The Organization of Extrinsic Neurons and Their Implications in the Functional Roles of the Mushroom Bodies in Drosophila melanogaster Meigen

  1. Kei Ito1,6,7,
  2. Kazumi Suzuki2,3,
  3. Patricia Estes4,
  4. Mani Ramaswami4,5,
  5. Daisuke Yamamoto1,2, and
  6. Nicholas J. Strausfeld5
  1. 1Yamamoto Behavior Genes Project, ERATO (Exploratory Research for Advanced Technology), Japan Science and Technology Corporation (JST), Mitsubishi Kasei Institute of Life Sciences, 194 Machida-shi, Tokyo, Japan, 2Mitsubishi Kasei Institute of Life Sciences, 194 Machida-shi, Tokyo, Japan, 3Tokyo University of Agriculture and Technology, 183 Fuchu-shi, Tokyo, Japan, 4Department of Molecular and Cellular Biology, University of Arizona, Tucson, Arizona 85721 USA, 5Arizona Research Laboratories Division of Neurobiology, University of Arizona, Tucson, Arizona 85721 USA

Abstract

Although the importance of theDrosophila mushroom body in olfactory learning and memory has been stressed, virtually nothing is known about the brain regions to which it is connected. Using Golgi and GAL4–UAS techniques, we performed the first systematic attempt to reveal the anatomy of its extrinsic neurons. A novel presynaptic reporter construct, UAS-neuronal synaptobrevin–green fluorescent protein(n-syb–GFP), was used to reveal the direction of information in the GAL4-labeled neurons. Our results showed that the main target of the output neurons from the mushroom body lobes is the anterior part of the inferior medial, superior medial, and superior lateral protocerebrum. The lobes also receive afferents from these neuropils. The lack of major output projections directly to the deutocerebrum’s premotor pathways discourages the view that the role of the mushroom body may be that of an immediate modifier of behavior. Our data, as well as a critical evaluation of the literature, suggest that the mushroom body may not by itself be a “center” for learning and memory, but that it can equally be considered as a preprocessor of olfactory signals en route to “higher” protocerebral regions.

Footnotes

  • 6 Present address: National Institute for Basic Biology, 444-8585 Okazaki-shi, Myodaiji-cho, Japan.

  • 7 Corresponding author.

    • Received January 27, 1998.
    • Accepted June 10, 1998.
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