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

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.

[1]  J. Mauelshagen,et al.  Neural correlates of olfactory learning paradigms in an identified neuron in the honeybee brain. , 1993, Journal of neurophysiology.

[2]  M Heisenberg,et al.  Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. , 1994, Science.

[3]  T. Préat,et al.  Genetic dissection of consolidated memory in Drosophila , 1994, Cell.

[4]  P. Salvaterra,et al.  Analysis of choline acetyltransferase protein in temperature sensitive mutant flies using newly generated monoclonal antibody , 1996, Neuroscience Research.

[5]  T. Godenschwege,et al.  Invertebrate Synapsins: A Single Gene Codes for Several Isoforms in Drosophila , 1996, The Journal of Neuroscience.

[6]  N. Strausfeld,et al.  The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. , 1998, Learning & memory.

[7]  R. Davis,et al.  Tripartite mushroom body architecture revealed by antigenic markers. , 1998, Learning & memory.

[8]  K. J. Sepp,et al.  Conversion of lacZ enhancer trap lines to GAL4 lines using targeted transposition in Drosophila melanogaster. , 1999, Genetics.

[9]  Liqun Luo,et al.  Mosaic Analysis with a Repressible Cell Marker for Studies of Gene Function in Neuronal Morphogenesis , 1999, Neuron.

[10]  F. Jackson,et al.  Presynaptic Glutamic Acid Decarboxylase Is Required for Induction of the Postsynaptic Receptor Field at a Glutamatergic Synapse , 2000, Neuron.

[11]  W. Neckameyer,et al.  Dopamine and senescence in Drosophila melanogaster ☆ , 2000, Neurobiology of Aging.

[12]  T. Préat,et al.  Localization of Long-Term Memory Within the Drosophila Mushroom Body , 2001, Science.

[13]  R. Davis,et al.  The Role of Drosophila Mushroom Body Signaling in Olfactory Memory , 2001, Science.

[14]  T. Kitamoto.  Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. , 2001, Journal of neurobiology.

[15]  T. Schwarz,et al.  Synaptotagmins I and IV promote transmitter release independently of Ca2+ binding in the C2A domain , 2002, Nature.

[16]  Richard Axel,et al.  Spatial Representation of the Glomerular Map in the Drosophila Protocerebrum , 2002, Cell.

[17]  T. Kitamoto.  Conditional disruption of synaptic transmission induces male–male courtship behavior in Drosophila , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[18]  I. Meinertzhagen,et al.  Synaptic organization of the mushroom body calyx in Drosophila melanogaster , 2002, The Journal of comparative neurology.

[19]  Kendal Broadie,et al.  Living synaptic vesicle marker: Synaptotagmin‐GFP , 2002, Genesis.

[20]  M. Heisenberg,et al.  Dopamine and Octopamine Differentiate between Aversive and Appetitive Olfactory Memories in Drosophila , 2003, The Journal of Neuroscience.

[21]  Ann-Shyn Chiang,et al.  Blockade of Neurotransmission in Drosophila Mushroom Bodies Impairs Odor Attraction, but Not Repulsion , 2003, Current Biology.

[22]  Z. Bashir.  On long-term depression induced by activation of G-protein coupled receptors , 2003, Neuroscience Research.

[23]  André Fiala,et al.  In Vivo Calcium Imaging of Brain Activity in Drosophila by Transgenic Cameleon Expression , 2003, Science's STKE.

[24]  Kei Ito,et al.  Integration of Chemosensory Pathways in the Drosophila Second-Order Olfactory Centers , 2004, Current Biology.

[25]  Thomas Preat,et al.  Exclusive Consolidated Memory Phases in Drosophila , 2004, Science.

[26]  Ronald L. Davis,et al.  Thirty years of olfactory learning and memory research in Drosophila melanogaster , 2005, Progress in Neurobiology.

[27]  R. Menzel,et al.  Neural plasticity of mushroom body-extrinsic neurons in the honeybee brain , 2005, Journal of Experimental Biology.

[28]  祐輝 橋本谷,et al.  Phospholipase Cβ serves as a coincidence detector through its Ca[2+] dependency for triggering retrograde endocannabinoid signal , 2005 .

[29]  Hee-Sup Shin,et al.  Phospholipase Cβ Serves as a Coincidence Detector through Its Ca2+ Dependency for Triggering Retrograde Endocannabinoid Signal , 2005, Neuron.

[30]  W. Quinn,et al.  Classical conditioning and retention in normal and mutantDrosophila melanogaster , 1985, Journal of Comparative Physiology A.

[31]  Ronald L. Davis,et al.  Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning. , 2006, Neuron.

[32]  Ronald L. Davis,et al.  Drosophila α/β Mushroom Body Neurons Form a Branch-Specific, Long-Term Cellular Memory Trace after Spaced Olfactory Conditioning , 2006, Neuron.

[33]  Vanessa A. Bender,et al.  Two Coincidence Detectors for Spike Timing-Dependent Plasticity in Somatosensory Cortex , 2006, The Journal of Neuroscience.

[34]  Kei Ito,et al.  Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula‐specific pathways , 2006, The Journal of comparative neurology.

[35]  S. Waddell,et al.  Drosophila olfactory memory: single genes to complex neural circuits , 2007, Nature Reviews Neuroscience.

[36]  R. Menzel,et al.  Learning-Related Plasticity in PE1 and Other Mushroom Body-Extrinsic Neurons in the Honeybee Brain , 2007, The Journal of Neuroscience.

[37]  S. Waddell,et al.  Rapid Consolidation to a radish and Protein Synthesis-Dependent Long-Term Memory after Single-Session Appetitive Olfactory Conditioning in Drosophila , 2008, The Journal of Neuroscience.

[38]  Akira Mamiya,et al.  Imaging of an Early Memory Trace in the Drosophila Mushroom Body , 2008, The Journal of Neuroscience.

[39]  Kei Ito,et al.  Neuronal assemblies of the Drosophila mushroom body , 2008, The Journal of comparative neurology.

[40]  Aaron DiAntonio,et al.  Visualizing glutamatergic cell bodies and synapses in Drosophila larval and adult CNS , 2008, The Journal of comparative neurology.

[41]  G. Rubin,et al.  Tools for neuroanatomy and neurogenetics in Drosophila , 2008, Proceedings of the National Academy of Sciences.

[42]  Y. Dan,et al.  Spike timing-dependent plasticity: a Hebbian learning rule. , 2008, Annual review of neuroscience.

[43]  P. Greengard,et al.  Writing Memories with Light-Addressable Reinforcement Circuitry , 2009, Cell.

[44]  Ronald L. Davis,et al.  Dynamics of Learning-Related cAMP Signaling and Stimulus Integration in the Drosophila Olfactory Pathway , 2009, Neuron.

[45]  Nicolas Y. Masse,et al.  Olfactory Information Processing in Drosophila , 2009, Current Biology.

[46]  Kristin Scott,et al.  Motor Control in a Drosophila Taste Circuit , 2009, Neuron.

[47]  Sreekanth H. Chalasani,et al.  Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators , 2009, Nature Methods.

[48]  T. Préat,et al.  Parametric and genetic analysis of Drosophila appetitive long‐term memory and sugar motivation , 2009, Genes, brain, and behavior.

[49]  T. Aigaki,et al.  The Drosophila TRPA channel, Painless, regulates sexual receptivity in virgin females , 2009, Genes, brain, and behavior.

[50]  Ronald L. Davis,et al.  The GABAergic anterior paired lateral neuron suppresses and is suppressed by olfactory learning , 2008, Nature Neuroscience.

[51]  Thomas Preat,et al.  PKA Dynamics in a Drosophila Learning Center: Coincidence Detection by Rutabaga Adenylyl Cyclase and Spatial Regulation by Dunce Phosphodiesterase , 2010, Neuron.

[52]  Yoshinori Aso,et al.  Specific Dopaminergic Neurons for the Formation of Labile Aversive Memory , 2010, Current Biology.

[53]  S. Ferrari,et al.  Author contributions , 2021 .