.cub.2022.06.019 · Cited by 57 · see citing works
Development‐based compartmentalization of the Drosophila central brain
Pereanu, W., Kumar, A., Jenett, A., Reichert, H., & Hartenstein, V. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22376 · Cited by 55 · see citing works
Matsuo, E., Seki, H., Asai, T., Morimoto, T., Miyakawa, H., Ito, K., & Kamikouchi, A. (2016) · Journal of Comparative Neurology · doi:10.1002/cne.23955 · Cited by 56 · see citing works
Self-citationSpatial readout of visual looming in the central brain of Drosophila
Morimoto, M. M., Nern, A., Zhao, A., Rogers, E. M., Wong, A. M., Isaacson, M. D., Bock, D. D., Rubin, G. M., & Reiser, M. B. (2020) · eLife · doi:10.7554/elife.57685 · Cited by 56 · see citing works
The Irre Cell Recognition Module (IRM) Proteins
Fischbach, K., Linneweber, G. A., Andlauer, T. F. M., Hertenstein, A., Bonengel, B., & Chaudhary, K. (2009) · Journal of Neurogenetics · doi:10.1080/01677060802471668 · Cited by 56 · see citing works
Mapping chromatic pathways in the Drosophila visual system
Lin, T., Luo, J., Shinomiya, K., Ting, C., Lu, Z., Meinertzhagen, I. A., & Lee, C. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23857 · Cited by 54 · see citing works
Anatomical organization of the brain of a diurnal and a nocturnal dung beetle
Immonen, E., Dacke, M., Heinze, S., & el Jundi, B. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24169 · Cited by 54 · see citing works
Otsuna, H., Shinomiya, K., & Ito, K. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00008 · Cited by 53 · see citing works
Self-citationNon-canonical Receptive Field Properties and Neuromodulation of Feature-Detecting Neurons in Flies
Städele, C., Keleş, M. F., Mongeau, J.-M., & Frye, M. A. (2020) · Current Biology · doi:10.1016/j.cub.2020.04.069 · Cited by 52 · see citing works
Inhibitory Interactions and Columnar Inputs to an Object Motion Detector in Drosophila
Keleş, M. F., Hardcastle, B. J., Städele, C., Xiao, Q., & Frye, M. A. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.01.061 · Cited by 50 · see citing works
Fischbach, K., & Hiesinger, P. R. (2009) · Advances in experimental medicine and biology · doi:10.1007/978-0-387-78261-4_8 · Cited by 49 · see citing works
Raghu, S. V., Joesch, M., Borst, A., & Reiff, D. F. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21319 · Cited by 48 · see citing works
Zhao, B., Sun, J., Zhang, X., Mo, H., Niu, Y., Li, Q., Wang, L., & Zhong, Y. (2019) · Nature Communications · doi:10.1038/s41467-019-12436-7 · Cited by 49 · see citing works
The brain of Cataglyphis ants: Neuronal organization and visual projections
Habenstein, J., Amini, E., Grübel, K., el Jundi, B., & Rößler, W. (2020) · The Journal of Comparative Neurology · doi:10.1002/cne.24934 · Cited by 48 · see citing works
Object-Displacement-Sensitive Visual Neurons Drive Freezing in Drosophila
Tanaka, R., & Clark, D. A. (2020) · Current Biology · doi:10.1016/j.cub.2020.04.068 · Cited by 44 · see citing works
Mapping model units to visual neurons reveals population code for social behaviour
Cowley, B. R., Calhoun, A. J., Rangarajan, N., Ireland, E., Turner, M. H., Pillow, J. W., & Murthy, M. (2024) · Nature · doi:10.1038/s41586-024-07451-8 · Cited by 45 · see citing works
Strausfeld, N. J., Sinakevitch, I. G., & Okamura, J.-Y. (2007) · Developmental Neurobiology · doi:10.1002/dneu.20396 · Cited by 45 · see citing works
Connectomic reconstruction predicts visual features used for navigation
Garner, D., Kind, E., Lai, J. Y. H., Nern, A., Zhao, A., Houghton, L., Sancer, G., Wolff, T., Rubin, G. M., Wernet, M. F., et al. (2024) · Nature · doi:10.1038/s41586-024-07967-z · Cited by 44 · see citing works
Drosophilafly straight by fixating objects in the face of expanding optic flow
Reiser, M. B., & Dickinson, M. H. (2010) · Journal of Experimental Biology · doi:10.1242/jeb.035147 · Cited by 44 · see citing works
Preserving Neural Function under Extreme Scaling
Cuntz, H., Förstner, F., Schnell, B., Ammer, G., Raghu, S. V., & Borst, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071540 · Cited by 43 · see citing works
Visual Input into the Drosophila melanogaster Mushroom Body
Li, J., Mahoney, B. D., Jacob, M. S., & Caron, S. J. C. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108138 · Cited by 43 · see citing works
From Form to Function: the Ways to Know a Neuron
Meinertzhagen, I. A., Takemura, S.-Y., Meinertzhagen, I. A., Takemura, S.-Y., Lu, Z., Huang, S., Gao, S., Ting, C., & Lee, C. (2009) · Journal of Neurogenetics · doi:10.1080/01677060802610604 · Cited by 42 · see citing works
- Authors
- Otsuna, H., & Ito, K.
- Affiliations
- National Institute for Basic Biology (JP)
- Corresponding author
- Ito, Kei
- Venue
- The Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2006
- Volume
- 497
- Issue
- 6
- Pages
- 928-958
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W1981666992
- Cited by
- 224
- References
- 64
- Citations by year
- 2026: 7 · 2025: 10 · 2024: 20 · 2023: 9 · 2022: 14 · 2021: 7 · 2020: 20 · 2019: 8 · 2018: 6 · 2017: 12 · 2016: 11 · 2015: 8 · 2014: 14 · 2013: 12 · 2012: 21
- FWCI
- 3.80
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- 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
- Drosophila melanogaster, optic lobe, lobula, central brain, visual processing, insect visual system
- MeSH terms
- Animals, Drosophila melanogaster, Female, Neurons, Optic Lobe, Nonmammalian, Visual Pathways
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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.
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