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Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila

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Aso, Yoshinori, Sitaraman, Divya, Ichinose, Toshiharu, Kaun, Karla R, Vogt, Katrin, Belliart-Guérin, Ghislain, Plaçais, Pierre-Yves, Robie, Alice A, Yamagata, Nobuhiro, Schnaitmann, Christopher, Rowell, William J, Johnston, Rebecca M, Ngo, Teri-T B, Chen, Nan, Korff, Wyatt, Nitabach, Michael N, Heberlein, Ulrike, Preat, Thomas, Branson, Kristin M, Tanimoto, Hiromu, Rubin, Gerald M·2014·eLife

Abstract

Animals discriminate stimuli, learn their predictive value and use this knowledge to modify their behavior. In Drosophila, the mushroom body (MB) plays a key role in these processes. Sensory stimuli are sparsely represented by ∼2000 Kenyon cells, which converge onto 34 output neurons (MBONs) of 21 types. We studied the role of MBONs in several associative learning tasks and in sleep regulation, revealing the extent to which information flow is segregated into distinct channels and suggesting possible roles for the multi-layered MBON network. We also show that optogenetic activation of MBONs can, depending on cell type, induce repulsion or attraction in flies. The behavioral effects of MBON perturbation are combinatorial, suggesting that the MBON ensemble collectively represents valence. We propose that local, stimulus-specific dopaminergic modulation selectively alters the balance within the MBON network for those stimuli. Our results suggest that valence encoded by the MBON ensemble biases memory-based action selection.

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Research works printed but not linked: 135

  1. Abel, 2001, Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera, The Journal of Comparative Neurology, 437, 363, 10.1002/cne.1289 · DOI
  2. Akalal, 2010, A late-phase, long-term memory trace forms in the gamma neurons of Drosophila mushroom bodies after olfactory classical conditioning, The Journal of Neuroscience, 30, 16699, 10.1523/JNEUROSCI.1882-10.2010 · DOI
  3. Akalal, 2011, The long-term memory trace formed in the Drosophila alpha/beta mushroom body neurons is abolished in long-term memory mutants, The Journal of Neuroscience, 31, 5643, 10.1523/JNEUROSCI.3190-10.2011 · DOI
  4. Anderson, 2014, A framework for studying emotions across species, Cell, 157, 187, 10.1016/j.cell.2014.03.003 · DOI · Paper page
  5. Ashburner, 1999, An exploration of the sequence of a 2.9-Mb region of the genome of Drosophila melanogaster: the Adh region, Genetics, 153, 179, 10.1093/genetics/153.1.179 · DOI
  6. Aso, 2009, The mushroom body of adult Drosophila characterized by GAL4 drivers, Journal of Neurogenetics, 23, 156, 10.1080/01677060802471718 · DOI
  7. Aso, 2014, The neuronal architecture of the mushroom body provides a logic for associative learning, eLife, 3, e04577, 10.7554/eLife.04577 · DOI · Paper page
  8. Aso, 2012, Three dopamine pathways induce aversive odor memories with different stability, PLOS Genetics, 8, e1002768, 10.1371/journal.pgen.1002768 · DOI · Paper page
  9. Aso, 2010, Specific dopaminergic neurons for the formation of labile aversive memory, Current Biology, 20, 1445, 10.1016/j.cub.2010.06.048 · DOI · Paper page
  10. Azanchi, 2013, Competing dopamine neurons drive oviposition choice for ethanol in Drosophila, Proceedings of the National Academy of Sciences of USA, 110, 21153, 10.1073/pnas.1320208110 · DOI
  11. Bang, 2011, Dopamine signalling in mushroom bodies regulates temperature-preference behaviour in Drosophila, PLOS Genetics, 7, e1001346, 10.1371/journal.pgen.1001346 · DOI
  12. Bath, 2014, FlyMAD: rapid thermogenetic control of neuronal activity in freely walking Drosophila, Nature Methods, 11, 756, 10.1038/nmeth.2973 · DOI
  13. Benton, 2009, Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila, Cell, 136, 149, 10.1016/j.cell.2008.12.001 · DOI
  14. Benzer, 1967, BEHAVIORAL MUTANTS OF Drosophila ISOLATED BY COUNTERCURRENT DISTRIBUTION, Proceedings of the National Academy of Sciences of USA, 58, 1112, 10.1073/pnas.58.3.1112 · DOI · Paper page
  15. Berry, 2012, Dopamine is required for learning and forgetting in Drosophila, Neuron, 74, 530, 10.1016/j.neuron.2012.04.007 · DOI · Paper page
  16. Blum, 2009, Short- and long-term memory in Drosophila require cAMP signaling in distinct neuron types, Current Biology, 19, 1341, 10.1016/j.cub.2009.07.016 · DOI
  17. Bracker, 2013, Essential role of the mushroom body in context-dependent CO(2) avoidance in Drosophila, Current Biology, 23, 1228, 10.1016/j.cub.2013.05.029 · DOI
  18. Branson, 2009, High-throughput ethomics in large groups of Drosophila, Nature Methods, 6, 451, 10.1038/nmeth.1328 · DOI · Paper page
  19. Brembs, 2009, Mushroom bodies regulate habit formation in Drosophila, Current Biology, 19, 1351, 10.1016/j.cub.2009.06.014 · DOI
  20. Cassenaer, 2007, Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts, Nature, 448, 709, 10.1038/nature05973 · DOI · Paper page
  21. Cassenaer, 2012, Conditional modulation of spike-timing-dependent plasticity for olfactory learning, Nature, 482, 47, 10.1038/nature10776 · DOI
  22. Cervantes-Sandoval, 2013, System-like consolidation of olfactory memories in Drosophila, The Journal of Neuroscience, 33, 9846, 10.1523/JNEUROSCI.0451-13.2013 · DOI
  23. Choi, 2011, Driving opposing behaviors with ensembles of piriform neurons, Cell, 146, 1004, 10.1016/j.cell.2011.07.041 · DOI
  24. Claridge-Chang, 2009, Writing memories with light-addressable reinforcement circuitry, Cell, 139, 405, 10.1016/j.cell.2009.08.034 · DOI · Paper page
  25. Comas, 2004, Drosophila long-term memory formation involves regulation of cathepsin activity, Nature, 430, 460, 10.1038/nature02726 · DOI
  26. Crittenden, 1998, Tripartite mushroom body architecture revealed by antigenic markers, Learning & Memory, 5, 38, 10.1101/lm.5.1.38 · DOI · Paper page
  27. Das, 2014, Drosophila learn opposing components of a compound food stimulus, Current Biology, 24, 1723, 10.1016/j.cub.2014.05.078 · DOI
  28. Davis, 2005, Olfactory memory formation in Drosophila: from molecular to systems neuroscience, Annual Review of Neuroscience, 28, 275, 10.1146/annurev.neuro.28.061604.135651 · DOI · Paper page
  29. de Belle, 1994, Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies, Science, 263, 692, 10.1126/science.8303280 · DOI · Paper page
  30. Donelson, 2012, High-resolution positional tracking for long-term analysis of Drosophila sleep and locomotion using the “tracker” program, PLOS ONE, 7, e37250, 10.1371/journal.pone.0037250 · DOI
  31. Donlea, 2011, Inducing sleep by remote control facilitates memory consolidation in Drosophila, Science, 332, 1571, 10.1126/science.1202249 · DOI · Paper page
  32. Dubnau, 2003, The staufen/pumilio pathway is involved in Drosophila long-term memory, Current Biology, 13, 286, 10.1016/S0960-9822(03)00064-2 · DOI
  33. Dubnau, 2001, Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory, Nature, 411, 476, 10.1038/35078077 · DOI · Paper page
  34. Dudai, 1976, dunce, a mutant of Drosophila deficient in learning, Proceedings of the National Academy of Sciences of USA, 73, 1684, 10.1073/pnas.73.5.1684 · DOI
  35. Dunipace, 2001, Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system, Current Biology, 11, 822, 10.1016/S0960-9822(01)00258-5 · DOI · Paper page
  36. Farris, 2011, Are mushroom bodies cerebellum-like structures?, Arthropod Structure & Development, 40, 368, 10.1016/j.asd.2011.02.004 · DOI
  37. Fishilevich, 2005, Genetic and functional subdivision of the Drosophila antennal lobe, Current Biology, 15, 1548, 10.1016/j.cub.2005.07.066 · DOI
  38. Fleischmann, 2001, Mushroom bodies and post-mating behaviors of Drosophila melanogaster females, Journal of Neurogenetics, 15, 117, 10.3109/01677060109066198 · DOI
  39. Folkers, 1993, Radish, a Drosophila mutant deficient in consolidated memory, Proceedings of the National Academy of Sciences of USA, 90, 8123, 10.1073/pnas.90.17.8123 · DOI
  40. Ganguly-Fitzgerald, 2006, Waking experience affects sleep need in Drosophila, Science, 313, 1775, 10.1126/science.1130408 · DOI · Paper page
  41. Gerber, 2004, An engram found? Evaluating the evidence from fruit flies, Current Opinion in Neurobiology, 14, 737, 10.1016/j.conb.2004.10.014 · DOI
  42. Gervasi, 2010, PKA dynamics in a Drosophila learning center: coincidence detection by rutabaga adenylyl cyclase and spatial regulation by dunce phosphodiesterase, Neuron, 65, 516, 10.1016/j.neuron.2010.01.014 · DOI
  43. Griffith, 2012, Identifying behavioral circuits in Drosophila melanogaster: moving targets in a flying insect, Current Opinion in Neurobiology, 22, 609, 10.1016/j.conb.2012.01.002 · DOI
  44. Hamada, 2008, An internal thermal sensor controlling temperature preference in Drosophila, Nature, 454, 217, 10.1038/nature07001 · DOI · Paper page
  45. Hanesch, 1989, Neuronal architecture of the Central complex in Drosophila melanogaster, Cell and Tissue Research, 257, 343, 10.1007/BF00261838 · DOI · Paper page
  46. Heisenberg, 1985, Drosophila mushroom body mutants are deficient in olfactory learning, Journal of Neurogenetics, 2, 1, 10.3109/01677068509100140 · DOI · Paper page
  47. Hendricks, 2000, Rest in Drosophila is a sleep-like state, Neuron, 25, 129, 10.1016/S0896-6273(00)80877-6 · DOI · Paper page
  48. Hendricks, 2004, Why a fly? Using Drosophila to understand the genetics of circadian rhythms and sleep, Sleep, 27, 334, 10.1093/sleep/27.2.334 · DOI
  49. Hirano, 2013, Hunger and memory; CRTC coordinates long-term memory with the physiological state, hunger, Communicative & Integrative Biology, 6, e25152, 10.4161/cib.25152 · DOI
  50. Hong, 2008, cAMP signalling in mushroom bodies modulates temperature preference behaviour in Drosophila, Nature, 454, 771, 10.1038/nature07090 · DOI
  51. Huang, 2012, A permissive role of mushroom body alpha/beta core neurons in long-term memory consolidation in Drosophila, Current Biology, 22, 1981, 10.1016/j.cub.2012.08.048 · DOI
  52. Isabel, 2004, Exclusive consolidated memory phases in Drosophila, Science, 304, 1024, 10.1126/science.1094932 · DOI
  53. Ito, 2013, Systematic analysis of neural projections reveals clonal composition of the Drosophila brain, Current Biology, 23, 644, 10.1016/j.cub.2013.03.015 · DOI · Paper page
  54. Ito, 1982, Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells, The Journal of Physiology, 324, 113, 10.1113/jphysiol.1982.sp014103 · DOI · Paper page
  55. Jan, 1976, L-glutamate as an excitatory transmitter at Drosophila Larval Neuromuscular-Junction, Journal of Physiology, 262, 215, 10.1113/jphysiol.1976.sp011593 · DOI · Paper page
  56. Jefferis, 2007, Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation, Cell, 128, 1187, 10.1016/j.cell.2007.01.040 · DOI · Paper page
  57. Joiner, 2006, Sleep in Drosophila is regulated by adult mushroom bodies, Nature, 441, 757, 10.1038/nature04811 · DOI · Paper page
  58. Kabra, 2013, JAABA: interactive machine learning for automatic annotation of animal behavior, Nature Methods, 10, 64, 10.1038/nmeth.2281 · DOI · Paper page
  59. Kaun, 2011, A Drosophila model for alcohol reward, Nature Neuroscience, 14, 612, 10.1038/nn.2805 · DOI
  60. Kim, 2007, D1 dopamine receptor dDA1 is required in the mushroom body neurons for aversive and appetitive learning in Drosophila, The Journal of Neuroscience, 27, 7640, 10.1523/JNEUROSCI.1167-07.2007 · DOI · Paper page
  61. Kitamoto, 2001, Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons, Journal of Neurobiology, 47, 81, 10.1002/neu.1018 · DOI · Paper page
  62. Knapek, 2013, Short neuropeptide F acts as a functional neuromodulator for olfactory memory in Kenyon cells of Drosophila mushroom bodies, The Journal of Neuroscience, 33, 5340, 10.1523/JNEUROSCI.2287-12.2013 · DOI
  63. Knapek, 2011, Bruchpilot, a synaptic active zone protein for anesthesia-resistant memory, The Journal of Neuroscience, 31, 3453, 10.1523/JNEUROSCI.2585-10.2011 · DOI
  64. Krashes, 2009, A neural circuit mechanism integrating Motivational state with memory expression in Drosophila, Cell, 139, 416, 10.1016/j.cell.2009.08.035 · DOI · Paper page
  65. Krashes, 2007, Sequential use of mushroom body neuron subsets during drosophila odor memory processing, Neuron, 53, 103, 10.1016/j.neuron.2006.11.021 · DOI · Paper page
  66. Krashes, 2008, Rapid consolidation to a radish and protein synthesis-dependent long-term memory after single-session appetitive olfactory conditioning in Drosophila, Journal of Neuroscience, 28, 3103, 10.1523/JNEUROSCI.5333-07.2008 · DOI · Paper page
  67. Laurent, 2002, Olfactory network dynamics and the coding of multidimensional signals, Nature Reviews Neuroscience, 3, 884, 10.1038/nrn964 · DOI · Paper page
  68. Laurent, 1994, Odorant-induced oscillations in the mushroom bodies of the locust, The Journal of Neuroscience, 14, 2993, 10.1523/JNEUROSCI.14-05-02993.1994 · DOI · Paper page
  69. Levy, 2010, Neural representation of subjective value under risk and ambiguity, Journal of Neurophysiology, 103, 1036, 10.1152/jn.00853.2009 · DOI
  70. Lin, 2007, A map of olfactory representation in the Drosophila mushroom body, Cell, 128, 1205, 10.1016/j.cell.2007.03.006 · DOI
  71. Liu, 2012, A subset of dopamine neurons signals reward for odour memory in Drosophila, Nature, 488, 512, 10.1038/nature11304 · DOI · Paper page
  72. Liu, 2006, Distinct memory traces for two visual features in the Drosophila brain, Nature, 439, 551, 10.1038/nature04381 · DOI
  73. Liu, 1999, Context generalization in Drosophila visual learning requires the mushroom bodies, Nature, 400, 753, 10.1038/22919 · DOI · Paper page
  74. Liu, 2013, Glutamate is an inhibitory neurotransmitter in the Drosophila olfactory system, Proceedings of the National Academy of Sciences of USA, 110, 10294, 10.1073/pnas.1220560110 · DOI · Paper page
  75. Mao, 2009, Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity, Frontiers in Neural Circuits, 3, 5, 10.3389/neuro.04.005.2009 · DOI · Paper page
  76. Marin, 2002, Representation of the glomerular olfactory map in the Drosophila brain, Cell, 109, 243, 10.1016/S0092-8674(02)00700-6 · DOI · Paper page
  77. Martin, 1998, Mushroom bodies suppress locomotor activity in Drosophila melanogaster, Learning & Memory, 5, 179, 10.1101/lm.5.1.179 · DOI
  78. Masek, 2010, Limited taste discrimination in Drosophila, Proceedings of the National Academy of Sciences of USA, 107, 14833, 10.1073/pnas.1009318107 · DOI
  79. Mcbride, 1999, Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster, Neuron, 24, 967, 10.1016/S0896-6273(00)81043-0 · DOI · Paper page
  80. McGuire, 2001, The role of Drosophila mushroom body signaling in olfactory memory, Science, 293, 1330, 10.1126/science.1062622 · DOI
  81. McGuire, 2003, Spatiotemporal rescue of memory dysfunction in Drosophila, Science, 302, 1765, 10.1126/science.1089035 · DOI · Paper page
  82. Okada, 2007, Learning-related plasticity in PE1 and other mushroom body-extrinsic neurons in the honeybee brain, The Journal of Neuroscience, 27, 11736, 10.1523/JNEUROSCI.2216-07.2007 · DOI
  83. Pai, 2013, Drosophila ORB protein in two mushroom body output neurons is necessary for long-term memory formation, Proceedings of the National Academy of Sciences of USA, 110, 7898, 10.1073/pnas.1216336110 · DOI
  84. Parisky, 2008, PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit, Neuron, 60, 672, 10.1016/j.neuron.2008.10.042 · DOI
  85. Pascual, 2001, Localization of long-term memory within the Drosophila mushroom body, Science, 294, 1115, 10.1126/science.1064200 · DOI · Paper page
  86. Perez-Orive, 2002, Oscillations and sparsening of odor representations in the mushroom body, Science, 297, 359, 10.1126/science.1070502 · DOI
  87. Perisse, 2013, Different kenyon cell populations drive learned approach and avoidance in Drosophila, Neuron, 79, 945, 10.1016/j.neuron.2013.07.045 · DOI
  88. Pfeiffer, 2010, Refinement of tools for targeted gene expression in Drosophila, Genetics, 186, 735, 10.1534/genetics.110.119917 · DOI · Paper page
  89. Pfeiffer, 2012, Using translational enhancers to increase transgene expression in Drosophila, Proceedings of the National Academy of Sciences of USA, 109, 6626, 10.1073/pnas.1204520109 · DOI · Paper page
  90. Pitman, 2011, A Pair of inhibitory neurons are required to Sustain labile memory in the Drosophila mushroom body, Current Biology, 21, 855, 10.1016/j.cub.2011.03.069 · DOI
  91. Pitman, 2006, A dynamic role for the mushroom bodies in promoting sleep in Drosophila, Nature, 441, 753, 10.1038/nature04739 · DOI · Paper page
  92. Placais, 2013, To favor survival under food shortage, the brain disables costly memory, Science, 339, 440, 10.1126/science.1226018 · DOI
  93. Placais, 2013, Two pairs of mushroom body efferent neurons are required for appetitive long-term memory retrieval in Drosophila, Cell Reports, 5, 769, 10.1016/j.celrep.2013.09.032 · DOI
  94. Placais, 2012, Slow oscillations in two pairs of dopaminergic neurons gate long-term memory formation in Drosophila, Nature Neuroscience, 15, 592, 10.1038/nn.3055 · DOI
  95. Qin, 2012, Gamma neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila, Current Biology, 22, 608, 10.1016/j.cub.2012.02.014 · DOI
  96. Schnaitmann, 2013, Color discrimination with broadband photoreceptors, Current Biology, 23, 2375, 10.1016/j.cub.2013.10.037 · DOI
  97. Schnaitmann, 2010, Appetitive and aversive visual learning in freely moving Drosophila, Frontiers in Behavioral Neuroscience, 4, 10, 10.3389/fnbeh.2010.00010 · DOI
  98. Schroll, 2006, Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae, Current Biology, 16, 1741, 10.1016/j.cub.2006.07.023 · DOI
  99. Schurmann, 1974, [On the functional anatomy of the corpora pedunculata in insects (author's transl)], Experimental Brain Research, 19, 406, 10.1007/BF00234464 · DOI
  100. Schwaerzel, 2003, Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila, Journal of Neuroscience, 23, 10495, 10.1523/JNEUROSCI.23-33-10495.2003 · DOI · Paper page
  101. Séjourné, 2011, Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila, Nature Neuroscience, 14, 903, 10.1038/nn.2846 · DOI
  102. Shang, 2013, Short neuropeptide F is a sleep-promoting inhibitory modulator, Neuron, 80, 171, 10.1016/j.neuron.2013.07.029 · DOI
  103. Shaw, 2000, Correlates of sleep and waking in Drosophila melanogaster, Science, 287, 1834, 10.1126/science.287.5459.1834 · DOI · Paper page
  104. Shen, 2008, Dichotomous dopaminergic control of striatal synaptic plasticity, Science, 321, 848, 10.1126/science.1160575 · DOI · Paper page
  105. Silbering, 2011, Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems, The Journal of Neuroscience, 31, 13357, 10.1523/JNEUROSCI.2360-11.2011 · DOI
  106. Strauss, 2002, The central complex and the genetic dissection of locomotor behaviour, Current Opinion in Neurobiology, 12, 633, 10.1016/S0959-4388(02)00385-9 · DOI · Paper page
  107. Suh, 2007, Light activation of an innate olfactory avoidance response in Drosophila, Current Biology, 17, 905, 10.1016/j.cub.2007.04.046 · DOI
  108. Tanaka, 2004, Integration of chemosensory pathways in the Drosophila second-order olfactory centers, Current Biology, 14, 449, 10.1016/j.cub.2004.03.006 · DOI · Paper page
  109. Tanaka, 2012, Organization of antennal lobe-associated neurons in adult Drosophila melanogaster brain, The Journal of Comparative Neurology, 520, 4067, 10.1002/cne.23142 · DOI
  110. Tanaka, 2008, Neuronal assemblies of the Drosophila mushroom body, The Journal of Comparative Neurology, 508, 711, 10.1002/cne.21692 · DOI · Paper page
  111. Tempel, 1983, Reward learning in normal and mutant Drosophila, Proceedings of the National Academy of Sciences of USA, 80, 1482, 10.1073/pnas.80.5.1482 · DOI
  112. Trannoy, 2011, Parallel processing of appetitive short- and long-term memories in Drosophila, Current Biology, 21, 1647, 10.1016/j.cub.2011.08.032 · DOI
  113. Tully, 1985, Classical-conditioning and retention in Normal and mutant Drosophila-Melanogaster, Journal of Comparative Physiology A-Sensory Neural and Behavioral Physiology, 157, 263, 10.1007/BF01350033 · DOI · Paper page
  114. Turner, 2008, Olfactory representations by Drosophila mushroom body neurons, Journal of Neurophysiology, 99, 734, 10.1152/jn.01283.2007 · DOI · Paper page
  115. van Swinderen, 2009, Shared visual attention and memory systems in the Drosophila brain, PLOS ONE, 4, e5989, 10.1371/journal.pone.0005989 · DOI
  116. Vasmer, 2014, Induction of aversive learning through thermogenetic activation of Kenyon cell ensembles in Drosophila, Frontiers in Behavioral Neuroscience, 8, 174, 10.3389/fnbeh.2014.00174 · DOI
  117. Venken, 2011, Genetic manipulation of genes and cells in the nervous system of the fruit fly, Neuron, 72, 202, 10.1016/j.neuron.2011.09.021 · DOI · Paper page
  118. Vet, 1983, An air-flow olfactometer for measuring olfactory responses of Hymenopterous Parasitoids and other small insects, Physiological Entomology, 8, 97, 10.1111/j.1365-3032.1983.tb00338.x · DOI · Paper page
  119. Vogt, 2014, Shared mushroom body circuits underlie visual and olfactory memories in Drosophila, eLife, 3, e02395, 10.7554/eLife.02395 · DOI
  120. Vosshall, 2007, Molecular architecture of smell and taste in Drosophila, Annual Review of Neuroscience, 30, 505, 10.1146/annurev.neuro.30.051606.094306 · DOI · Paper page
  121. Wolf, 2002, High-resolution analysis of ethanol-induced locomotor stimulation in Drosophila, The Journal of Neuroscience, 22, 11035, 10.1523/JNEUROSCI.22-24-11035.2002 · DOI
  122. Wong, 2002, Spatial representation of the glomerular map in the Drosophila protocerebrum, Cell, 109, 229, 10.1016/S0092-8674(02)00707-9 · DOI · Paper page
  123. Wu, 2007, Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body, Nature Neuroscience, 10, 1578, 10.1038/nn2005 · DOI
  124. Xia, 2005, NMDA receptors mediate olfactory learning and memory in Drosophila, Current Biology, 15, 603, 10.1016/j.cub.2005.02.059 · DOI
  125. Yamagata, In press, Distinct dopamine neurons mediate reward signals for short- and long-term memories, Proceedings of the National Academy of Sciences of USA, 10.1073/pnas.1421930112 · DOI
  126. Yanike, 2014, Representation of outcome risk and action in the anterior caudate nucleus, The Journal of Neuroscience, 34, 3279, 10.1523/JNEUROSCI.3818-13.2014 · DOI
  127. Yin, 1994, Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila, Cell, 79, 49, 10.1016/0092-8674(94)90399-9 · DOI · Paper page
  128. Young, 2010a, Building the central complex in Drosophila: the generation and development of distinct neural subsets, The Journal of Comparative Neurology, 518, 1525, 10.1002/cne.22285 · DOI
  129. Young, 2010b, Structure of the adult central complex in Drosophila: organization of distinct neuronal subsets, The Journal of Comparative Neurology, 518, 1500, 10.1002/cne.22284 · DOI
  130. Yu, 2006, Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning, Neuron, 52, 845, 10.1016/j.neuron.2006.10.030 · DOI · Paper page
  131. Yu, 2010, A complete developmental sequence of a Drosophila neuronal lineage as revealed by twin-spot MARCM, PLOS Biology, 8, e1000461, 10.1371/journal.pbio.1000461 · DOI · Paper page
  132. Zars, 2000, Localization of a short-term memory in Drosophila, Science, 288, 672, 10.1126/science.288.5466.672 · DOI · Paper page
  133. Zhang, 2007, Dopamine-mushroom body circuit regulates saliency-based decision-making in Drosophila, Science, 316, 1901, 10.1126/science.1137357 · DOI
  134. Zhang, 2013, Parallel pathways for cross-modal memory retrieval in Drosophila, The Journal of Neuroscience, 33, 8784, 10.1523/JNEUROSCI.4631-12.2013 · DOI
  135. Zhu, 2009, Peripheral visual circuits functionally segregate motion and phototaxis behaviors in the fly, Current Biology, 19, 613, 10.1016/j.cub.2009.02.053 · DOI

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Metadata

Authors
Aso, Y., Sitaraman, D., Ichinose, T., Kaun, K. R., Vogt, K., Belliart-Guérin, G., Plaçais, P.-Y., Robie, A. A., Yamagata, N., Schnaitmann, C., Rowell, W. J., Johnston, R. M., Ngo, T.-T. B., Chen, N., Korff, W., Nitabach, M. N., Heberlein, U., Preat, T., Branson, K. M., Tanimoto, H., & Rubin, G. M.
Venue
eLife
Published
2014-12-23
Volume
3
Pages
e04580-e04580
ISSN
2050-084X (ISSN-L)
OpenAlex
W1999985543
Cited by
696
References
13
FWCI
18.65
Type
journal article
Language
en
Open access
gold
Funders
  • Howard Hughes Medical Institute (Janelia Visiting Scientist Program)
  • Agence Nationale de la Recherche
  • Labex MemoLife
  • Bundesministerium für Bildung und Forschung (Bernstein Focus Neurobiology of Learning 01GQ0932)
  • Max-Planck-Gesellschaft
  • Deutsche Forschungsgemeinschaft (TA 552/5-1)
  • Japan Society for the Promotion of Science (MEXT/JSPS KAKENHI 25890003, 26120705, 26119503 and 26250001)
  • Naito Foundation
  • National Institute of Neurological Disorders and Stroke (R01NS055035, R01NS056443, R01NS091070)
  • National Institute of General Medical Sciences (R01GM098931)

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Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.