Localization of the Contacts Between Kenyon Cells and Aminergic Neurons in the Drosophila melanogaster Brain Using SplitGFP Reconstitution

ABSTRACT The mushroom body of the insect brain represents a neuronal circuit involved in the control of adaptive behavior, e.g., associative learning. Its function relies on the modulation of Kenyon cell activity or synaptic transmitter release by biogenic amines, e.g., octopamine, dopamine, or sero...

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Published in:Journal of comparative neurology (1911) 2013-12, Vol.521 (17), p.3992-4026
Main Authors: Pech, Ulrike, Pooryasin, Atefeh, Birman, Serge, Fiala, André
Format: Article
Language:English
Subjects:
Animals
Animals, Genetically Modified
biogenic amines
Biogenic Amines - analysis
Biogenic Amines - metabolism
Brain - cytology
Brain - metabolism
Cell Communication - physiology
Drosophila melanogaster
GRASP
Green Fluorescent Proteins - analysis
Green Fluorescent Proteins - metabolism
Mushroom Bodies - chemistry
Mushroom Bodies - cytology
Mushroom Bodies - metabolism
mushroom body
neural circuit
neuromodulation
Neurons - chemistry
Neurons - metabolism
splitGFP
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Summary:ABSTRACT The mushroom body of the insect brain represents a neuronal circuit involved in the control of adaptive behavior, e.g., associative learning. Its function relies on the modulation of Kenyon cell activity or synaptic transmitter release by biogenic amines, e.g., octopamine, dopamine, or serotonin. Therefore, for a comprehensive understanding of the mushroom body, it is of interest not only to determine which modulatory neurons interact with Kenyon cells but also to pinpoint where exactly in the mushroom body they do so. To accomplish the latter, we made use of the GRASP technique and created transgenic Drosophila melanogaster that carry one part of a membrane‐bound splitGFP in Kenyon cells, along with a cytosolic red fluorescent marker. The second part of the splitGFP is expressed in distinct neuronal populations using cell‐specific Gal4 drivers. GFP is reconstituted only if these neurons interact with Kenyon cells in close proximity, which, in combination with two‐photon microscopy, provides a very high spatial resolution. We characterize spatially and microstructurally distinct contact regions between Kenyon cells and dopaminergic, serotonergic, and octopaminergic/tyraminergic neurons in all subdivisions of the mushroom body. Subpopulations of dopaminergic neurons contact complementary lobe regions densely. Octopaminergic/tyraminergic neurons contact Kenyon cells sparsely and are restricted mainly to the calyx, the α′‐lobes, and the γ‐lobes. Contacts of Kenyon cells with serotonergic neurons are heterogeneously distributed over the entire mushroom body. In summary, the technique enables us to localize precisely a segmentation of the mushroom body by differential contacts with aminergic neurons. J. Comp. Neurol. 521:3992–4026, 2013. © 2013 Wiley Periodicals, Inc. The authors report a transgenic fly that is used to visualize the spatial contacts of mushroom body Kenyon cells with mushroom body extrinsic neurons. A detailed characterization of which structures of the mushroom bodies contact modulatory, bioaminergic neurons in the Drosophila brain is provided.
ISSN:0021-9967
1096-9861
DOI:10.1002/cne.23388