Physiology and biochemistry of Drosophila learning mutants

Physiological Reviews

Volumn 76, Issue 2, 1996, Pages 299-317

  Davis, Ronald L ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; LEARNING; MUTATION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 0029906425     PISSN: 00319333     EISSN: None     Source Type: Journal    
DOI: 10.1152/physrev.1996.76.2.299     Document Type: Review

References (98)

1. 2-/ealmodulin and transmitter. J. Neurosci. 11: 2655-2665, 1091.
2. ACEVES-PINA, E. O., AND W. G. QUINN. Learning in normal and mutant Drosophila larvae. Science Wash. DC 206: 93-96, 1979.
3. ASZTALOS, Z., J. VON WEGERER, G. WUSTMANN, V. DOMBRADI, J. GAUSZ, H.-C. SPATZ, AND P. FRIEDRICH. Protein phosphatase 1-deficient mutant Drosophila is affected in habituation and associative learning. J. Neurosci. 13: 924-930, 1993.
4. BELLEN, H. J., B. K. GREGORY, C. L. OLSSON, AND J. A. KIGER, JR. Two Drosophila learning mutants, dunce and rutabaga, provide evidence of a maternal role for cAMP on embryogenesis. Dev. Biol. 121: 432-444, 1987.
5. BITTERMAN, M. E., R. MENZEL, A. FIETZ, AND S. SCHÅFER. Classical conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Psychol. 97: 107-119, 1983.
6. BOLWIG, G. M., M. DEL VECCHIO, AND T. TULLY. Molecular cloning of linotte in Drosophila: a novel gene that functions in adults during associative learning. Neuron 15: 829-842, 1995.
7. BOOKER, R., AND W. G. QUINN. Conditioning of leg position in normal and mutant Drosophila. Proc. Natl. Acad. Sci. USA 78: 3940-3944, 1981.
8. BOUHOUCHE, A., G. VAYSEE, AND M. CORBIERE. Immunocytochemical and learning studies of Drosophila melanogaster neurological mutant, no-bridge KS49, as an approach to the possible role of the central complex. J. Neurogenet. 9: 105-121, 1993.
9. BOYNTON, S. Behavioral Genetic Studies on Learning and Memory in Drosophila melanogaster (PhD thesis). Waltham, MA: Brandeis University, 1994.
10. BYERS, D., R. L. DAVIS, AND J. A. KIGER, JR. Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster. Nature Lond. 289: 79-81, 1981.
11. CARLSON, J. Olfaction in Drosophila: genetic and molecular analysis. Trends Neurosci. 14: 520-524, 1991.
12. + locus, the structure gene for cAMP phosphodiesterase. Proc. Natl. Acad. Sci. USA 86: 3599-3603, 1986.
13. 2+/calmodulin-dependent protein kinase is highly conserved in Drosophila. Neuron 7: 439-450, 1991.
14. CHOI, K.-W., R. F. SMITH, R. M. BURATOWSKI, AND W. G. QUINN. Deficient protein kinase C activity in turnip, a Drosophila learning mutant. J. Biol. Chem. 266: 15999-16006, 1991.
15. CORFAS, G., AND Y. DUDAI. Habituation and dishabituation of a cleaning reflex in normal and mutant Drosophila. J. Neurosci. 9: 56-62, 1989.
16. COWAN, T. M., AND R. W. SIEGEL. Mutational and pharmacological alterations of neuronal membrane function disrupt conditioning in Drosophila. J. Neurogenet. 1: 333-344, 1984.
17. COWAN, T. M., AND R. W. SIEGEL. Drosophila mutations that alter ionic conduction disrupt acquisition and retention of a conditioned odor avoidance response. J. Neurogenet. 3: 187-201, 1086.
18. DAUWALDER, B., AND R. L. DAVIS. Conditional rescue of the dunce phenotypes with inducible transgenes. J. Neurosci. 15: 3490-3499, 1995.
19. DAVIS, H. P., AND L. R. SQUIRE. Protein synthesis and memory: a review. Psychol. Bull. 96: 518-559, 1984.
20. DAVIS, R. L. Mushroom bodies and Drosophila learning. Neuron 11: 1-14, 1993.
21. DAVIS, R. L., AND L. KAUVAR. Drosophila cyclic nucleotide phosphodiesterases. In: Advances in Cyclic Nucleotide and Protein Phosphorylation Research, edited by S. J. Strada and W. J. Thompson. New York: Raven. 1984, vol. 16, p. 393-402.
22. DAVIS, R. L., AND J. A. KIGER, JR. Dunce mutants of Drosophila melanogaster. mutants defective in the cyclic AMP phosphodiesterase enzyme system. J. Cell Biol. 90: 101-107, 1981.
23. DEBELLE, J. S., AND M. HEISENBERG. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science Wash. DC 263: 692-695, 1994.
24. + channel in Drosophila larval muscle is persistently activated in dunce. Proc. Natl. Acad. Sci. USA 88: 557-560, 1991.
25. +-channel blockers restore synaptic plasticity in the neuromuscular junction of dunce, a Drosophila learning and memory mutant. Proc. R. Soc. Lond. B Biol, Sci. 250: 181-185, 1992.
26. DRAIN, P., E. FOLKERS, AND W. G. QUINN. cAMP-dependent protein kinase and the disruption of learning in transgenic flies. Neuron 6: 71-82, 1991.
27. DUDAI, Y. Mutations affect storage and use of memory differentially in Drosophila. Proc. Natl. Acad. Sci. USA 80: 5445-5448, 1983.
28. DUDAI, Y., Y.-N. JAN, D. BYERS, W. QUINN, AND S. BENZER. Dunce, a mutant of Drosophila deficient in learning. Proc. Natl. Acad. Sci. USA 73: 1684-1688, 1976.
29. DUERR, J. S., AND W. G. QUINN. Three Drosophila mutations that block associative learning also affect habituation and sensitazation. Proc. Natl. Acad. Sci. USA 79: 3646-3650, 1982.
30. DURA, J.-M., T. PREAT, AND T. TULLY. Identification of linotte, a new gene affecting learning and memory in Drosophila melanogaster J. Neurogenet. 9: 1-14, 1993.
31. ERBER, J. Response characteristics and after effects of multimodal neurons in the mushroom body area of the honeybee. Physiol. Entomol. 3: 77-89, 1978.
32. FEANY, M. B., AND W. G. QUINN. A neuropeptide gene defined by the Drosophila memory mutant amnesiac. Science Wash. DC 268: 825-826, 1995.
33. FISCHBACH, K. F. Habituation and sensitization of the landing response of Drosophila melanogaster. Naturwissenschaften 68: 332, 1981.
34. FISCHBACH, K. F., AND M. HEISENBERG. Structural brain mutant of Drosophila metanogaster with reduced cell number in the medulla cortex and with normal optomotor yaw response. Proc. Natl. Acad. Sci. USA 78: 1105-1109, 1981.
35. 1, amnesiac, turnip and rutabaga. J. Insect Physiol. 28: 535-539, 1982.
36. FOLKERS, E., P. F. DRAIN, AND W. G. QUINN. Radish, a Drosophila mutant deficient in consolidated memory. Proc. Natl. Acad. Sci. USA 90: 8123-8127, 1993.
37. FORTE, M., F. QUAN, D. HYDE, AND W. WOLFGANG. Gα proteins in Drosophila: structure and developmental expression. In: GTPases in Biology, edited by B. Dickey and L. Birnbaumer. Heidelberg, Germany: Springer-Verlag, 1993, p. 319-334.
38. FOSTER, J. L., J. J. GUTTMAN, L. M. HALL, AND O. M. ROSEN. Drosophila cAMP-dependent protein kinase. J. Biol. Chem. 259: 13049-13055, 1984.
39. FUNHASHI, S., C. J. BRUCE, AND P. S. GOLDMAN-RAKIC. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J. Neurophysiol. 61: 331-349, 1989.
40. FUSTER, J. M., AND J. P. JERVEY. Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task. J. Neurosci. 2: 361-375, 1982.
41. GAILEY, D A., F. R. JACKSON, AND R. W. SIEGEL. Male courtship in Drosophila: the conditioned response to immature males and its genetic control. Genetics 102: 771-782, 1982.
42. GONZALEZ, G. A., AND M. R. MONTMONY. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59: 675-680, 1989.
43. GRIFFITH, L. C., L. M. VERSELIS, K. M. AITKEN, C. P. KYRIACOU, W. DANHO, AND R. J. GREENSPAN. Inhibition of calcium/calmodulin-dependent protein kinase in Drosophila behavioral plasticity. Neuron 10: 501-509. 1993.
44. GRIFFITH, L. C., J. WANG, Y. ZHONG, C.-F. WU, AND R. J. GREENSPAN. Calcium/calmodulin-dependent protein kinase II and potassium channel subunit Eag similarly affect plasticity in Drosophila. Proc Natl. Acad. Sci USA 91: 10044-10048, 1994.
45. HAN, P.-L., L R. LEVIN, R. R. REED, AND R. L. DAVIS. Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron 9: 619-627, 1992.
46. HEISENBERG, M. Genetic approach to learning and memory (mnemogenetics) in Drosophila melanogaster. In: Fundamentals of Memory Formation: Neuronal Plasticity and Brain Function, edited by H. Rahmann. New York: Gustav Fischer Verlag, 1989, vol. 37, p. 3-45.
47. HEISENBERG, M., A. BORST, S. WAGNER, AND D. BYERS. Drosophila mushroom body mutants are deficient in olfactory learning, J Neurogenet. 2: 1-30, 1985.
48. HEISENBERG, M., M. HEUSIPP, AND C. WANKE. Structural plasticity in the Drosophila brain. J. Neurosci. 15: 1951-1960, 1095.
49. JELLIES, J. A. Associative Olfactory Conditioning in Drosophila melanogaster and Memory Retention Through Metamorphosis (Master thesis). Normal: Illinois State University, 1981.
50. KALDERON, D., AND G. M. RUBIN. Isolation and characterization of Drosophila cAMP-dependent protein kinase genes. Genes Dev. 2 1539-1556, 1988.
51. KAMB, A., J. TSENG-CRANK, AND M. A. TANOUYE. Multiple prod ucts of the Drosophila Shaker gene contribute to potassium channel diversity. Neuron 1: 421-430, 1988.
52. KIGER, J. A., JR. The consequences of nullosomy for a chromosomal region affecting cyclic AMP phosphodicsterase activity in Drosophila. Genetics 85: 623-628, 1977.
53. KRUPINSKI, J., F. COUSSEN, H. A. BAKALYAR, W.-J. TANG, P. G FEINSTEIN, K ORTH, C. SLAUGHTER, R. R. REED, AND A. G GILMAN. Adenylyl cyclase amino acid sequence: possible channel- of transporter-like structure. Science Wash. DC 244: 1558-1564, 1989.
54. KYRIACOU, C. P., AND J. C. HALL. Learning and memory mutations impair acoustic priming of mating behavior in Drosophila. Nature Lond. 308: 62-65, 1984.
55. LANE, M. E., AND D. KALDERON. Genetic investigation of cAMP dependent protein kinase function in Drosophila development Genes Dev. 7. 1229-1243, 1993.
56. LAURENT, G., AND H. DAVIDOWITZ. Encoding of olfactory information with oscillating neural assemblies. Science Wash. DC 265: 1872-1875, 1994
57. LAURENT, G., AND M. NARAGHI. Odorant-induced oscillations in the mushroom bodies of the locust. J. Neurosci. 14: 2993-3004, 1994.
58. 2+/calmodulin-responsive adenylyl cyclase Cell 68: 479-489, 1992.
59. LISMAN, J. E., AND M. A. IDIART. Storage of 7±2 short term memories in oscillatory subcycles. Science Wash. DC 267: 1512-1515, 1995
60. LIVINGSTONE, M. S., P. P. SZIBER, AND W. G. QUINN. Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga a Drosophila learning mutant Cell 37: 205-215, 1984.
61. LIVINGSTONE, M. S., AND B. L. TEMPEL. Genetic dissection of monoamine neurotransmitter synthesis in Drosophila. Nature Lond 303: 67-70, 1983.
62. MANNING, A. Pre-imaginal conditioning in Drosophila. Nature Lond. 216: 338-340, 1967.
63. 2+-dependent proteolytic modifi cation of the cAMP-dependent protein kinase in Drosophila wildtype and dunce memory mutants. J. Neurogenet. 6: 95-114, 1989.
64. NASSEL, D. R., AND K. ELEKES. Aminergic neurons in the brain of blowflies and Drosophila: dopamine- and tyrosine hydroxylaseimmunoreactive neurons and their relationship with putative histaminergic neurons. Cell Tissue Res. 267: 147-167, 1992.
65. NIGHORN, A., M. J. HEALY, AND R. L. DAVIS. The cyclic AMP phosphodiesterase encoded by the Drosophila dunce gene is concentrated in the mushroom body neuropil. Neuron 6: 455-467, 1991.
66. PONGS, O., N. KECSKEMETHY, R. MULLER, I. KRAH-JENTGENS. A. BAUMANN, H. H. KILTZ, I. CANAL, S. LLAMAZARES, AND A FARRUS. Shaker encodes a family of putative potassium channel proteins in the nervous system of Drosophila. EMBO J. 7: 10878-1096, 1988.
67. PREAT, T., E. TAILLEBOURG, AND J.-M. DURA. The Drosophila learning and memory gene linotte encodes a putative receptor tyrosine kinase homologous to the human RYK gene product. FEBS Lett 370: 250-254, 1995.
68. QUAN, F., L. THOMAS, AND M. FORTE. Drosophila stimulatory G protein α subunit activates mammalian adenylyl cyclase but interacts poorly with mammalian receptors: implications for receptor-G protein interaction. Proc. Natl. Acad, Sci. USA 88: 1898-1902, 1991.
69. QUAN, F., W. A. WOLFGANG, AND M. A FORTE. The Drosophila gene coding for the α subunit of a stimulatory G protein is preferentially expressed in the nervous system. Proc. Natl. Acad. Sci. USA 86: 4321-4325, 1989.
70. QUI, Y., C.-N. CHEN, T. MALONE, L. RICHTER, S. K. BECKENDORF, AND R. L. DAVIS. Characterization of the memory gene dunce of Drosophila melanogaster. J. Mol. Biol. 222: 553-565, 1991.
71. QUI, Y., AND R. L. DAVIS. Genetic dissection of the learning/memory gene dunce of Drosophila melanogaster. Genes Dev. 7: 1447-1458, 1993.
72. QUINN, W. G., W. A HARRIS, AND S. BENZER. Conditioned behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 71: 708-712, 1974.
73. QUINN, W. G., P. P. SZIBER, AND R. BOOKER. The Drosophila memory mutant amnesiac. Nature Lond. 277: 212-214, 1979.
74. REES, C. T., AND H.-C. SPATZ. Habituation of the landing response of Drosophila wild-type and mutants defective in olfactory learning. J. Neurogenet. 5: 105-118, 1989.
75. SALZ, H. K., R. L. DAVIS, AND J. A KIGER. Genetic analysis of chromosome 3D4 in Drosophila melanogaster. the dunce and spermamotile genes. Genetics 100: 587-596, 1982.
76. SCHAFER, S., H. ROSENBOOM, AND R. MENZEL. Ionic currents of kenyon cells from the mushroom body of the honeybee. J. Neurosci. 14: 4600-4612, 1994.
77. 2+/calmodulin-dependent protein kinase. Adv. Second Messenger Phosphoprotein Res. 22: 39-112, 1988.
78. SCHWARTZ, J. H., AND S. M. GREENBERG. Molecular mechanisms for memory: second-messenger induced modifications of protein Kinases in nerve cells. Annu. Rev. Neurosci. 10: 459-76, 1987.
79. + channel components from the Shaker locus and differential distribution of splicing variants in Drosophila. Neuron 2: 119-127, 1980.
80. SCHWARZ, T. L., B. L. TEMPEL, D. M. PAPAZIAN, Y.-N. JAN, AND L.-Y. JAN. Multiple potassium components are produced by alternative splicing at the Shaker locus in Drosophila. Nature Lond. 331: 137-142, 1988.
81. SKOULAKIS, E. M., D. KALDERON, AND R. L. DAVIS. Preferential expression in mushroom bodies of the catalytic subunit of protein kinase A and its role in learning and memory. Neuron 11: 1-14, 1993.
82. STRAUSFELD, N. J. Atlas of an Insect Brain. Berlin: Springer-Verlag, 1976.
83. STRAUSS, R., AND M. HEISENBERG. A higher control center of locomotor behavior in the Drosophila brain. J. Neurosci. 13: 1852-1861, 1993.
84. TEJEDOR, F., X. R. ZHU, E. KALTENBACH, A. ACKERMANN, A BAUMANN, I. CANAL, M. HEISENBERG, K F. FISCHBACK, AND O. PONGS. Minibrain: a new protein kinase family involved in postembryonic neurogenesis in Drosophila. Neuron 14: 287-301, 1995.
85. TEMPEL, B. L., N. BONINI, D. R. DAWSON, AND W. G. QUINN. Reward learning in normal and mutant Drosophila. Proc. Natl. Acad. Sci. USA 80: 1482-1486, 1983.
86. TEMPEL, B. L., M. S. LTVINGSTONE, AND W. G. QUINN. Mutations in the dopa decarboxylase gene affect learning in Drosophila. Proc. Natl. Acad. Sci. USA 81: 3577-3581, 1984.
87. TOMPKINS, L., R. W. SIEGEL, D. A. GAILEY, AND J. C. HALL Conditioned courtship in Drosophila and its mediation by association of chemical cues. Behav. Genet. 13: 565-578, 1983.
88. TULLY, T., V. CAMBIAZO, AND L. KRUSE. Memory through metamorphosis in normal and mutant Drosophila. J Neurosci. 14: 68-74, 1994.
89. TULLY, T., S. C. PREAT, S. C. BOYNTON, AND M. DEL VECCHIO. Genetic dissection of consolidated memory in Drosophila. Cell 79: 35-47, 1994.
90. TULLY, T., AND W. G. QUINN. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Camp. Physiol A Sens. Neural. Behav. Physiol. 157: 263-277, 1985.
91. WANG, J., J. J. RENGER, L. C. GRIFFITH, R. J. GREENSPAN, AND C.-F. WU. Concomitant alterations of physiological and developmental plasticity in Drosophila CaM Kinase II-inhibited synapses. Neuron 13: 1-12, 1994.
92. WITTEKIND, W. C., AND H.-C. SPATZ. Habituation of the landing response of Drosophila. In: Modulation of Synaptic Transmission and Plasticity in Nervous Systems, edited by G. Herting and H. C. Spatz. Berlin: Springer-Verlag, 1988, p. 351-368.
93. WOLF, R., AND M. HEISENBERG. Basic organization of operant behavior as revealed in Drosophila flight orientation. J. Comp. Physiol. A Sens. Neural Behav. Physiol. 169: 699-715, 1991.
94. + currents and the cAMP dependent modulation in cultured Drosophila mushroom body neurons identified by lacZ expression. J. Neurosci. 15: 1025-1034, 1995.
95. YIN, J., J. S. WALLACH, M. DELVECCHIO, E. L. WILDER, H. ZHOU, W. G. QUINN, AND T. TULLY. Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79: 49-58, 1994.
96. ZHONG, Y., AND C.-F. WU. Altered synaptic plasticity in Drosophila memory mutants with a defective cyclic AMP cascade. Science Wash. DC 251: 198-201, 1991.
97. + currents in Drosophila muscle by mutations in eag. Science Wash. DC 252: 1562-1564, 1991.
98. ZHONG, Y., AND C.-F. WU. Differential modulation of potassium currents by cAMP and its long-term and short-term effects: dunce and rutabaga mutants of Drosophila. J. Neurogenet. 9: 15-27, 1993.