Drosophila olfactory memory: Single genes to complex neural circuits

Nature Reviews Neuroscience

Volumn 8, Issue 5, 2007, Pages 341-354

  Keene, Alex C ^a,b   Waddell, Scott ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; COMPLEMENTARY DNA; DOPAMINE; G PROTEIN COUPLED RECEPTOR; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; LEXA PROTEIN; MONOAMINE; TRANSCRIPTION FACTOR GAL4;

ANIMAL BEHAVIOR; CALCIUM CELL LEVEL; CELLULAR DISTRIBUTION; DENDRITE; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC MANIPULATION; GENETIC PROCEDURES; IMMUNOHISTOCHEMISTRY; LEARNING; MUSHROOM BODY; NEUROBIOLOGY; NONHUMAN; OLFACTORY MEMORY; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; SHORT TERM MEMORY; SPINAL CORD; SYNAPTIC TRANSMISSION;

ANIMALS; DROSOPHILA; GENES, INSECT; MEMORY; NERVE NET; OLFACTORY PATHWAYS;

ANIMALIA; DROSOPHILA MELANOGASTER;

EID: 34247516099     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn2098     Document Type: Review

References (183)

1. McGuire, S. E., Deshazer, M. & Davis, R. L. Thirty years of olfactory learning and memory research in Drosophila melanogaster. Prog. Neurobiol. 76, 328-347 (2005).
2. Davis, R. L. Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annu. Rev. Neurosci. 28, 275-302 (2005).
3. Margulies, C., Tully, T. & Dubnau, J. Deconstructing memory in Drosophila. Curr. Biol. 15, R700-R713 (2005).
4. Venken, K. J. & Bellen, H. J. Emerging technologies for gene manipulation in Drosophila melanogaster. Nature Rev. Genet. 6, 167-178 (2005).
5. Kitamoto, T. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J. Neurobiol. 47, 81-92 (2001).
6. Tobin, D. et al. Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35, 307-318 (2002).
7. Lima, S. Q. & Miesenbock, G. Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121, 141-152 (2005). A spectacular demonstration of experimenter-controlled behaviour by photostimulation of genetically defined neurons in an intact living fly. A laser was used to activate an injected caged-ATP that depolarizes target neurons expressing a transgenically encoded mammalian ionotropic ATP receptor.
8. Marella, S. et al. Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49, 285-295 (2006).
9. Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. Millisecond-timescale, genetically targeted optical control of neural activity. Nature Neurosci. 8, 1263-1268 (2005).
10. Nagel, G. et al. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15, 2279-2284 (2005).
11. Schroll, C. et al. Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr. Biol. 16, 1741-1747 (2006). In larval olfactory conditioning experiments the authors replaced US presentation with photostimulation of monoaminergic neurons expressing transgenic channelrhodopsin 2.
12. Fiala, A. et al. Genetically expressed cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons. Curr. Biol. 12, 1877-1884 (2002).
13. Ng, M. et al. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36, 463-474 (2002).
14. Wang, J. W., Wong, A. M., Flores, J., Vosshall, L. B. & Axel, R. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112, 271-282 (2003).
15. 2+ imaging. J. Neurosci. 24, 6507-6514 (2004).
16. Yu, D., Ponomarev, A. & Davis, R. L. Altered representation of the spatial code for odors after olfactory classical conditioning; memory trace formation by synaptic recruitment. Neuron 42, 437-449 (2004). The first study coupling live optical imaging of genetically defined neurons in the D. melanogaster brain with an olfactory conditioning protocol performed under the microscope. Conditioning changed odour-evoked activity in the antennal lobe.
17. Wilson, R. I., Turner, G. C. & Laurent, G. Transformation of olfactory representations in the Drosophila antennal lobe. Science 303, 366-370 (2003).
18. Schroder-Lang, S. et al. Fast manipulation of cellular cAMP level by light in vivo. Nature Methods 4, 39-42 (2007).
19. Quinn, W. G., Harris, W. A. & Benzer, S. Conditioned behavior in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 71, 708-712 (1974).
20. Duerr, J. S. & Quinn, W. G. Three Drosophila mutations that block associative learning also affect habituation and sensitization. Proc. Natl Acad. Sci. USA 79, 3646-3650 (1982).
21. Tempel, B. L., Bonini, N., Dawson, D. R. & Quinn, W. G. Reward learning in normal and mutant Drosophila. Proc. Natl Acad. Sci. USA 80, 1482-1486 (1983).
22. Tully, T. & Quinn, W. G. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. [A] 157, 263-277 (1985). The original description of the now standard olfactory conditioning procedure.
23. Wolf, R. et al. Drosophila mushroom bodies are dispensable for visual, tactile, and motor learning. Learn. Mem. 5, 166-178 (1998).
24. Mery, F. & Kawecki, T. J. Experimental evolution of learning ability in fruit flies. Proc. Natl Acad. Sci. USA 99, 14274-14279 (2002).
25. Wustmann, G. & Heisenberg, M. Behavioral manipulation of retrieval in a spatial memory task for Drosophila melanogaster. Learn. Mem. 4, 328-336 (1997).
26. Schwaerzel, M. et al. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J. Neurosci. 23, 10495-10502 (2003). This important paper demonstrated a differential requirement for dopamine and octopamine in aversive and appetitive conditioning.
27. Tully, T., Preat, T., Boynton, S. C. & Del, V. M. Genetic dissection of consolidated memory in Drosophila. Cell 79, 35-47 (1994). A landmark paper demonstrating that multiple spaced-training trials form protein synthesis-dependent long-term memory in D. melanogaster. This paper defined a new era of long-term memory study in D. melanogaster.
28. Quinn, W. G. & Dudai, Y. Memory phases in Drosophila. Nature 262, 576-577 (1976).
29. Folkers, E., Drain, P. & Quinn, W. G. Radish, a Drosophila mutant deficient in consolidated memory. Proc. Natl Acad. Sci. USA 90, 8123-8127 (1993).
30. Isabel, G., Pascual, A. & Preat, T. Exclusive consolidated memory phases in Drosophila. Science 304, 1024-1027 (2004).
31. Davis, R. L. Olfactory learning. Neuron 44, 31-48 (2004).
32. Clyne, P. J. et al. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22, 327-338 (1999).
33. 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).
34. Gao, Q. & Chess, A. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60, 31-39 (1999).
35. Hallem, E. A. & Carlson, J. R. The odor coding system of Drosophila. Trends Genet. 20, 453-459 (2004).
36. Vosshall, L. B. The molecular logic of olfaction in Drosophila. Chem. Senses 26, 207-213 (2001).
37. de Bruyne, M., Clyne, P. J. & Carlson, J. R. Odor coding in a model olfactory organ: the Drosophila maxillary palp. J. Neurosci. 19, 4520-4532 (1999).
38. de Bruyne, M., Foster, K. & Carlson, J. R. Odor coding in the Drosophila antenna. Neuron 30, 537-552 (2001).
39. Hallem, E. A., Ho, M. G. & Carlson, J. R. The molecular basis of odor coding in the Drosophila antenna. Cell 117, 965-979 (2004).
40. Hallem, E. A. & Carlson, J. R. Coding of odors by a receptor repertoire. Cell 125, 143-160 (2006).
41. Elmore, T., Ignell, R., Carlson, J. R. & Smith, D. P. Targeted mutation of a Drosophila odor receptor defines receptor requirement in a novel class of sensillum. J. Neurosci. 23, 9906-9912 (2003).
42. Larsson, M. C. et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703-714 (2004).
43. Jones, W. D., Nguyen, T. A., Kloss, B., Lee, K. J. & Vosshall, L. B. Functional conservation of an insect odorant receptor gene across 250 million years of evolution. Curr. Biol. 15, R119-R121 (2005).
44. Goldman, A. L., Van der Goes van Naters, W., Lessing, D., Warr, C. G. & Carlson, J. R. Coexpression of two functional odor receptors in one neuron. Neuron 45, 661-666 (2005).
45. Jones, W. D., Cayirlioglu, P., Kadow, I. G. & Vosshall, L. B. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445, 86-90 (2007).
46. 2 reception in Drosophila. Proc. Natl Acad. Sci. USA 104, 3574-3578 (2007).
47. Vosshall, L. B., Wong, A. M. & Axel, R. An olfactory sensory map in the fly brain. Cell 102, 147-159 (2000).
48. Gao, Q., Yuan, B. & Chess, A. Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nature Neurosci. 3, 780-785 (2000).
49. Couto, A., Alenius, M. & Dickson, B. J. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15, 1535-1547 (2005).
50. Fishilevich, E. & Vosshall, L. B. Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15, 1548-1553 (2005).
51. Stocker, R. F., Heimbeck, G., Gendre, N. & de Belle. J. S. Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J. Neurobiol. 32, 443-456 (1997).
52. Jefferis, G. S., Marin, E. C., Stocker, R. F. & Luo, L. Target neuron prespecification in the olfactory map of Drosophila. Nature 414, 204-208 (2001).
53. Marin, E. C., Jefferis, G. S., Komiyama, T., Zhu, H. & Luo, L. Representation of the glomerular olfactory map in the Drosophila brain. Cell 109, 243-255 (2002).
54. Wilson, R. I. & Laurent, G. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J. Neurosci. 25, 9069-9079 (2005).
55. Shang, Y., Claridge-Chang, A., Sjulson, L., Pypaert, M. & Miesenbock, G. Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128, 601-612 (2007).
56. Stocker, R. F. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res. 275, 3-26 (1994).
57. Ito, K. et al. The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn. Mem. 5, 52-77 (1998).
58. Miesenbock, G., De, A. D. A. & Rothman, J. E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192-195 (1998).
59. 2+ probe composed of a single green fluorescent protein. Nature Biotechnol. 19, 137-141 (2001).
60. Christensen, T. A. & Hildebrand, J. G. Pheromonal and host-odor processing in the insect antennal lobe: how different. Curr. Opin. Neurobiol. 12, 393-399 (2002).
61. Christensen, T. A., Lei, H. & Hildebrand, J. G. Coordination of central odor representations through transient, non-oscillatory synchronization of glomerular output neurons. Proc. Natl Acad. Sci. USA 100, 11076-11081 (2003).
62. Friedrich, R. W. & Stopfer, M. Recent dynamics in olfactory population coding. Curr. Opin. Neurobiol. 11, 468-474 (2001).
63. Laurent, G. Olfactory network dynamics and the coding of multidimensional signals. Nature Rev. Neurosci. 3, 884-895 (2002).
64. Laurent, G. et al. Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu. Rev. Neurosci. 24, 263-297 (2001).
65. Menzel, R., Leboulle, G. & Eisenhardt, D. Small brains, bright minds. Cell 124, 237-239 (2006).
66. Hammer, M. & Menzel, R. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn. Mem. 5, 146-156 (1998).
67. Faber, T., Joerges, J. & Menzel, R. Associative learning modifies neural representations of odors in the insect brain. Nature Neurosci. 2, 74-78 (1999).
68. Daly, K. C., Christensen, T. A., Lei, H., Smith, B. H. & Hildebrand, J. G. Learning modulates the ensemble representations for odors in primary olfactory networks. Proc. Natl Acad. Sci. USA 101, 10476-10481 (2004).
69. Peele, P., Ditzen, M., Menzel, R. & Galizia, C. G. Appetitive odor learning does not change olfactory coding in a subpopulation of honeybee antennal lobe neurons. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 192, 1083-1103 (2006).
70. Ashraf, S. I., McLoon, A. L., Sclarsic, S. M. & Kunes, S. Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 124, 191-205 (2006).
71. Golic, K. G. & Lindquist, S. The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59, 499-509 (1989).
72. Lee, T. & Luo, L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461 (1999).
73. Wong, A. M., Wang, J. W. & Axel, R. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109, 229-241 (2002).
74. Jefferis, G. S. et al. Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128, 1187-1203 (2007).
75. Zhu, H. et al. Dendritic patterning by Dscam and synaptic partner matching in the Drosophila antennal lobe. Nature Neurosci. 9, 349-355 (2006).
76. Tanaka, N. K., Awasaki, T., Shimada, T. & Ito, K. Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr. Biol. 14, 449-457 (2004).
77. Lin, H., Lai, J. S., Chin, A., Chen, Y. & Chiang, A. A map of olfactory representation in the Drosophila mushroom body. Cell 128, 1205-1217 (2007).
78. Heimbeck, G., Bugnon, V., Gendre, N., Keller, A. & Stocker, R. F. A central neural circuit for experience-independent olfactory and courtship behavior in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 98, 15336-15341 (2001).
79. de Belle, J. S. & Heisenberg, M. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263, 692-695 (1994).
80. Wang, Y. et al. Blockade of neurotransmission in Drosophila mushroom bodies impairs odor attraction, but not repulsion. Curr. Biol. 13, 1900-1904 (2003).
81. Crittenden, J. R., Skoulakis, E. M., Han, K. A., Kalderon, D. & Davis, R. L. Tripartite mushroom body architecture revealed by antigenic markers. Learn. Mem. 5, 38-51 (1998).
82. Lee, T., Lee, A. & Luo, L. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126, 4065-4076 (1999).
83. Yang, M. Y., Armstrong, J. D., Vilinsky, I., Strausfeld, N. J. & Kaiser, K. Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 15, 45-54 (1995).
84. Strausfeld, N. J., Sinakevitch, I. & Vilinsky, I. The mushroom bodies of Drosophila melanogaster: an immunocytological and golgi study of Kenyon cell organization in the calyces and lobes. Microsc. Res. Tech. 62, 151-169 (2003).
85. Aceves-Pina, E. O. & Quinn, W. G. Learning in normal and mutant Drosophila larvae. Science 206, 93-96 (1979).
86. Gerber, B. & Stocker, R. F. The Drosophila larva as a model for studying chemosensation and chemosensory learning: a review. Chem. Senses 32, 65-89 (2007).
87. Scherer, S., Stocker, R. F. & Gerber, B. Olfactory learning in individually assayed Drosophila larvae. Learn. Mem. 10, 217-225 (2003).
88. Hendel, T. et al. The carrot, not the stick: appetitive rather than aversive gustatory stimuli support associative olfactory learning in individually assayed Drosophila larvae. J. Comp. Physiol. A 191, 265-279 (2005).
89. Tissot, M., Gendre, N., Hawken, A., Stortkuhl, K. F. & Stocker, R. F. Larval chemosensory projections and invasion of adult afferents in the antennal lobe of Drosophila. J. Neurobiol. 32, 281-297 (1997).
90. Ramaekers, A. et al. Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Curr. Biol. 15, 982-992 (2005).
91. Masuda-Nakagawa, L. M., Tanaka, N. K. & O'Kane, C. J. Stereotypic and random patterns of connectivity in the larval mushroom body calyx of Drosophila. Proc. Natl Acad. Sci. USA 102, 19027-19032 (2005).
92. Zhu, S., Chiang, A. S. & Lee, T. Development of the Drosophila mushroom bodies: elaboration, remodeling and spatial organization of dendrites in the calyx. Development 130, 2603-2610 (2003).
93. Yasuyama, K., Meinertzhagen, I. A. & Schurmann, F. W. Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J. Comp. Neurol. 445, 211-226 (2002).
94. Perez-Orive, J. et al. Oscillations and sparsening of odor representations in the mushroom body. Science 297, 359-365 (2002).
95. Perez-Orive, J., Bazhenov, M. & Laurent, G. Intrinsic and circuit properties favor coincidence detection for decoding oscillatory input. J. Neurosci. 24, 6037-6047 (2004).
96. 2+ measurements using improved cameleons. Proc. Natl Acad. Sci. USA 96, 2135-2140 (1999).
97. Yu, D., Akalal, D. B. & Davis, R. L. Drosophila α/β mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning. Neuron 52, 845-855 (2006).
98. Hammer, M. An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366, 59-63 (1993).
99. Krashes, M. J., Keene, A. C., Leung, B., Armstrong, J. D. & Waddell, S. Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron 53, 103-115 (2007).
100. Scott, K. Taste recognition: food for thought. Neuron 48, 455-464 (2005).
101. Amrein, H. & Thorne, N. Gustatory perception and behavior in Drosophila melanogaster. Curr. Biol. 15, R673-R684 (2005).
102. Clyne, P. J., Warr, C. G. & Carlson, J. R. Candidate taste receptors in Drosophila. Science 287, 1830-1834 (2000).
103. Scott, K. et al. A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104, 661-673 (2001).
104. Chyb, S., Dahanukar, A., Wickens, A. & Carlson, J. R. Drosophila Gr5a encodes a taste receptor tuned to trehalose. Proc. Natl Acad. Sci. USA 100, 14526-14530 (2003).
105. Wang, Z., Singhvi, A., Kong, P. & Scott, K. Taste representations in the Drosophila brain. Cell 117, 981-991 (2004).
106. Thorne, N., Chromey, C., Bray, S. & Amrein, H. Taste perception and coding in Drosophila. Curr. Biol. 14, 1065-1079 (2004).
107. Neckameyer, W. S. & White, K. Drosophila tyrosine hydroxylase is encoded by the pale locus. J. Neurogenet. 8, 189-199 (1993).
108. Livingstone, M. S. & Tempel, B. L. Genetic dissection of monoamine neurotransmitter synthesis in Drosophila. Nature 303, 67-70 (1983).
109. Friggi-Grelin, F. et al. Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J. Neurobiol. 54, 618-627 (2003).
110. Riemensperger, T., Voller, T., Stock, P., Buchner, E. & Fiala, A. Punishment prediction by dopaminergic neurons in Drosophila. Curr. Biol. 15, 1953-1960 (2005).
111. Yellman, C., Tao, H., He, B. & Hirsh, J. Conserved and sexually dimorphic behavioral responses to biogenic amines in decapitated Drosophila. Proc. Natl Acad. Sci. USA 94, 4131-4136 (1997).
112. Neckameyer, W. S. Dopamine and mushroom bodies in Drosophila: experience-dependent and-independent aspects of sexual behavior. Learn. Mem. 5, 157-165 (1998).
113. Bainton, R. J. et al. Dopamine modulates acute responses to cocaine, nicotine and ethanol in Drosophila. Curr. Biol. 10, 187-194 (2000).
114. Andretic, R., van Swinderen, B. & Greenspan, R. J. Dopaminergic modulation of arousal in Drosophila. Curr. Biol. 15, 1165-1175 (2005).
115. Kume, K., Kume, S., Park, S. K., Hirsh, J. & Jackson, F. R. Dopamine is a regulator of arousal in the fruit fly. J. Neurosci. 25, 7377-7384 (2005).
116. Sinakevitch, I. & Strausfeld, N. J. Comparison of octopamine-like immunoreactivity in the brains of the fruit fly and blow fly. J. Comp. Neurol. 494, 460-475 (2006).
117. Cole, S. H. et al. Two functional but noncomplementing Drosophila tyrosine decarboxylase genes: distinct roles for neural tyramine and octopamine in female fertility. J. Biol. Chem. 280, 14948-14955 (2005).
118. Heisenberg, M. Mushroom body memoir: from maps to models. Nature Rev. Neurosci. 4, 266-275 (2003).
119. Han, K. A., Millar, N. S., Grotewiel, M. S. & Davis, R. L. DAMB, a novel dopamine receptor expressed specifically in Drosophila mushroom bodies. Neuron 16, 1127-1135 (1996).
120. Kim, Y. C., Lee, H. G., Seong, C. S. & Han, K. A. Expression of a D1 dopamine receptor dDA1/DmDOP1 in the central nervous system of Drosophila melanogaster. Gene Expr. Patterns 3, 237-245 (2003).
121. Han, K. A., Millar, N. S. & Davis, R. L. A novel octopamine receptor with preferential expression in Drosophila mushroom bodies. J. Neurosci. 18, 3650-3658 (1998).
122. Heisenberg, M., Borst, A., Wagner, S. & Byers, D. Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenet. 2, 1-30 (1985). The first paper suggesting a role for the D. melanogaster mushroom bodies in olfactory memory. Includes a nice discussion of the caveats of studying anatomically defective flies.
123. Dudai, Y., Jan, Y. N., Byers, D., Quinn, W. G. & Benzer, S. dunce, a mutant of Drosophila deficient in learning. Proc. Natl Acad. Sci. USA 73, 1684-1688 (1976). dunce was the first identified learning mutant. This paper contains an important discussion of the specificity of the mutant phenotype.
124. Byers, D., Davis, R. L. & Kiger, J. A. J. Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster. Nature 289, 79-81 (1981).
125. Davis, R. L. & Kiger, J. A. J. Dunce mutants of Drosophila melanogaster: mutants defective in the cyclic AMP phosphodiesterase enzyme system. J. Cell Biol. 90, 101-107 (1981).
126. Chen, C. N., Denome, S. & Davis, R. L. Molecular analysis of cDNA clones and the corresponding genomic coding sequences of the Drosophila dunce + gene, the structural gene for cAMP phosphodiesterase. Proc. Natl Acad. Sci. USA 83, 9313-9317 (1986).
127. Qiu, Y. H. et al. Characterization of the memory gene dunce of Drosophila melanogaster. J. Mol. Biol. 222, 553-565 (1991).
128. Livingstone, M. S., Sziber, P. P. & Quinn, W. G. Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant. Cell 37, 205-215 (1984).
129. 2+/Calmodulin-responsive adenylyl cyclase. Cell 68, 479-489 (1992).
130. Nighorn, A., Healy, M. J. & Davis, R. L. The cyclic AMP phosphodiesterase encoded by the Drosophila dunce gene is concentrated in the mushroom body neuropil. Neuron 6, 455-467 (1991).
131. Han, P. L., Levin, L. R., Reed, R. R. & Davis, R. L. Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron 9, 619-627 (1992).
132. Skoulakis, E. M., 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).
133. Folkers, E., Waddell, S. & Quinn, W. G. The Drosophila radish gene encodes a protein required for anesthesia-resistant memory. Proc. Natl Acad. Sci. USA (2006).
134. Zars, T., Fischer, M., Schulz, R. & Heisenberg, M. Localization of a short-term memory in Drosophila. Science 288, 672-675 (2000).
135. McGuire, S. E., Le, P. T., Osborn, A. J., Matsumoto, K. & Davis, R. L. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302, 1765-1768 (2003). The description and use of TARGET: a system that permits spatial and temporal control of transgene expression based on a temperature sensitive variant of the GAL80 repressor of GAL4. Using this method, and that detailed in reference 136, the authors restrict expression of a rutabaga transgene to adulthood in rut mutant flies and determine that RUT adenylate cyclase functions acutely in the adult mushroom bodies.
136. Mao, Z., Roman, G., Zong, L. & Davis, R. L. Pharmacogenetic rescue in time and space of the rutabaga memory impairment by using Gene-Switch. Proc. Natl Acad. Sci. USA 101, 198-203 (2004).
137. Connolly, J. B. et al. Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274, 2104-2107 (1996).
138. Grotewiel, M. S., Beck, C. D., Wu, K. H., Zhu, X. R. & Davis, R. L. Integrin-mediated short-term memory in Drosophila. Nature 391, 455-460 (1998).
139. Cheng, Y. et al. Drosophila fasciclinII is required for the formation of odor memories and for normal sensitivity to alcohol. Cell 105, 757-768 (2001).
140. Dubnau, J. et al. The staufen/pumilio pathway is involved in Drosophila long-term memory. Curr. Biol. 13, 286-296 (2003). Reports a large screen for long-term memory-defective flies. This mutant collection provides a considerable resource for future study.
141. Qiu, Y. & Davis, R. L. Genetic dissection of the learning/memory gene dunce of Drosophila melanogaster. Genes Dev. 7, 1447-1458 (1993).
142. Kalidas, S. & Smith, D. P. Novel genomic cDNA hybrids produce effective RNA interference in adult Drosophila. Neuron 33, 177-184 (2002).
143. Didelot, G. et al. Tequila, a neurotrypsin ortholog, regulates long-term memory formation in Drosophila. Science 313, 851-853 (2006).
144. ts1 transgene expressed in mushroom bodies to test the role of mushroom body neuron activity in memory acquisition, storage and retrieval.
145. McGuire, S. E., Le, P. T. & Davis, R. L. The role of Drosophila mushroom body signaling in olfactory memory. Science 293, 1330-1333 (2001).
146. Schwaerzel, M., Heisenberg, M. & Zars, T. Extinction antagonizes olfactory memory at the subcellular level. Neuron 35, 951-960 (2002).
147. Akalal, D. B. et al. Roles for Drosophila mushroom body neurons in olfactory learning and memory. Learn. Mem. 13, 659-668 (2006).
148. 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). Describes the identification of DPM neurons and the demonstration that their function is vital for memory stability in adult flies.
149. Quinn, W. G., Sziber, P. P. & Booker, R. The Drosophila memory mutant amnesiac. Nature 277, 212-214 (1979).
150. Feany, M. B. & Quinn, W. G. A neuropeptide gene defined by the Drosophila memory mutant amnesiac. Science 268, 869-873 (1995).
151. 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).
152. Tamura, T. et al. Aging specifically impairs amnesiac-dependent memory in Drosophila. Neuron 40, 1003-1011 (2003).
153. Keene, A. C. et al. Diverse odor-conditioned memories require uniquely timed dorsal paired medial neuron output. Neuron 44, 521-533 (2004).
154. Keene, A. C., Krashes, M. J., Leung, B., Bernard, J. A. & Waddell, S. Drosophila dorsal paired medial neurons provide a general mechanism for memory consolidation. Curr. Biol. 16, 1524-1530 (2006).
155. Yu, D., Keene, A. C., Srivatsan, A., Waddell, S. & Davis, R. L. Drosophila DPM neurons form a delayed and branch-specific memory trace after olfactory classical conditioning. Cell 123, 945-957 (2005). Coupled live optical imaging of DPM neurons with an olfactory learning protocol performed under the microscope. An odour-specific memory trace formed with a similar delayed temporal kinetic to the behavioural memory requirement for DPM neuron activity.
156. Gu, H. & O'Dowd, D. K. Cholinergic synaptic transmission in adult Drosophila Kenyon cells in situ. J. Neurosci. 26, 265-272 (2006).
157. Perry, T., McKenzie, J. A. & Batterham, P. A Dα6 knockout strain of Drosophila melanogaster confers a high level of resistance to spinosad. Insect Biochem. Mol. Biol. 37, 184-188 (2007).
158. Fayyazuddin, A., Zaheer, M. A., Hiesinger, P. R. & Bellen, H. J. The nicotinic acetylcholine receptor Dα7 is required for an escape behavior in Drosophila. PLoS Biol. 4, e63 (2006).
159. Millar, N. S. et al. Functional expression of a cloned Drosophila muscarinic acetylcholine receptor in a stable Drosophila cell line. J. Exp. Biol. 198, 1843-1850 (1995).
160. Cordova, D., Delpech, V. R., Sattelle, D. B. & Rauh, J. J. Spatiotemporal calcium signaling in a Drosophila melanogaster cell line stably expressing a Drosophila muscarinic acetylcholine receptor. Invert. Neurosci. 5, 19-28 (2003).
161. Ponsioen, B. et al. Detecting cAMP-induced Epac activation by fluorescence resonance energy transfer: Epac as a novel cAMP indicator. EMBO Rep. 5, 1176-1180 (2004).
162. Lai, S. L. & Lee, T. Genetic mosaic with dual binary transcriptional systems in Drosophila. Nature Neurosci. 9, 703-709 (2006).
163. Miesenbock, G. & Kevrekidis, I. G. Optical imaging and control of genetically designated neurons in functioning circuits. Annu. Rev. Neurosci. 28, 533-563 (2005).
164. Awasaki, T. et al. The Drosophila trio plays an essential role in patterning of axons by regulating their directional extension. Neuron 26, 119-131 (2000).
165. Choi, K. W., Smith, R. F., Buratowski, R. M. & Quinn, W. G. Deficient protein kinase C activity in turnip, a Drosophila learning mutant. J. Biol. Chem. 266, 15999-15606 (1991).
166. Goodwin, S. F. et al. Defective learning in mutants of the Drosophila gene for a regulatory subunit of cAMP-dependent protein kinase. J. Neurosci. 17, 8817-8827 (1997).
167. Guo, H. F., Tong, J., Hannan, F., Luo, L. & Zhong, Y. A neurofibromatosis-1-regulated pathway is required for learning in Drosophila. Nature 403, 895-898 (2000).
168. Skoulakis, E. M. & Davis, R. L. Olfactory learning deficits in mutants for leonardo, a Drosophila gene encoding a 14-3-3 protein. Neuron 17, 931-944 (1996).
169. Putz, G., Bertolucci, F., Raabe, T., Zars, T. & Heisenberg, M. The S6KII (rsk) gene of Drosophila melanogaster differentially affects an operant and a classical learning task. J. Neurosci. 24, 9745-9751 (2004).
170. 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).
171. DeZazzo, J. et al. nalyot, a mutation of the Drosophila myb-related Adf1 transcription factor, disrupts synapse formation and olfactory memory. Neuron 27, 145-158 (2000).
172. Dura, J. M., Preat, T. & Tully, T. Identification of linotte, a new gene affecting learning and memory in Drosophila melanogaster. J. Neurogenet. 9, 1-14 (1993).
173. Xia, S. et al. NMDA receptors mediate olfactory learning and memory in Drosophila. Curr. Biol. 15, 603-615 (2005).
174. Yin, J. C. et al. Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79, 49-58 (1994).
175. Chang, K. T., Shi, Y. J. & Min, K. T. The Drosophila homolog of Down's syndrome critical region 1 gene regulates learning: implications for mental retardation. Proc. Natl Acad. Sci. USA 100, 15794-15799 (2003).
176. Presente, A., Boyles, R. S., Serway, C. N., de Belle, J. S. & Andres, A. J. Notch is required for long-term memory in Drosophila. Proc. Natl Acad. Sci. USA 101, 1764-1768 (2004).
177. Ge, X. et al. Notch signaling in Drosophila long-term memory formation. Proc. Natl Acad. Sci. USA 101, 10172-10176 (2004).
178. Comas, D., Petit, F. & Preat, T. Drosophila long-term memory formation involves regulation of cathepsin activity. Nature 430, 460-463 (2004).
179. Drier, E. A. et al. Memory enhancement and formation by atypical PKM activity in Drosophila melanogaster. Nature Neurosci. 5, 316-324 (2002).
180. Michels, B. et al. A role for Synapsin in associative learning: the Drosophila larva as a study case. Learn. Mem. 12, 224-231 (2005).
181. Brand, A. H. & Perrimon, N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415 (1993).
182. 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).
183. Ferris, J., Ge, H., Liu, L. & Roman, G. G(o) signaling is required for Drosophila associative learning. Nature Neurosci. 9, 1036-1040 (2006).