Genetic dissociation of acquisition and memory strength in the heat-box spatial learning paradigm in Drosophila

Learning and Memory

Volumn 13, Issue 1, 2006, Pages 72-83

  Diegelmann, Soeren ^a   Zars, Melissa ^a   Zars, Troy ^a  

^a UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DROSOPHILA; GENETIC ASSOCIATION; INSTRUMENTAL CONDITIONING; LEARNING; MEMORY; NONHUMAN; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; RUTABAGA; SMELLING; TEMPERATURE; WILD TYPE;

ADENYLATE CYCLASE; ANIMALS; ASSOCIATION LEARNING; ATP-BINDING CASSETTE TRANSPORTERS; CONDITIONING, OPERANT; DROSOPHILA; DROSOPHILA PROTEINS; EYE PROTEINS; FEMALE; MALE; MEMORY; MUTATION; REINFORCEMENT (PSYCHOLOGY); SPATIAL BEHAVIOR; TEMPERATURE;

EID: 32044439132     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.45506     Document Type: Article

References (77)

1. Annilo, T., Tammur, J., Hutchinson, A., Rzhetsky, A., Dean, M., and Allikmets, R. 2001. Human and mouse orthologs of a new ATP-binding cassette gene, ABCG4. Cytogenet. Cell Genet. 94: 196-201.
2. Antonov, I., Antonova, I., Kandel, E.R., and Hawkins, R.D. 2003. Activity-dependent presynaptic facilitation and hebbian LTP are both required and interact during classical conditioning in Aplysia. Neuron 37: 135-147.
3. Bingham, P.M. and Chapman, C.H. 1986. Evidence that white-blood is a novel type of temperature-sensitive mutation resulting from temperature- dependent effects of a transposon insertion on formation of white transcripts. EMBO J. 5: 3343-3351.
4. Bingham, P.M. and Judd, B.H. 1981. A copy of copia transposable element is very tightly linked to the w[a] allele at the white locus of D. melanogaster. Cell 25: 705-711.
5. Birchler, J.A. and Hiebert, J.C. 1989. Interaction of the Enhancer of white-apricot with transposable element alleles at the white locus in Drosophila melanogaster. Genetics 122: 129-138.
6. Bitterman, M.E., Menzel, R., Fietz, A., and Schaefer, S. 1983. Classical conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Psychol. 97: 107-119.
7. Brembs, B. 2000. An analysis of associative learning in Drosophila at the flight simulator. In Department of Genetics and Neurobiology, pp. 40. University of Wuerzburg, Wuerzburg, Germany.
8. Campbell, J.L. and Nash, H.A. 2001. Volatile general anesthetics reveal a neurobiological role for the white and brown genes of Drosophila melanogaster. J. Neurobiol. 49: 339-349.
9. Chen, H., Rossier, C., Lalioti, M.D., Lynn, A., Chakravarti, A., Perrin, G., and Antonarakis, S.E. 1996. Cloning of the cDNA for a human homologue of the Drosophila white gene and mapping to chromosome 21q22.3. Am. J. Hum. Genet. 59: 66-75.
10. Croop, J.M., Tiller, G.E., Fletcher, J.A., Lux, M.L., Raab, E., Goldenson, D., Son, D., Arciniegas, S., and Wu, R.L. 1997. Isolation and characterization of a mammalian homolog of the Drosophila white gene. Gene 185: 77-85.
11. Dean, M., Rzhetsky, A., and Allikmets, R. 2001. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 11: 1156-1166.
12. de Belle, J.S. and Heisenberg, M. 1994. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263: 692-695.
13. Detera-Wadleigh, S.D., Badner, J.A., Goldin, L.R., Berrettini, W.H., Sanders, A.R., Rollins, D.Y., Turner, G., Moses, T., Haerian, H., Muniec, D., et al. 1996. Affected-sib-pair analyses reveal support of prior evidence for a susceptibility locus for bipolar disorder, on 21q. Am. J. Hum. Genet. 58: 1279-1285.
14. Detera-Wadleigh, S.D., Badner, J.A., Yoshikawa, T., Sanders, A.R., Goldin, L.R., Turner, G., Rollins, D.Y., Moses, T., Guroff, J.J., Kazuba, D., et al. 1997. Initial genome scan of the NIMH genetics initiative bipolar pedigrees: Chromosomes 4, 7, 9, 18, 19, 20, and 21q. Am. J. Med. Genet. 74: 254-262.
15. Dill, M., Wolf, R., and Heisenberg, M. 1995. Behavioral analysis of Drosophila landmark learning in the flight simulator. Learn. Mem. 2: 152-160.
16. Dragoi, V. and Staddon, J.E. 1999. The dynamics of operant conditioning. Psychol. Rev. 106: 20-61.
17. Dreesen, T.D., Johnson, D.H., and Henikoff, S. 1988. The brown protein of Drosophila melanogaster is similar to the white protein and to components of active transport complexes. Mol. Cell. Biol. 8: 5206-5215.
18. Dura, J.M., Preat, T., and Tully, T. 1993. Identification of linotte, a new gene affecting learning and memory in Drosophila melanogaster. J. Neurogenet. 9: 1-14.
19. bl). Genetics 30: 62-70.
20. Guo, A., Liu, L., Xia, S.-z., Feng, C.-h., Wolf, R., and Heisenberg, M. 1996. Conditioned visual flight orientation in Drosophila: Dependence on age, practice, and diet. Learn. Mem. 3: 49-59.
21. Hammer, M. 1993. An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366: 59-63.
22. Hammer, M. and Menzel, R. 1998. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn. Mem. 5: 146-156.
23. Han, P.L., Levin, L.R., Reed, R.R., and Davis, R.L. 1992. Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron 9: 619-627.
24. Hazelrigg, T., Levis, R., and Rubin, G.M. 1984. Transformation of white locus DNA in Drosophila: Dosage compensation, zeste interaction, and position effects. Cell 36: 469-481.
25. Heimbeck, G., Bugnon, V., Gendre, N., Keller, A., and Stocker, R.F. 2001. A central neural circuit for experience-independent olfactory and courtship behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. 98: 15336-15341.
26. Heisenberg, M. and Wolf, R. 1984. Vision in Drosophila: Genetics of microbehavior. Springer-Verlag, Berlin.
27. Herrnstein, R.J. 1997. The matching law: Papers in psychology and economics. Harvard University Press, Cambridge, MA.
28. Hing, A.L. and Carlson, J.R. 1996. Male-male courtship behavior induced by ectopic expression of the Drosophila white gene: Role of sensory function and age. J. Neurobiol. 30: 454-464.
29. Hollerman, J.R. and Schultz, W. 1998. Dopamine neurons report an error in the temporal prediction of reward during learning. Nat. Neurosci. 1: 304-309.
30. Ikemoto, S. and Panksepp, J. 1996. Dissociations between appetitive and consummatory responses by pharmacological manipulations of reward-relevant brain regions. Behav. Neurosci. 110: 331-345.
31. Isabel, G., Pascual, A., and Preat, T. 2004. Exclusive consolidated memory phases in Drosophila. Science 304: 1024-1027.
32. Kandel, E.R. 2001. The molecular biology of memory storage: A dialogue between genes and synapses. Science 294: 1030-1038.
33. Killeen, P.R. 1994. Mathematical principles of reinforcement. Behav. Brain Sci. 17: 105-172.
34. Lechner, H.A. and Byrne, J.H. 1998. New perspectives on classical conditioning: A synthesis of Hebbian and non-Hebbian mechanisms. Neuron 20: 355-358.
35. Levin, L.R., Han, P.L., Hwang, P.M., Feinstein, P.G., Davis, R.L., and Reed, R.R. 1992. The Drosophila learning and memory gene rutabaga encodes a Ca2+/Calmodulin-responsive adenylyl cyclase. Cell 68: 479-489.
36. Loo, S.K. and Bitterman, M.E. 1992. Learning in honeybees (Apis mellifera) as a function of sucrose concentration. J. Comp. Psychol. 106: 29-36.
37. Malleret, G., Haditsch, U., Genoux, D., Jones, M.W., Bliss, T.V., Vanhoose, A.M., Weitlauf, C., Kandel, E.R., Winder, D.G., and Mansuy, I.M. 2001. Inducible and reversible enhancement of learning, memory, and long-term potentiation by genetic inhibition of calcineurin. Cell 104: 675-686.
38. Martin, K.C., Casadio, A., Zhu, H., Yaping, E., Rose, J.C., Chen, M., Bailey, C.H., and Kandel, E.R. 1997. Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: A function for local protein synthesis in memory storage. Cell 91: 927-938.
39. Menzel, R. and Erber, J. 1972. The influence of the quantity of reward on the learning performance in honeybees. Behaviour 41: 27-42.
40. Menzel, R., Heyne, A., Kinzel, C., Gerber, B., and Fiala, A. 1999. Pharmacological dissociation between the reinforcing, sensitizing, and response-releasing functions of reward in honeybee classical conditioning. Behav. Neurosci. 113: 744-754.
41. Montague, P.R., Hyman, S.E., and Cohen, J.D. 2004. Computational roles for dopamine in behavioural control. Nature 431: 760-767.
42. Nakamura, M., Ueno, S., Sano, A., and Tanabe, H. 1999. Polymorphisms of the human homologue of the Drosophila white gene are associated with mood and panic disorders. Mol. Psychiatry 4: 155-162.
43. Nestler, E.J., Barrot, M., DiLeone, R.J., Eisch, A.J., Gold, S.J., and Monteggia, L.M. 2002. Neurobiology of depression. Neuron 34: 13-25.
44. Nilsson, E.E., Asztalos, Z., Lukacsovich, T., Awano, W., Usui-aoki, K., and Yamamoto, D. 2000. Fruitless is in the regulatory pathway by which ectopic mini-white and transformer induce bisexual courtship in Drosophila. J. Neurogenet. 13: 213-232.
45. O'Hare, K., Alley, M.R., Cullingford, T.E., Driver, A., and Sanderson, M.J. 1991. DNA sequence of the Doc retroposon in the white-one mutant of Drosophila melanogaster and of secondary insertions in the phenotypically altered derivatives white-honey and white-eosin. Mol. Gen. Genet. 225: 17-24.
46. Oldfield, S., Lowry, C., Ruddick, J., and Lightman, S. 2002. ABCG4: A novel human white family ABC-transporter expressed in the brain and eye. Biochim. Biophys. Acta 1591: 175-179.
47. Pirotta, V., Hadfield, C., and Pretorius, G.H.J. 1983. Microdissection and cloning of the white locus and the 3B1-3C2 region of the Drosophila X chromosome. EMBO J. 2: 927-934.
48. Putz, G. 2002. Characterization of memories and ignorant (S6KII) mutants in operant conditioning in the heat-box. In Department of Genetics and Neurobiology, pp. 115. Julius Maximillians Universitaet Wuerzburg, Wuerzburg, Germany.
49. Putz, G. and Heisenberg, M. 2002. Memories in Drosophila heat-box learning. Learn. Mem. 9: 349-359.
50. Savary, S., Denizot, F., Luciani, M., Mattei, M., and Chimini, G. 1996. Molecular cloning of a mammalian ABC transporter homologous to Drosophila white gene. Mamm. Genome 7: 673-676.
51. Sayeed, O. and Benzer, S. 1996. Behavioral genetics of thermosensation and hygrosensation in Drosophila. Proc. Natl. Acad. Sci. 93: 6079-6084.
52. Scholz, H., Ramond, J., Singh, C.M., and Heberlein, U. 2000. Functional ethanol tolerance in Drosophila. Neuron 28: 261-271.
53. Schultz, W. 2004. Neural coding of basic reward terms of animal learning theory, game theory, microeconomics and behavioural ecology. Curr. Opin. Neurobiol. 14: 139-147.
54. Schwaerzel, M., Monastirioti, M., Scholz, H., Friggi-Grelin, F., Birman, S., and Heisenberg, M. 2003. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J. Neurosci. 23: 10495-10502.
55. Skinner, B.F. 1950. Are theories of learning necessary? Psychol. Rev. 57: 193-216.
56. Smith, R.F. and Konopka, R.J. 1981. Circadian clock phenotypes of chromosome aberrations with a breakpoint at the per locus. Mol. Gen. Genet. 183: 243-251.
57. Smyth, C., Kalsi, G., Curtis, D., Brynjolfsson, J., O'Neill, J., Rifkin, L., Moloney, E., Murphy, P., Petursson, H., and Gurling, H. 1997. Two-locus admixture linkage analysis of bipolar and unipolar affective disorder supports the presence of susceptibility loci on chromosomes 11p15 and 21q22. Genomics 39: 271-278.
58. Straub, R.E., Lehner, T., Luo, Y., Loth, J.E., Shao, W., Sharpe, L., Alexander, J.R., Das, K., Simon, R., Fieve, R.R., et al. 1994. A possible vulnerability locus for bipolar affective disorder on chromosome 21q22.3. Nat. Genet. 8: 291-296.
59. Strauss, R. and Heisenberg, M. 1993. A higher control center of locomotor behavior in the Drosophila brain. J. Neurosci. 13: 1852-1861.
60. Tanimoto, H., Heisenberg, M., and Gerber, B. 2004. Experimental psychology: Event timing turns punishment to reward. Nature 430: 983.
61. Tearle, R.G., Belote, J.M., McKeown, M., Baker, B.S., and Howells, A.J. 1989. Cloning and characterization of the scarlet gene of Drosophila melanogaster. Genetics 122: 595-606.
62. Tully, T. and Quinn, W.G. 1985. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. [A] 157: 263-277.
63. Waelti, P., Dickinson, A., and Schultz, W. 2001. Dopamine responses comply with basic assumptions of formal learning theory. Nature 412: 43-48.
64. Wang, H., Pineda, V.V., Chan, G.C., Wong, S.T., Muglia, L.J., and Storm, D.R. 2003. Type 8 adenylyl cyclase is targeted to excitatory synapses and required for mossy fiber long-term potentiation. J. Neurosci. 23: 9710-9718.
65. Wei, F., Qiu, C.S., Kim, S.J., Muglia, L., Maas, J.W., Pineda, V.V., Xu, H.M., Chen, Z.F., Storm, D.R., Muglia, L.J., et al. 2002. Genetic elimination of behavioral sensitization in mice lacking calmodulin-stimulated adenylyl cyclases. Neuron 36: 713-726.
66. Wolf, R. and Heisenberg, M. 1986. Visual orientation in motion-blind flies in an operant behavior. Nature 323: 154-156.
67. _. 1991. Basic organization of operant behavior as revealed in Drosophila flight orientation. J. Comp. Physiol. [A] 169: 699-705.
68. Wolf, R., Voss, A., Hein, S., and Heisenberg, M. 1992. Can a fly ride a bicycle? Phil. Trans. R. Soc. Lond. B 337: 261-269.
69. Wu, Z.L., Thomas, S.A., Villacres, E.C., Xia, Z., Simmons, M.L., Chavkin, C., Palmiter, R.D., and Storm, D.R. 1995. Altered behavior and long-term potentiation in type I adenylyl cyclase mutant mice. Proc. Natl. Acad. Sci. 92: 220-224.
70. Wustmann, G. and Heisenberg, M. 1997. Behavioral manipulation of retrieval in a spatial memory task for Drosophila melanogaster. Learn. Mem. 4: 328-336.
71. Wustmann, G., Rein, K., Wolf, R., and Heisenberg, M. 1996. A new paradigm for operant conditioning of Drosophila melanogaster. J. Comp. Physiol. [A] 179: 429-436.
72. Zachar, Z. and Bingham, P.M. 1982. Regulation of white locus expression: The structure of mutant alleles at the white locus of Drosophila melanogaster. Cell 30: 529-541.
73. Zars, T. 2001. Two thermosensors in Drosophila have different behavioral functions. J. Comp. Physiol. [A] 187: 235-242.
74. Zars, T., Fischer, M., Schulz, R., and Heisenberg, M. 2000a. Localization of a short-term memory in Drosophila. Science 288: 672-675.
75. Zars, T., Wolf, R., Davis, R., and Heisenberg, M. 2000b. Tissue-specific expression of a type I adenylyl cyclase rescues the rutabaga mutant memory defect: In search of the engram. Learn. Mem. 7: 18-31.
76. Zhang, S.D. and Odenwald, W.F. 1995. Misexpression of the white (w) gene triggers male-male courtship in Drosophila. Proc. Natl. Acad. Sci. 92: 5525-5529.
77. Zhang, X., Gainetdinov, R.R., Beaulieu, J.M., Sotnikova, T.D., Burch, L.H., Williams, R.B., Schwartz, D.A., Krishnan, K.R., and Caron, M.G. 2005. Loss-of-function mutation in tryptophan hydroxylase-2 identified in unipolar major depression. Neuron 45: 11-16.