Serotonin receptor activity is necessary for olfactory learning and memory in Drosophila melanogaster

Neuroscience

Volumn 192, Issue , 2011, Pages 372-381

  Johnson, O ^a   Becnel, J ^a   Nichols, C D ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

5 HT1A; 5 HT2; 5 HT7; Ellipsoid body; Learning and memory; Serotonin

Indexed keywords

MESSENGER RNA; SEROTONIN 1A RECEPTOR; SEROTONIN 1B RECEPTOR; SEROTONIN 2 RECEPTOR; SEROTONIN 7 RECEPTOR; SEROTONIN AGONIST; SEROTONIN ANTAGONIST; SEROTONIN RECEPTOR;

ARTICLE; COGNITION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ELECTROENCEPHALOGRAM; ENZYME ACTIVITY; LEARNING; LONG TERM MEMORY; MEMORY CONSOLIDATION; NONHUMAN; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; SENSORY MEMORY; SHORT TERM MEMORY;

ANIMALS; BRAIN; CONDITIONING, CLASSICAL; DROSOPHILA MELANOGASTER; FEMALE; LEARNING; MALE; MEMORY; RECEPTORS, SEROTONIN; SMELL;

EID: 80052261680     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.06.058     Document Type: Article

References (53)

1. Baker J.G., Hall I.P., Hill S.J. Agonist actions of "beta-blockers" provide evidence for two agonist activation sites or conformations of the human beta1-adrenoceptor. Mol Pharmacol 2003, 63:1312-1321.
2. Barnes N.M., Sharp T. A review of central 5-HT receptors and their function. Neuropharmacology 1999, 38:1083-1152.
3. Becnel J., Johnson O., Luo J., Nässel D.R., Nichols C.D. The serotonin 5-HT7Dro receptor is expressed in the brain of Drosophila, and is essential for normal courtship and mating. PLoS ONE 2011, 6:e20800.
4. Cayre M., Malaterre J., Scotto-Lomassese S., Strambi C., Strambi A. The common properties of neurogenesis in the adult brain: from invertebrates to vertebrates. Comp Biochem Physiol B Biochem Mol Biol 2002, 132:1-15.
5. Colas J.F., Launay J.M., Kellermann O., Rosay P., Maroteaux L. Drosophila 5-HT2 serotonin receptor: coexpression with fushi-tarazu during segmentation. Proc Natl Acad Sci U S A 1995, 92:5441-5445.
6. Dubnau J. Neurogenetic dissection of conditioned behavior: evolution by analogy or homology?. J Neurogenet 2003, 17:295-326.
7. Elia J., Ambrosini P.J., Rapoport J.L. Treatment of attention-deficit-hyperactivity disorder. N Engl J Med 1999, 340:780-788.
8. Hedlund P.B., Sutcliffe J.G. Functional, molecular and pharmacological advances in 5-HT7 receptor research. Trends Pharmacol Sci 2004, 25:481.
9. Hendricks J.C., Kirk D., Panckeri K., Miller M.S., Pack A.I. Modafinil maintains waking in the fruit fly Drosophila melanogaster. Sleep 2003, 26:139-146.
10. Hong S.T., Bang S., Paik D., Kang J., Hwang S., Jeon K., Chun B., Hyun S., Lee Y., Kim J. Histamine and its receptors modulate temperature-preference behaviors in Drosophila. J Neurosci 2006, 26:7245-7256.
11. Johnson O., Becnel J., Nichols C.D. Serotonin 5-HT(2) and 5-HT(1A)-like receptors differentially modulate aggressive behaviors in Drosophila melanogaster. Neuroscience 2009, 158:1292-1300.
12. 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, 27:7640-7647.
13. Krashes M.J., DasGupta S., Vreede A., White B., Armstrong J.D., Waddell S. A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 2009, 139:416-427.
14. 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, 28:3103-3113.
15. Leal S.M., Kumar N., Neckameyer W.S. GABAergic modulation of motor-driven behaviors in juvenile Drosophila and evidence for a nonbehavioral role for GABA transport. J Neurobiol 2004, 61:189-208.
16. Liu T., Dartevelle L., Yuan C., Wei H., Wang Y., Ferveur J.F., Guo A. Increased dopamine level enhances male-male courtship in Drosophila. J Neurosci 2008, 28:5539-5546.
17. Liu X., Krause W.C., Davis R.L. GABAA receptor RDL inhibits Drosophila olfactory associative learning. Neuron 2007, 56:1090-1102.
18. Lucki I. The spectrum of behaviors influenced by serotonin. Biol Psychiatry 1998, 44:151-162.
19. Mailman R.B. GPCR functional selectivity has therapeutic impact. Trends Pharmacol Sci 2007, 28:390-396.
20. McCall R.B., Romero A.G., Bienkowski M.J., Harris D.W., McGuire J.C., Piercey M.F., Shuck M.E., Smith M.W., Svensson K.A., Schreur P.J., et al. Characterization of U-92016A as a selective, orally active, high intrinsic activity 5-hydroxytryptamine1A agonist. J Pharmacol Exp Ther 1994, 271:875-883.
21. McGuire T.R. Learning in three species of Diptera: the blow fly Phormia regina, the fruit fly Drosophila melanogaster, and the house fly Musca domestica. Behav Genet 1984, 14:479-526.
22. Meneses A. 5-HT system and cognition. Neurosci Biobehav Rev 1999, 23:1111-1125.
23. Menne D., Spatz H.C. Colour vision in Drosophila melanogaster. J Comp Physiol 1977, 114:301-312.
24. Nichols C.D. 5-HT2 receptors in Drosophila are expressed in the brain and modulate aspects of circadian behaviors. Dev Neurobiol 2007, 67:752-763.
25. Nichols C.D., Ronesi J., Pratt W., Sanders-Bush E. Hallucinogens and Drosophila: linking serotonin receptor activation to behavior. Neuroscience 2002, 115:979-984.
26. Nichols D.E. Hallucinogens. Pharmacol Ther 2004, 101:131.
27. Nichols D.E., Nichols C.D. Serotonin receptors. Chem Rev 2008, 108:1614-1641.
28. Ogren S.O., Eriksson T.M., Elvander-Tottie E., D'Addario C., Ekström J.C., Svenningsson P., Meister B., Kehr J., Stiedl O. The role of 5-HT(1A) receptors in learning and memory. Behav Brain Res 2008, 195:54-77.
29. Pan Y., Zhou Y., Guo C., Gong H., Gong Z., Liu L. Differential roles of the fan-shaped body and the ellipsoid body in Drosophila visual pattern memory. Learn Mem 2009, 16:289-295.
30. Paul D. Experimental designs for the study of receptor-receptor interactions. Neuromethods: G protein-coupled receptor technology 2011, Springer-Verlag, New York. C. Stevens (Ed.).
31. Platt S.A., Holliday M., Drudge O.W. Discrimination learning of an instrumental response in individual Drosophila melanogaster. J Exp Psychol Anim Behav Process 1980, 6:301-311.
32. Putz G., Heisenberg M. Memories in drosophila heat-box learning. Learn Mem 2002, 9:349-359.
33. Quinn W.G., Harris W.A., Benzer S. Conditioned behavior in Drosophila melanogaster. Proc Natl Acad Sci U S A 1974, 71:708-712.
34. Raymond J.R., Mukhin Y.V., Gelasco A., Turner J., Collinsworth G., Gettys T.W., Grewal J.S., Garnovskaya M.N. Multiplicity of mechanisms of serotonin receptor signal transduction. Pharmacol Ther 2001, 92:179-212.
35. Saudou F., Boschert U., Amlaiky N., Plassat J.L., Hen R. A family of Drosophila serotonin receptors with distinct intracellular signalling properties and expression patterns. EMBO J 1992, 11:7-17.
36. 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, 23:10495-10502.
37. Sitaraman D., Zars M., Laferriere H., Chen Y.C., Sable-Smith A., Kitamoto T., Rottinghaus G.E., Zars T. Serotonin is necessary for place memory in Drosophila. Proc Natl Acad Sci U S A 2008, 105:5579-5584.
38. Strauss R. The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 2002, 12:633-638.
39. Strauss R., Heisenberg M. A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 1993, 13:1852-1861.
40. Tallarida R.J. The interaction index: a measure of drug synergism. Pain 2002, 98:163-168.
41. Tallarida R.J., Porreca F., Cowan A. Statistical analysis of drug-drug and site-site interactions with isobolograms. Life Sci 1989, 45:947-961.
42. Tempel B.L., Bonini N., Dawson D.R., Quinn W.G. Reward learning in normal and mutant Drosophila. Proc Natl Acad Sci U S A 1983, 80:1482-1486.
43. Thomas D.R., Gittins S.A., Collin L.L., Middlemiss D.N., Riley G., Hagan J., Gloger I., Ellis C.E., Forbes I.T., Brown A.M. Functional characterisation of the human cloned 5-HT7 receptor (long form); antagonist profile of SB-258719. Br J Pharmacol 1998, 124:1300-1306.
44. Tully T. Drosophila learning: behavior and biochemistry. Behav Genet 1984, 14:527-557.
45. Tully T., Quinn W.G. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A 1985, 157:263-277.
46. Urban J.D., Clarke W.P., von Zastrow M., Nichols D.E., Kobilka B., Weinstein H., Javitch J.A., Roth B.L., Christopoulos A., Sexton P.M., Miller K.J., Spedding M., Mailman R.B. Functional selectivity and classical concepts of quantitative pharmacology. J Pharmacol Exp Ther 2007, 320:1-13.
47. Waddell S. Dopamine reveals neural circuit mechanisms of fly memory. Trends Neurosci 2010, 33:457-464.
48. Williams G.V., Rao S.G., Goldman-Rakic P.S. The physiological role of 5-HT2A receptors in working memory. J Neurosci 2002, 22:2843-2854.
49. Witz P., Amlaiky N., Plassat J.L., Maroteaux L., Borrelli E., Hen R. Cloning and characterization of a Drosophila serotonin receptor that activates adenylate cyclase. Proc Natl Acad Sci U S A 1990, 87:8940-8944.
50. Wu C.L., Xia S., Fu T.F., Wang H., Chen Y.H., Leong D., Chiang A.S., Tully T. Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body. Nat Neurosci 2007, 10:1578-1586.
51. Xia S., Miyashita T., Fu T.F., Lin W.Y., Wu C.L., Pyzocha L., Lin I.R., Saitoe M., Tully T., Chiang A.S. NMDA receptors mediate olfactory learning and memory in Drosophila. Curr Biol 2005, 15:603-615.
52. Yuan Q., Joiner W.J., Sehgal A. A sleep-promoting role for the Drosophila serotonin receptor 1A. Curr Biol 2006, 16:1051-1062.
53. Yuan Q., Lin F., Zheng X., Sehgal A. Serotonin modulates circadian entrainment in Drosophila. Neuron 2005, 47:115-127.