Synaptic circuits of the Drosophila optic lobe: The input terminals to the medulla
Open accessAbstract
Understanding the visual pathways of the fly's compound eye has been blocked for decades at the second optic neuropil, the medulla, a two-part relay comprising 10 strata (M1-M10), and the largest neuropil in the fly's brain. Based on the modularity of its composition, and two previous reports, on Golgi-impregnated cell types (Fischbach and Dittrich, Cell Tissue Res.,1989; 258:441-475) and their synaptic circuits in the first neuropil, the lamina, we used serial-section electron microscopy to examine inputs to the distal strata M1-M6. We report the morphology of the reconstructed medulla terminals of five lamina cells, L1-L5, two photoreceptors, R7 and R8, and three neurons, medulla cell T1 and centrifugal cells C2 and C3. The morphology of these conforms closely to previous reports from Golgi impregnation. This fidelity provides assurance that our reconstructions are complete and accurate. Synapses of these terminals broadly localize to the terminal and provide contacts to unidentified targets, mostly medulla cells, as well as sites of connection between the terminals themselves. These reveal that R8 forms contacts upon R7 and thus between these two spectral inputs; that L3 provides input upon both pathways, adding an achromatic input; that the terminal of L5 reciprocally connects to that of L1, thus being synaptic in the medulla despite lacking synapses in the lamina; that the motion-sensing input cells L1 and L2 lack direct interconnection but both receive input from C2 and C3, resembling lamina connections of these cells; and that, as in the lamina, T1 provides no output chemical synapses.
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The vast majority of optic lobe cell types are based on previous literature.
“The vast majority of these types are based on previous literature42,93–99.”
From Whole-brain annotation and multi-connectome cell typing of Drosophila (2024) · cites this paper as [98]
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Cites
The structure of the nervous system of the nematode <i>Caenorhabditis elegans</i>
White, J. G., Southgate, E., Thomson, J. N., & Brenner, S. (1986) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1986.0056 · Cited by 5,589 · see citing works
Estimation of nuclear population from microtome sections
Abercrombie, M. (1946) · The Anatomical Record · doi:10.1002/ar.1090940210 · Cited by 4,363 · see citing works
Patterns of projection in the visual system of the fly. I. Retina-lamina projections
Braitenberg, V. (1967) · Experimental Brain Research · doi:10.1007/bf00235589 · Cited by 432 · see citing works
Otsuna, H., & Ito, K. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21015 · Cited by 224 · see citing works
Flagged first, then by citations
Research works printed but not linked: 64
- Bausenwein B Fischbach K-F 1992 Activity labeling patterns in the medulla of Drosophila melanogaster caused by motion stimuli Cell Tiss Res 270 25 35 1423522
- Bausenwein B Dittrich APM Fischbach K-F 1992 The optic lobe of Drosophila melanogaster II. Sorting of retinotopic pathways in the medulla Cell Tissue Res 267 17 28 1735111
- Bodian D 1962 The generalized vertebrate neuron Science 137 323 326 13870420
- Borst A 2000 Models of motion detection Nat Neurosci 3 Suppl 1168 11127831
- Borst A Egelhaaf M 1989 Principles of visual motion detection Trends Neurosci 12 297 306 2475948
- Borycz JA Borycz J Kubów A Kostyleva R Meinertzhagen IA 2005 Histamine compartments of the Drosophila brain with an estimate of the quantum content at the photoreceptor synapse J Neurophysiol 93 1611 1619 15738275
- Boschek CB 1971 On the fine structure of the peripheral retina and lamina ganglionaris of the fly, Musca domestica Z Zellforsch mikrosk Anat 118 369 409 5566322
- Braitenberg V 1970 Ordnung und Orientierung der Elemente im Sehsystem der Fliege Kybernetik 7 235 242 4324777
- Braitenberg V Hauser-Holschuh H 1972 Patterns of projection in the visual system of the fly II. Quantitative aspects of second order neurons in relation to models of movement perception Exp Brain Res 16 184 209 4647183
- Brand AH Perrimon N 1993 Targeted gene expression as a means of altering cell fates and generating dominant phenotypes Development 118 401 415 8223268
- Buchner E Bader R Buchner S Cox J Emson PC Flory E Heizmann CW Hemm S Hofbauer A Oertel WH 1988 Cell-specific immuno-probes for the brain of normal and mutant Drosophila melanogaster. I. Wildtype visual system Cell Tiss Res 253 357 370 2900684
- Campos-Ortega JA Strausfeld NJ Wehner R 1972 Columns and layers in the second synaptic region of the fly’s visual system: The case for two superimposed neuronal architectures Information processing in the visual systems of arthropods 31 36 Springer-Verlag Berlin, Heidelberg, New York
- Chou WH Huber A Bentrop J Schulz S Schwab K Chadwell LV Paulsen R Britt SG 1999 Patterning of the R7 and R8 photoreceptor cells of Drosophila: evidence for induced and default cell-fate specification Development 126 607 616 9895309
- Cohen E Sterling P 1990 Demonstration of cell types among cone bipolar neurons of cat retina Phil Trans Biol Sci 330 305 321 1982357
- Cook T Desplan C 2001 Photoreceptor subtype specification: from flies to humans Semin Cell Dev Biol 12 509 18 11735387
- Douglass JK Strausfeld NJ 1995 Visual motion detection circuits in flies: Peripheral motion computation by identified small-field retinotopic neurons J Neurosci 15 5596 5611 7643204 PMC6577634
- Douglass JK Strausfeld NJ 1996 Visual motion detection circuits in flies: Parallel direction- and non-direction-sensitive pathways between medulla and lobula plate J Neurosci 16 4551 4562 8764644 PMC6579027
- Dowling JE 1987 The Retina Harvard University Press Cambridge, MA
- Dowling JE Boycott BB 1966 Organization of the primate retina: electron microscopy Proc Roy Soc Lond B 166 80 111 4382694
- Fabian-Fine R Verstreken P Hiesinger PR Horne JA Kostyleva R Zhou Y Bellen HJ Meinertzhagen IA 2003 Endophilin promotes a late step in endocytosis at glial invaginations in Drosophila photoreceptor terminals J Neurosci 23 10732 10744 14627659 PMC6740933
- Fiala JC 2005 Reconstruct: a free editor for serial section microscopy J Microsc 218 52 61 15817063
- Fiala JC Harris KM 2001 Extending unbiased stereology of brain ultrastructure to three-dimensional volumes J Am Med Inform Assoc 8 1 16 11141509 PMC134588
- Franceschini N Kirschfeld K Minke B 1981 Fluorescence of photoreceptor cells observed in vivo Science 213 1264 1267 7268434
- Hardie RC Autrum H Ottoson D Perl ER Schmidt RF Shimazu H Willis WD 1985 Functional organization of the fly retina Progress in Sensory Physiology 5 New York Springer-Verlag 1 79
- Hardie RC Stavenga DG Hardie RC 1989 Neurotransmitters in compound eyes Facets of Vision Berlin, Heidelberg Springer-Verlag 235 256
- Hausen K Ali MA 1984 The lobula-complex of the fly: Structure, function and significance in visual behavior Photoreception and Vision in Invertebrates New York Plenum Press 523 559
- Jack JJB Noble D Tsien RW 1975 Electric Current Flow in Excitable Cells Oxford Clarendon Press
- Kolodziejczyk A Sun X Meinertzhagen IA Nässel DR 2008 Glutamate, GABA and acetylcholine signaling components in the lamina of the fly’s visual system PLoS ONE resubmitted PMC2373871 18464935
- Koshitaka H Kinoshita M Vorobyev M Arikawa K 2008 Tetrachromacy in a butterfly that has eight varieties of spectral receptors Proc Biol Sci 275 947 954 18230593 PMC2599938
- Langley K Grant NJ 1997 Are exocytosis mechanisms neurotransmitter specific? Neurochem Int 31 739 757 9413835
- Lee T Luo L 1999 Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis Neuron 22 451 461 10197526
- Masland RH 2004 Neuronal cell types Curr Biol 14 R497 500 15242626
- Masland RH Raviola E 2000 Confronting complexity: strategies for understanding the microcircuitry of the retina Ann Rev Neurosci 23 249 284 10845065
- Meinertzhagen IA 1976 The organization of perpendicular fibre pathways in the insect optic lobe Phil Trans Roy Soc Lond Ser B 274 555 596 11512
- Meinertzhagen IA O’Neil SD 1991 The synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster J Comp Neurol 305 232 263 1902848
- Meinertzhagen IA Sorra KE 2001 Synaptic organisation in the fly’s optic lamina: few cells, many synapses and divergent microcircuits Progr Brain Res 131 53 69 11420968
- Milo R Shen-Orr S Itzkovitz S Kashtan N Chklovskii D Alon U 2002 Network motifs: simple building blocks of complex networks Science 298 824 827 12399590
- Morante J Desplan C 2004 Building a projection map for photoreceptor neurons in the Drosophila optic lobes Semin Cell Dev Biol 15 137 43 15036216
- Morante J Desplan C 2008 The visual circuit in the medulla of Drosophila: function in color vision Submitted PMC2430089 18403201
- Nicol D Meinertzhagen IA 1982 An analysis of the number and composition of the synaptic populations formed by photoreceptors of the fly J Comp Neurol 207 29 44 7096637
- Palay SF Chan-Palay V 1974 Cerebellar Cortex: Cytology and Organization New York Springer-Verlag
- Pichaud F Briscoe A Desplan C 1999 Evolution of color vision Curr Opin Neurobiol 9 622 627 10508742
- Pollack I Hofbauer A 1991 Histamine-like immunoreactivity in the visual system and brain of Drosophila melanogaster Cell Tiss Res 266 391 398 1684918
- Rall W Burke RE Holmes WR Jack JJ Redman SJ Segev I 1992 Matching dendritic neuron models to experimental data Physiol Rev 72 Suppl S159 186 1438585
- Ready DF Hanson TE Benzer S 1976 Development of the Drosophila retina, a neurocrystalline lattice Dev Biol 53 217 240 825400
- Reichardt W Rosenblith WA 1961 Autocorrelation, a principle for the evaluation of sensory information by the central nervous system Sensory communication Cambridge, MA MIT Press 303 317
- Rein K Zöckler M Mader MT Grübel C Heisenberg M 2002 The Drosophila standard brain Curr Biol 12 227 231 11839276
- Rister J Pauls D Schnell B Ting CY Lee CH Sinakevitch I Morante J Strausfeld NJ Ito K Heisenberg M 2007 Dissection of the peripheral motion channel in the visual system of Drosophila melanogaster Neuron 56 155 170 17920022
- Scott EK Raabe T Luo L 2002 Structure of the vertical and horizontal system neurons of the lobula plate in Drosophila J Comp Neurol 454 470 481 12455010
- Shaw SR 1984 Early visual processing in insects J Exp Biol 112 225 251 6392468
- Sinakevitch I Douglass JK Scholtz G Loesel R Strausfeld NJ 2003 Conserved and convergent organization in the optic lobes of insects and isopods, with reference to other crustacean taxa J Comp Neurol 467 150 172 14595766
- Sinakevitch I Strausfeld NJ 2004 Chemical neuroanatomy of the fly’s movement detection pathway J Comp Neurol 468 6 23 14648688
- Stark WS Carlson SD 1986 Ultrastructure of capitate projections in the optic neuropil of Diptera Cell Tiss Res 246 481 486 3098431
- Sterling P Shepherd GM 1998 Retina The Synaptic Organization of the Brain New York Oxford University Press 4 205 253
- Strausfeld NJ 1970 Golgi studies on insects. Part II: The optic lobes of Diptera Phil Trans Roy Soc Lond B 258 135 223 22408826
- Strausfeld NJ 1976 Atlas of an Insect Brain Springer-Verlag Berlin, Heidelberg
- Strausfeld NJ Campos-Ortega JA Wehner R 1972 Some interrelationships between the first and second synaptic regions of the fly’s (Musca domestica L.) visual system Information Processing in the Visual Systems of Arthropods Berlin, Heidelberg, New York Springer-Verlag 23 30
- Strausfeld NJ Campos-Ortega JA 1977 Vision in insects: Pathways possibly underlying neural adaptation and lateral inhibition Science 195 894 897 841315
- Strausfeld NJ Lee JK 1991 Neuronal basis for parallel visual processing in the fly Vis Neurosci 7 13 33 1931797
- Takemura SY Arikawa K 2006 Ommatidial type-specific interphotoreceptor connections in the lamina of the swallowtail butterfly, Papilio xuthus J Comp Neurol 494 663 672 16374804
- Trujillo-Cenóz O 1965 Some aspects of the structural organization of the intermediate retina of dipterans J Ultrastruct Res 13 1 33 5840545
- Wernet MF Labhart T Baumann F Mazzoni EO Pichaud F Desplan C 2003 Homothorax switches function of Drosophila photoreceptors from color to polarized light sensors Cell 115 267 79 14636555
- Yasuyama K Kitamoto T Salvaterra PM 1995 Immunocytochemical study of choline acetyltransferase in Drosophila melanogaster: An analysis of cis-regulatory regions controlling expression in the brain of cDNA-transformed flies J Comp Neurol 361 25 37 8550879
- Zheng L de Polavieja GG Wolfram V Asyali MH Hardie RC Juusola M 2006 Feedback network controls photoreceptor output at the layer of first visual synapses in Drosophila J Gen Physiol 127 495 510 16636201 PMC2151524
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- Authors
- Takemura, S., Lu, Z., & Meinertzhagen, I. A.
- Affiliations
- Dalhousie University (CA)
- Corresponding author
- Meinertzhagen, Ian A.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2008-06-06
- Volume
- 509
- Issue
- 5
- Pages
- 493-513
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- PMC
- PMC2481516
- OpenAlex
- W2047572290
- Cited by
- 199
- References
- 4
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 5 · 2023: 6 · 2022: 11 · 2021: 7 · 2020: 12 · 2019: 11 · 2018: 16 · 2017: 10 · 2016: 7 · 2015: 9 · 2014: 24 · 2013: 13 · 2012: 15
- FWCI
- 6.78
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Eye Institute (EY-03592, R01EY003592)
- 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
- medulla, synaptic circuits, lamina, visual pathway, synaptic terminals, serial section electron microscopy, compound eye
- MeSH terms
- Animals, Drosophila, Medulla Oblongata, Nerve Net, Optic Lobe, Nonmammalian, Synapses, Visual Pathways
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