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Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila

Nature Neuroscience volume 14, pages 903–910 (2011)Cite this article

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Abstract

Aversive olfactory memory is formed in the mushroom bodies in Drosophila melanogaster. Memory retrieval requires mushroom body output, but the manner in which a memory trace in the mushroom body drives conditioned avoidance of a learned odor remains unknown. To identify neurons that are involved in olfactory memory retrieval, we performed an anatomical and functional screen of defined sets of mushroom body output neurons. We found that MB-V2 neurons were essential for retrieval of both short- and long-lasting memory, but not for memory formation or memory consolidation. MB-V2 neurons are cholinergic efferent neurons that project from the mushroom body vertical lobes to the middle superiormedial protocerebrum and the lateral horn. Notably, the odor response of MB-V2 neurons was modified after conditioning. As the lateral horn has been implicated in innate responses to repellent odorants, we propose that MB-V2 neurons recruit the olfactory pathway involved in innate odor avoidance during memory retrieval.

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Figure 1: MB-V2 neurons connect the mushroom body to the lateral horn and middle superior medial protocerebrum.
Figure 2: Output of the MB-V2 neurons is specifically required for the retrieval of short-lasting memory.
Figure 3: Suppressing MB-V2 neurons in MZ160 rescues the memory defect.
Figure 4: Output of the MB-V2 neurons is required for retrieval of consolidated long-lasting memories.
Figure 5: MB-V2 neurons are cholinergic.
Figure 6: MB-V2 neurons in naive flies respond to olfactory stimuli.
Figure 7: MB-V2 neurons show a reduced response to the trained odor after conditioning.

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Acknowledgements

We thank J. Urban and G.M. Technau for the MZ160 line, the members of the NP consortium for the NP2492 line, J.-M. Dura for the y1w1118;GAL80[y+],Sb line and for discussions, L.L. Looger for the UAS-GCaMP3 line, T. Kitamoto for the GAD1-GAL80 and Cha3.3kb-GAL80 lines, and V. Hakim, I. Rivals and members of our laboratories for discussions. This work was supported by grants from the Japan Society for the Promotion of Science (K.I.), the Agence Nationale pour la Recherche (T.P.), the Fondation Bettencourt-Schueler (T.P.), the Fondation pour la Recherche Médicale (T.P.), the Emmy-Noether Program from Deutsche Forschungsgemeinschaft (H.T.), the Bernstein Focus Learning from Bundesministerium für Bildung und Forschung (H.T.) and the Max-Planck-Gesellschaft (H.T.). J.S. and G.I. were supported by the Fondation pour la Recherche Médicale, P.-Y.P. was supported by a grant from Région Ile-de-France and Y.A. was supported by Deutscher Akademischer Austausch Dienst.

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Author notes

  1. Hiromu Tanimoto and Thomas Preat: These authors contributed equally to this work.

Authors and Affiliations

  1. Genes and Dynamics of Memory Systems, Neurobiology Unit, CNRS, Ecole Supérieure de Physique et de Chimie Industrielles, Paris, France

    Julien Séjourné, Pierre-Yves Plaçais, Séverine Trannoy, Paul Tchénio, Guillaume Isabel & Thomas Preat

  2. Max-Planck-Institut für Neurobiologie, Martinsried, Germany

    Yoshinori Aso, Igor Siwanowicz, Vladimiros Thoma, Stevanus R Tedjakumala & Hiromu Tanimoto

  3. Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia, USA

    Yoshinori Aso & Gerald M Rubin

  4. Nanooptique et Physiologie Intégrée, Université Paris-Sud, CNRS UPR 3321, Orsay, France

    Paul Tchénio

  5. Institute of Molecular and Cellular Biosciences, The University of Tokyo, Bunkyo-ku, Tokyo, Japan

    Kei Ito

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Contributions

Y.A. and H.T. designed and I.S., S.R.T. and V.T. carried out anatomical experiments. I.S., Y.A. and H.T. analyzed the microscopic data and assembled figures. K.I. and G.M.R. provided Gal4 lines with their expression patterns. J.S., G.I. and T.P. designed and J.S., S.T. and P.-Y.P. carried out behavior experiments. J.S. generated the NP2492-Gal80 mutant. P.-Y.P., T.P. and P.T. designed the in vivo imaging experiments and P.-Y.P. carried them out. J.S., P.-Y.P., I.S., Y.A., H.T. and T.P. wrote the paper. T.P. and H.T. supervised the work.

Corresponding authors

Correspondence to Hiromu Tanimoto or Thomas Preat.

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Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–9 (PDF 16348 kb)

Supplementary Video 1

Expression pattern of NP2492 in the brain (MOV 3358 kb)

Supplementary Video 2

Expression pattern of MZ160 in the brain (MOV 2495 kb)

Supplementary Video 3

Expression pattern of MZ160, Cha3.3kb-GAL80 in the brain (MOV 1968 kb)

Supplementary Video 4

Expression pattern of MZ160, NP2492-GAL80 in the brain (MOV 2207 kb)

Supplementary Video 5

Expression pattern of R71D08 in the brain (MOV 2700 kb)

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Séjourné, J., Plaçais, PY., Aso, Y. et al. Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila. Nat Neurosci 14, 903–910 (2011). https://doi.org/10.1038/nn.2846

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