Tissue-specific expression of a type I adenylyl cyclase rescues the rutabaga mutant memory defect: In search of the engram

Learning and Memory

Volumn 7, Issue 1, 2000, Pages 18-31

  Zars, Troy ^a   Wolf, Reinhard ^a   Davis, Ron ^b   Heisenberg, Martin ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; LEARNING; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPATIAL MEMORY; TISSUE SPECIFICITY;

ADENYLATE CYCLASE; ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM; CONDITIONING, OPERANT; CROSSES, GENETIC; DNA, COMPLEMENTARY; DROSOPHILA; ENHANCER ELEMENTS (GENETICS); FEMALE; FUNGAL PROTEINS; GANGLIA, INVERTEBRATE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MALE; MEMORY; MUTAGENESIS; ORGAN SPECIFICITY; PHENOTYPE; SACCHAROMYCES CEREVISIAE PROTEINS; SPATIAL BEHAVIOR; TEMPERATURE; TRANSCRIPTION FACTORS;

EID: 0033981741     PISSN: 10720502     EISSN: None     Source Type: Journal    
DOI: 10.1101/lm.7.1.18     Document Type: Article

References (53)

1. Aceves-Pina, E.O., R. Booker, J.S. Duerr, M.S. Livingstone, W.G. Quinn, R.F. Smith, P.P. Sziber, B.L. Tempel, and T.P. Tully. 1983. Learning and memory in Drosophila, studied with mutants. Cold Spring Harb. Symp. Quant. Biol. 48: 831-840.
2. Altner, H. and R. Loftus. 1985. Ultrastructure and function of insect thermo-and hygroreceptors. Ann. Rev. Entomol. 30: 273-295.
3. Armstrong, J.D., J.S. de Belle, Z. Wang, and K. Kaiser. 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. Balling, A., G.M. Technau, and M. Heisenberg. 1987. Are the structural changes in adul: Drosophila mushroom bodies memory traces? Studies on biochemical learning mutants. J. Neurogenet. 4: 65-73.
5. Barth, M., H.V.B. Hirsch, I.A. Meinertzhagen, and M. Heisenberg. 1997. Experience-dependent developmental plasticity in the optic lobe of Drosophila melanogaster. J. Neurosci. 17: 1493-1504.
6. Brand, A.H. and N. Perrimon. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
7. Brunelli, M., V. Castellucci, and E.R. Kandel. 1976. Synaptic facilitation and behavioral sensitization in Aplysia: Possible role of serotonin and cyclic AMP. Science 194: 1178-1181.
8. Connolly, J.B., I.J. Roberts, J.D. Armstrong, K. Kaiser, M. Forte, T. Tully, and C.J. O'Kane. 1996. Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274: 2104-2107.
9. Corfas, G. and Y. Dudai. 1990. Adaptation and fatigue of a mechanosensory neuron in wild-type Drosophila and in memory mutants. J. Neurosci. 10: 491-499.
10. _. 1991. Morphology of a sensory neuron in Drosophila is abnormal in memory mutants and changes during aging. Proc. Natl. Acad. Sci. 88: 7252-7256.
11. Crittenden, J.R., E.M.C. Skoulakis, K.-A. Han, D. Kalderon, and R.L. Davis. 1998. Tripartite mushroom body architecture revealed by antigenic markers. Learn. & Mem. 5: 38-51.
12. Davis, R.L. 1996. Physiology and biochemistry of Drosophila learning mutants. Physiol. Rev. 76: 299-317.
13. de Belle, J.S. and M. Heisenberg. 1994. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263: 692-695.
14. Duerr, J.S. and W.G. Quinn. 1982. Three Drosophila mutations that block associative learning also affect habituation and sensitization. Proc. Natl. Acad. Sci. 79: 3646-3650.
15. Engel, J.E. and C.F. Wu. 1996. Altered habituation of an identified escape circuit in Drosophila memory mutants. J. Neurosci. 16: 3486-3499.
16. Folkers, E. 1982. Visual learning and memory of Drosophila melanogaster wild-type C-S and the mutants dunce, amnesiac, turnip, and rutabaga. J. Insect Physiol. 28: 535-539.
17. Gailey, D.A., F.R. Jackson, and R.W. Siegel. 1984. Conditioning mutations in Drosophila melanogaster affect an experience-dependent behavioral modification in courting males. Genetics 106: 613-623.
18. Guo, H.-F., F. Hannan, A. Bernards, and Y. Zhong. 1997. Requirement of Drosophila NF1 for activation of adenylyl cyclase by PACAP38-like neuropeptides. Science 276: 795-798.
19. Hammer, M. and R. Menzel. 1995. Learning and memory in the honeybee. J. Neurosci. 15: 1617-1630.
20. Han, P.L., L.R. Levin, R.R. Reed, and R.L. Davis. 1992. Preferntial expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron 9: 619-627.
21. Hanesch, U., K.-F. Fischbach, and M. Heisenberg. 1989. Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res. 257: 343-366.
22. Heisenberg, M. 1998. What do the mushroom bodies do for the insect brain? An introduction. Learn. & Mem. 5: 1-10.
23. Heisenberg, M. and K. Boehl. 1979. Isolation of anatomical brain mutants of Drosophila melanogaster by histological means. Z. Naturforsch. C 34: 143-147.
24. Heisenberg, M. and R. Wolf. 1984. Vision in Drosophila; Genetics of microbehavior. In Studies of brain function (ed. V. Braitenberg, H.B. Barlow, T.H. Bullock, E. Florey, O.-J. Gruesser, A. Peters), Vol. 12. Springer-Verlag, Berlin, Germany.
25. Heisenberg, M., A. Borst, S. Wagner, and D. Byers. 1985. Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenet. 2: 1-30.
26. GAL4-tau as a tool for studying the anatomy and development of the Drosophila central nervous system. Cell Tissue Res. 290: 1-10.
27. Ito, K., K. Suzuki, P. Estes, M. Ramaswami, D. Yamamoto, and N.J. Strausfeld. 1998. The organization of extinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn. & Mem. 5: 52-77.
28. Joiner, M.-I.A. and L.C. Griffith. 1999. Mapping of the anatomical circuit of CaM kinase-dependent courtship conditioning in Drosophila. Learn. & Mem. 6: 177-192.
29. Klein, M. and E.R. Kandel. 1980. Mechanism of calcium current modulation underlying presynaptic facilitation and behavioral sensitization in Aplysia. Proc. Natl. Acad. Sci. 77: 6912-6916.
30. Lechner, H.A. and J.H. Byrne. 1998. New perspectives on classical conditioning: A synthesis of Hebbian and non-Hebbian mechanisms. Neuron 20: 355-358.
31. 2+/ Calmodulin-responsive adenylyl cyclase. Cell 68: 479-489.
32. Luo, L., Y.J. Liao, L.Y. Jan, and Y.N. Jan. 1994. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes & Dev. 8: 1787-1802.
33. Milner, B., L.R. Squire, and E.R. Kandel. 1998. Cognitive neuroscience and the study of memory. Neuron 20: 445-468.
34. O'Dell, K.M., J.D. Armstrong, M.Y. Yang, and K. Kaiser. 1995. Functional dissection of the Drosophila mushroom bodies by selective feminization of genetically defined subcompartments. Neuron 15: 55-61.
35. Power, M.E. 1948. The thoracico-abdominal nervous system of an adult insect, Drosophila melanogaster. J. Comp. Neurol. 88: 347-409.
36. Rees, C.T. and H.C. Spatz. 1989. Habituation of the landing response of Drosophila wild-type and mutants defective in olfactory learning. J. Neurogenet. 5: 105-118.
37. Sachs, L. 1992. Angewandte Statistik. Springer-Verlag, Berlin, Germany.
38. Sayeed, O. and S. Benzer. 1996. Behavioral genetics of thermosensation and hygrosensation in Drosophila. Proc. Natl. Acad. Sci. 93: 6079-6084.
39. Schacher, S., E.R. Kandel, and P. Montarolo. 1993. cAMP and arachidonic acid simulate long-term structural and functional changes produced by neurotransmitters in Aplysia sensory neurons. Neuron 10: 1079-1088.
40. Strausfeld, N.J. 1976. Atlas of an insect brain. Springer-Verlag, Berlin, Germany.
41. Tettamanti, M., J.D. Armstrong, K. Endo, M.Y. Yang, K. Furukubo-Tokunaga, K. Kaiser, and H. Reichert. 1997. Early development of the Drosophila mushroom bodies, brain centres for associative learning and memory. Dev. Genes Evol. 207: 242-252.
42. Tsien, J.Z., P.T. Huerta, and S. Tonegawa. 1996. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87: 1327-1338.
43. Wehner, R. 1992. Arthropods. In Animal homing (ed. F. Papi), pp. 45-144. Chapman and Hall, London, UK.
44. _. 1996. Middle-scale navigation: The insect case. J. Exp. Biol. 199: 125-127.
45. Wolf, R., T. Wittig, L. Liu, G. Wustmann, D. Eyding, and M. Heisenberg. 1998. Drosophila mushroom bodies are dispensible for visual, tactile, and motor learning. Learn. & Mem. 5: 166-178.
46. Wu, Z.L., S.A. Thomas, E.C. Villacres, Z. Xia, M.L. Simmons, C. Chavkin, R.D. Palmiter, and D.R. Storm. 1995. Altered behavior and long-term potentiation in type I adenylyl cyclase mutant mice. Proc. Natl. Acad. Sci. 92: 220-224.
47. Wustmann, G. and M. Heisenberg. 1997. Behavioral manipulation of retrieval in a spatial memory task for Drosophila melanogaster. Learn. & Mem. 4: 328-336.
48. Wustmann, G., K. Rein, R. Wolf, and M. Heisenberg. 1996. A new paradigm for operant conditioning of Drosophila melanogaster. J. Comp. Physiol. [A] 179: 429-436.
49. Yang, M.Y., J.D. Armstrong, I. Vilinsky, N.J. Strausfeld, and K. Kaiser. 1995. Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 15: 45-54.
50. Yao, K.M. and K. White. 1994. Neural specificity of elav expression: Defining a Drosophila promoter for directing expression to the nervous system. J. Neurochem. 63: 41-51.
51. Zhong, Y. 1995. Mediation of PACAP-like neuropeptide transmission by coactivation of Ras/Raf and cAMP signal transduction pathways in Drosophila. Nature 375: 588-592.
52. Zhong, Y. and L.A. Pena. 1995. A novel synaptic transmission mediated by a PACAP-like neuropeptide in Drosophila. Neuron 14: 527-536.
53. Zhong, Y. and C.F. Wu. 1991. Altered synaptic plasticity in Drosophila memory mutants with a defective cyclic AMP cascade. Science 251: 198-201.