Drosophila as a model organism for the study of neuropsychiatric disorders

Current Topics in Behavioral Neurosciences

Volumn 7, Issue 1, 2011, Pages 37-60

  O'Kane, Cahir J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Addiction; Aggression; Autism; Courtship; Dopamine; Drosophila; Learning; Memory; Neuropeptides; Schizophrenia; Serotonin; Sleep

Indexed keywords

ACETYLCHOLINE; DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN; DYSBINDIN; HISTAMINE; MONOAMINE; NEU DIFFERENTIATION FACTOR; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS;

ADDICTION; ADRENERGIC SYSTEM; ANIMAL BEHAVIOR; ARTICLE; ATTENTION; AUTISM; BIPOLAR DISORDER; DISC1 GENE; DISEASE MODEL; DOPAMINERGIC SYSTEM; DROSOPHILA; DYSBINDIN GENE; GENE; LEARNING; MEMORY; MENTAL DISEASE; MENTAL STRESS; MOOD DISORDER; NEUREGULIN GENE; NEUROANATOMY; NEUROPSYCHIATRY; NONHUMAN; PDE4B GENE; PRIORITY JOURNAL; SCHIZOPHRENIA; SEROTONINERGIC SYSTEM; SLEEP PATTERN; SOCIAL BEHAVIOR; ANIMAL; BIOLOGICAL MODEL; BRAIN; HUMAN; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; DROSOPHILA; HUMANS; MODELS, BIOLOGICAL; NEUROTRANSMITTER AGENTS; SIGNAL TRANSDUCTION;

EID: 80054835016     PISSN: 18663370     EISSN: 18663389     Source Type: Book Series    
DOI: 10.1007/7854_2010_110     Document Type: Article

References (149)

1. Abrahams BS, Geschwind DH (2008) Advances in autism genetics: on the threshold of a new neurobiology. Nat Revs Genetics 9:341-356.
2. Agosto J, Choi JC, Parisky KM et al (2008) Modulation of GABAA receptor desensitization uncouples sleep onset and maintenance in Drosophila. Nat Neurosci 11:354-359.
3. Andretic R, Chaney S, Hirsh J (1999) Requirement of circadian genes for cocaine sensitization in Drosophila. Science 285:1066-1068.
4. Ashton K, Wagoner AP, Carrillo R, Gibson G (2001) Quantitative trait loci for the monoaminerelated traits heart rate and headless behavior in Drosophila melanogaster. Genetics 157:283-294.
5. Bainton RJ, Tsai LT, Singh CM et al (2000) Dopamine modulates acute responses to cocaine, nicotine and ethanol in Drosophila. Curr Biol 10:187-194.
6. Ballas N, Lioy DT, Grunseich C, Mandel G (2009) Non-cell autonomous influence of MeCP2- deficient glia on neuronal dendritic morphology. Nat Neurosci 12:311-317.
7. Berger KH, Heberlein U, Moore MS (2004) Rapid and chronic: two distinct forms of ethanol tolerance in Drosophila. Alcohol Clin Exp Res 28:1469-1480.
8. Bhandar P, Kendler KS, Bettinger JC et al (2009) An assay for evoked locomotor behavior in Drosophila reveals a role for integrins in ethanol sensitivity and rapid ethanol tolerance. Alcohol Clin Exp Res 33:1794-1805.
9. Bourtchuladze R, Frenguelli B, Blendy J et al (1994) Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79:59-68.
10. Buckingham SD, Biggin PC, Sattelle BM et al (2005) Insect GABA receptors: splicing, editing and targeting by antiparasitics and insecticides. Mol Pharmacol 68:942-951.
11. Bushey D, Tononi G, Cirelli C (2009) The Drosophila fragile X mental retardation gene regulates sleep need. J Neurosci 29:1948-1961.
12. Campusano JM, Su H, Jiang SA et al (2007) nAChR-mediated calcium response and plasticity in Drosophila Kenyon cells. Dev Neurobiol 67:1520-1532.
13. Cattaert D, Birman S (2001) Blockade of the central generator of locomotor rhythm by noncompetitive NMDA receptor antagonists in Drosophila larvae. J Neurobiol 48:58-73.
14. Chabaud M-A, Isabel G, Kaiser L, Preat T (2009) Social facilitation of long-lasting memory retrieval in Drosophila. Curr Biol 19:1654-1659.
15. Chang S, Bray SM, Li Z et al (2008) Identification of small molecules rescuing fragile X syndrome phenotypes in Drosophila. Nat Chem Biol 4:256-263.
16. Chen S, Lee AY, Bowens NM et al (2002) Fighting fruit flies: a model system for the study of aggression. Proc Natl Acad Sci USA 99:5664-5668.
17. Chen J, Zhang Y, Shen P (2008) A protein kinase C activity localized to neuropeptide Y-like neurons mediates ethanol intoxication in Drosophila melanogaster. Neuroscience 156:42-47.
18. Chubb JE, Bradshaw NJ, Soares DC et al (2008) The DISC locus in psychiatric illness. Mol Psychiat 13:36-64.
19. Chumakov I, Blumenfeld M, Guerassimenko O et al (2002) Genetic and physiological data implicating the new human gene G72 and the gene for D-amino acid oxidase in schizophrenia. Proc Natl Acad Sci USA 99:13675-13680.
20. Chung BY, Kilman VL, Keath JR et al (2009) The GABAA receptor RDL acts in peptidergic PDF neurons to promote sleep in Drosophila. Curr Biol 19:386-390.
21. Clyne JD, Miesenböck G (2008) Sex-specific control and tuning of the pattern generator for courtship song in Drosophila. Cell 133:354-363.
22. Cowmeadow RB, Krishnan HR, Atkinson NS (2005) The slowpoke gene is necessary for rapid ethanol tolerance in Drosophila. Alcohol Clin Exp Res 29:1777-1786.
23. Cowmeadow RB, Krishnan HR, Ghezzi A et al (2006) Ethanol tolerance caused by slowpoke induction in Drosophila. Alcohol Clin Exp Res 30:745-753.
24. Craddock N, Sklar P (2009) Genetics of bipolar disorder: a successful start to a long journey. Trends Genet 25:99-105.
25. Daneman R, Barres BA (2005) The blood-brain barrier - lessons from moody flies. Cell 123:9-12.
26. Demchyshyn LL, Pristupa ZB, Sugamori KS et al (1994) Cloning, expression, and localization of a chloride-facilitated, cocaine-sensitive serotonin transporter from Drosophila melanogaster. Proc Natl Acad Sci USA 91:5158-5162.
27. DeZazzo J, Xia S, Christensen J, Velinzon K, Tully T (1999) Developmental expression of an amn+ transgene rescues the mutant memory defect of amnesiac adults. J Neurosci 19:8740-8746.
28. Dickman DK, Davis GW (2009) The schizophrenia susceptibility gene dysbindin controls synaptic homeostasis. Science 326:1127-1131.
29. Dickson BJ (2008) Wired for sex: the neurobiology of Drosophila mating decisions. Science 322:904-909.
30. Dolezelova E, Nothacker H-P, Civelli O et al (2007) A Drosophila adenosine receptor activates cAMP and calcium signaling. Insect Biochem Mol Biol 37:318-329.
31. Eaton K, Sallee FR, Sah R (2007) Relevance of neuropeptide Y (NPY) in psychiatry. Curr Top Med Chem 7:1645-1659.
32. Enell L, Hamasaka Y, Kolodziejczyk A, Nässel D (2007) gamma-Aminobutyric acid (GABA) signaling components in Drosophila: immunocytochemical localization of GABA(B) receptors in relation to the GABA(A) receptor subunit RDL and a vesicular GABA transporter. J Comp Neurol 505:18-31.
33. Fergestad T, Olson L, Patel KP et al (2008) Neuropathology in Drosophila mutants with increased seizure susceptibility. Genetics 178:947-956.
34. Foltenyi K, Greenspan RJ, Newport JW (2007) Activation of EGFR and ERK by rhomboid signaling regulates the consolidation and maintenance of sleep in Drosophila. Nat Neurosci 10:1160-1167.
35. Freeman MR, Doherty J (2006) Glial cell biology in Drosophila and vertebrates. Trends Neurosci 29:82-90.
36. Gatto CL, Broadie K (2009) Temporal requirements of the fragile X mental retardation protein in modulating circadian clock circuit synaptic architecture. Front Neural Circuits 3:8.
37. Gilestro GF, Toning G, Cirelli C (2009) Widespread changes in synaptic markers as a function of sleep and wakefulness in Drosophila. Science 324:109-112.
38. Glessner JT, Wang K, Cai G et al (2009) Autism genome-wide copy number variation reveals ubiquitin and neuronal genes. Nature 459:569-574.
39. Gogos JA, Santha M, Takacz Z et al (1999) The gene encoding proline dehydrogenase modulates sensorimotor gating in mice. Nat Genet 21:434-439.
40. Gondo Y, Murata T, Makino S, Fukumura R, Ishitsuka Y (2011) Mouse mutagenesis and disease models for neuropsychiatric disorders. In: Current topics in behavioral neurosciences. Springer, Heidelberg. doi: 10.1007/7854_2010_106.
41. Gothelf D, Eliez S, Thompson T et al (2005) COMT genotype predicts longitudinal cognitive decline and psychosis in 22q11.2 deletion syndrome. Nat Neurosci 8:1500-1502.
42. Greer CL, Grygoruk A, Patton DE et al (2005) A splice variant of the Drosophila vesicular monoamine transporter contains a conserved trafficking domain and functions in the storage of dopamine, serotonin, and octopamine. J Neurobiol 64:239-258.
43. Greer PL, Hanayama R, Bloodgood BL et al (2010) The Angelman syndrome protein Ube3A regulates synapse development by ubiquitinating arc. Cell 140:704-716.
44. Harbison ST, Sehgal A (2008) Quantitative genetic analysis of sleep in Drosophila melanogaster. Genetics 178:2341-2360.
45. Hauser F, Cazzamali G, Williamson M et al (2006) A review of neurohormone GPCRs present in the fruitfly Drosophila melanogaster and the honey bee Apis mellifera. Prog Neurobiol 80:1-19.
46. Hawkins RD (1984) A cellular mechanism of classical conditioning in Aplysia. J Exp Biol 112:13-128.
47. Heberlein U, Tsai LT-Y, Kapfhamer D, Lasek AW (2009) Drosophila, a genetic model system to study cocaine-related behaviors: A review with focus on LIM-only proteins. Neuropharmacology 56:97-106.
48. Heidbreder C (2011) Advances in animal models of drug addiction. In: Current topics in behavioural neuroscience. Springer, Heidelberg. doi: 10.1007/7854_2010_107.
49. Hendricks JC, Finn SM, Panckeri KA et al (2000) Rest in Drosophila is a sleep-like state. Neuron 25:129-138.
50. Hewes RS, Taghert PH (2001) Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Res 11:1126-1142.
51. Hoyer SC, Eckart A, Herrel A, Zars T, Fischer SA, Hardie SL, Heisenberg M (2008) Octopamine in male aggression in Drosophila. Curr Biol 18:159-167.
52. Isabel G, Pascual A, Preat T (2004) Exclusive consolidated memory phases in Drosophila. Science 304:1024-1027.
53. Joiner WJ, Crocker A, White BH, Sehgal A (2006) Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441:757-760.
54. Karayiorgou M, Morris MA, Morrow B et al (1995) Schizophrenia susceptibility associated with interstitial deletions of chromosome 22q11. Proc Natl Acad Sci USA 92:7612-7616.
55. Kauer J, Malenka RC (2007) Synaptic plasticity and addiction. Nat Rev Neurosci 8:844-858.
56. Kent C, Azanchi R, Smith B et al (2008) Social context influences chemical communication in D melanogaster males. Curr Biol 18:1384-1389.
57. Koh K, Joiner WJ, Wu MN et al (2008) Identification of sleepless, a sleep-promoting factor. Science 321:372-376.
58. Krishnan V, Nestler EJ (2011) Animal models of depression: molecular perspectives. In: Current topics in behavioural neuroscience. Springer, Heidelberg. doi: 10.1007/7854_2010_108.
59. Krupp JJ, Kent C, Billeter J-C et al (2008) Social experience modifies pheromone expression and mating behavior in male Drosophila melanogaster. Curr Biol 18:1373-1383.
60. Kume K, Kume S, Park SK et al (2005) Dopamine is a regulator of arousal in the fruit fly. J Neurosci 25:7377-7384.
61. Lee H-G, Kim Y-C, Dunning JS, Han K-A (2008) Recurring ethanol exposure induces disinhibited courtship in Drosophila. PLoS ONE 3(1):e1391.
62. Lefranc A, Jeune B, Thomas-Orillard M, Danchin E (2001) Non-independence of individuals in a population of Drosophila melanogaster: effects on spatial distribution and dispersal. C R Acad Sci Paris Life Sci 324:219-227.
63. Leonardo ED, Hen R (2006) Genetics of affective and anxiety disorders. Annu Rev Psychol 57:117-137.
64. Li H, Chaney S, Roberts IJ et al (2000) Ectopic G-protein expression in dopamine and serotonin neurons blocks cocaine sensitization in Drosophila melanogaster. Curr Biol 10:211-214.
65. Li C, Zhao X, Cao X et al (2008) The Drosophila homolog of jwa is required for ethanol tolerance. Alcohol Alcohol 43:529-536.
66. Littleton JT, Ganetzky B (2000) Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 26:35-43.
67. Liu W, Guo F, Lu B, Guo A (2008) Amnesiac regulates sleep onset and maintenance in Drosophila melanogaster. Biochem Biophys Res Commun 372:798-803.
68. Luo L, Callaway EM, Svoboda K (2008) Genetic dissection of neural circuitry. Neuron 57:634-660.
69. Maas JW Jr, Vogt SK, Chan GCK et al (2005) Calcium-stimulated adenylyl cyclases are critical modulators of neuronal ethanol sensitivity. J Neurosci 25:4118-4126.
70. Manev H, Uz T (2006) Clock genes: influencing and being influenced by psychoactive drugs. Trends Pharm Sci 27:186-189.
71. Mao Z, Davis RL (2009) Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity. Front Neural Circuits 3:1.
72. McClung C, Hirsh J (1998) Stereotypic behavioral responses to free-base cocaine and the development of behavioral sensitization in Drosophila. Curr Biol 8:109-112.
73. McGuire SE, Deshazer M, Davis RL (2005) Thirty years of olfactory learning and memory research in Drosophila melanogaster. Prog Neurobiol 76:328-347.
74. McMahon FJ, Akula N, Schulze TG et al (2010) Meta-analysis of genome-wide association data identifies a risk locus for major mood disorders on 3p21.1. Nat Genet 42:128-132.
75. McMonagle P, Hutchinson M, Lawlor B (2006) Hereditary spastic paraparesis and psychosis. Eur J Neurol 13:874-879.
76. McPartland J, Di Marzo V, De Petrocellis L et al (2001) Cannabinoid receptors are absent in insects. J Comp Neurol 436:423-429.
77. McPartland JM, Matias I, Di Marzo V, Glass M (2006) Evolutionary origins of the endocannabinoid system. Gene 370:64-74.
78. Mery F, Varela SAM, Danchin E et al (2009) Public versus personal information for mate copying in an invertebrate. Curr Biol 19:730-734.
79. Millar JK, Pikard BS, Mackie S et al (2005) DISC1 and PDE4B are interacting genetic factors in schizophrenia that regulate cAMP signaling. Science 310:1187-1191.
80. Moore MS, DeZazzo J, Luk AY et al (1998) Ethanol intoxication in Drosophila: genetic and pharmacological evidence for regulation by the cAMP signaling pathway. Cell 93:997-1007.
81. Morozova TV, Anholt RRH, Mackay TFC (2006) Transcriptional response to alcohol exposure in Drosophila melanogaster. Genome Biol 7:R95.
82. Morozova TV, Anholt RRH, Mackay TFC (2007) Phenotypic and transcriptional response to selection for alcohol sensitivity in Drosophila melanogaster. Genome Biol 8:R231.
83. Morozova TV, Ayroles JF, Jordan KW et al (2009) Alcohol sensitivity in Drosophila: Translational potential of systems genetics. Genetics 183:733-745.
84. Nässel DR, Homberg U (2006) Neuropeptides in interneurons of the insect brain. Cell Tissue Res 326:1-24.
85. Nilsen SP, Chan YB, Huber R, Kravitz EA (2004) Gender-selective patterns of aggressive behavior in Drosophila melanogaster. Proc Natl Acad Sci USA 101:12342-12347.
86. O'Tuathaigh CMP, Desbonnet L, Moran PM, Kirby BP, Waddington JL (2011) Molecular genetic models related to schizophrenia and psychotic illness: heuristics and challenges. In: Current topics in behavioral neurosciences. Springer, Heidelberg. doi: 10.1007/7854_2010_111.
87. Olsen SR, Wilson RI (2008) Cracking neural circuits in a tiny brain: new approaches for understanding the neural circuitry of Drosophila. Trends Neurosci 31:512-520.
88. Parisky KM, Agosto J, Pulver SR et al (2008) PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 60:672-682.
89. Petersen CI, DeFelice LJ (1999) Ionic interactions in the Drosophila serotonin transporter identify it as a serotonin channel. Nat Neurosci 2:605-610.
90. Reaper CM, Fanelli F, Buckingham SD et al (1998) Antagonist profile and molecular dynamic situation of a Drosophila melanogaster muscarinic acetylcholine receptor. Receptors Channels 5:331-345.
91. Reichert H (2005) A tripartite organization of the urbilaterian brain: developmental genetic evidence from Drosophila. Brain Res Bull 66:491-494.
92. Rideout EJ, Dornan AJ, Neville MC et al (2010) Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat Neurosci 13:458-467.
93. Riemensperger T, Völler T, Stock P et al (2005) Punishment prediction by dopaminergic neurons in Drosophila. Curr Biol 15:1953-1960.
94. Rival T, Soustelle L, Strambi C et al (2004) Decreasing glutamate buffering capacity triggers oxidative stress and neuropil degeneration in the Drosophila brain. Curr Biol 14:599-605.
95. Rodan AR, Kiger JA Jr, Heberlein U (2002) Functional dissection of neuroanatomical loci regulating ethanol sensitivity in Drosophila. J Neurosci 22:9490-9501.
96. Roeder T (2005) Tyramine and octopamine: ruling behavior and metabolism. Annu Rev Entomol 50:447-477.
97. Romero-Calderón R, Uhlenbrock G, Borycz J (2006) A glial variant of the monoamine transporter is required to store histamine in the Drosophila visual system. PLoS Genet 4:e1000245.
98. Rose GM, Hopper A, De Vivo M, Tehim A (2005) Phosphodiesterase inhibitors for cognitive enhancement. Curr Pharm Des 11:3329-3334.
99. Ross CA, Margolis RL, Reading SAJ et al (2006) Neurobiology of schizophrenia. Neuron 52:139-153.
100. Rothenfluh A, Threlkeld RJ, Bainton RJ et al (2006) Distinct behavioral responses to ethanol are regulated by alternate RhoGAP18B isoforms. Cell 127:199-211.
101. Ryder PV, Faundez V (2009) Schizophrenia: the "BLOC" may be in the endosomes. Sci Signal 2(93):pe66.
102. Sakurai T (2007) The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat Revs Neurosci 8:171-181.
103. Schenk A, Bardoni B, Langmann C et al (2003) CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1.GTPase pathway to the Fragile X protein. Neuron 38:887-898.
104. Scholz H, Ramond J, Singh CM, Heberlein U (2000) Functional ethanol tolerance in Drosophila. Neuron 28:261-271.
105. Scholz H, Franz M, Heberlein U (2005) The hangover gene defines a stress pathway required for ethanol tolerance development. Nature 436:845-847.
106. Schroll C, Riemensperger T, Bucher D et al (2006) Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr Biol 16:1741-1747.
107. Schwaerzel M, Monastirioti M, Scholz H et al (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23: 10495-10502.
108. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287:1834-1837.
109. Shayan AJ, Brodin L, Ottersen OP et al (2000) Neurotransmitter levels and synaptic strength at the Drosophila larval neuromuscular junction are not altered by mutation in the sluggish-A gene, which encodes proline oxidase and affect adult locomotion. J Neurogenet 14:165-192.
110. Sheeba V, Fogle KJ, Kaneko M et al (2008) Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr Biol 18:1537-1545.
111. Silva AJ, Kogan JH, Frankland PW, Kida S (1998) CREB and memory. Annu Rev Neurosci 21:127-148.
112. Sinakevitch I, Grau Y, Strausfeld NJ, Birman S (2010) Dynamics of glutamatergic signaling in the mushroom body of young adult Drosophila. Neural Dev 5:10.
113. Sitaraman D, Zars M, LaFerriere H et al (2008) Serotonin is necessary for place memory in Drosophila. Proc Natl Acad Sci USA 105:5579-5584.
114. Sjulson L, Miesenböck G (2008) Photocontrol of neuronal activity: biophysical mechanisms and performance in vivo. Chem Rev 108:1588-1602.
115. Stefansson H, Rujescu D, Cichon S et al (2008) Large recurrent microdeletions associated with schizophrenia. Nature 455:232-237.
116. Stefansson H, Ophoff RA, Steinberg S et al (2009) Common variants conferring risk of schizophrenia. Nature 460:744-748.
117. Stork T, Thomas S, Rodriques F et al (2009) Drosophila neurexin IV stabilizes neuron-glia interactions at the CNS midline by binding to Wrapper. Development 136:1251-1261.
118. Straub RE, Jiang Y, MacLean CJ et al (2002) Genetic variation in the 6p22.3 gene DTNBP1, the human ortholog of the mouse dysbindin gene, is associated with schizophrenia. Am J Hum Genet 71:337-348.
119. Sweeney ST, Davis GW (2002) Unrestricted synaptic growth in spinster - a late endosomal protein implicated in TGF-b-mediated synaptic growth regulation. Neuron 36:403-416.
120. Sweeney ST, Broadie K, Keane J et al (1995) Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14:341-351.
121. Tanaka NK, Ito K, Stopfer M (2009) Odor-evoked neural oscillations in Drosophila are mediated by widely branching interneurons. J Neurosci 29:8595-8603.
122. Tavaziole SF, Alvarez VA, Ridenour DA et al (2005) Regulation of neuronal morphology and function by the tumor suppressors Tsc1 and Tsc2. Nat Neurosci 8:1727-1734.
123. Tessmar-Raible C (2007) The evolution of neurosecretory centers in bilaterian forebrains: insights from protostomes. Sem Cell Dev Biol 18:492-501.
124. The International Schizophrenia Consortium (2008) Rare chromosomal deletions and duplications increase risk of schizophrenia. Nature 455:237-241.
125. The International Schizophrenia Consortium (2009) Common polygenic variation contributes to schizophrenia and bipolar disorder. Nature 460:748-752.
126. Tinette S, Zhang L, Robichon A (2004) Cooperation between Drosophila flies in searching behavior. Genes Brain Behav 3:39-50.
127. Tsai LT-Y, Bainton RJ, Blau J, Heberlein U (2004) Lmo mutants reveal a novel role for circadian pacemaker neurons in cocaine-induced behaviors. PLoS Biol 2(12):e408.
128. Tully T, Preat T, Boynton SC, Del Vecchio M (1994) Genetic dissection of consolidated memory in Drosophila. Cell 79:35-47.
129. Urizar NL, Yang Z, Edenberg HJ, Davis RL (2007) Drosophila Homer is required in a small set of neurons including the ellipsoid body for normal ethanol sensitivity and tolerance. J Neurosci 27:4541-4551.
130. Vargas MA, Luo N, Yamaguchi A, Kapahi P (2010) A role for S6 kinase and serotonin in postmating dietery switch and balance of nutrients in D. melanogaster. Curr Biol 20(11):1006-1011.
131. Vosshall LB (2007) Into the mind of a fly. Nature 450:193-197.
132. Walsh T, McClellan JM, McCarthy SE et al (2008) Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science 320:539-545.
133. Wang X, Shaw WR, Tsang HTH et al (2007) Drosophila spichthyin inhibits BMP signaling and regulates synaptic growth and axonal microtubules. Nat Neurosci 10:177-185.
134. Wang K, Zhang H, Ma D (2009a) Common genetic variants on 5p14.1 associate with autism spectrum disorders. Nature 459:528-532.
135. Wang Y, Ghezzi A, Yin JC, Atkinson NS (2009b) CREB regulation of BK channel expression underlies rapid drug tolerance. Genes Brain Behav 8:369-376.
136. Weiss LA, Arking DE, The Gene Discovery Project of Johns Hopkins and the Autism Consortium (2009) A genome-wide linkage and association scan reveals novel loci for autism. Nature 461:802-811.
137. Wen T, Parrish CA, Xu D et al (2005) Drosophila neuropeptide F and its receptor NPFR1 define a signaling pathway that acutely modulates alcohol sensitivity. Proc Natl Acad Sci USA 102:2141-2146.
138. Wheeler SR, Banerjee S, Blauth K et al (2009) Neurexin IV and Wrapper interactions mediate Drosophila midline glial migration and axonal ensheathment. Development 136:1147-1157.
139. Wilson RI, Laurent G (2005) Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J Neurosci 25:9069-9079.
140. Wu MN, Ho K, Crocker A et al (2009) The effects of caffeine on sleep in Drosophila require PKA activity but not the adenosine receptor. J Neurosci 29:11029-11037.
141. Wucherpfennig T, Wilsch-Bräuninger M, González-Gaitán M (2003) Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J Cell Biol 161:609-624.
142. Xu J, Li M, Shen P (2010) A G-protein-coupled neuropeptide Y-like receptor suppresses behavioral and sensory responses to multiple stressful responses in Drosophila. J Neurosci 30:2504-2512.
143. Yuan Q, Joiner WJ, Sehgal A (2006) A sleep-promoting role for the Drosophila serotonin receptor 1A. Curr Biol 16:1051-1062.
144. Yuan C, O'Connell RJ, Wilson A et al (2008) Acute alcohol tolerance is intrinsic to the BKCa protein, but is modulated by the lipid environment. J Biol Chem 283:5090-5098.
145. Yurkovic A, Wang O, Basu AC, Kravitz EA (2006) Learning and memory associated with aggression in Drosophila melanogaster. Proc Natl Acad Sci USA 103:17519-17524.
146. Zarnescu DC, Shan G, Warren ST, Jin P (2005) Come FLY with us: towards understanding fragile X syndrome. Genes Brain Behav 4:385-392.
147. Zhang D, Kuromi H, Kidokoro Y (1999) Activation of metabotropic glutamate receptors enhances synaptic transmission at the Drosophila neuromuscular junction. Neuropharmacology 38:645-657.
148. Zhou C, Rao Y, Rao Y (2008) A subset of octopaminergic neurons are important for Drosophila aggression. Nat Neurosci 11:1059-1067.
149. Zlatic M, Li F, Strigini M, Grueber W, Bate M (2009) Positional cues in the Drosophila nerve cord: semaphorins pattern the dorsoventral axis. PLoS Biol 7(6):e1000135