Two pairs of mushroom body efferent neurons are required for appetitive long-term memory retrieval in Drosophila.

One of the challenges facing memory research is to combine network- and cellular-level descriptions of memory encoding. In this context, Drosophila offers the opportunity to decipher, down to single-cell resolution, memory-relevant circuits in connection with the mushroom bodies (MBs), prominent structures for olfactory learning and memory. Although the MB-afferent circuits involved in appetitive learning were recently described, the circuits underlying appetitive memory retrieval remain unknown. We identified two pairs of cholinergic neurons efferent from the MB α vertical lobes, named MB-V3, that are necessary for the retrieval of appetitive long-term memory (LTM). Furthermore, LTM retrieval was correlated to an enhanced response to the rewarded odor in these neurons. Strikingly, though, silencing the MB-V3 neurons did not affect short-term memory (STM) retrieval. This finding supports a scheme of parallel appetitive STM and LTM processing.

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

[2]  T. Bliss,et al.  Synaptic plasticity, memory and the hippocampus: a neural network approach to causality , 2012, Nature Reviews Neuroscience.

[3]  Ann-Shyn Chiang,et al.  Drosophila ORB protein in two mushroom body output neurons is necessary for long-term memory formation , 2013, Proceedings of the National Academy of Sciences.

[4]  Robert A. A. Campbell,et al.  Cellular-Resolution Population Imaging Reveals Robust Sparse Coding in the Drosophila Mushroom Body , 2011, The Journal of Neuroscience.

[5]  Kei Ito,et al.  A map of octopaminergic neurons in the Drosophila brain , 2009, The Journal of comparative neurology.

[6]  Daryl M. Gohl,et al.  Layered reward signaling through octopamine and dopamine in Drosophila , 2012, Nature.

[7]  Glenn C. Turner,et al.  Olfactory representations by Drosophila mushroom body neurons. , 2008, Journal of neurophysiology.

[8]  E. Kandel,et al.  Toward a molecular definition of long-term memory storage. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[10]  Thomas Preat,et al.  Parallel Processing of Appetitive Short- and Long-Term Memories In Drosophila , 2011, Current Biology.

[11]  S. Waddell,et al.  Sequential Use of Mushroom Body Neuron Subsets during Drosophila Odor Memory Processing , 2007, Neuron.

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

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

[14]  Gilles Laurent,et al.  Olfactory network dynamics and the coding of multidimensional signals , 2002, Nature Reviews Neuroscience.

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

[16]  E R Kandel,et al.  Genetic approaches to memory storage. , 1999, Trends in genetics : TIG.

[17]  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.

[18]  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.

[19]  John Tyler Bonner,et al.  Morphogenesis , 1965, The Physics of Living Matter: Space, Time and Information.

[20]  Guan-Yu Chen,et al.  Three-Dimensional Reconstruction of Brain-wide Wiring Networks in Drosophila at Single-Cell Resolution , 2011, Current Biology.

[21]  Gerald M Rubin,et al.  Using translational enhancers to increase transgene expression in Drosophila , 2012, Proceedings of the National Academy of Sciences.

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

[23]  W. Quinn,et al.  Reward learning in normal and mutant Drosophila. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

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

[25]  A. Barco,et al.  CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models , 2010, Trends in Neurosciences.

[26]  Yoshinori Aso,et al.  The Mushroom Body of Adult Drosophila Characterized by GAL4 Drivers , 2009, Journal of neurogenetics.

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

[28]  Yoshinori Aso,et al.  Three Dopamine Pathways Induce Aversive Odor Memories with Different Stability , 2012, PLoS genetics.

[29]  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.

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

[31]  M. Heisenberg Mushroom body memoir: from maps to models , 2003, Nature Reviews Neuroscience.

[32]  Shamik Dasgupta,et al.  A Neural Circuit Mechanism Integrating Motivational State with Memory Expression in Drosophila , 2009, Cell.

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

[34]  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.

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

[36]  S. J. Martin,et al.  Synaptic plasticity and memory: an evaluation of the hypothesis. , 2000, Annual review of neuroscience.

[37]  T. Préat,et al.  To Favor Survival Under Food Shortage, the Brain Disables Costly Memory , 2013, Science.

[38]  Karel Svoboda,et al.  Stereotyped Odor-Evoked Activity in the Mushroom Body of Drosophila Revealed by Green Fluorescent Protein-Based Ca2+ Imaging , 2004, The Journal of Neuroscience.

[39]  Matthias Landgraf,et al.  Genetically encoded dendritic marker sheds light on neuronal connectivity in Drosophila , 2010, Proceedings of the National Academy of Sciences.

[40]  G. Rubin,et al.  A subset of dopamine neurons signals reward for odour memory in Drosophila , 2012, Nature.

[41]  J. Dubnau,et al.  Gene discovery in Drosophila: new insights for learning and memory. , 1998, Annual review of neuroscience.

[42]  Ronald L. Davis,et al.  System-Like Consolidation of Olfactory Memories in Drosophila , 2013, The Journal of Neuroscience.

[43]  Eric R Kandel,et al.  In search of general mechanisms for long-lasting plasticity: Aplysia and the hippocampus. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

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

[46]  Fasting Launches Crtc to Facilitate Long-term Memory Formation , 2022 .

[47]  Stefan R. Pulver,et al.  An internal thermal sensor controlling temperature preference in Drosophila , 2008, Nature.

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

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

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

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

[52]  Ghislain Belliart-Guérin,et al.  Slow oscillations in two pairs of dopaminergic neurons gate long-term memory formation in Drosophila , 2012, Nature Neuroscience.

[53]  G. Rubin,et al.  Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila , 2011, Nature Neuroscience.