Drosophila larvae establish appetitive olfactory memories via mushroom body neurons of embryonic origin

Journal of Neuroscience

Volumn 30, Issue 32, 2010, Pages 10655-10666

  Pauls, Dennis ^a   Selcho, Mareike ^a   Gendre, Nanae ^a   Stocker, Reinhard F ^a   Thum, Andreas S ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FEMALE; MALE; MUSHROOM BODY; NERVE CELL; NONHUMAN; OLFACTORY CORTEX; OLFACTORY MEMORY; PRIORITY JOURNAL; ANIMAL; ANIMAL EMBRYO; APPETITE; BIOLOGICAL MODEL; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; LARVA; MEMORY; METABOLISM; NONPARAMETRIC TEST; ODOR; OLFACTORY SYSTEM; PHYSIOLOGY; PRENATAL DEVELOPMENT; SYNAPSE; TRANSGENIC ANIMAL;

CD8 ANTIGEN; DROSOPHILA PROTEIN; ENZYME INHIBITOR; HYDROXYUREA; TRANSCRIPTION FACTOR;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIGENS, CD8; APPETITIVE BEHAVIOR; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HYDROXYUREA; LARVA; MEMORY; MODELS, BIOLOGICAL; MUSHROOM BODIES; NEURONS; OLFACTORY PATHWAYS; SMELL; STATISTICS, NONPARAMETRIC; SYNAPSES; TRANSCRIPTION FACTORS;

EID: 77956217611     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1281-10.2010     Document Type: Article

References (81)

1. Aceves-Piña EO, Quinn WG (1979) Learning in normal and mutant Drosophila larvae. Science 206:93-96.
2. Amrein H, Axel R (1997) Genes expressed in neurons of adult male Drosophila. Cell 88:459-469.
3. Armstrong JD, de Belle JS, Wang Z, Kaiser K (1998) Metamorphosis of the mushroom bodies; large-scale rearrangements of the neural substrates for associative learning and memory in Drosophila. Learn Mem 5:102-114.
4. Aso Y, Grübel K, Busch S, Friedrich AB, Siwanowicz I, Tanimoto H (2009) The mushroom body of adult Drosophila characterized by GAL4 drivers. J Neurogenet 23:156-172.
5. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
6. Cayre M, Scotto-Lomassese S, Malaterre J, Strambi C, Strambi A (2007) Understanding the regulation and function of adult neurogenesis: contribution from an insect model, the house cricket. Chem Senses 32:385-395.
7. Claridge-Chang A, Roorda RD, Vrontou E, Sjulson L, Li H, Hirsh J, Miesenbo ̈ck G (2009) Writing memories with light-addressable reinforcement circuitry. Cell 139:405-415.
8. Connolly JB, Roberts IJ, Armstrong JD, Kaiser K, Forte M, Tully T, O'Kane CJ (1996) Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274:2104-2107.
9. Crittenden JR, Skoulakis EM, Han KA, Kalderon D, Davis RL (1998) Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 5:38-51.
10. de Belle JS, Heisenberg M (1994) Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263:692-695.
11. Duffy JB (2002) GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis 34:1-15.
12. Dumstrei K, Wang F, Nassif C, Hartenstein V (2003) Early development of the Drosophila brain: V. Pattern of postembryonic neuronal lineages expressing DE-cadherin. J Comp Neurol 455:451-462.
13. Farris SM, Robinson GE, Davis RL, Fahrbach SE (1999) Larval and pupal development of the mushroom bodies in the honey bee, Apis mellifera. J Comp Neurol 414:97-113.
14. Fishilevich E, Domingos AI, Asahina K, Naef F, Vosshall LB, Louis M (2005) Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila. Curr Biol 15:2086-2096.
15. Gerber B, Hendel T (2006) Outcome expectations drive learned behaviour in larval Drosophila. Proc Biol Sci 273:2965-2968.
16. Gerber B, Stocker RF (2007) The Drosophila larva as a model for studying chemosensation and chemosensory learning: a review. Chem Senses 32:65-89.
17. Gerber B, Tanimoto H, Heisenberg M (2004) An engram found? Evaluating the evidence from fruit flies. Curr Opin Neurobiol 14:737-744.
18. Gerber B, Stocker RF, Tanimura T, Thum AS (2009) Smelling, tasting, learning: Drosophila as a study case. Results Probl Cell Differ 47:139-185.
19. Hayashi S, Ito K, Sado Y, Taniguchi M, Akimoto A, Takeuchi H, Aigaki T, Matsuzaki F, Nakagoshi H, Tanimura T, Ueda R, Uemura T, Yoshihara M, Goto S (2002) GETDB, a database compiling expression patterns and molecular locations of a collection of Gal4 enhancer traps. Genesis 34:58-61.
20. Heimbeck G, Bugnon V, Gendre N, Häberlin C, Stocker RF (1999) Smell and taste perception in Drosophila melanogaster larva: toxin expression studies in chemosensory neurons. J Neurosci 19:6599-6609.
21. Heimbeck G, Bugnon V, Gendre N, Keller A, Stocker RF (2001) A central neural circuit for experience-independent olfactory and courtship behavior in Drosophila melanogaster. Proc Natl Acad Sci U S A 98:15336-15341.
22. Heisenberg M (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4:266-275.
23. Heisenberg M, Borst A, Wagner S, Byers D (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 2:1-30.
24. Hendel T, Michels B, Neuser K, Schipanski A, Kaun K, Sokolowski MB, Marohn F, Michel R, Heisenberg M, Gerber B (2005) The carrot, not the stick: appetitive rather than aversive gustatory stimuli support associative olfactory learning in individually assayed Drosophila larvae. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191:265-279.
25. Hertweck H (1931) Anatomie und Variabilitaet des Nervensystems und der Sinnesorgane von Drosophila melanogaster (Meigen). Z Wiss Zool 139:559-663.
26. Honjo K, Furukubo-Tokunaga K (2005) Induction of cAMP response element-binding protein-dependent medium-term memory by appetitive gustatory reinforcement in Drosophila larvae. J Neurosci 25:7905-7913.
27. Honjo K, Furukubo-Tokunaga K (2009) Distinctive neuronal networks and biochemical pathways for appetitive and aversive memory in Drosophila larvae. J Neurosci 29:852-862.
28. Ikeya T, Galic M, Belawat P, Nairz K, Hafen E (2002) Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr Biol 12:1293-1300.
29. Ito K, Hotta Y (1992) Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Dev Biol 149:134-148.
30. Ito K, Suzuki K, Estes P, Ramaswami M, Yamamoto D, Strausfeld NJ (1998) The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn Mem 5:52-77.
31. Iyengar BG, Chou CJ, Sharma A, Atwood HL (2006) Modular neuropile organization in the Drosophila larval brain facilitates identification and mapping of central neurons. J Comp Neurol 499:583-602.
32. Jefferis GS, Vyas RM, Berdnik D, Ramaekers A, Stocker RF, Tanaka NK, Ito K, Luo L (2004) Developmental origin of wiring specificity in the olfactory system of Drosophila. Development 131:117-130.
33. Kaun KR, Hendel T, Gerber B, Sokolowski MB (2007) Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase. Learn Mem 14:342-349.
34. Keene AC, Waddell S (2007) Drosophila olfactory memory: single genes to complex neural circuits. Nat Rev Neurosci 8:341-354.
35. Keleman K, Krüttner S, Alenius M, Dickson BJ (2007) Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat Neurosci 10:1587-1593.
36. Kido A, Ito K (2002) Mushroom bodies are not required for courtship behavior by normal and sexually mosaic Drosophila. J Neurobiol 52:302-311.
37. Kitamoto T (2001) Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol 47:81-92.
38. Kitamura T, Saitoh Y, Takashima N, Murayama A, Niibori Y, Ageta H, Sekiguchi M, Sugiyama H, Inokuchi K (2009) Adult neurogenesis modulates the hippocampus-dependent period of associative fear memory. Cell 139:814-827.
39. Koushika SP, Lisbin MJ, White K (1996) ELAV, a Drosophila neuron-specific protein, mediates the generation of an alternatively spliced neural protein isoform. Curr Biol 6:1634-1641.
40. Kraft R, Levine RB, Restifo LL (1998) The steroid hormone 20-hydroxyecdysone enhances neurite growth of Drosophila mushroom body neurons isolated during metamorphosis. J Neurosci 18:8886-8899.
41. Krashes MJ, Keene AC, Leung B, Armstrong JD, Waddell S (2007) Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron 53:103-115.
42. Krashes MJ, DasGupta S, Vreede A, White B, Armstrong JD, Waddell S (2009) A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139:416-427.
43. Kurusu M, Awasaki T, Masuda-Nakagawa LM, Kawauchi H, Ito K, Furukubo-Tokunaga K (2002) Embryonic and larval development of the Drosophila mushroom bodies: concentric layer subdivisions and the role of fasciclin II. Development 129:409-419.
44. Lee T, Lee A, Luo L (1999) Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126:4065-4076.
45. Leiss F, Groh C, Butcher NJ, Meinertzhagen IA, Tavosanis G (2009) Synaptic organization in the adult Drosophila mushroom body calyx. J Comp Neurol 517:808-824.
46. Manoli DS, Foss M, Villella A, Taylor BJ, Hall JC, Baker BS (2005) Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436:395-400.
47. Mao Z, Davis RL (2009) Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity. Front Neural Circuits 3:5.
48. Marin EC, Watts RJ, Tanaka NK, Ito K, Luo L (2005) Developmentally programmed remodeling of the Drosophila olfactory circuit. Development 132:725-737.
49. Masuda-Nakagawa LM, Tanaka NK, O'Kane CJ (2005) Stereotypic and random patterns of connectivity in the larval mushroom body calyx of Drosophila. Proc Natl Acad Sci U S A 102:19027-19032.
50. Masuda-Nakagawa LM, Gendre N, O'Kane CJ, Stocker RF (2009) Localized olfactory representation in mushroom bodies of Drosophila larvae. Proc Natl Acad Sci U S A 106:10314-10319.
51. McBride SM, Giuliani G, Choi C, Krause P, Correale D, Watson K, Baker G, Siwicki KK (1999) Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster. Neuron 24:967-977.
52. McGuire SE, Le PT, Davis RL (2001) The role of Drosophila mushroom body signaling in olfactory memory. Science 293:1330-1333.
53. McGuire SE, Deshazer M, Davis RL (2005) Thirty years of olfactory learning and memory research in Drosophila melanogaster. Prog Neurobiol 76:328-347.
54. Menzel R, Leboulle G, Eisenhardt D (2006) Small brains, bright minds. Cell 124:237-239.
55. Michels B, Diegelmann S, Tanimoto H, Schwenkert I, Buchner E, Gerber B (2005) A role for Synapsin in associative learning: the Drosophila larva as a study case. Learn Mem 12:224-231.
56. Moreau-Fauvarque C, Taillebourg E, Boissoneau E, Mesnard J, Dura JM (1998) The receptor tyrosine kinase gene linotte is required for neuronal pathway selection in the Drosophila mushroom bodies. Mech Dev 78:47-61.
57. Nassif C, Noveen A, Hartenstein V (2003) Early development of the Drosophila brain: III. The pattern of neuropile founder tracts during the larval period. J Comp Neurol 455:417-434.
58. O'Dell KM, Armstrong JD, Yang MY, Kaiser K (1995) Functional dissection of the Drosophila mushroom bodies by selective feminization of genetically defined subcompartments. Neuron 15:55-61.
59. Osborne KA, Robichon A, Burgess E, Butland S, Shaw RA, Coulthard A, Pereira HS, Greenspan RJ, Sokolowski MB (1997) Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277:834-836.
60. Pascual A, Préat T (2001) Localization of long-term memory within the Drosophila mushroom body. Science 294:1115-1117.
61. Ramaekers A, Magnenat E, Marin EC, Gendre N, Jefferis GS, Luo L, Stocker RF (2005) Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Curr Biol 15:982-992.
62. Riemensperger T, Völler T, Stock P, Buchner E, Fiala A (2005) Punishment prediction by dopaminergic neurons in Drosophila. Curr Biol 15:1953-1960.
63. Scherer S, Stocker RF, Gerber B (2003) Olfactory learning in individually assayed Drosophila larvae. Learn Mem 10:217-225.
64. Schroll C, Riemensperger T, Bucher D, Ehmer J, Völler T, Erbguth K, Gerber B, Hendel T, Nagel G, Buchner E, Fiala A (2006) Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr Biol 16:1741-1747.
65. Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23:10495-10502.
66. Selcho M, Pauls D, Han KA, Stocker RF, Thum AS (2009) The role of dopamine in Drosophila larval classical olfactory conditioning. PLoS One 4:e5897.
67. Stocker RF, Heimbeck G, Gendre N, de Belle JS (1997) Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J Neurobiol 32:443-456.
68. Strausfeld NJ, Sinakevitch I, Vilinsky I (2003) The mushroom bodies of Drosophila melanogaster: an immunocytological and golgi study of Kenyon cell organization in the calyces and lobes. Microsc Res Tech 62:151-169.
69. Tanaka NK, Tanimoto H, Ito K (2008) Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 508:711-755.
70. Technau G, Heisenberg M (1982) Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature 295:405-407.
71. Tettamanti M, Armstrong JD, Endo K, Yang MY, Furukubo-Tokunaga K, Kaiser K, Reichert H (1997) Early development of the Drosophila mushroom bodies, brain centres for associative learning and memory. Dev Genes Evol 207:242-252.
72. Truman JW, Bate M (1988) Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev Biol 125:145-157.
73. Vosshall LB, Stocker RF (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505-533.
74. Waddell S, Armstrong JD, Kitamoto T, Kaiser K, Quinn WG (2000) The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 103:805-813.
75. Wang J, Ma X, Yang JS, Zheng X, Zugates CT, Lee CH, Lee T (2004) Transmembrane/ juxtamembrane domain-dependent Dscam distribution and function during mushroom body neuronal morphogenesis. Neuron 43:663-672.
76. Wang Y, Chiang AS, Xia S, Kitamoto T, Tully T, Zhong Y (2003) Blockade of neurotransmission in Drosophila mushroom bodies impairs odor attraction, but not repulsion. Curr Biol 13:1900-1904.
77. Wong AM, Wang JW, Axel R (2002) Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109:229-241.
78. Yang MY, Armstrong JD, Vilinsky I, Strausfeld NJ, Kaiser K (1995) Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 15:45-54.
79. Yu D, Keene AC, Srivatsan A, Waddell S, Davis RL (2005) Drosophila DPM neurons form a delayed and branch-specific memory trace after olfactory classical conditioning. Cell 123:945-957.
80. Yu D, Akalal DB, Davis RL (2006) Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning. Neuron 52:845-855.
81. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645-660.