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The Journal of Neuroscience, October 10, 2007, 27(41):11132-11138; doi:10.1523/JNEUROSCI.2712-07.2007

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Behavioral/Systems/Cognitive
Multiple Memory Traces for Olfactory Reward Learning in Drosophila

Andreas S. Thum,1 Arnim Jenett,1 Kei Ito,2 Martin Heisenberg,1 and Hiromu Tanimoto1

1Lehrstuhl für Genetik und Neurobiologie, Biozentrum, Universität Würzburg, Am Hubland, D-97074 Würzburg, Germany, and 2Institute of Molecular and Cellular Biosciences, University of Tokyo, 113-0032 Tokyo, Japan

Correspondence should be addressed to Hiromu Tanimoto at his present address: Max-Planck-Institut für Neurobiologie, Am Klopferspitz 18, D-82152 Martinsried, Germany. Email: hiromut{at}biozentrum.uni-wuerzburg.de or Email: hiromut{at}neuro.mpg.de

Physical traces underlying simple memories can be confined to a single group of cells in the brain. In the fly Drosophila melanogaster, the Kenyon cells of the mushroom bodies house traces for both appetitive and aversive odor memories. The adenylate cyclase protein, Rutabaga, has been shown to mediate both traces. Here, we show that, for appetitive learning, another group of cells can additionally accommodate a Rutabaga-dependent memory trace. Localized expression of rutabaga in either projection neurons, the first-order olfactory interneurons, or in Kenyon cells, the second-order interneurons, is sufficient for rescuing the mutant defect in appetitive short-term memory. Thus, appetitive learning may induce multiple memory traces in the first- and second-order olfactory interneurons using the same plasticity mechanism. In contrast, aversive odor memory of rutabaga is rescued selectively in the Kenyon cells, but not in the projection neurons. This difference in the organization of memory traces is consistent with the internal representation of reward and punishment.

Key words: learning; memory; insect; memory trace; olfaction; adenylate cyclase; Drosophila; short-term memory


Received Feb. 15, 2007; revised Aug. 29, 2007; accepted Aug. 29, 2007.

Correspondence should be addressed to Hiromu Tanimoto at his present address: Max-Planck-Institut für Neurobiologie, Am Klopferspitz 18, D-82152 Martinsried, Germany. Email: hiromut{at}biozentrum.uni-wuerzburg.de or Email: hiromut{at}neuro.mpg.de




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