Drosophila: genetics meets behaviour

Nature Reviews Genetics

Volumn 2, Issue 11, 2001, Pages 879-890

  Sokolowski, Marla B ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA MELANOGASTER; MELANOGASTER;

ANIMAL; ANIMAL BEHAVIOR; CIRCADIAN RHYTHM; DROSOPHILA; DROSOPHILA MELANOGASTER; GENETICS; LEARNING; MEMORY; MOTOR ACTIVITY; PHENOTYPE; PHYSIOLOGY; REVIEW; SEXUAL BEHAVIOR;

ANIMAL; BEHAVIOR, ANIMAL; CIRCADIAN RHYTHM; DROSOPHILA; DROSOPHILA MELANOGASTER; LEARNING; MEMORY; MOTOR ACTIVITY; PHENOTYPE; SEX BEHAVIOR, ANIMAL; SUPPORT, NON-U.S. GOV'T;

EID: 0035515462     PISSN: 14710056     EISSN: None     Source Type: Journal    
DOI: 10.1038/35098592     Document Type: Review

References (121)

1. Nusslein-Volhard, C., Frohnhofer, H. G. & Lehman, R. Determination of anteroposterior polarity in Drosophila. Science 238, 1675-1681 (1987).
2. Adams, M. D. et al. The genome sequence of Drosophila melanogaster. Science 287, 2185-2195 (2000).
3. Greenspan, R. J. & Ferveur, J.-F. Courtship in Drosophila. Annu. Rev. Genet. 34, 205-232 (2000).
4. Yamamoto, D., Jallon, J. M. & Komatsu, A. Genetic dissection of sexual behavior in Drosophila melanogaster. Annu. Rev. Entomol. 42, 551-585 (1997).
5. Hendricks, J. C. et al. Rest in Drosophila is a sleep-like state. Neuron 25, 129-138 (2000).
6. Shaw, P. J., Cirelli, C., Greenspan, R. J. & Tononi, G. Correlates of sleep and waking in Drosophila melanogaster. Science 287, 1834-1837 (2000). References 5 and 6 indicate that Drosophila show many of the characteristics of the mammalian states of sleep and waking, allowing the fly to be used as a model for the genetic analysis of activity-rest cycles.
7. Williams, J. A. & Seghal, A. Molecular components of the circadian system in Drosophila. Annu. Rev. Physiol. 63, 729-755 (2001).
8. Sokolowski, M. B. & Riedl, C. in Molecular-Genetic Techniques for Brain and Behaviour (eds Gerlai, R. & Crusio, W.) 517-532 (Elsevier, Amsterdam, 1999).
9. Dubnau, J. & Tully, T. Gene discovery in Drosophila: new insights for learning and memory. Annu. Rev. Neurosci. 21, 407-444 (1998).
10. Waddell, S. & Quinn, W. G. Res, genes, and learning. Annu. Rev. Neurosci. 24, 1283-1309 (2001).
11. Jacobs, M. E. Influence of β-alanine on mating and territorialism in Drosophila melanogaster. Behav. Genet. 8, 487-502 (1978).
12. Hemmat, M. & Eggleston, P. Competitive interactions in Drosophila melanogaster: recurrent selection for aggression and response. Heredity 60, 129-137 (1988).
13. Hoffmann, A. A. Geographic variation in the territorial success of Drosophila melanogaster males. Behav. Genet. 19, 241-255 (1989).
14. Ruiz-Dubreuil, G., Bumet, B. & Connolly, K. Behavioural correlates of selection for oviposition by Drosophila melanogaster females in a patchy environment. Heredity 73, 103-110 (1994).
15. Cheng, Y. et al. Drosophila fasciclinll is required for the formation of odor memories and for normal sensitivity to alcohol. Cell 105, 757-776 (2001).
16. Moore, M. S. et al. Ethanol intoxication in Drosophila: genetic and pharmacological evidence for regulation by the CAMP signaling pathway. Cell 93, 997-1007 (1998).
17. Scholz, H., Ramond, J., Singh, C. M. & Heberlein, U. Functional ethanol tolerance in Drosophila. Neuron 28, 261-271 (2000).
18. Park, S. K., Sedore, S. A., Cronmiller, C. & Hirsh, J. Type II cAMP-dependent protein kinase-deficient Drosophila are viable but show developmental, circadian, and drug response phenotypes. J. Biol. Chem. 275, 20583-20596 (2000).
19. Andretic, R., Chaney, S. & Hirsh, J. Requirement of circadian genes for cocaine sensitization in Drosophila. Science 285, 1066-1068 (1999). References 15-19 show that many of the same genes are involved In many behavioural phenotypes, such as In learning and sensitivity to ethanol, or circadian rhythms and cocaine response. These findings support the involvement of overlapping pathways and gene networks in behaviour.
20. Ueno, K. et al. Trehalose sensitivity in Drosophila correlates with mutations in and expression of the gustatory receptor gene Gr5a. Curr. Biol. 11, 1451-1455 (2001).
21. de Bruyne, M., Foster, K. & Carlson, J. R. Odor coding in the Drosophila antenna. Neuron 30, 537-552 (2001).
22. Clyne, P. J. et al. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22, 327-338 (1999).
23. Vosshall, L. B., Amrein, H., Morozov, P. S., Rzhetsky, A. & Axel, R. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96, 725-736 (1999).
24. Clyne, P. J., Warr, C. G. & Carlson, J. R. Candidate taste receptors in Drosophila, Science 287, 1830-1834 (2000).
25. Scott, K. et al. A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104, 661-673 (2001). References 21-25 show how the computational analysis of fly genome sequence data allowed the discovery and analysis of taste and olfactory receptor families. These receptors had previously remained elusive.
26. Kernan, M., Cowan, D. & Zuker, C. Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron 12, 1195-1206 (1994).
27. Eberl, D. F., Hardy, R. W. & Kernan, M. J. Genetically similar transduction mechanisms for touch and hearing in Drosophila. J. Neurosci. 20, 5931-5988 (2000).
28. Pflugfelder, G. O. Genetic lesions in Drosophila behavioural mutants. Behav. Brain Res. 95, 3-15 (1998).
29. Eberl, D. F., Duyk, G. M. & Perrimon, N. A genetic screen for mutations that disrupt an auditory response in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 94, 14837-14842 (1997).
30. Sokolowski, M. B. Genes for normal behavioral variation: recent clues from flies and worms. Neuron 21, 1-4 (1998).
31. Sawyer, L. A. et al. Natural variation in the Drosophila clock gene and temperature compensation. Science 278, 2117-2120 (1997).
32. Mackay, T. F. C. Quantitative trait loci in Drosophila. Nature Rev. Genet. 2, 11-20 (2001). This review provides a road map for quantitative trait loci analysis, which can be applied to Drosophila behavioural traits.
33. Sokolowski, M. B. Foraging strategies of Drosophila melanogaster, a chromosomal analysis. Behav. Genet. 10, 291-302 (1980). Discovery of the rover-sitter behavioural polymorphism.
34. Sokolowski, M. B., Pereira, H. S. & Hughes, K. Evolution of foraging behavior in Drosophila by density dependent selection. Proc. Natl Acad Sci. USA 94, 7373-7377 (1997). A good example of experimental evolution in the laboratory, In which larvae with rover or sitter alleles were selected for depending on the degree of crowding.
35. de Belle, J. S. & Sokolowski, M. B. Heredity of rover/sitter: alternative foraging strategies of Drosophila melanogaster. Heredity 59, 73-83 (1987).
36. de Belle, J. S., Hilliker, A. J. & Sokolowski, M. B. Genetic localization of foraging (for): a major gene for larval behaviour in Drosophila melanogaster. Genetics 123, 157-164 (1989). This reference reports the genetic localization of the rover-sitter trait by lethal tagging.
37. Graf, S. A. & Sokolowski, M. B. The rover/sitter Drosophila foraging polymorphism as a function of larval development, food patch quality and starvation. J. Insect Behav. 2, 301-313 (1989).
38. Wahlsten, D. & Gottlieb, G. in Intelligence, Heredity, and Environment (eds Sternberg, R. J. & Grigorenko, E. L.) 163-192 (Cambridge Univ. Press, New York, 1997).
39. Wahlsten, D. in Theoretical Advances in Behavioral Genetics (eds Royce, J. R. & Mos, L) 426-481 (Sijthoff & Nordhoff, Germantown, Maryland, 1979).
40. de Belle, J. S., Sokolowski, M. B. & Hilliker, A. J. Genetic analysis of the foraging microregion of Drosophila melanogaster. Genome 36, 94-101 (1993).
41. Osborne, K. A. et al. Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277, 834-836 (1997). Cloning of the rover-sitter trait; the first example of the molecular Identification of a naturally occurring behavioural variation.
42. de Bono, M. & Bargmann, C. I. Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94, 679-689 (1998).
43. Kaga, T., Fujimiya, M. & Inui, A. Emerging functions of neuropeptide Y Y(2) receptors in the brain. Peptides 22, 501-506 (2001).
44. Hirsch, J. & Erlenmeyer-Kimling, L. Sign of taxis as a property of the genotype. Science 134, 835-836 (1961). One of the first papers to show that a fly behavioural phenotype can be artificially selected for.
45. Benzer, S. Genetic dissection of behavior. Sci. Am. 229, 24-37 (1973). The ideas behind the single-gene mutant approach to fly behaviour genetics are clearly set out in this article and are as valid today as they were almost 30 years ago.
46. Feany, M. B. & Bender, W. W. A Drosophila model of Parkinson's disease. Nature 404, 394-398 (2000).
47. Konopka, R. J. & Benzer, S. Clock mutants of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 68, 2112-2116 (1971). This paper reported for the first time a gene (the period gene) that is involved in circadian rhythmicity. This discovery enabled the later genetic and molecular analysis of clock function in many organisms.
48. Sehgal, A., Price, J. L., Man, B. & Young, M. W. Loss of circadian behavioral rhythms and per RNA oscillations in the Drosophila mutant timeless. Science 263, 1603-1606 (1994).
49. Vosshall, L. B., Price, J. L., Sehgal, A., Saez, L. & Young, M. W. Block in nuclear localization of period protein by a second clock mutation, timeless. Science 263, 1606-1609 (1994).
50. Myers, M. R. Wager, S. K., Wesley, C. S., Young, M. W. & Sehgal, A. Positional cloning and sequence analysis of the Drosophila clock gene, timeless. Science 270, 805-808 (1995).
51. So, W. V. & Rosbash, M. Post-transcriptional regulation contributes to Drosophila clock gene mRNA cycling. EMBO J. 16, 146-155 (1997).
52. Hardin, P. E., Hall, J. C. & Rosbash, M. Feedback of the Drosophila period gene on circadian cycling of its messenger RNA levels. Nature 343, 536-540 (1990).
53. Sehgal, A. et al. Rhythmic expression of timeless: a basis for promoting circadian cycles in period gene autoregulation. Science 270, 808-810 (1995).
54. Gekakis, N. et al. Isolation of timeless by PER protein interaction: defective interaction between timeless protein and long-period mutant PERL. Science 270, 811-815 (1995).
55. Curtin, K. D., Huang, Z. J. & Rosbash, M. Temporally regulated nuclear entry of the Drosophila period protein contributes to the circadian dock. Neuron 14, 365-372 (1995).
56. Marrus, S. B., Zeng, H. & Rosbash, M. Effect of constant light and circadian entrainment of perS flies: evidence for light-mediated delay of the negative feedback loop in Drosophila. EMBO J. 15, 6877-6886 (1996).
57. Frisch, B., Hardin, P. E., Hamblen, C. M., Rosbash, M. & Hall, J. C. A promoterless period gene mediates behavioral rhythmicity and cyclical per expression in a restricted subset of the Drosophila nervous system. Neuron 12, 555-570 (1994).
58. Ewer, J., Frish, B., Hamblen, C. M., Rosbash, M. & Hall, J. C. Expression of the period clock gene within different cell types in the brain of Drospohila adults and mosaic analysis of these cells' influence on circadian behavioral rhythms. J. Neurosci. 12, 3321-3349 (1992).
59. Renn, S. C. P., Park, J. H., Rosbash, M., Hall, J. C. & Taghert, P. H. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99, 791-802 (1999). The discovery of a neuropeptide that is thought to function in the output of the clock.
60. Toh, K. L. et al. An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science 291, 1040-1043 (2001).
61. Price, J. L. et al. double-time is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell 94, 83-95 (1998).
62. Greenspan, R. J. Understanding the genetic construction of behavior. Sci. Am. 272, 74-79 (1995).
63. Baker, B. S., Taylor, B. J. & Hall, J. C. Are complex behaviors specified by dedicated regulatory genes? Reasoning from Drosophila. Cell 105, 13-24 (2001).
64. Goodwin, S. F. et al. Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics 154, 7225-7245 (2000). Details of the fru splicing pattern were worked out in this paper.
65. Villella. A. et al. Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. Genetics 147, 1107-1130 (1997).
66. Anand, A. et al. Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless. Genetics 158, 1569-1595 (2001).
67. Ryner, L. C. et al. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87, 1079-1089 (1996).
68. Ito, H. et al. Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc. Natl Acad. Sci. USA 93, 9687-9692 (1996). References 67 and 68 show that fru, which was known to affect sexual behaviour, acts in the sex-determination pathway.
69. Lee, G. et al. Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila CNS. J. Neurobiol. 43, 404-426 (2000).
70. Belote, J. M. & Baker, B. S. Sexual behavior: its genetic control during development and adulthood in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 84, 8026-8030 (1987).
71. Arthur, B. I., Hauschteck-Jungen, E., Nothiger, R. & Ward, P. I. A female nervous system is necessary for normal sperm storage in Drosophila melanogaster. a masculinized nervous system is as good as none. Proc. R. Soc. Lond. B 265, 1749-1753 (1998).
72. Ackerman, S. L. & Siegel, R. W. Chemically reinforced conditioned courtship in Drosophila: responses of wild-type and the dunce, amnesiac and don giovanni mutants. J. Neurogenet. 3, 111-123 (1986).
73. Tully, T. & Quinn, W. G. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. A 157, 263-277 (1985).
74. 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, 613-623 (1984).
75. Siegel, R. W. & Hall, J. C. Conditioned responses in courtship behavior of normal and mutant Drosophila. Proc. Natl Acad. Sci. USA 76, 3430-3434 (1979).
76. Griffith, L. C. et al. Inhibition of calcium/calmodulin-dependent protein kinase in Drosophila disrupts behavioral plasticity. Neuron 10, 501-509 (1994).
77. Griffith, L. C., Wang, J., Zhong, Y., Wu, C.-F. & Greenspan, R. J. Calcium/calmodulin dependent protein kinase II and potassium channel subunit eag similarly affect plasticity in Drosophila. Proc. Natl Acad. Sci. USA 91, 10044-10047 (1994).
78. Kane, N. S., Robichon, A., Dickinson, J. A. & Greenspan, R. J. Learning without performance in PKC-delicient Drosophila. Neuron 18, 307-314 (1997).
79. Quinn, W. G., Harris, W. A. & Benzer, S. Conditioned behavior in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 71, 707-712 (1974).
80. Zhong, Y., Budnik, V. & Wu, C. F. Synaptic plasticity in Drosophila memory and hyper-excitable mutants: role of the cAMP cascade. J. Neurosci. 12, 644-651 (1992).
81. Zhong, Y. & Wu, C. F. Altered synaptic plasticity in Drosophila memory mutants with a defective cAMP cascade. Science 251, 198-201 (1991).
82. de Belle, J. S. S. Heisenberg, M. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263, 692-695 (1994). In this study, the mushroom bodies of flies were chemically ablated to show that these structures have a definitive role in olfactory-based shock-avoidance learning.
83. Connolly, J. B. et al. Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274, 2104-2106 (1996).
84. Zars, T., Fischer, M., Schulz, R. & Heisenberg, M. Localization of a short-term memory in Drosophila. Science 288, 672-675 (2000). These authors showed that synaptic plasticity in a small region of the mushroom bodies was sufficient for memory formation. They targeted expression of a rut transgene in a rut-background to regions of the adult brain.
85. Dubnau, J., Grady, L., Kitamoto, T. & Tully, T. Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 411, 476-480 (2001). This paper shows that synaptic transmission between mushroom body neurons is required during memory retrieval, but not during its acquisition or storage.
86. Bartsch, D. et al. Enhancement of memory-related long-term facilitation by ApAF, a novel transcription factor that acts downstream from both CREB1 and CREB2. Cell 103, 595-608 (2000).
87. Sutton, M. A., Masters, S. E., Bagnall, M. W. & Carew, T. J. Molecular mechanisms underlying a unique intermediate phase of memory in aplysia. Neuron 31, 143-154 (2001).
88. Chain, D. G., Schwartz, J. H. & Hegde, A. N. Ubiquitin-mediated proteolysis in learning and memory. Mol. Neurobol. 201, 25-42 (1999).
89. Skoulakis, E. M. C., Kalderon, D. & Davis, R. L. Preferential expression in mushroom bodies of the catalytic subunit of protein kinase A and its role in learning and memory. Neuron 11, 197-208 (1993).
90. Li, W., Tully, T. & Kalderon, D. Effects of a conditional Drosophila PKA mutant on olfactory learning and memory. Learn. Mem. 2, 320-333 (1976).
91. Quinn, W. G., Sziber, P. P. & Booker, R. The Drosophila memory mutant amnesiac. Nature 277, 212-214 (1979).
92. Feany, M. B. & Quinn, W. G. A neuropeptide gene defined by the Drosophila memory mutant amnesiac. Science 268, 869-873 (1995).
93. 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, 805-813 (2000).
94. Rosay, P., Armstrong, J. D., Wang, Z. & Kaiser, K. Synchronized neural activity in the Drosophila memory centers and its modulation by amnesiac. Neuron 30, 759-770 (2001). References 91-94 present the Identification, cloning and spatial requirements of the putative neuropetide amnesiac and its role in memory.
95. Yin, J. C. P. et al. Induction of a dominant-negative CREB transgene blocks long-term memory in Drosophila. Cell 79, 49-58 (1994).
96. Yin, J. C. P., Vecchio, M. D., Zhou, H. & Tully, T. CREB as a memory modulator: induced expression of a dCREB2 isoform enhances long-term memory in Drosophila. Cell 81, 107-115 (1995). References 95 and 96 define a role for CREB In long-term memory. The dominant-negative CREB transgene had opposing effects on long-term memory to that of the CREB overexpressing transgene.
97. Gass, P. et al. Deficits in memory tasks of mice with CREB mutations depend on gene dosage. Learn. Mem. 5, 274-288 (1998).
98. Cherry, J. A. & Davis, R. L. Cyclic AMP phosphodiesterases are localized in regions of the mouse brain associated with reinforcement, movement, and affect. J. Comp. Neurol. 407, 287-301 (1999).
99. Hall, J. C. in Flexibility and Constraint in Behavioral Systems (eds Greenspan, R. J. & Kyriacou, C. P.) 15-27 (Wiley, New York, 1994).
100. Heisenberg, M. Genetic approach to neuroethology. Bioessays 19, 1065-1073 (1997).
101. Schutt, C. & Nothiger, R. Structure, function and evolution of sex-determining systems in dipteran insects. Development 127, 667-677 (2000).
102. Gerlai, R. Gene-targeting studies of mammalian behavior is it the mutation or the background genotype? Trends Neurosci. 19, 177-181 (1996).
103. Greenspan, R. J. The flexible genome. Nature Rev. Genet. 2, 383-387 (2001).
104. Yang, P., Shaver, S. A., Hilliker, A. J. & Sokolowski, M. B. Abnormal turning behavior in Drosophila larvae: identification and molecular analysis of scribbler (sbb). Genetics 155, 1161-1174 (2000).
105. Boynton, S. & Tully, T. latheo, a new gene involved in associative learning and memory in Drosophila melanogaster identified from P element mutagenesis. Genetics 131, 655-672 (1992).
106. Greenspan, R. J. A kinder, gentler genetic analysis of behavior: dissection gives way to modulation. Curr. Opin. Neurobiol. 7, 805-811 (1997).
107. Yao, W. D. & Wu, C. F. Distinct roles of CaMKII and PKA in regulation of firing patterns and K(+) currents in Drosophila neurons. J. Neurophysiol. 85, 1384-1394 (2001).
108. Renger, J. J., Yao, W.-D., Sokolowski, M. B. & Wu, C.-F. Neuronal polymorphism among natural alleles of a cGMP-dependent kinase gene, foraging in Drosophila. J. Neurosci. 19, RC28 1-8 (1999).
109. Engel, J. E., Xian-Jin, X. J., Sokolowski, J. B. & Wu, C.-F. A cGMP dependent protein kinase gene, foraging, modifies habituation of the giant fiber escape response in Drosophila. Learn. Mem. 7, 341-352 (2000).
110. Trimarchi, J. R., Jin, P. & Murphey, R. K. Controlling the motor neuron. Int. Rev. Neurobiol. 43, 241-264 (1999).
111. Brand, A. H. & Perrimons, N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415 (1993).
112. Sweeney, S. T., Broadie, K., Keane, J., Niemann, H. & O'Kane, C. J. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14, 341-351 (1995).
113. Baines, R. A., Uhler, J. P., Thompson, A., Sweeney, S. T. & Bate, M. Alterered electrical properties in Drosophila neurons developing without synaptic transmission. J. Neurosci. 21, 1523-1531 (2001).
114. Cattaert, D. & Birman, S. Blockade of the central generator of locomotor mythm by noncompetitive NMDA receptor antagonists in Drosophila larvae. J. Neurobiol. 48, 58-73 (2001).
115. Wang, Y. et al. Genetic manipulation of the odor-evoked distributed neural activity in the Drosophila mushroom body. Neuron 29, 267-276 (2001).
116. Sokolowski, M. B. in Techniques for the Genetic Analysis of Brain and Behavior (eds Goldowitz, D., Wahlsten D. & Wimer, R. E.) 497 (Elsevier, Amsterdam, 1992).
117. Sokolowski, M. B. & Wahlsten, D. in Methods in Genomic Neuroscience (ed. Moldin, S. O.) 3-27 (CRC Press, New York, 2001).
118. Kaneto, M., Hamblen, M. J. & Hall, J. C. Involvement of the period gene in developmental time-memory: effect of the perShort mutation on phase shifts induced by light pulses delivered to Drosophila larvae. J. Biol. Rhythms 15, 13-30 (2000).
119. de Belle, J. S. & Heisenberg, M. Expression of Drosophila mushroom body mutations in alternative genetic backgrounds: a case study of the mushroom body miniature gene (mbm). Proc. Natl Acad. Sci. USA 93, 9875-9880 (1996). This is the only paper to have systematically tested for genetic background effects on a behaviour, in this case learning.
120. Davis, R. L. Mushroom bodies. Ca(2+) oscillations, and the memory gene amnesiac. Neuron 30, 653-656 (2001).
121. Yamamoto, D. & Nakano, Y. Sexual behaviour mutants revisited: molecular and cellular basis of Drosophila mating. Cell Mol. Life Sci. 56, 634-646 (1999).