Advertisement
JOURNAL ARTICLES
Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast
T. Lee, A. Lee, L. Luo
Development 1999 126: 4065-4076;

Summary

The mushroom bodies (MBs) are prominent structures in the Drosophila brain that are essential for olfactory learning and memory. Characterization of the development and projection patterns of individual MB neurons will be important for elucidating their functions. Using mosaic analysis with a repressible cell marker (Lee, T. and Luo, L. (1999) Neuron 22, 451–461), we have positively marked the axons and dendrites of multicellular and single-cell mushroom body clones at specific developmental stages. Systematic clonal analysis demonstrates that a single mushroom body neuroblast sequentially generates at least three types of morphologically distinct neurons. Neurons projecting into the (gamma) lobe of the adult MB are born first, prior to the mid-3rd instar larval stage. Neurons projecting into the alpha' and beta' lobes are born between the mid-3rd instar larval stage and puparium formation. Finally, neurons projecting into the alpha and beta lobes are born after puparium formation. Visualization of individual MB neurons has also revealed how different neurons acquire their characteristic axon projections. During the larval stage, axons of all MB neurons bifurcate into both the dorsal and medial lobes. Shortly after puparium formation, larval MB neurons are selectively pruned according to birthdays. Degeneration of axon branches makes early-born gamma neurons retain only their main processes in the peduncle, which then project into the adult gamma lobe without bifurcation. In contrast, the basic axon projections of the later-born (alpha'/beta') larval neurons are preserved during metamorphosis. This study illustrates the cellular organization of mushroom bodies and the development of different MB neurons at the single cell level. It allows for future studies on the molecular mechanisms of mushroom body development.

Reference

    1. Aceves-Pina E. O.,
    2. Quinn W. G.
    (1979) Learning in normal and mutant Drosophila larvae. Science 206, 93–95
    OpenUrlAbstract/FREE Full Text
    1. Cepko C. L.,
    2. Austin C. P.,
    3. Yang X.,
    4. Alexiades M.,
    5. Ezzeddine D.
    (1996) Cell fate determination in the vertebrate retina. Proc. Natl. Acad. Sci. USA 93, 589–595
    OpenUrlAbstract/FREE Full Text
    1. Cepko C. L.,
    2. Fields-Berry S.,
    3. Ryder E.,
    4. Austin C.,
    5. Golden J.
    (1998) Lineage analysis using retroviral vectors. Curr. Top. Dev. Biol 36, 51–74
    OpenUrlPubMedWeb of Science
    1. Connolly J. B.,
    2. Roberts I. J. H.,
    3. Armstrong J. D.,
    4. Kaiser K.,
    5. Forte M.,
    6. Tully T.,
    7. O'Kane C. J.
    (1996) Associative learning disrupted by impaired Gssigaling in Drosophila mushroom bodies. Science 274, 2104–2107
    OpenUrlAbstract/FREE Full Text
    1. Cowan W. M.
    (1998) The emergence of modern neuroanatomy and developmental neurobiology. Neuron 20, 413–426
    OpenUrlCrossRefPubMed
    1. de Belle J. S.,
    2. Heisenberg M.
    (1994) Associative Odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263, 692–695
    OpenUrlAbstract/FREE Full Text
    1. Doe C. Q.,
    2. Technau G. M.
    (1993) Identification and cell lineage of individual neural precursors in the Drosophila CNS. Trends Neurosci 16, 510–514
    OpenUrlCrossRefPubMedWeb of Science
    1. Edlund T.,
    2. Jessell T. M.
    (1999) Progression from extrinsic to intrinsic signaling in cell fate specification: a view from the nervous system. Cell 96, 211–224
    OpenUrlCrossRefPubMedWeb of Science
    1. Fisk G. J.,
    2. Thummel C. S.
    (1998) The DHR78 nuclear receptor is required for ecdysteroid signaling during the onset of Drosophila metamorphosis. Cell 93, 543–555
    OpenUrlCrossRefPubMed
    1. Ghosh A.,
    2. Antonini A.,
    3. McConnell S. K.,
    4. Shatz C. J.
    (1990) Requirement for subplate neurons in the formation of thalamocortical connections. Nature 347, 179–181
    OpenUrlCrossRefPubMedWeb of Science
    1. Heisenberg M.,
    2. Borst A.,
    3. Wagner S.,
    4. Byers D.
    (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenet 2, 1–30
    OpenUrlCrossRefPubMedWeb of Science
    1. Heisenberg M.,
    2. Heusipp M.,
    3. Wanke C.
    (1995) Structural plasticity in the Drosophila brain. J. Neurosci 15, 1951–1960
    OpenUrlAbstract
    1. Ito K.,
    2. Awano W.,
    3. Suzuki K.,
    4. Hiromi Y.,
    5. Yamamoto D.
    (1997) The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurons and glial cells. Development 124, 761–771
    OpenUrlAbstract
    1. Ito K.,
    2. Hotta Y.
    (1992) Proliferation pattern of postembryonicneuroblasts in the brain of Drosophila melanogaster. Dev. Biol 149, 134–148
    OpenUrlCrossRefPubMedWeb of Science
    1. Lee T.,
    2. Luo L.
    (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451–461
    OpenUrlCrossRefPubMedWeb of Science
    1. McConnell S. K.,
    2. Ghosh A.,
    3. Shatz C. J.
    (1989) Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 245, 978–982
    OpenUrlAbstract/FREE Full Text
    1. Sanes J. R.
    (1989) Analysing cell lineage with a recombinant retrovirus. Trends Neurosci 12, 21–28
    OpenUrlCrossRefPubMedWeb of Science
    1. Schubiger M.,
    2. Wade A. A.,
    3. Carney G. E.,
    4. Truman J. W.,
    5. Bender M.
    (1998) Drosophila EcR-B ecdysone receptor isoforms are required for larval molting and for neuron remodeling during metamorphosis. Development 125, 2053–2062
    OpenUrlAbstract
    1. Technau G.
    (1984) Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex, and experience. J. Neurogenet 1, 113–126
    OpenUrlPubMed
    1. Technau G.,
    2. Heisenberg M.
    (1982) Neural reorganization duringmetamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature 295, 405–407
    OpenUrlCrossRefPubMed
    1. Thummel C. S.
    (1996) Flies on steroids—Drosophila metamorphosis and the mechanisms of steroid hormone action. Trends Genetics 12, 306–310
    OpenUrlCrossRefPubMedWeb of Science
    1. Truman J. W.
    (1990) Metamorphosis of the central nervous system of Drosophila. J. Neurobiol 21, 1072–1084
    OpenUrlCrossRefPubMedWeb of Science
    1. Truman J. W.,
    2. Bate M.
    (1988) Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev. Biol 125, 145–157
    OpenUrlCrossRefPubMedWeb of Science
    1. Tully T.,
    2. Cambiazo V.,
    3. Kruse L.
    (1994) Memory through metamorphosis in normal and mutant Drosophila. J. Neurosci 14, 68–74
    OpenUrlAbstract
    1. Yang M. Y.,
    2. Armstrong J. D.,
    3. Vilinsky I.,
    4. Strausfeld N. J.,
    5. Kaiser K.
    (1995) Subdivision of the Drosophila mushroom bodies by enhancer-trap expression pattern. Neuron 15, 45–54
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast
T. Lee, A. Lee, L. Luo
Development 1999 126: 4065-4076;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

Kathryn Virginia Anderson (1952-2020)

Developmental geneticist Kathryn Anderson passed away at home on 30 November 2020. Tamara Caspary, a former postdoc and friend, remembers Kathryn and her remarkable contribution to developmental biology.

Zooming into 2021

In a new Editorial, Editor-in-Chief James Briscoe and Executive Editor Katherine Brown reflect on the triumphs and tribulations of the last 12 months, and look towards a hopefully calmer and more predictable year.

Read & Publish participation extends worldwide

Over 60 institutions in 12 countries are now participating in our Read & Publish initiative. Here, James Briscoe explains what this means for his institution, The Francis Crick Institute. Find out more and view our full list of participating institutions.

Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Sign up to join our next session:

10 February
Time: 13:00 (GMT)
Chaired by: preLights