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Development of the Drosophila Mushroom Bodies: Sequential Generation of Three Distinct Types of Neurons from a Neuroblast

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Tzumin Lee, Arthur Lee, and Liqun Luo*

Department of Biological Sciences, Stanford University, Stanford, CA 94305

Originially published in: Development 126:4065-76 (1999)

*Correspondence: lluo@stanford.edu


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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 and Luo, Neuron 22: 451-461, 1999), we have positively marked the axons and dendrites of multi-cellular and single-cell mushroom body clones at specific developmental stages. Systematic clonal analysis demonstrates that a single mushroom body neuroblast sequentially generates at least 3 types of morphologically distinct neurons. Neurons projecting into the g lobe of the adult MB are born first, prior to the mid-3rd instar larval stage. Neurons projecting into the a' and b' lobes are born between the mid-3rd instar larval stage and puparium formation. Finally, neurons projecting into the a and b 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 (g) neurons retain only their main processes in the peduncle, which then project into the adult g lobe without bifurcation. In contrast, the basic axon projections of the later born (a'/b') 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.


Figure 1 - The organization of the adult mushroom bodies (MBs) and clonal analysis using MARCM.


Figure 2 - Development of MB neuroblast clones.


Figure 2-2 - Development of MB neuroblast clones.


Figure 3 - Lobe compositions of MB Nb clones generated at different stages.


Figure 4 - Sequential generation of three distinct types of MB neurons with characteristic axonal projections.


Figure 5 - Morphological characterization of three types of MB neurons.


Figure 6 - Different behaviors of g and a'/b' neurons during metamorphosis.


Figure 7 - Axon reorganization of g neurons during metamorphosis.


Figure 8 - Summary of the mushroom body development.


 

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