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

• Published in: Nature neuroscience Vol. 14; no. 7; pp. 903 - 910
• Main Authors: Tanimoto, Hiromu, Preat, Thomas, Séjourné, Julien, Plaçais, Pierre-Yves, Aso, Yoshinori, Siwanowicz, Igor, Trannoy, Séverine, Thoma, Vladimiros, Tedjakumala, Stevanus R, Rubin, Gerald M, Tchénio, Paul, Ito, Kei, Isabel, Guillaume
• Format: Journal Article
• Language: English
• Published: New York Nature Publishing Group US 01.07.2011; Nature Publishing Group
• Subjects: 631/378/1697; 631/378/2624; Afferent Pathways - physiology; Analysis of Variance; Animal Genetics and Genomics; Animals; Animals, Genetically Modified; Avoidance Learning - physiology; Behavior, Animal; Behavioral Sciences; Biological Techniques; Biomedical and Life Sciences; Biomedicine; CD8 Antigens - metabolism; Choline O-Acetyltransferase - metabolism; Conditioning (Psychology); Drosophila; Drosophila melanogaster; Drosophila Proteins - genetics; Drosophila Proteins - metabolism; Gene Expression Regulation - physiology; Glutamate Decarboxylase - metabolism; Green Fluorescent Proteins - genetics; Insects; Memory; Memory, Short-Term - physiology; Mental Recall - physiology; Models, Biological; Motor Neurons - classification; Motor Neurons - physiology; Mushroom Bodies - cytology; Mushrooms; Neurobiology; Neurons; Neurosciences; Odorants; Odors; Olfactory Pathways; Physiological aspects; Smell - physiology; Synapsins - metabolism; Temperature; Time Factors; Transcription Factors - metabolism; Tyrosine 3-Monooxygenase - metabolism; Vesicular Glutamate Transport Proteins - metabolism; France; United States; Germany; Learning; Neuroimaging; Animal behaviour; Behaviour; Neurogenetics; Memory
• ISSN: 1097-6256; 1546-1726
• DOI: 10.1038/nn.2846

This study reports an anatomical and functional screen of mushroom body–extrinsic neurons in Drosophila and finds that MB-V2 cholinergic efferent neurons are essential for retrieval of aversive short- and long-term memory, but not for memory formation or consolidation. During memory retrieval, MB-V2 neurons reinforce the olfactory pathway involved in innate odor avoidance. 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.