Skip to main content
SpringerLink
Log in

The Development of the Drosophila Larval Brain

  • Chapter
Brain Development in Drosophila melanogaster

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 628))

Abstract

In this chapter we will start out by describing in more detail the progenitors of the nervous system, the neuroblasts and ganglion mother cells. Subsequently we will survey the generic cell types that make up the developing Drosophila brain, namely neurons, glial cells and tracheal cells. Finally, we will attempt a synopsis of the neuronal connectivity of the larval brain that can be deduced from the analysis of neural lineages and their relationship to neuropile compartments.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Urbach R, Technau GM. Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 2003; 130(16):3621–3637.

    Article  PubMed  CAS  Google Scholar 

  2. Younossi-Hartenstein A, Nassif C, Green P et al. Early neurogenesis of the Drosophila brain. J Comp Neurol 1996; 370(3):313–329.

    Article  PubMed  CAS  Google Scholar 

  3. Hartenstein V, Rudloff E, Campos-Ortega JA. The pattern of proliferation of the neuroblasts in the wild-type embryo of Drosophila melanogaster. Dev Genes Evol 1987; 196:473–485.

    Google Scholar 

  4. Brody T, Odenwald WF. Cellular diversity in the developing nervous system: a temporal view from Drosophila. Development 2002; 129(16):3763–3770.

    PubMed  CAS  Google Scholar 

  5. Ito K, Hotta Y. Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Dev Biol 1992; 149(1):134–148.

    Article  PubMed  CAS  Google Scholar 

  6. Ceron J, Gonzalez C, Tejedor FJ. Patterns of cell division and expression of asymmetric cell fate deter minants in postembryonic neuroblast lineages of Drosophila. Dev Biol 2001; 230(2):125–138.

    Article  PubMed  CAS  Google Scholar 

  7. 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(8):3325–3335.

    PubMed  CAS  Google Scholar 

  8. Dumstrei K, Wang F, Nassif C et al. Early development of the Drosophila brain: V. Pattern of postembryonic neuronal lineages expressing DE-cadherin. J Comp Neurol 2003; 455(4):451–462.

    Article  PubMed  Google Scholar 

  9. Rolls MM, Albertson R, Shih HP et al. Drosophila aPKC regulates cell polarity and cell proliferation in neuroblasts and epithelia. J Cell Biol 2003; 163(5):1089–1098.

    Article  PubMed  CAS  Google Scholar 

  10. Schaefer M, Shevchenko A, Knoblich JA et al. A protein complex containing Inscuteable and the Galpha-binding protein Pins orients asymmetric cell divisions in Drosophila. Curr Biol 2000; 10(7):353–362.

    Article  PubMed  CAS  Google Scholar 

  11. Schober M, Schaefer M, Knoblich JA. Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts. Nature 1999; 402(6761):548–551.

    Article  PubMed  CAS  Google Scholar 

  12. Wodarz A, Ramrath A, Kuchinke U et al. Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature 1999; 402(6761):544–547.

    Article  PubMed  CAS  Google Scholar 

  13. Maurange C, Gould AP. Brainy but not too brainy: starting and stopping neuroblast divisions in Drosophila. Trends Neurosci 2005; 28(1):30–36.

    Article  PubMed  CAS  Google Scholar 

  14. 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(4):511–521.

    Article  PubMed  CAS  Google Scholar 

  15. Bilder D. Cell polarity: squaring the circle. Curr Biol 2001; 11(4):R132–135.

    Article  PubMed  CAS  Google Scholar 

  16. Doe CQ, Bowerman B. Asymmetric cell division: fly neuroblast meets worm zygote. Curr Opin Cell Biol 2001; 13(1):68–75.

    Article  PubMed  CAS  Google Scholar 

  17. Ebens AJ, Garren H, Cheyette BN et al. The Drosophila anachronism locus: a glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 1993; 74(1): 15–27.

    Article  PubMed  CAS  Google Scholar 

  18. Bello BC, Hirth F, Gould AP. A pulse of the Drosophila Hox protein Abdominal-A schedules the end of neural proliferation via neuroblast apoptosis. Neuron 2003; 37(2):209–219.

    Article  PubMed  CAS  Google Scholar 

  19. Voigt A, Pflanz R, Schafer U et al. Perlecan participates in proliferation activation of quiescent Drosophila neuroblasts. Dev Dyn 2002; 224(4):403–412.

    Article  PubMed  CAS  Google Scholar 

  20. Park Y, Rangel C, Reynolds MM et al. Drosophila perlecan modulates FGF and hedgehog signals to activate neural stem cell division. Dev Biol 2003; 253(2):247–257.

    Article  PubMed  CAS  Google Scholar 

  21. Datta S. Control of proliferation activation in quiescent neuroblasts of the Drosophila central nervous system. Development 1995; 121(4):1173–1182.

    PubMed  CAS  Google Scholar 

  22. Caldwell MC, Datta S. Expression of cyclin E or DP/E2F rescues the G1 arrest of trol mutant neuroblasts in the Drosophila larval central nervous system. Mech Dev 1998; 79(1–2):121–130.

    Article  PubMed  CAS  Google Scholar 

  23. Park Y, Ng C, Datta S. Induction of string rescues the neuroblast proliferation defect in trol mutant animals. Genesis 2003; 36(4): 187–195.

    Article  PubMed  CAS  Google Scholar 

  24. Almeida MS, Bray SJ. Regulation of post-embryonic neuroblasts by Drosophila Grainyhead. Mech Dev 2005; 122(12):1282–1293.

    Article  PubMed  CAS  Google Scholar 

  25. Akong K, Grevengoed EE, Price MH et al. Drosophila APC2 and APC1 play overlapping roles in wingless signaling in the embryo and imaginal discs. Dev Biol 2002; 250(1):91–100.

    Article  PubMed  CAS  Google Scholar 

  26. Strausfeld NJ. Altas of an Insect Brain. Springer, 1976.

    Google Scholar 

  27. Crittenden JR, Skoulakis EM, Han KA et al. Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 1998; 5(1–2):38–51.

    PubMed  CAS  Google Scholar 

  28. 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(4):761–771.

    PubMed  CAS  Google Scholar 

  29. Noveen A, Daniel A, Hartenstein V. Early development of the Drosophila mushroom body: the roles of eyeless and dachshund. Development 2000; 127(16):3475–3488.

    PubMed  CAS  Google Scholar 

  30. Tettamanti M, Armstrong JD, Endo K et al. Early development of the Drosophila mushroom bodies, brain centres for associative learning and memory. Dev Genes Evol 1997; 207(4):242–252.

    Article  Google Scholar 

  31. 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(1–2):52–77.

    PubMed  CAS  Google Scholar 

  32. 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(1):41–64.

    Article  PubMed  CAS  Google Scholar 

  33. 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(2):186–204.

    Article  PubMed  CAS  Google Scholar 

  34. Prokop A, Meinertzhagen IA. Development and structure of synaptic contacts in Drosophila. Semin Cell Dev Biol 2006; 17(1):20–30.

    Article  PubMed  CAS  Google Scholar 

  35. Sanchez-Soriano N, Bottenberg W, Fiala A et al. Are dendrites in Drosophila homologous to vertebrate dendrites? Dev Biol 2005; 288(1):126–138.

    Article  PubMed  CAS  Google Scholar 

  36. Clark IE, Jan LY, Jan YN. Reciprocal localization of Nod and kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium, neuron and muscle. Development 1997; 124(2):461–470.

    PubMed  CAS  Google Scholar 

  37. Chang T, Younossi-Hartenstein A, Hartenstein V. Development of neural lineages derived from the sine oculis positive eye field of Drosophila. Arhtropod Stru Dev 2003; 32:303–317.

    Article  Google Scholar 

  38. 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(20):5534–5553.

    Article  PubMed  CAS  Google Scholar 

  39. Camera R. Glial cells in adult and developing prothoracic ganglion of the hawk moth Manduca sexta. Cell Tiss Res 1993; 272:93–108.

    Article  Google Scholar 

  40. Hoyle G. Glial cells of an insect ganglion. J Comp Neurol 1986; 246(1):85–103.

    Article  PubMed  CAS  Google Scholar 

  41. Ito K, Urbach R, Technau GM. Distribution, classification and development of Drosophila glia cells in the late embryonic and early larval ventral nerve cord. Dev Genes Evol 1995; 204:284–307.

    Google Scholar 

  42. Saint Marie RL, Carlson SD, Chi C. The Glial Cells of Insects. New York, NY: Plenum 1984.

    Google Scholar 

  43. Lane N. Insect intercellular junctions: Their structure and development. New York: Plenum 1982.

    Google Scholar 

  44. Hoyle G, Williams M, Phillips C. Functional morphology of insect neuronal cell-surface/glial contacts: the trophospongium. J Comp Neurol 1986; 246(1):113–128.

    Article  PubMed  CAS  Google Scholar 

  45. Hidalgo A. Neuron-glia interactions during axon guidance in Drosophila. Biochem Soc Trans 2003; 31 (Pt l):50–55.

    Article  PubMed  CAS  Google Scholar 

  46. Pielage J, Klambt C. Glial cells aid axonal target selection. Trends Neurosci 2001; 24(8):432–433.

    Article  PubMed  CAS  Google Scholar 

  47. Sepp KJ, Auld VJ. Reciprocal interactions between neurons and glia are required for Drosophila peripheral nervous system development. J Neurosci 2003; 23(23):8221–8230.

    PubMed  CAS  Google Scholar 

  48. Sepp KJ, Schulte J, Auld VJ. Peripheral glia direct axon guidance across the CNS/PNS transition zone. Dev Biol 2001; 238(1):47–63.

    Article  PubMed  CAS  Google Scholar 

  49. Oland LA, Tolbert LP. Key interactions between neurons and glial cells during neural development in insects. Annu Rev Entomol 2003; 48:89–110.

    Article  PubMed  CAS  Google Scholar 

  50. Hartenstein V, Nassif C, Lekven A. Embryonic development of the Drosophila brain. II. Pattern of glial cells. J Comp Neurol 1998; 402(1):32–47.

    Article  PubMed  CAS  Google Scholar 

  51. Pereanu W, Shy D, Hartenstein V. Morphogenesis and proliferation of the larval brain glia in Drosophila. Dev Biol 2005; 283(1):191–203.

    Article  PubMed  CAS  Google Scholar 

  52. Younossi-Hartenstein A, Nguyen B, Shy D et al. Embryonic origin of the Drosophila brain neuropile. J Comp Neurol 2006; 497(6):981–998.

    Article  PubMed  Google Scholar 

  53. Pereanu W, Spindler S, Cruz L et al. Tracheal development in the Drosophila brain is constrained by glial cells. Dev Biol 2006.

    Google Scholar 

  54. Manning G, Krasnow MA. Development of the Drosophila tracheal system. New York: Cold Spring Harbor, Laboratory Press 1993.

    Google Scholar 

  55. Englund C, Uv AE, Cantera R et al. adrift, a novel bnl-induced Drosophila gene, required for tracheal pathfinding into the CNS. Development 1999; 126(7):1505–1514.

    PubMed  CAS  Google Scholar 

  56. Nassif C, Noveen A, Hartenstein V. Embryonic development of the Drosophila brain. I. Pattern of pioneer tracts. J Comp Neurol 1998; 402(1):10–31.

    Article  PubMed  CAS  Google Scholar 

  57. 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(4):417–434.

    Article  PubMed  Google Scholar 

  58. Goodman CS, Doe CQ. Embryonic development of the Drosophila central nervous system. New York: Cold Spring Harbor Laboratory Press, 1993.

    Google Scholar 

  59. Hirth F, Kammermeier L, Frei E et al. An urbilaterian origin of the tripartite brain: developmental genetic insights from Drosophila. Development 2003; 130(11):2365–2373.

    Article  PubMed  CAS  Google Scholar 

  60. Therianos S, Leuzinger S, Hirth F et al. Embryonic development of the Drosophila brain: formation of commissural and descending pathways. Development 1995; 121(11):3849–3860.

    PubMed  CAS  Google Scholar 

  61. Strausfeld NJ, Bassemir U, Singh RN et al. Organizational principles of outputs from Dipteran brains. J Ins Physiol 1984; 30(1):73–93.

    Article  Google Scholar 

  62. Armstrong JD, de Belle JS, Wang Z et al. Metamorphosis of the mushroom bodies; large-scale rearrangements of the neural substrates for associative learning and memory in Drosophila. Learn Mem 1998; 5(1–2):102–114.

    PubMed  CAS  Google Scholar 

  63. 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(12):2603–2610.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Cell and Developmental Biology, University of California, Los Angeles, Los Angeles, California, 90095, USA

    Volker Hartenstein, Shana Spindler, Wayne Pereanu & Siaumin Fung

Authors
  1. Volker Hartenstein
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shana Spindler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wayne Pereanu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Siaumin Fung
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Institute of Genetics, University of Mainz, Mainz, Germany

    Gerhard M. Technau PhD

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Landes Bioscience and Springer Science+Business Media

About this chapter

Cite this chapter

Hartenstein, V., Spindler, S., Pereanu, W., Fung, S. (2008). The Development of the Drosophila Larval Brain. In: Technau, G.M. (eds) Brain Development in Drosophila melanogaster . Advances in Experimental Medicine and Biology, vol 628. Springer, New York, NY. https://doi.org/10.1007/978-0-387-78261-4_1

Download citation

Publish with us

Policies and ethics

Search

Navigation