Clonal Unit Architecture of the Adult Fly Brain

  • Kei Ito
  • Takeshi Awasaki
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 628)


During larval neurogenesis, neuroblasts repeat asymmetric cell divisions to generate clonally related progeny. When the progeny of a single neuroblast is visualized in the larval brain, their cell bodies form a cluster and their neurites form a tight bundle. This structure persists in the adult brain. Neurites deriving from the cells in this cluster form bundles to innervate distinct areas of the brain. Such clonal unit structure was first identified in the mushroom body, which is formed by four nearly identical clonal units each of which consists of diverse types of neurons. Organised structures in other areas of the brain, such as the central complex and the antennal lobe projection neurons, also consist of distinct clonal units. Many clonally related neural circuits are observed also in the rest of the brain, which is often called diffused neuropiles because of the apparent lack of clearly demarcated structures. Thus, it is likely that the clonal units are the building blocks of a significant portion of the adult brain circuits. Arborisations of the clonal units are not mutually exclusive, however. Rather, several clonal units contribute together to form distinct neural circuit units, to which other clones contribute relatively marginally. Construction of the brain by combining such groups of clonally related units would have been a simple and efficient strategy for building the complicated neural circuits during development as well as during evolution.


Mushroom Body Optic Lobe Kenyon Cell Neurite Bundle Larval Brain 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Power ME. The brain of Drosophila. J Morph 1943; 72:517–559.CrossRefGoogle Scholar
  2. 2.
    Strausfeld NJ. Atlas of an Insect Brain. Berlin, Heidelberg, New York, Tokyo: Springer-Verlag, 1976.Google Scholar
  3. 3.
    Crittenden JR, Skoulakis EM, Han KA et al. Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 1998; 5:38–51.PubMedGoogle Scholar
  4. 4.
    Tanaka NK, Awasaki T, Shimada T et al. Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr Biol 2004; 14:449–457.PubMedCrossRefGoogle Scholar
  5. 5.
    Otsuna H, Ito K. Systematic analysis of the visual projection neurons of Drosophila melanogaster I. Lobula-specific pathways. J Comp Neurol 2006; 497:928–958.PubMedCrossRefGoogle Scholar
  6. 6.
    Truman JW, Bate M. Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev Biol 1988; 125:145–157.PubMedCrossRefGoogle Scholar
  7. 7.
    Ito K, Hotta Y. Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Dev Biol 1992; 149:134–148.PubMedCrossRefGoogle Scholar
  8. 8.
    Fischbach KF, Dittrich APM. The optic lobe of Drosophila melanogaster I. A golgi analysis of wild-type structure. Cell Tissue Res 1989; 258:441–475.CrossRefGoogle Scholar
  9. 9.
    Bausenwein B, Dittrich APM, Fischbach KF. The optic lobe of Drosophila melanogaster II. Sorting of retinotopic pathways in the medulla. Cell Tissue Res 1992; 267:17–28.PubMedCrossRefGoogle Scholar
  10. 10.
    Ito K, Suzuki K, Estes P et al. The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn Mem 1998; 5:52–77.PubMedGoogle Scholar
  11. 11.
    Wagh DA, Rasse TM, Asan E et al. Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 2006; 49:833–844.PubMedCrossRefGoogle Scholar
  12. 12.
    Ito K, Urban J, Technau GM. Distribution, classification and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Roux’s Arch Dev Biol 1995; 204:284–307.CrossRefGoogle Scholar
  13. 13.
    Stocker RF, Lienhard MC, Borst A et al. Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 1990; 262:9–34.PubMedCrossRefGoogle Scholar
  14. 14.
    Stocker RF. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 1994; 275:3–26.PubMedCrossRefGoogle Scholar
  15. 15.
    Kamikouchi A, Shimada T, Ito K. Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster. J Comp Neurol 2006; 499:317–356.PubMedCrossRefGoogle Scholar
  16. 16.
    Hofbauer A, Campos-Ortega JA. Proliferation pattern and early differentiation of the optic lobes in Drosophila melanogaster. Roux’s Arch Dev Biol 1990; 198:264–274.CrossRefGoogle Scholar
  17. 17.
    Prokop A, Technau GM. The origin of postembryonic neuroblasts in the ventral nerve cord of Drosophila melanogaster. Development 1991; 111:79–88.PubMedGoogle Scholar
  18. 18.
    Urbach R, Schnabel R, Technau GM. The pattern of neuroblast formation, mitotic domains and proneural gene expression during early brain development in Drosophila. Development 2003; 130:3589–3606.PubMedCrossRefGoogle Scholar
  19. 19.
    Urbach R, Technau GM. Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 2003; 130:3621–3637.PubMedCrossRefGoogle Scholar
  20. 20.
    Technau GM, Campos-Ortega JA. Fate-mapping in wild-type Drosophila melanogaster. II. Injections of horseradish peroxidase in cells of the early gatrula stage. Roux’s Arch Dev Biol 1985; 194:196–212.Google Scholar
  21. 21.
    Bossing T, Technau GM. The fate of the CNS midline progenitors in Drosophila as revealed by a new method for single cell labelling. Development 1994; 120:1895–1906.PubMedGoogle Scholar
  22. 22.
    Bossing T, Udolph G, Doe CQ et al. The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev Biol 1996; 179:41–64.PubMedCrossRefGoogle Scholar
  23. 23.
    Schmidt H, Rickert C, Bossing T et al. The embryonic central nervous system lineages of Drosophila melanogaster II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev Biol 1997; 189:186–204.PubMedCrossRefGoogle Scholar
  24. 24.
    Schmid A, Chiba A, Doe CQ. Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 1999; 126:4653–4689.PubMedGoogle Scholar
  25. 25.
    Technau GM. Lineage analysis of transplanted individual cells in embryos of Drosophila melanogaster I. The method. Roux’s Arch Dev Biol 1986; 195:389–398.CrossRefGoogle Scholar
  26. 26.
    Technau GM, Campos-Ortega JA. Lineage analysis of transplanted individual cells in embryos of Drosophila melanogaster II. Commitment and proliferative capabilities of neural and epidermal cell progenitors. Roux’s Arch Dev Biol 1986; 195:445–454.CrossRefGoogle Scholar
  27. 27.
    Technau GM, Campos-Ortega JA. Lineage analysis of transplanted individual cells in embryos of Drosophila melanogaster III. Commitment and proliferative capabilities of pole cells and midgut progenitors. Roux’s Arch Dev Biol 1986; 195:489–498.CrossRefGoogle Scholar
  28. 28.
    Prokop A, Technau GM. Early tagma-specific commitment of Drosophila CNS progenitor NB1-1. Development 1994; 120:2567–2578.PubMedGoogle Scholar
  29. 29.
    Fischer JA, Ginigar E, Maniatis T et al. GAL4 activates transcription in Drosophila. Nature 1988; 332:853–856.PubMedCrossRefGoogle Scholar
  30. 30.
    Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993; 118:401–415.PubMedGoogle Scholar
  31. 31.
    Brand AH, Dormand EL. The GAL4 system as a tool for unravelling the mysteries of the Drosophila nervous system. Curr Opin Neurobiol 1995; 5:572–578.PubMedCrossRefGoogle Scholar
  32. 32.
    Golic KG, Lindquist S. The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 1989; 59:499–509.PubMedCrossRefGoogle Scholar
  33. 33.
    Dang DT, Perrimon N. Use of a yeast site-specific recombinase to generate embryonic mosaics in Drosophila. Dev Genet 1992; 13:367–375.PubMedCrossRefGoogle Scholar
  34. 34.
    Xu T, Rubin GM. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 1993; 117:1223–1237.PubMedGoogle Scholar
  35. 35.
    Struhl G, Basler K. Organizing activity of wingless protein in Drosophila. Cell 1993; 72:527–540.PubMedCrossRefGoogle Scholar
  36. 36.
    Ito K, Awano W, Suzuki K et al. The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 1997; 124:761–771.PubMedGoogle Scholar
  37. 37.
    Basler K, Struhl G. Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 1994; 368:208–214.PubMedCrossRefGoogle Scholar
  38. 38.
    Wong AM, Wang JW, Axel R. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 2002; 109:229–241.PubMedCrossRefGoogle Scholar
  39. 39.
    Lee T, Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999; 22:451–461.PubMedCrossRefGoogle Scholar
  40. 40.
    Yang MY, Armstrong JD, Vilinsky I et al. Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 1995; 15:45–54.PubMedCrossRefGoogle Scholar
  41. 41.
    Lee T, Lee A, Luo L. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 1999; 126:4065–4076.PubMedGoogle Scholar
  42. 42.
    Masuda-Nakagawa LM, Tanaka NK, O’Kane CJ. Stereotypic and random patterns of connectivity in the larval mushroom body calyx of Drosophila. Proc Natl Acad Sci USA 2005; 102:19027–19032.PubMedCrossRefGoogle Scholar
  43. 43.
    Ramaekers A, Magnenat E, Marin EC et al. Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Curr Biol 2005; 15:982–992.PubMedCrossRefGoogle Scholar
  44. 44.
    Zhu S, Chiang AS, Lee T. Development of the Drosophila mushroom bodies: elaboration, remodeling and spatial organization of dendrites in the calyx. Development 2003; 130:2603–2610.PubMedCrossRefGoogle Scholar
  45. 45.
    Hanesch U, Fischbach KF, Heisenberg M. Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res 1989; 257:343–366.CrossRefGoogle Scholar
  46. 46.
    Strauss R, Heisenberg M. A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 1993; 13:1852–1861.PubMedGoogle Scholar
  47. 47.
    Strauss R. The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 2002; 12:633–638.PubMedCrossRefGoogle Scholar
  48. 48.
    Liu G, Seiler H, Wen A et al. Distinct memory traces for two visual features in the Drosophila brain. Nature 2006; 439:551–556.PubMedCrossRefGoogle Scholar
  49. 49.
    Jefferis GS, Marin EC, Stocker RF et al. Target neuron prespecification in the olfactory map of Drosophila. Nature 2001; 414:204–208.PubMedCrossRefGoogle Scholar
  50. 50.
    Marin EC, Jefferis GS, Komiyama T et al. Representation of the glomerular olfactory map in the Drosophila brain. Cell 2002; 109:243–255.PubMedCrossRefGoogle Scholar
  51. 51.
    Pereanu W, Hartenstein V. Neural lineages of the Drosophila brain: a three-dimensional digital atlas of the pattern of lineage location and projection at the late larval stage. J Neurosci 2006; 26:5534–5553.PubMedCrossRefGoogle Scholar
  52. 52.
    Akong K, McCartney BM, Peifer M. Drosophila APC2 and APC1 have overlapping roles in the larval brain despite their distinct intracellular localizations. Dev Biol 2002; 250:71–90.PubMedCrossRefGoogle Scholar
  53. 53.
    Nassif C, Noveen A, Hartenstein V. Early development of the Drosophila brain: III. The pattern of neuropile founder tracts during the larval period. J Comp Neurol 2003; 455:417–434.PubMedCrossRefGoogle Scholar
  54. 54.
    Dumstrei K, Wang F, Hartenstein V. Role of DE-cadherin in neuroblast proliferation, neural morphogenesis and axon tract formation in Drosophila larval brain development. J Neurosci 2003; 23:3325–3335.PubMedGoogle Scholar
  55. 55.
    Pereanu W, Shy D, Hartenstein V. Morphogenesis and proliferation of the larval brain glia in Drosophila. Dev Biol 2005; 283:191–203.PubMedCrossRefGoogle Scholar
  56. 56.
    Tessier-Lavigne M, Goodman CS. The molecular biology of axon guidance. Science 1996; 274:1123–1133.PubMedCrossRefGoogle Scholar
  57. 57.
    Isshiki T, Pearson B, Holbrook S et al. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 2001; 106:511–21.PubMedCrossRefGoogle Scholar
  58. 58.
    Zhu S, Lin S, Kao CF et al. Gradients of the Drosophila Chinmo BTB-zinc finger protein govern neuronal temporal identity. Cell 2006; 127:409–422.PubMedCrossRefGoogle Scholar
  59. 59.
    Endo K, Aoki T, Yoda Y et al. Notch signal organizes the Drosophila olfactory circuitry by diversifying the sensory neuronal lineages. Nat Neurosci 2007; 10:153–160.PubMedCrossRefGoogle Scholar
  60. 60.
    Vowles D. The structure and connections of the corpora pedunculata in bees and ants. QJ Microsc Sci 1955; 96:239–255.Google Scholar
  61. 61.
    Pearson L. The corpora pedunculata of Sphinx ligustri L. and other Lepidoptera: an anatomical study. Philos Trans R Soc Lond B 1972; 259:477–516.CrossRefGoogle Scholar
  62. 62.
    Heisenberg M. Mutants of brain structure and function: what is the significance of the mushroom bodies for behavior? Basic Life Sci 1980; 16:373–390.PubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2008

Authors and Affiliations

  • Kei Ito
    • 1
  • Takeshi Awasaki
    • 1
    • 2
  1. 1.Institute of Molecular and Cellular Biosciencesthe University of TokyoTokyoJapan
  2. 2.Department of NeurobiologyUniversity of Massachusetts Medical SchoolWorcesterUSA

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