Sequential learning of pheromonal cues modulates memory consolidation in trainer-specific associative courtship conditioning

Current Biology

Volumn 15, Issue 3, 2005, Pages 194-206

  Ejima, Aki ^a   Smith, Benjamin P C ^b   Lucas, Christophe ^b   Levine, Joel D ^b   Griffith, Leslie C ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; INSECTA;

EID: 13444250121     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2005.01.035     Document Type: Article

References (68)

1. Tully T., Quinn W.G. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. [A]. 157:1985;263-277
2. Quinn W.G., Harris W.A., Benzer S. Conditioned behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA. 71:1974;708-712
3. Wasserman E.A., Miller R.R. What's elementary about associative learning? Annu. Rev. Psychol. 48:1997;573-607
4. Abraham W.C., Tate W.P. Metaplasticity. A new vista across the field of synaptic plasticity Prog. Neurobiol. 52:1997;303-323
5. Hall J.C. The mating of a fly. Science. 264:1994;1702-1714
6. Siegel R.W., Hall J.C. Conditioned responses in courtship behavior of normal and mutant Drosophila. Proc. Natl. Acad. Sci. USA. 76:1979;565-578
7. Ackerman S.L., Siegel R.W. Chemically reinforced conditioned courtship in Drosophila: Responses to wild-type and the dunce, amnesiac and don giovanni mutants. J. Neurogenet. 3:1986;111-123
8. Tompkins L., Siegel R.W., Gailey D.A., Hall J.C. Conditioned courtship in Drosophila and its mediation by association of chemical cues. Behav. Genet. 13:1983;565-578
9. Joiner M.A., Griffith L.C. CaM kinase II and visual input modulate memory formation in the neuronal circuit controlling courtship conditioning. J. Neurosci. 17:1997;9384-9391
10. Siwicki K.K., Ladewski L. Associative learning and memory in Drosophila. Beyond olfactory conditioning Behav. Processes. 64:2003;225-238
11. Griffith L.C., Verselis L.M., Aitken K.M., Kyriacou C.P., Greenspan R.J. Inhibition of calcium/calmodulin-dependent protein kinase in Drosophila disrupts behavioral plasticity. Neuron. 10:1993;501-509
12. Kane N.S., Robichon A., Dickinson J.A., Greenspan R.J. Learning without performance in PKC-deficient Drosophila. Neuron. 18:1997;307-314
13. Ferveur J.F. The pheromonal role of cuticular hydrocarbons in Drosophila melanogaster. Bioessays. 19:1997;353-358
14. Savarit F., Ferveur J.F. Temperature affects the ontogeny of sexually dimorphic cuticular hydrocarbons in Drosophila melanogaster. J. Exp. Biol. 205:2002;3241-3249
15. Wicker C., Jallon J.-M. Hormonal control of sex pheromone biosynthesis in Drosophila melanogaster. J. Insect Physiol. 41:1995;65-70
16. Jallon J.M. A few chemical words exchanged by Drosophila during courtship and mating. Behav. Genet. 14:1984;441-478
17. Cook R., Cook A. The attractiveness to males of female Drosophila melanogaster: Effects of mating, age and diet. Anim. Behav. 23:1975;521-526
18. Eastwood L., Burnet B. Courtship latency in male Drosophila melanogaster. Behav. Genet. 7:1977;359-372
19. Gailey D.A., Lacaillade R.C., Hall J.C. Chemosensory elements of courtship in normal and mutant, olfaction-deficient Drosophila melanogaster. Behav. Genet. 16:1986;375-405
20. Jackson F.R. The isolation of biological rhythm mutations on the autosomes of Drosophila melanogaster. J. Neurogenet. 1:1983;3-15
21. Gailey D.A., Jackson F.R., Siegel R.W. Conditioning mutations in Drosophila melanogaster affect an experience-dependent behavioral modification in courting males. Genetics. 106:1984;613-623
22. Gailey D.A., Hall J.C., Siegel R.W. Reduced reproductive success for a conditioning mutant in experimental populations of Drosophila melanogaster. Genetics. 111:1985;795-804
23. Cowan T.M., Siegel R.W. Mutational and pharmacological alterations of neuronal membrane function disrupt conditioning in Drosophila. J. Neurogenet. 1:1984;333-344
24. Manning A. The control of sexual receptivity in female Drosophila. Anim. Behav. 15:1967;239-250
25. Spieth H.T. Drosophilid mating behavior. The behaviour of decapitated females Anim. Behav. 14:1966;226-235
26. Doi M., Tomaru M., Matsubayashi H., Yamanoi K., Oguma Y. Genetic analysis of Drosophila virilis sex pheromone. genetic mapping of the locus producing Z-(11)-pentacosene Genet. Res. 68:1996;17-21
27. Trabalon M., Campan M., Clement J.L., Lange C., Miquel M.T. Cuticular hydrocarbons of Calliphora vomitoria (Diptera). Relation to age and sex Gen. Comp. Endocrinol. 85:1992;208-216
28. Gibbs A., Kuenzli M., Blomquist G.J. Sex- and age-related changes in the biophysical properties of cuticular lipids of the housefly, Musca domestica. Arch. Insect Biochem. Physiol. 29:1995;87-97
29. Chapman R.F., Espelie K.E., Sword G.A. Use of cuticular lipids in grasshopper taxonomy. Biochem. Syst. Ecol. 23:1995;383-395
30. Tregenza T., Buckley S.H., Pritchard V.L., Butlin R.K. Inter- and intra-population effects of sex and age on epicuticular composition of meadow grasshopper Clorthippus parallelus. J. Chem. Ecol. 26:2000;259-278
31. Lucas C., Pho D.B., Fresneau D., Jallon J.M. Hydrocarbon circulation and colonial signature in Pachycondyla villosa. J. Insect Physiol. 50:2004;595-607
32. Toolson E.C., Kuper-Simbron R. Laboratory evolution of epicuticular lipid composition and cuticular permeability in Drosophila pseudoobscura: Effects on sexual dimorphism and thermal acclimation ability. Evolution Int. J. Org. Evolution. 43:1989;468-473
33. Gibbs A.G. Water-proofing properties of cuticular lipids. Am. Zool. 38:1998;471-482
34. Gibbs A.G., Pomonis J.G. Physical properties of insect cuticular hydrocarbons. The effects of chain length, methyl-branching and unsaturation Comp. Biochem. Physiol. 112B:1995;243-249
35. Antony C., Jallon J.-M. The chemical basis for sex recognition in Drosophila melanogaster. J. Insect Physiol. 28:1982;873-880
36. Pechine J.M., Jallon J.-M. Precise characterization of cuticular compounds in young Drosophila by mass spectrometry. J. Chem. Ecol. 14:1988;1071-1085
37. Gailey D.A., Jackson F.R., Siegel R.W. Male courtship in Drosophila: The conditioned response to immature males and its genetic control. Genetics. 102:1982;771-782
38. Vaias L.J., Napolitano L.M., Tompkins L. Identification of stimuli that mediate experience-dependent modification of homosexual courtship in Drosophila melanogaster. Behav. Genet. 23:1993;91-97
39. Reilly S., Trifunovic R. Gustatory thalamus lesions eliminate successive negative contrast in rats. evidence against a memory deficit Behav. Neurosci. 117:2003;606-615
40. Grigson P.S., Flaherty C.F. Cyproheptadine prevents the initial occurrence of successive negative contrast. Pharmacol. Biochem. Behav. 40:1991;433-442
41. Hellstern F., Malaka R., Hammer M. Backward inhibitory learning in honeybees. A behavioral analysis of reinforcement processing Learn. Mem. 4:1998;429-444
42. Shorey H.H., Bartell R.J. Role of a volatile female sex pheromone in stimulating male courtship behaviour in Drosophila melanogaster. Anim. Behav. 18:1970;159-164
43. Ayer R.K. Jr., Carlson J. Olfactory physiology in the Drosophila antenna and maxillary palp. acj6 distinguishes two classes of odorant pathways J. Neurobiol. 23:1992;965-982
44. Markow T.A. Behavioral and sensory basis of courtship success in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA. 84:1987;6200-6204
45. Bray S., Amrein H. A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron. 39:2003;1019-1029
46. Dudai Y., Jan Y.N., Byers D., Quinn W.G., Benzer S. dunce, a mutant of Drosophila deficient in learning. Proc. Natl. Acad. Sci. USA. 73:1976;1684-1688
47. Quinn W.G., Sziber P.P., Booker R. The Drosophila memory mutant amnesiac. Nature. 277:1979;212-214
48. O'Dell K.M., Jamieson D., Goodwin S.F., Kaiser K. Abnormal courtship conditioning in males mutant for the RI regulatory subunit of Drosophila protein kinase A. J. Neurogenet. 13:1999;105-118
49. Devaud J.M., Keane J., Ferrus A. Blocking sensory inputs to identified antennal glomeruli selectively modifies odorant perception in Drosophila. J. Neurobiol. 56:2003;1-12
50. Martin F., Charro M.J., Alcorta E. Mutations affecting the cAMP transduction pathway modify olfaction in Drosophila. J. Comp. Physiol. [A]. 187:2001;359-370
51. Gomez-Diaz C., Martin F., Alcorta E. The cAMP transduction cascade mediates olfactory reception in Drosophila melanogaster. Behav. Genet. 34:2004;395-406
52. DeZazzo J., Tully T. Dissection of memory formation. From behavioral pharmacology to molecular genetics Trends Neurosci. 18:1995;212-218
53. Xia S.Z., Feng C.H., Guo A.K. Multiple-phase model of memory consolidation confirmed by behavioral and pharmacological analyses of operant conditioning in Drosophila. Pharmacol. Biochem. Behav. 60:1998;809-816
54. Gong Z., Xia S., Liu L., Feng C., Guo A. Operant visual learning and memory in Drosophila mutants dunce, amnesiac and radish. J. Insect Physiol. 44:1998;1149-1158
55. McBride S.M., Giuliani G., Choi C., Krause P., Correale D., Watson K., Baker G., Siwicki K.K. Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster. Neuron. 24:1999;967-977
56. Kucharski D., Spear N.E. Potentiation and overshadowing in preweanling and adult rats. J. Exp. Psychol. Anim. Behav. Process. 11:1985;15-34
57. Abraham W.C., Bear M.F. Metaplasticity. The plasticity of synaptic plasticity Trends Neurosci. 19:1996;126-130
58. Bainton R.J., Tsai L.T., Singh C.M., Moore M.S., Neckameyer W.S., Heberlein U. Dopamine modulates acute responses to cocaine, nicotine and ethanol in Drosophila. Curr. Biol. 10:2000;187-194
59. 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. 23:2003;10495-10502
60. Joiner M.A., Griffith L.C. Mapping of the anatomical circuit of CaM kinase-dependent courtship conditioning in Drosophila. Learn. Mem. 6:1999;177-192
61. Wang J.W., Wong A.M., Flores J., Vosshall L.B., Axel R. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell. 112:2003;271-282
62. Yu D., Ponomarev A., Davis R.L. Altered representation of the spatial code for odors after olfactory classical conditioning. Memory trace formation by synaptic recruitment Neuron. 42:2004;437-449
63. Feany M.B., Quinn W.G. A neuropeptide gene defined by the Drosophila memory mutant amnesiac. Science. 268:1995;869-873
64. 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. 103:2000;805-813
65. 2+ oscillations, and the memory gene amnesiac. Neuron. 30:2001;653-656
66. Zhou Q., Poo M.M. Reversal and consolidation of activity-induced synaptic modifications. Trends Neurosci. 27:2004;378-383
67. Lindsley D.L., Zimm G.G. The genome of Drosophila melanogaster. 1992;Academic Press, San Diego
68. Moore M.S., DeZazzo J., Luk A.Y., Tully T., Singh C.M., Heberlein U. Ethanol intoxication in Drosophila. Genetic and pharmacological evidence for regulation by the cAMP signaling pathway Cell. 93:1998;997-1007