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Original

The Mushroom Body of Adult Drosophila Characterized by GAL4 Drivers

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Pages 156-172 | Received 30 Aug 2008, Published online: 11 Jul 2009

References

  • Akalal D. B., Wilson C. F., Zong L., Tanaka N. K., Ito K., Davis R. L. Roles for Drosophila mushroom body neurons in olfactory learning and memory. Learn Mem 2006; 13(5)659–668
  • Balling A., Technau G. M., Heisenberg M. Are the structural changes in adult Drosophila mushroom bodies memory traces? Studies on biochemical learning mutants. J Neurogenet 1987; 4(2–3)65–73
  • Crittenden J. R., Skoulakis E. M., Han K. A., Kalderon D., Davis R. L. Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 1998; 5(1–2)38–51
  • Fahrbach S. E. Structure of the mushroom bodies of the insect brain. Annu Rev Entomol 2006; 51: 209–232
  • Heisenberg M. Mutants of brain structure and function: what is the significance of the mushroom bodies for behavior?. Basic Life Sci 1980; 16: 373–390
  • Heisenberg M. Mushroom body memoir: from maps to models. Nat Rev Neurosci 2003; 4(4)266–275
  • Heisenberg M., Heusipp M., Wanke C. Structural plasticity in the Drosophila brain. J Neurosci 1995; 15(3 Pt 1)1951–1960
  • Hinke W. Das relative postembryonale Wachstum der Hirnteile von Culex pipiens, Drosophila melanogaster und Drosophila-Mutanten. [The relative postembryonic growth of brain regions in Culex pipens, Drosophila melanogaster and Drosphila Mutants]. Z Morph Ökol Tiere 1961; 50: 81–118
  • Isabel G., Pascual A., Preat T. Exclusive consolidated memory phases in Drosophila. Science 2004; 304(5673)1024–1027
  • Ito K., Hotta Y. Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Dev Biol 1992; 149(1)134–148
  • Ito K., Okada R., Tanaka N. K., Awasaki T. Cautionary observations on preparing and interpreting brain images using molecular biology-based staining techniques. Microsc Res Tech 2003; 62(2)170–186
  • Ito K., Sass H., Urban J., Hofbauer A., Schneuwly S. GAL4-responsive UAS-tau as a tool for studying the anatomy and development of the Drosophila central nervous system. Cell Tissue Res 1997; 290(1)1–10
  • Ito K., Suzuki K., Estes P., Ramaswami M., Yamamoto D., Strausfeld N. J. The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn Mem 1998; 5(1–2)52–77
  • Jefferis G. S., Marin E. C., Watts R. J., Luo L. Development of neuronal connectivity in Drosophila antennal lobes and mushroom bodies. Curr Opin Neurobiol 2002; 12(1)80–86
  • Jefferis G. S., Potter C. J., Chan A. M., Marin E. C., Rohlfing T., Maurer C. R., Jr, et al. Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 2007; 128(6)1187–1203
  • Johard H. A., Enell L. E., Gustafsson E., Trifilieff P., Veenstra J. A., Nassel D. R. Intrinsic neurons of Drosophila mushroom bodies express short neuropeptide F: relations to extrinsic neurons expressing different neurotransmitters. J Comp Neurol 2008; 507(4)1479–1496
  • Keene A. C., Waddell S. Drosophila olfactory memory: single genes to complex neural circuits. Nat Rev Neurosci 2007; 8(5)341–354
  • Keleman K., Kruttner S., Alenius M., Dickson B. J. Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat Neurosci 2007; 10(12)1587–1593
  • Klagges B. R., Heimbeck G., Godenschwege T. A., Hofbauer A., Pflugfelder G. O., Reifegerste R., et al. Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 1996; 16(10)3154–3165
  • Kurusu M., Awasaki T., Masuda-Nakagawa L. M., Kawauchi H., Ito K., Furukubo-Tokunaga K. Embryonic and larval development of the Drosophila mushroom bodies: concentric layer subdivisions and the role of fasciclin II. Development 2002; 129(2)409–419
  • Lee T., Lee A., Luo L. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 1999; 126(18)4065–4076
  • Leitch B., Laurent G. GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system. J Comp Neurol 1996; 372(4)487–514
  • Lin H. H., Lai J. S., Chin A. L., Chen Y. C., Chiang A. S. A map of olfactory representation in the Drosophila mushroom body. Cell 2007; 128(6)1205–1217
  • Luan H., Peabody N. C., Vinson C. R., White B. H. Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron 2006; 52(3)425–436
  • Mader, M. T. 2004. Analyse von Expressionsmustern in den Pilzkörpern von Drosophila melanogaster [Analysis of expression pattern in the mushroom body of Drosophila melanogaster] [diploma thesis]. University of Würzburg, WürzburgGermany.
  • Maurange C., Cheng L., Gould A. P. Temporal transcription factors and their targets schedule the end of neural proliferation in Drosophila. Cell 2008; 133(5)891–902
  • McGuire S. E., Le P. T., Osborn A. J., Matsumoto K., Davis R. L. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 2003; 302(5651)1765–1768
  • Mobbs P. G. Neural networks in the mushroom bodies of the honeybee. J Insect Physiol 1984; 30(1)43–58
  • Neder R. Allometrisches Wachstum von Hirnteilen bei drei verschieden großen Schabenarten. [Allometric growth of brain regions in three different large cockroaches]. Zool Jahrb Abt Anat Ontogenie Tiere 1959; 4: 411–464
  • Nicolaï M., Lasbleiz C., Dura J. M. Gain-of-function screen identifies a role of the Src64 oncogene in Drosophila mushroom body development. J Neurobiol 2003; 57(3)291–302
  • Osterwalder T., Yoon K. S., White B. H., Keshishian H. A conditional tissue-specific transgene expression system using inducible GAL4. Proc Natl Acad Sci U S A 2001; 98(22)12596–12601
  • Prokop A., Meinertzhagen I. A. Development and structure of synaptic contacts in Drosophila. Semin Cell Dev Biol 2006; 17(1)20–30
  • Roman G., Endo K., Zong L., Davis R. L. P[Switch], a system for spatial and temporal control of gene expression in Drosophila melanogaster. Proc Natl Acad Sci U S A 2001; 98(22)12602–12607
  • Rybak J., Menzel R. Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha-lobe. J Comp Neurol 1993; 334(3)444–465
  • Sjöholm M., Sinakevitch I., Strausfeld N. J., Ignell R., Hansson B. S. Functional division of intrinsic neurons in the mushroom bodies of male Spodoptera littoralis revealed by antibodies against aspartate, taurine, FMRF-amide, Mas-allatotropin, and DC0. Arthropod Struct Dev 2006; 35(3)153–168
  • Stocker R. F., Lienhard M. C., Borst A., Fischbach K. F. Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 1990; 262(1)9–34
  • Strausfeld N. J. Organization of the honey bee mushroom body: representation of the calyx within the vertical and gamma lobes. J Comp Neurol 2002; 450(1)4–33
  • Strausfeld N. J., Sinakevitch I., Vilinsky I. The mushroom bodies of Drosophila melanogaster: an immunocytological and golgi study of Kenyon cell organization in the calyces and lobes. Microsc Res Tech 2003; 62(2)151–169
  • Suster M. L., Seugnet L., Bate M., Sokolowski M. B. Refining GAL4-driven transgene expression in Drosophila with a GAL80 enhancer trap. Genesis 2004; 39(4)240–245
  • Tanaka N. K., Awasaki T., Shimada T., Ito K. Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr Biol 2004; 14(6)449–457
  • Tanaka N. K., Tanimoto H., Ito K. Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 2008; 508(5)711–755
  • Technau G., Heisenberg M. Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature 1982; 295(5848)405–407
  • Technau G. M. Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex, and experience. J Neurogenet 1984; 1(2)113–126
  • Turner G. C., Bazhenov M., Laurent G. Olfactory representations by Drosophila mushroom body neurons. J Neurophysiol 2008; 99(2)734–746
  • Venken K. J., Bellen H. J. Emerging technologies for gene manipulation in Drosophila melanogaster. Nat Rev Genet 2005; 6(3)167–178
  • Wang Y., Guo H. F., Pologruto T. A., Hannan F., Hakker I., Svoboda K., et al. Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2+ imaging. J Neurosci 2004; 24(29)6507–6514
  • Witthöft W. Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene. [Absolute number and distribution of cells in the honey bee brain]. Zoomorphology 1967; 61(1)160–184
  • Yang M. Y., Armstrong J. D., Vilinsky I., Strausfeld N. J., Kaiser K. Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 1995; 15(1)45–54
  • Yasuyama K., Meinertzhagen I. A., Schürmann F. W. Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J Comp Neurol 2002; 445(3)211–226
  • Zhu S., Chiang A. S., Lee T. Development of the Drosophila mushroom bodies: elaboration, remodeling, and spatial organization of dendrites in the calyx. Development 2003; 130(12)2603–2610
  • Acevedo S. F., Froudarakis E. I., Kanellopoulos A., Skoulakis E. M. Protection from premature habituation requires functional mushroom bodies in Drosophila. Learn Mem 2007; 14(5)376–384
  • Acevedo S. F., Froudarakis E. I., Tsiorva A. A., Skoulakis E. M. Distinct neuronal circuits mediate experience-dependent, non-associative osmotactic responses in Drosophila. Mol Cell Neurosci 2007; 34(3)378–389
  • Adachi Y., Hauck B., Clements J., Kawauchi H., Kurusu M., Totani Y., et al. Conserved cis-regulatory modules mediate complex neural expression patterns of the eyeless gene in the Drosophila brain. Mech Dev 2003; 120(10)1113–1126
  • Agrawal N., Pallos J., Slepko N., Apostol B. L., Bodai L., Chang L. W., et al. Identification of combinatorial drug regimens for treatment of Huntington's disease using Drosophila. Proc Natl Acad Sci U S A 2005; 102(10)3777–3781
  • Akalal D. B., Wilson C. F., Zong L., Tanaka N. K., Ito K., Davis R. L. Roles for Drosophila mushroom body neurons in olfactory learning and memory. Learn Mem 2006; 13(5)659–668
  • Amrein H., Axel R. Genes expressed in neurons of adult male Drosophila. Cell 1997; 88(4)459–469
  • Astle J., Kozlova T., Thummel C. S. Essential roles for the Dhr78 orphan nuclear receptor during molting of the Drosophila tracheal system. Insect Biochem Mol Biol 2003; 33(12)1201–1209
  • Awasaki T., Ito K. Engulfing action of glial cells is required for programmed axon pruning during Drosophila metamorphosis. Curr Biol 2004; 14(8)668–677
  • Baker D. A., Beckingham K. M., Armstrong J. D. Functional dissection of the neural substrates for gravitaxic maze behavior in Drosophila melanogaster. J Comp Neurol 2007; 501(5)756–764
  • Belgacem Y. H., Martin J. R. Neuroendocrine control of a sexually dimorphic behavior by a few neurons of the pars intercerebralis in Drosophila. Proc Natl Acad Sci U S A 2002; 99(23)15154–15158
  • Billuart P., Winter C. G., Maresh A., Zhao X., Luo L. Regulating axon branch stability: the role of p190 RhoGAP in repressing a retraction signaling pathway. Cell 2001; 107(2)195–207
  • Boyle M., Nighorn A., Thomas J. B. Drosophila Eph receptor guides specific axon branches of mushroom body neurons. Development 2006; 133(9)1845–1854
  • Broughton S. J., Kitamoto T., Greenspan R. J. Excitatory and inhibitory switches for courtship in the brain of Drosophila melanogaster. Curr Biol 2004; 14(7)538–547
  • Campusano J. M., Su H., Jiang S. A., Sicaeros B., O'Dowd D. K. nAChR-mediated calcium responses and plasticity in Drosophila Kenyon cells. Dev Neurobiol 2007; 67(11)1520–1532
  • Casares F., Calleja M., Sanchez-Herrero E. Functional similarity in appendage specification by the Ultrabithorax and abdominal-A Drosophila HOX genes. EMBO J 1996; 15(15)3934–3942
  • Chang K. T., Shi Y. J., Min K. T. The Drosophila homolog of Down's syndrome critical region 1 gene regulates learning: implications for mental retardation. Proc Natl Acad Sci U S A 2003; 100(26)15794–15799
  • Chen G., Li W., Zhang Q. S., Regulski M., Sinha N., Barditch J., et al. Identification of synaptic targets of Drosophila pumilio. PLoS Comput Biol 2008; 4(2)1000026
  • Cheng Y., Endo K., Wu K., Rodan A. R., Heberlein U., Davis R. L. Drosophila fasciclinII is required for the formation of odor memories and for normal sensitivity to alcohol. Cell 2001; 105(6)757–768
  • Comas D., Petit F., Preat T. Drosophila long-term memory formation involves regulation of cathepsin activity. Nature 2004; 430(6998)460–463
  • Connolly J. B., Roberts I. J., Armstrong J. D., Kaiser K., Forte M., Tully T., et al. Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 1996; 274(5295)2104–2107
  • DeZazzo J., Sandstrom D., de Belle S., Velinzon K., Smith P., Grady L., et al. nalyot, a mutation of the Drosophila myb-related Adf1 transcription factor, disrupts synapse formation and olfactory memory. Neuron 2000; 27(1)145–158
  • Diegelmann S., Fiala A., Leibold C., Spall T., Buchner E. Transgenic flies expressing the fluorescence calcium sensor Cameleon 2.1 under UAS control. Genesis 2002; 34(1-2)95–98
  • Dubnau J., Grady L., Kitamoto T., Tully T. Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 2001; 411(6836)476–480
  • Enerly E., Larsson J., Lambertsson A. Silencing the Drosophila ribosomal protein L14 gene using targeted RNA interference causes distinct somatic anomalies. Gene 2003; 320: 41–48
  • Fushima K., Tsujimura H. Precise control of fasciclin II expression is required for adult mushroom body development in Drosophila. Dev Growth Differ 2007; 49(3)215–227
  • Garcia-Lopez A., Monferrer L., Garcia-Alcover I., Vicente-Crespo M., Alvarez-Abril M. C., Artero R. D. Genetic and chemical modifiers of a CUG toxicity model in Drosophila. PLoS ONE 2008; 3(2)1595
  • Gatti S., Ferveur J. F., Martin J. R. Genetic identification of neurons controlling a sexually dimorphic behaviour. Curr Biol 2000; 10(11)667–670
  • Goldstein A. Y., Jan Y. N., Luo L. Function and regulation of Tumbleweed (RacGAP50C) in neuroblast proliferation and neuronal morphogenesis. Proc Natl Acad Sci U S A 2005; 102(10)3834–3839
  • Grammenoudi S., Kosmidis S., Skoulakis E. M. Cell type-specific processing of human Tau proteins in Drosophila. FEBS Lett 2006; 580(19)4602–4606
  • Grillenzoni N., Flandre A., Lasbleiz C., Dura J. M. Respective roles of the DRL receptor and its ligand WNT5 in Drosophila mushroom body development. Development 2007; 134(17)3089–3097
  • Gu G., Yang J., Mitchell K. A., O'Tousa J. E. Drosophila ninaB and ninaD act outside of retina to produce rhodopsin chromophore. J Biol Chem 2004; 279(18)18608–18613
  • Gu H., O'Dowd D. K. Cholinergic synaptic transmission in adult Drosophila Kenyon cells in situ. J Neurosci 2006; 26(1)265–272
  • Hayashi S., Ito K., Sado Y., Taniguchi M., Akimoto A., Takeuchi H., et al. GETDB, a database compiling expression patterns and molecular locations of a collection of Gal4 enhancer traps. Genesis 2002; 34(1-2)58–61
  • Honjo K., Furukubo-Tokunaga K. Induction of cAMP response element-binding protein-dependent medium-term memory by appetitive gustatory reinforcement in Drosophila larvae. J Neurosci 2005; 25(35)7905–7913
  • Isabel G., Pascual A., Preat T. Exclusive consolidated memory phases in Drosophila. Science 2004; 304(5673)1024–1027
  • Ito K., Urban J., Technau G. Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Dev Genes Evol 1995; 204(5)284–307
  • Johard H. A., Enell L. E., Gustafsson E., Trifilieff P., Veenstra J. A., Nässel D. R. Intrinsic neurons of Drosophila mushroom bodies express short neuropeptide F: relations to extrinsic neurons expressing different neurotransmitters. J Comp Neurol 2008; 507(4)1479–1496
  • Joiner M. A., Griffith L. C. Visual input regulates circuit configuration in courtship conditioning of Drosophila melanogaster. Learn Mem 2000; 7(1)32–42
  • Joiner W. J., Crocker A., White B. H., Sehgal A. Sleep in Drosophila is regulated by adult mushroom bodies. Nature 2006; 441(7094)757–760
  • Kammermeier L., Leemans R., Hirth F., Flister S., Wenger U., Walldorf U., et al. Differential expression and function of the Drosophila Pax6 genes eyeless and twin of eyeless in embryonic central nervous system development. Mech Dev 2001; 103(1-2)71–78
  • Kaun K. R., Hendel T., Gerber B., Sokolowski M. B. Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase. Learn Mem 2007; 14(5)342–349
  • Keleman K., Kruttner S., Alenius M., Dickson B. J. Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat Neurosci 2007; 10(12)1587–1593
  • Kido A., Ito K. Mushroom bodies are not required for courtship behavior by normal and sexually mosaic Drosophila. J Neurobiol 2002; 52(4)302–311
  • Kim Y. C., Lee H. G., Han K. A. D1 dopamine receptor dDA1 is required in the mushroom body neurons for aversive and appetitive learning in Drosophila. J Neurosci 2007; 27(29)7640–7647
  • Kim Y. C., Lee H. G., Seong C. S., Han K. A. Expression of a D1 dopamine receptor dDA1/DmDOP1 in the central nervous system of Drosophila melanogaster. Gene Expr Patterns 2003; 3(2)237–245
  • Kitamoto T. Conditional disruption of synaptic transmission induces male-male courtship behavior in Drosophila. Proc Natl Acad Sci U S A 2002; 99(20)13232–13237
  • Kobayashi M., Michaut L., Ino A., Honjo K., Nakajima T., Maruyama Y., et al. Differential microarray analysis of Drosophila mushroom body transcripts using chemical ablation. Proc Natl Acad Sci U S A 2006; 103(39)14417–14422
  • Komiyama T., Sweeney L. B., Schuldiner O., Garcia K. C., Luo L. Graded expression of semaphorin-1a cell-autonomously directs dendritic targeting of olfactory projection neurons. Cell 2007; 128(2)399–410
  • Koushika S. P., Lisbin M. J., White K. ELAV, a Drosophila neuron-specific protein, mediates the generation of an alternatively spliced neural protein isoform. Curr Biol 1996; 6(12)1634–1641
  • Koushika S. P., Soller M., White K. The neuron-enriched splicing pattern of Drosophila erect wing is dependent on the presence of ELAV protein. Mol Cell Biol 2000; 20(5)1836–1845
  • Kraft R., Levine R. B., Restifo L. L. The steroid hormone 20-hydroxyecdysone enhances neurite growth of Drosophila mushroom body neurons isolated during metamorphosis. J Neurosci 1998; 18(21)8886–8899
  • Krashes M. J., Keene A. C., Leung B., Armstrong J. D., Waddell S. Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron 2007; 53(1)103–115
  • Krashes M. J., Waddell S. Rapid consolidation to a radish and protein synthesis-dependent long-term memory after single-session appetitive olfactory conditioning in Drosophila. J Neurosci 2008; 28(12)3103–3113
  • Kurusu M., Awasaki T., Masuda-Nakagawa L. M., Kawauchi H., Ito K., Furukubo-Tokunaga K. Embryonic and larval development of the Drosophila mushroom bodies: concentric layer subdivisions and the role of fasciclin II. Development 2002; 129(2)409–419
  • Lee H., Stultz B. G., Hursh D. A. The Zic family member, odd-paired, regulates the Drosophila BMP, decapentaplegic, during adult head development. Development 2007; 134(7)1301–1310
  • Lee T., Lee A., Luo L. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 1999; 126(18)4065–4076
  • Lee T., Marticke S., Sung C., Robinow S., Luo L. Cell-autonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron 2000; 28(3)807–818
  • Lin H. H., Lai J. S., Chin A. L., Chen Y. C., Chiang A. S. A map of olfactory representation in the Drosophila mushroom body. Cell 2007; 128(6)1205–1217
  • Liu X., Krause W. C., Davis R. L. GABAA receptor RDL inhibits Drosophila olfactory associative learning. Neuron 2007; 56(6)1090–1102
  • Liu Z., Steward R., Luo L. Drosophila Lis1 is required for neuroblast proliferation, dendritic elaboration and axonal transport. Nat Cell Biol 2000; 2(11)776–783
  • Luo L., Lee T., Nardine T., Null B., Reuter J. Using the MARCM system to positively mark mosaic clones in Drosophila. Dros Inf Serv 1999; 82: 102–105
  • Manoli D. S., Foss M., Villella A., Taylor B. J., Hall J. C., Baker B. S. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 2005; 436(7049)395–400
  • Manseau L., Baradaran A., Brower D., Budhu A., Elefant F., Phan H., et al. GAL4 enhancer traps expressed in the embryo, larval brain, imaginal discs, and ovary of Drosophila. Dev Dyn 1997; 209(3)310–322
  • Martin J. R., Rogers K. L., Chagneau C., Brulet P. In vivo bioluminescence imaging of Ca signalling in the brain of Drosophila. PLoS ONE 2007; 2(3)275
  • Martini S. R., Roman G., Meuser S., Mardon G., Davis R. L. The retinal determination gene, dachshund, is required for mushroom body cell differentiation. Development 2000; 127(12)2663–2672
  • Masuda-Nakagawa L. M., Tanaka N. K., O'Kane C. J. Stereotypic and random patterns of connectivity in the larval mushroom body calyx of Drosophila. Proc Natl Acad Sci U S A 2005; 102(52)19027–19032
  • McBride S. M., Giuliani G., Choi C., Krause P., Correale D., Watson K., et al. Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster. Neuron 1999; 24(4)967–977
  • McGuire S. E., Le P. T., Davis R. L. The role of Drosophila mushroom body signaling in olfactory memory. Science 2001; 293(5533)1330–1333
  • McGuire S. E., Le P. T., Osborn A. J., Matsumoto K., Davis R. L. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 2003; 302(5651)1765–1768
  • Mehren J. E., Griffith L. C. Calcium-independent calcium/calmodulin-dependent protein kinase II in the adult Drosophila CNS enhances the training of pheromonal cues. J Neurosci 2004; 24(47)10584–10593
  • Mery F., Belay A. T., So A. K., Sokolowski M. B., Kawecki T. J. Natural polymorphism affecting learning and memory in Drosophila. Proc Natl Acad Sci U S A 2007; 104(32)13051–13055
  • Michel C. I., Kraft R., Restifo L. L. Defective neuronal development in the mushroom bodies of Drosophila fragile X mental retardation 1 mutants. J Neurosci 2004; 24(25)5798–5809
  • Moreau-Fauvarque C., Taillebourg E., Boissoneau E., Mesnard J., Dura J. M. The receptor tyrosine kinase gene linotte is required for neuronal pathway selection in the Drosophila mushroom bodies. Mech Dev 1998; 78(1-2)47–61
  • Ng J., Luo L. Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron 2004; 44(5)779–793
  • Ng J., Nardine T., Harms M., Tzu J., Goldstein A., Sun Y., et al. Rac GTPases control axon growth, guidance and branching. Nature 2002; 416(6879)442–447
  • Nicolai M., Lasbleiz C., Dura J. M. Gain-of-function screen identifies a role of the Src64 oncogene in Drosophila mushroom body development. J Neurobiol 2003; 57(3)291–302
  • Niimi T., Clements J., Gehring W. J., Callaerts P. Dominant-negative form of the Pax6 homolog eyeless for tissue-specific loss-of-function studies in the developing eye and brain in Drosophila. Genesis 2002; 34(1-2)74–75
  • Nishimura I., Sakoda J. Y., Yoshikawa K. Drosophila MAGE controls neural precursor proliferation in postembryonic neurogenesis. Neuroscience 2008; 154(2)572–581
  • Nitz D. A., van Swinderen B., Tononi G., Greenspan R. J. Electrophysiological correlates of rest and activity in Drosophila melanogaster. Curr Biol 2002; 12(22)1934–1940
  • Noveen A., Daniel A., Hartenstein V. Early development of the Drosophila mushroom body: the roles of eyeless and dachshund. Development 2000; 127(16)3475–3488
  • O'Dell K. M., Armstrong J. D., Yang M. Y., Kaiser K. Functional dissection of the Drosophila mushroom bodies by selective feminization of genetically defined subcompartments. Neuron 1995; 15(1)55–61
  • Orihara-Ono M., Suzuki E., Saito M., Yoda Y., Aigaki T., Hama C. The slender lobes gene, identified by retarded mushroom body development, is required for proper nucleolar organization in Drosophila. Dev Biol 2005; 281(1)121–133
  • Pan L., Zhang Y. Q., Woodruff E., Broadie K. The Drosophila fragile X gene negatively regulates neuronal elaboration and synaptic differentiation. Curr Biol 2004; 14(20)1863–1870
  • Parker C. G., Fessler L. I., Nelson R. E., Fessler J. H. Drosophila UDP-glucose:glycoprotein glucosyltransferase: sequence and characterization of an enzyme that distinguishes between denatured and native proteins. EMBO J 1995; 14(7)1294–1303
  • Pascual A., Huang K. L., Preat T. Conditional UAS-targeted repression in Drosophila. Nucleic Acids Res 2005; 33(1)7
  • Pascual A., Preat T. Localization of long-term memory within the Drosophila mushroom body. Science 2001; 294(5544)1115–1117
  • Peng Y., Guo A. Novel stimulus-induced calcium efflux in Drosophila mushroom bodies. Eur J Neurosci 2007; 25(7)2034–2044
  • Peng Y., Xi W., Zhang W., Zhang K., Guo A. Experience improves feature extraction in Drosophila. J Neurosci 2007; 27(19)5139–5145
  • Pitman J. L., McGill J. J., Keegan K. P., Allada R. A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 2006; 441(7094)753–756
  • Plaza S., Prince F., Jaeger J., Kloter U., Flister S., Benassayag C., et al. Molecular basis for the inhibition of Drosophila eye development by Antennapedia. EMBO J 2001; 20(4)802–811
  • Presente A., Boyles R. S., Serway C. N., de Belle J. S., Andres A. J. Notch is required for long-term memory in Drosophila. Proc Natl Acad Sci U S A 2004; 101(6)1764–1768
  • Qiu Y., Davis R. L. Genetic dissection of the learning/memory gene dunce of Drosophila melanogaster. Genes Dev 1993; 7(7B)1447–1458
  • Ramaekers A., Magnenat E., Marin E. C., Gendre N., Jefferis G. S., Luo L., et al. Glomerular Maps without Cellular Redundancy at Successive Levels of the Drosophila Larval Olfactory Circuit. Curr Biol 2005; 15(11)982–992
  • Reeve S. P., Bassetto L., Genova G. K., Kleyner Y., Leyssen M., Jackson F. R., et al. The Drosophila fragile X mental retardation protein controls actin dynamics by directly regulating profilin in the brain. Curr Biol 2005; 15(12)1156–1163
  • Rodan A. R., Kiger J. A., Jr, Heberlein U. Functional dissection of neuroanatomical loci regulating ethanol sensitivity in . Drosophila. J Neurosci 2002; 22(21)9490–9501
  • Rosay P., Armstrong J. D., Wang Z., Kaiser K. Synchronized neural activity in the Drosophila memory centers and its modulation by amnesiac. Neuron 2001; 30(3)759–770
  • Sakai T., Kitamoto T. Differential roles of two major brain structures, mushroom bodies and central complex, for Drosophila male courtship behavior. J Neurobiol 2006; 66(8)821–834
  • Schneeberger D., Raabe T. Mbt, a Drosophila PAK protein, combines with Cdc42 to regulate photoreceptor cell morphogenesis. Development 2003; 130(3)427–437
  • Schuldiner O., Berdnik D., Levy J. M., Wu J. S., Luginbuhl D., Gontang A. C., et al. piggyBac-based mosaic screen identifies a postmitotic function for cohesin in regulating developmental axon pruning. Dev Cell 2008; 14(2)227–238
  • Schulz R. A., Chromey C., Lu M. F., Zhao B., Olson E. N. Expression of the D-MEF2 transcription in the Drosophila brain suggests a role in neuronal cell differentiation. Oncogene 1996; 12(8)1827–1831
  • Schwaerzel M., Heisenberg M., Zars T. Extinction antagonizes olfactory memory at the subcellular level. Neuron 2002; 35(5)951–960
  • Schwaerzel M., Monastirioti M., Scholz H., Friggi-Grelin F., Birman S., Heisenberg M. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 2003; 23(33)10495–10502
  • Scott E. K., Lee T., Luo L. enok encodes a Drosophila putative histone acetyltransferase required for mushroom body neuroblast proliferation. Curr Biol 2001; 11(2)99–104
  • Shi L., Lin S., Grinberg Y., Beck Y., Grozinger C. M., Robinson G. E., et al. Roles of Drosophila Krüppel-homolog 1 in neuronal morphogenesis. Dev Neurobiol 2007; 67(12)1614–1626
  • Soller M., Haussmann I. U., Hollmann M., Choffat Y., White K., Kubli E., et al. Sex-peptide-regulated female sexual behavior requires a subset of ascending ventral nerve cord neurons. Curr Biol 2006; 16(18)1771–1782
  • Su H., O'Dowd D. K. Fast synaptic currents in Drosophila mushroom body Kenyon cells are mediated by alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors and picrotoxin-sensitive GABA receptors. J Neurosci 2003; 23(27)9246–9253
  • Suh G. S., Wong A. M., Hergarden A. C., Wang J. W., Simon A. F., Benzer S., et al. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 2004; 431(7010)854–859
  • Tanaka N. K., Awasaki T., Shimada T., Ito K. Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr Biol 2004; 14(6)449–457
  • Tanaka N. K., Tanimoto H., Ito K. Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 2008; 508(5)711–755
  • Tettamanti M., Armstrong J. D., Endo K., Yang M. Y., Furukubo-Tokunaga K., Kaiser K., et al. Early development of the Drosophila mushroom bodies, brain centres for associative learning and memory. Development Genes and Evolution 1997; 207(4)242–252
  • Thum A. S., Jenett A., Ito K., Heisenberg M., Tanimoto H. Multiple memory traces for olfactory reward learning in Drosophila. J Neurosci 2007; 27(41)11132–11138
  • Verkhusha V. V., Otsuna H., Awasaki T., Oda H., Tsukita S., Ito K. An enhanced mutant of red fluorescent protein DsRed for double labeling and developmental timer of neural fiber bundle formation. J Biol Chem 2001; 276(32)29621–29624
  • Villella A., Ferri S. L., Krystal J. D., Hall J. C. Functional analysis of fruitless gene expression by transgenic manipulations of Drosophila courtship. Proc Natl Acad Sci U S A 2005; 102(46)16550–16557
  • Waddell S., Armstrong J. D., Kitamoto T., Kaiser K., Quinn W. G. The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 2000; 103(5)805–813
  • Walker J. A., Tchoudakova A. V., McKenney P. T., Brill S., Wu D., Cowley G. S., et al. Reduced growth of Drosophila neurofibromatosis 1 mutants reflects a non-cell-autonomous requirement for GTPase-Activating Protein activity in larval neurons. Genes Dev 2006; 20(23)3311–3323
  • Wang J., Lee C. H., Lin S., Lee T. Steroid hormone-dependent transformation of polyhomeotic mutant neurons in the Drosophila brain. Development 2006; 133(7)1231–1240
  • Wang J., Ma X., Yang J. S., Zheng X., Zugates C. T., Lee C. H., et al. Transmembrane/juxtamembrane domain-dependent Dscam distribution and function during mushroom body neuronal morphogenesis. Neuron 2004; 43(5)663–672
  • Wang J., Zugates C. T., Liang I. H., Lee C. H., Lee T. Drosophila Dscam is required for divergent segregation of sister branches and suppresses ectopic bifurcation of axons. Neuron 2002; 33(4)559–571
  • Wang Y., Chiang A. S., Xia S., Kitamoto T., Tully T., Zhong Y. Blockade of neurotransmission in Drosophila mushroom bodies impairs odor attraction, but not repulsion. Curr Biol 2003; 13(21)1900–1904
  • Wang Y., Guo H. F., Pologruto T. A., Hannan F., Hakker I., Svoboda K., et al. Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2+ imaging. J Neurosci 2004; 24(29)6507–6514
  • Wang Y., Mamiya A., Chiang A. S., Zhong Y. Imaging of an early memory trace in the Drosophila mushroom body. J Neurosci 2008; 28(17)4368–4376
  • Watts R. J., Hoopfer E. D., Luo L. Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 2003; 38(6)871–885
  • Watts R. J., Schuldiner O., Perrino J., Larsen C., Luo L. Glia engulf degenerating axons during developmental axon pruning. Curr Biol 2004; 14(8)678–684
  • Whited J. L., Robichaux M. B., Yang J. C., Garrity P. A. Ptpmeg is required for the proper establishment and maintenance of axon projections in the central brain of Drosophila. Development 2007; 134(1)43–53
  • Wilson R. I., Laurent G. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J Neurosci 2005; 25(40)9069–9079
  • Wojtowicz W. M., Flanagan J. J., Millard S. S., Zipursky S. L., Clemens J. C. Alternative splicing of Drosophila Dscam generates axon guidance receptors that exhibit isoform-specific homophilic binding. Cell 2004; 118(5)619–633
  • Wu C. L., Xia S., Fu T. F., Wang H., Chen Y. H., Leong D., et al. Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body. Nat Neurosci 2007; 10(12)1578–1586
  • Xi W., Peng Y., Guo J., Ye Y., Zhang K., Yu F., et al. Mushroom bodies modulate salience-based selective fixation behavior in Drosophila. Eur J Neurosci 2008; 27(6)1441–1451
  • Yang M. Y., Armstrong J. D., Vilinsky I., Strausfeld N. J., Kaiser K. Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 1995; 15(1)45–54
  • Yang Z., Edenberg H. J., Davis R. L. Isolation of mRNA from specific tissues of Drosophila by mRNA tagging. Nucleic Acids Res 2005; 33(17)148
  • Yeh E., Gustafson K., Boulianne G. L. Green fluorescent protein as a vital marker and reporter of gene expression in Drosophila. Proc Natl Acad Sci U S A 1995; 92(15)7036–7040
  • Yoshihara M., Ito K. Improved Gal4 screening kit for large-scale generation of enhancer-trap strains. Dros Inf Serv 2000; 83: 199–202
  • Yu D., Baird G. S., Tsien R. Y., Davis R. L. Detection of calcium transients in Drosophila mushroom body neurons with camgaroo reporters. J Neurosci 2003; 23(1)64–72
  • Zars T., Fischer M., Schulz R., Heisenberg M. Localization of a short-term memory in Drosophila. Science 2000; 288(5466)672–675
  • Zars T., Wolf R., Davis R., Heisenberg M. Tissue-specific expression of a type I adenylyl cyclase rescues the rutabaga mutant memory defect: in search of the engram. Learn Mem 2000; 7(1)18–31
  • Zelhof A. C., Hardy R. W. WASp is required for the correct temporal morphogenesis of rhabdomere microvilli. J Cell Biol 2004; 164(3)417–426
  • Zhang K., Guo J. Z., Peng Y., Xi W., Guo A. Dopamine-mushroom body circuit regulates saliency-based decision-making in Drosophila. Science 2007; 316(5833)1901–1904
  • Zheng X., Wang J., Haerry T. E., Wu A. Y., Martin J., O'Connor M. B., et al. TGF-beta signaling activates steroid hormone receptor expression during neuronal remodeling in the Drosophila brain. Cell 2003; 112(3)303–315
  • Zheng X., Zugates C. T., Lu Z., Shi L., Bai J. M., Lee T. Baboon/dSmad2 TGF-beta signaling is required during late larval stage for development of adult-specific neurons. EMBO J 2006; 25(3)615–627
  • Zhu S., Chiang A. S., Lee T. Development of the Drosophila mushroom bodies: elaboration, remodeling and spatial organization of dendrites in the calyx. Development 2003; 130(12)2603–2610
  • Zhu S., Lin S., Kao C. F., Awasaki T., Chiang A. S., Lee T. Gradients of the Drosophila Chinmo BTB-zinc finger protein govern neuronal temporal identity. Cell 2006; 127(2)409–422
  • Zhu S., Perez R., Pan M., Lee T. Requirement of Cul3 for axonal arborization and dendritic elaboration in Drosophila mushroom body neurons. J Neurosci 2005; 25(16)4189–4197