Skip to main content

Deciphering the Adult Brain: From Neuroanatomy to Behavior

  • Protocol
  • First Online:
The Making and Un-Making of Neuronal Circuits in Drosophila

Part of the book series: Neuromethods ((NM,volume 69))

Abstract

The Drosophila brain with an estimated 100,000 neurons provides at once an excellent opportunity to describe a complex brain in great detail and to identify the genetic and neurobiological basis of a wide array of behaviors. Furthermore, the sequencing of the genome with the concurrent identification of the elaborate homology of human and Drosophila genes and numerous functional studies have established the high relevance of Drosophila to understand diseases of the human brain. An overview is provided of available techniques to visualize neurons and neural circuitry and to study their function in behavior. Various resources are listed, and future and emerging technologies are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 149.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Otsuna H, Ito K (2006) Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobulu-specific pathways. J Comp Neurol 497:928–958

    PubMed  Google Scholar 

  2. Shinomiya K, Matsudat K, Oishi T, Otsuna H, Ito K (2011) Flybrain neuron database: a comprehensive database system of the Drosophila brain neurons. J Comp Neurol 519:807–833

    PubMed  Google Scholar 

  3. Heisenberg M, Böhl K (1979) Isolation of anatomical brain mutants of Drosophila by histological means. Z Naturforsch 34:143–147

    Google Scholar 

  4. Blest AD (1961) Some modifications of Holme’s silver method for insect central nervous system. Q J Microsc Sci 102:413–417

    CAS  Google Scholar 

  5. Bodian D (1937) The staining of paraffin sections with activated protargol. The role of fixatives. Anat Rec 69:153–162

    CAS  Google Scholar 

  6. Protocol at: http://flybrain.neurobio.arizona.edu/Flybrain/html/atlas/golgi/index.html

  7. Fischbach KF, Götz C (1981) Das Experiment: ein Blick ins Fliegenhirn: Golgi-gefärbte Nervenzellen bei Drosophila. Biol Z 11:183–187

    Google Scholar 

  8. Colonnier M (1964) The tangential organization of the visual cortex. J Anat 98:327–344

    PubMed  CAS  Google Scholar 

  9. Nässel D (1996) Advances in the immunocytochemical localization of neuroactive substances in the insect nervous system. J Neurosci Methods 69:3–23

    PubMed  Google Scholar 

  10. Hamasaka Y, Nässel D (2006) Mapping of serotonin, dopamine, and histamine in relation to different clock neurons in the brain of Drosophila. J Comp Neurol 494:314–330

    PubMed  CAS  Google Scholar 

  11. Kolodziejczyk A, Sun X, Meinertzhagen IA, Nässel DR (2008) Glutamate, GABA and acetylcholine signaling components in the lamina of the Drosophila visual system. PLoS One 3:e2110

    PubMed  Google Scholar 

  12. Nässel D, Winther A (2010) Drosophila neuropeptides in regulation of physiology and behavior. Prog Neurobiol 92:42–104

    PubMed  Google Scholar 

  13. Goossens T, Kang YY, Wuytens G, Zimmermann P, Callaerts-Vegh Z, Pollarolo G, Islam R, Hortsch M, Callaerts P (2011) The Drosophila L1CAM homolog neuroglian signals through distinct pathways to control different aspects of mushroom body axon development. Development 138:1595–1605

    PubMed  CAS  Google Scholar 

  14. Mardon G, Solomon NM, Rubin GM (2004) dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development 120(12):3473–3486

    Google Scholar 

  15. Clements J, Hens K, Francis C, Schellens A, Callaerts P (2008) Conserved role for the Drosophila Pax6 homolog eyeless in differentiation and function of insulin-producing neurons. Proc Natl Acad Sci U S A 105(42):16183–16188

    PubMed  CAS  Google Scholar 

  16. O’Kane CJ, Gehring WJ (1987) Detection in situ of genomic regulatory elements in Drosophila. Proc Natl Acad Sci U S A 84:9123–9127

    PubMed  Google Scholar 

  17. Bellen HJ, O’Kane CJ, Wilson C, Grossniklaus U, Pearson RK, Gehring WJ (1989) P-element-mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev 3:1288–1300

    PubMed  CAS  Google Scholar 

  18. Yang MY, Armstrong JD, Vilinsky I, Strausfeld NJ, Kaiser K (1995) Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 15:45–54

    PubMed  Google Scholar 

  19. Han P-L, Meller V, Davis RL (1996) The Drosophila brain revisited by enhancer detection. J Neurobiol 31:88–102

    PubMed  CAS  Google Scholar 

  20. Ito K, Suzuki K, Estes P, Ramaswami M, Yamamoto D, Strausfeld NJ (1998) 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

    PubMed  CAS  Google Scholar 

  21. Renn SCP, Armstrong JD, Yang M, Wang Z, An X, Kaiser K, Taghert PH (1999) Genetic analysis of the Drosophila ellipsoid body neuropil: organization and development of the central complex. J Neurobiol 41:189–207

    PubMed  CAS  Google Scholar 

  22. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415

    PubMed  CAS  Google Scholar 

  23. Duffy JB (2002) GAL4 system in Drosophila: a fly geneticist’s Swiss army knife. Genesis 34:1–15

    PubMed  CAS  Google Scholar 

  24. Elliott DA, Brand AH (2008) The GAL4 system: a versatile system for the expression of genes. Methods Mol Biol 420:79–95

    PubMed  CAS  Google Scholar 

  25. Salvaterra PM, Kitamoto T (2001) Drosophila cholinergic neurons and processes visualized with GAL4/UAS-GFP. Brain Res Gene Expr Patterns 1:73–82

    PubMed  CAS  Google Scholar 

  26. Ng M, Roorda RD, Lima SQ, Zemelman BV, Morcillo P, Miesenböck G (2002) Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36:463–474

    PubMed  CAS  Google Scholar 

  27. Daniels RW, Gelfand MV, Collins CA, DiAntonio A (2008) Visualizing glutamatergic cell bodies and synapses in Drosophila larval and adult CNS. J Comp Neurol 508:131–152

    PubMed  CAS  Google Scholar 

  28. Alekseyenko OV, Lee C, Kravitz EA (2010) Targeted manipulation of serotonergic neurotransmission affects the escalation of aggression in adult male Drosophila melanogaster. PLoS One 5:e10806

    PubMed  Google Scholar 

  29. Friggi-Grelin F, Coulom H, Meller M, Gomez D, Hirsh J, Birman S (2003) Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J Neurobiol 54:618–627

    PubMed  CAS  Google Scholar 

  30. Cole SH, Carney GE, McClung CA, Willard SS, Taylor BJ, Hirsh J (2005) Two functional but noncomplementing Drosophila tyrosine decarboxylase genes: distinct roles for neural tyramine and octopamine in female fertility. J Biol Chem 280:14948–14955

    PubMed  CAS  Google Scholar 

  31. Li H, Chaney S, Roberts IJ, Forte M, Hirsh J (2000) Ectopic G-protein expression in dopamine and serotonin neurons blocks cocaine sensitization in Drosophila melanogaster. Curr Biol 10:211–214

    PubMed  CAS  Google Scholar 

  32. Tanaka NK, Tanimoto H, Ito K (2008) Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 508:711–755

    PubMed  Google Scholar 

  33. Aso Y, Grübel K, Busch S, Friedrich AB, Siwanowicz I, Tanimoto H (2009) The mushroom body of adult Drosophila characterized by GAL4 drivers. J Neurogenet 23:156–172

    PubMed  CAS  Google Scholar 

  34. Miyazaki T, Ito K (2010) Neural architecture of the primary gustatory center of Drosophila melanogaster visualized with GAL4 and LexA enhancer-trap systems. J Comp Neurol 518:4147–4181

    PubMed  Google Scholar 

  35. Kamikouchi A, Shimada T, Ito K (2006) Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster. J Comp Neurol 499:317–356

    PubMed  Google Scholar 

  36. Tanaka NK, Awasaki T, Shimada T, Ito K (2004) Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr Biol 14:449–457

    PubMed  CAS  Google Scholar 

  37. Young JM, Armstrong JD (2010) Structure of the adult central complex in Drosophila: organization of distinct neuronal subsets. J Comp Neurol 518:1500–1524

    PubMed  CAS  Google Scholar 

  38. Benzer S (1967) Behavioral mutants of Drosophila isolated by countercurrent distribution. Proc Natl Acad Sci U S A 58: 1112–1119

    PubMed  CAS  Google Scholar 

  39. Konopka RJ, Benzer S (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A 68:2112–2116

    PubMed  CAS  Google Scholar 

  40. de Belle JS, Heisenberg M (1994) Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263:692–695

    PubMed  Google Scholar 

  41. Strauss R, Hanesch U, Kinkelin M, Wolf R, Heisenberg M (1992) No-bridge of Drosophila melanogaster: portrait of a structural brain mutant of the central complex. J Neurogenet 8:125–155

    PubMed  CAS  Google Scholar 

  42. Strauss R, Heisenberg M (1993) A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 13: 1852–1861

    PubMed  CAS  Google Scholar 

  43. Coombe PE, Heisenberg M (1986) The structural brain mutant vacuolar medulla of Drosophila melanogaster with specific behavioral defects and cell degeneration in the adult. J Neurogenet 3:135–158

    PubMed  CAS  Google Scholar 

  44. Perrimon N, Ni JQ, Perkins L (2010) In vivo RNAi: today and tomorrow. Cold Spring Harb Perspect Biol 2:a003640

    PubMed  Google Scholar 

  45. Kitamoto T (2001) Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol 47:81–92

    PubMed  CAS  Google Scholar 

  46. Parisky KM, Agosto J, Pulver SR, Shang Y, Kuklin E, Hodge JJ, Kang K, Liu X, Garrity PA, Rosbash M, Griffith LC (2008) PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 60:672–682

    PubMed  CAS  Google Scholar 

  47. Shang Y, Griffith LC, Rosbash M (2008) Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. Proc Natl Acad Sci U S A 105:19587–19594

    PubMed  CAS  Google Scholar 

  48. Hodge JJ (2009) Ion channels to inactivate neurons in Drosophila. Front Mol Neurosci 2:13

    PubMed  Google Scholar 

  49. Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A, Jegla TJ, Garrity PA (2008) An internal thermal sensor controlling temperature preference in Drosophila. Nature 454:217–220

    PubMed  CAS  Google Scholar 

  50. Pulver SR, Pashkovski SL, Hornstein NJ, Garrity PA, Griffith LC (2009) Temporal dynamics of neuronal activation by channelrhodopsin-2 and TRPA1 determine behavioral output in Drosophila larvae. J Neurophysiol 101:3075–3088

    PubMed  Google Scholar 

  51. Lima SQ, Miesenböck G (2005) Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121:141–152

    PubMed  CAS  Google Scholar 

  52. Schroll C, Riemensperger T, Bucher D, Ehmer J, Völler T, Erbguth K, Gerber B, Hendel T, Nagel G, Buchner E, Fiala A (2006) Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr Biol 16:1741–1747

    PubMed  CAS  Google Scholar 

  53. Fiala A, Suska A, Schlüter OM (2010) Optogenetic approaches in neuroscience. Curr Biol 20:R897–R903

    PubMed  CAS  Google Scholar 

  54. Hoffman AA (1987) A laboratory study of male territoriality in the sibling species Drosophila melanogaster and D. simulans. Anim Behav 35:807–818

    Google Scholar 

  55. Hoffman AA (1987) Territorial encounters between Drosophila males of different sizes. Anim Behav 35:1899–1901

    Google Scholar 

  56. Hoffman AA (1989) Geographic variation in the territorial success of Drosophila melanogaster males. Behav Genet 19:241–255

    Google Scholar 

  57. Hoffman AA (1990) The influence of age and experience with conspecifics on territorial behaviour in Drosophila melanogaster. J Insect Behav 3:1–12

    Google Scholar 

  58. Hoffmann AA (1988) Heritable variation for territorial success in two Drosophila melanogaster populations. Anim Behav 36: 1180–1189

    Google Scholar 

  59. Nilsen SP, Chan YB, Huber R, Kravitz EA (2004) Gender-selective patterns of aggressive behavior in Drosophila melanogaster. Proc Natl Acad Sci U S A 101:12342–12347

    PubMed  CAS  Google Scholar 

  60. Yurkovic A, Wang O, Basu AC, Kravitz EA (2006) Learning and memory associated with aggression in Drosophila melanogaster. Proc Natl Acad Sci U S A 103:17519–17524

    PubMed  CAS  Google Scholar 

  61. Penn JK, Zito MF, Kravitz EA (2010) A single social defeat reduces aggression in a highly aggressive strain of Drosophila. Proc Natl Acad Sci U S A 107:12682–12686

    PubMed  CAS  Google Scholar 

  62. Baier A, Wittek B, Brembs B (2002) Drosophila as a new model organism for the neurobiology of aggression? J Exp Biol 205:1233–1240

    PubMed  Google Scholar 

  63. Certel SJ, Leung A, Lin CY, Perez P, Chiang AS, Kravitz EA (2010) Octopamine neuromodulatory effects on a social behavior decision-making network in Drosophila males. PLoS One 5:e13248

    PubMed  Google Scholar 

  64. Certel SJ, Savella MG, Schlegel DC, Kravitz EA (2007) Modulation of Drosophila male behavioral choice. Proc Natl Acad Sci U S A 104:4706–4711

    PubMed  CAS  Google Scholar 

  65. Chan YB, Kravitz EA (2007) Specific subgroups of FruM neurons control sexually dimorphic patterns of aggression in Drosophila melanogaster. Proc Natl Acad Sci U S A 104:19577–19582

    PubMed  CAS  Google Scholar 

  66. Dierick HA, Greenspan RJ (2007) Serotonin and neuropeptide F have opposite modulatory effects on fly aggression. Nat Genet 39:678–682

    PubMed  CAS  Google Scholar 

  67. Hoyer SC, Eckart A, Herrel A, Zars T, Fischer SA, Hardie SL, Heisenberg M (2008) Octopamine in male aggression of Drosophila. Curr Biol 18:159–167

    PubMed  CAS  Google Scholar 

  68. Johnson O, Becnel J, Nichols CD (2009) Serotonin 5-HT(2) and 5-HT(1A)-like receptors differentially modulate aggressive behaviors in Drosophila melanogaster. Neuroscience 158:1292–1300

    PubMed  CAS  Google Scholar 

  69. Lee G, Hall JC (2000) A newly uncovered phenotype associated with the fruitless gene of Drosophila melanogaster: aggression-like head interactions between mutant males. Behav Genet 30:263–275

    PubMed  CAS  Google Scholar 

  70. Mundiyanapurath S, Chan YB, Leung AK, Kravitz EA (2009) Feminizing cholinergic neurons in a male Drosophila nervous system enhances aggression. Fly (Austin) 3:179–184

    CAS  Google Scholar 

  71. Potter CJ, Luo L (2008) Octopamine fuels fighting flies. Nat Neurosci 11:989–990

    PubMed  CAS  Google Scholar 

  72. Rollmann SM, Zwarts L, Edwards AC, Yamamoto A, Callaerts P, Norga K, Mackay TF, Anholt RR (2008) Pleiotropic effects of Drosophila neuralized on complex behaviors and brain structure. Genetics 179:1327–1336

    PubMed  CAS  Google Scholar 

  73. Zhou C, Rao Y (2008) A subset of octopaminergic neurons are important for Drosophila aggression. Nat Neurosci 11: 1059–1067

    PubMed  CAS  Google Scholar 

  74. Edwards AC, Rollmann SM, Morgan TJ, Mackay TF (2006) Quantitative genomics of aggressive behavior in Drosophila melanogaster. PLoS Genet 2:e154

    PubMed  Google Scholar 

  75. Edwards AC, Ayroles JF, Stone EA, Carbone MA, Lyman RF, Mackay TF (2009) A transcriptional network associated with natural variation in Drosophila aggressive behavior. Genome Biol 10:R76

    PubMed  Google Scholar 

  76. Edwards AC, Zwarts L, Yamamoto A, Callaerts P, Mackay TF (2009) Mutations in many genes affect aggressive behavior in Drosophila melanogaster. BMC Biol 7:29

    PubMed  Google Scholar 

  77. Dierick HA, Greenspan RJ (2006) Molecular analysis of flies selected for aggressive behavior. Nat Genet 38:1023–1031

    PubMed  CAS  Google Scholar 

  78. Ueda A, Wu CF (2009) Effects of social isolation on neuromuscular excitability and aggressive behaviors in Drosophila: altered responses by Hk and gsts1, two mutations implicated in redox regulation. J Neurogenet 23:378–394

    PubMed  CAS  Google Scholar 

  79. Mundiyanapurath S, Certel S, Kravitz EA (2007) Studying aggression in Drosophila (fruit flies). J Vis Exp 2:155

    PubMed  Google Scholar 

  80. Dankert H, Wang L, Hoopfer ED, Anderson DJ, Perona P (2009) Automated monitoring and analysis of social behavior in Drosophila. Nat Methods 6:297–303

    PubMed  CAS  Google Scholar 

  81. Dierick HA (2007) A method for quantifying aggression in male Drosophila melanogaster. Nat Protoc 2:2712–2718

    PubMed  CAS  Google Scholar 

  82. Hardin PE (2005) The circadian timekeeping system of Drosophila. Curr Biol 15:R714–R722

    PubMed  CAS  Google Scholar 

  83. Allada R, Chung BY (2010) Circadian organization of behavior and physiology in Drosophila. Annu Rev Physiol 72:605–624

    PubMed  CAS  Google Scholar 

  84. Nitabach MN, Taghert PH (2008) Organization of the Drosophila circadian control circuit. Curr Biol 18:R84–R93

    PubMed  CAS  Google Scholar 

  85. Shaw P (2003) Awakening to the behavioral analysis of sleep in Drosophila. J Biol Rhythms 18:4–11

    PubMed  Google Scholar 

  86. Harbison ST, Mackay TF, Anholt RR (2009) Understanding the neurogenetics of sleep: progress from Drosophila. Trends Genet 25: 262–269

    PubMed  CAS  Google Scholar 

  87. Crocker A, Sehgal A (2010) Genetic analysis of sleep. Genes Dev 24:1220–1235

    PubMed  CAS  Google Scholar 

  88. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287: 1834–1837

    PubMed  CAS  Google Scholar 

  89. Hendricks JC, Finn SM, Panckeri KA, Chavkin J, Williams JA, Sehgal A, Pack AI (2000) Rest in Drosophila is a sleep-like state. Neuron 25:129–138

    PubMed  CAS  Google Scholar 

  90. Shaw PJ, Tononi G, Greenspan RJ, Robinson DF (2002) Stress response genes protect against lethal effects of sleep deprivation in Drosophila. Nature 417:287–291

    PubMed  CAS  Google Scholar 

  91. Hamblen M, Zehring WA, Kyriacou CP, Reddy P, Yu Q, Wheeler DA, Zwiebel LJ, Konopka RJ, Rosbash M, Hall JC (1986) Germ-line transformation involving DNA from the period locus in Drosophila melanogaster: overlapping genomic fragments that restore circadian and ultradian rhythmicity to per0 and per-mutants. J Neurogenet 3:249–291

    PubMed  CAS  Google Scholar 

  92. Nitz DA, van Swinderen B, Tononi G, Greenspan RJ (2002) Electrophysiological correlates of rest and activity in Drosophila melanogaster. Curr Biol 12:1934–1940

    PubMed  CAS  Google Scholar 

  93. Van Swinderen B, Nitz DA, Greenspan RJ (2004) Uncoupling of brain activity from movement defines arousal states in Drosophila. Curr Biol 14:81–87

    PubMed  Google Scholar 

  94. Kume K, Kume S, Park SK, Hirsh J, Jackson FR (2005) Dopamine is a regulator of arousal in the fruit fly. J Neurosci 25:7377–7384

    PubMed  CAS  Google Scholar 

  95. Lebestky T, Chang JS, Dankert H, Zelnik L, Kim YC, Han KA, Wolf FW, Perona P, Anderson DJ (2009) Two different forms of arousal in Drosophila are oppositely regulated by the dopamine D1 receptor ortholog DopR via distinct neural circuits. Neuron 64:522–536

    PubMed  CAS  Google Scholar 

  96. Yamamoto A, Zwarts L, Callaerts P, Norga K, Mackay TF, Anholt RR (2008) Neurogenetic networks for startle-induced locomotion in Drosophila melanogaster. Proc Natl Acad Sci U S A 105:12393–12398

    PubMed  CAS  Google Scholar 

  97. Wu Z, Gong Z, Feng C, Guo A (2000) An emergent mechanism of selective visual attention in Drosophila. Biol Cybern 82:61–68

    PubMed  CAS  Google Scholar 

  98. van Swinderen B, Flores KA (2007) Attention-like processes underlying optomotor performance in a Drosophila choice maze. Dev Neurobiol 67:129–145

    PubMed  Google Scholar 

  99. O’Dell KM (2003) The voyeurs’ guide to Drosophila melanogaster courtship. Behav Processes 64:211–223

    PubMed  Google Scholar 

  100. Ferveur JF (2010) Drosophila female courtship and mating behaviors: sensory signals, genes, neural structures and evolution. Curr Opin Neurobiol 20:764–769

    PubMed  CAS  Google Scholar 

  101. Siwicki KK, Kravitz EA (2009) Fruitless, doublesex and the genetics of social behavior in Drosophila melanogaster. Curr Opin Neurobiol 19:200–206

    PubMed  CAS  Google Scholar 

  102. Villella A, Gailey DA, Berwald B, Ohshima S, Barnes PT, Hall JC (1997) Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioural analysis of new fru mutants. Genetics 147:1107–1130

    PubMed  CAS  Google Scholar 

  103. Rybak F, Sureau G, Aubin T (2002) Functional coupling of acoustic and chemical signals in the courtship behaviour of the male Drosophila melanogaster. Proc Biol Sci 269:695–701

    PubMed  CAS  Google Scholar 

  104. MacBean IT, Parsons PA (1967) Directional selection for duration of copulation in Drosophila melanogaster. Genetics 56:233–239

    PubMed  CAS  Google Scholar 

  105. Siegel RW, Hall JC (1979) Conditioned responses in courtship behavior of normal and mutant Drosophila. Proc Natl Acad Sci U S A 76:3430–3434

    PubMed  CAS  Google Scholar 

  106. Jallon JM, Hotta Y (1979) Genetic and behavioral studies of female sex appeal in Drosophila. Behav Genet 9:257–275

    PubMed  CAS  Google Scholar 

  107. Ejima A, Griffith LC (2007) Measurement of courtship behavior in Drosophila melanogaster. Cold Spring Harb Protoc. doi:10.1101/pdb.prot4847

  108. Melcher C, Bader R, Pankratz MJ (2007) Amino acids, taste circuits, and feeding behavior in Drosophila: towards understanding the psychology of feeding in flies and man. J Endocrinol 192:467–472

    PubMed  CAS  Google Scholar 

  109. Britton JS, Lockwood WK, Li L, Cohen SM, Edgar BA (2002) Drosophila’s insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev Cell 2:239–249

    PubMed  CAS  Google Scholar 

  110. Junger MA, Rintelen F, Stocker H, Wasserman D, Végh M, Radimerski T, Greenberg ME, Hafen E (2003) The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J Biol 2:20

    PubMed  Google Scholar 

  111. Kramer JM, Davidge JT, Lockyer JM, Staveley BE (2003) Expression of Drosophila FOXO regulates growth and can phenocopy starvation. BMC Dev Biol 3:5

    PubMed  Google Scholar 

  112. Melcher C, Bader R, Walther S, Simakov O, Pankratz MJ (2006) Neuromedin U and its putative Drosophila homolog hugin. PLoS Biol 4:e68

    PubMed  Google Scholar 

  113. Melcher C, Pankratz MJ (2005) Candidate gustatory interneurons modulating feeding behavior in the Drosophila brain. PLoS Biol 3:e305

    PubMed  Google Scholar 

  114. Meng X, Wahlström G, Immonen T, Kolmer M, Tirronen M, Predel R, Kalkkinen N, Heino TI, Sariola H, Roos C (2002) The Drosophila hugin gene codes for myostimulatory and ecdysis-modifying neuropeptides. Mech Dev 117:5–13

    PubMed  CAS  Google Scholar 

  115. Zinke I, Kirchner C, Chao LC, Tetzlaff MT, Pankratz MJ (1999) Suppression of food intake and growth by amino acids in Drosophila: the role of pumpless, a fat body expressed gene with homology to vertebrate glycine cleavage system. Development 126:5275–5284

    PubMed  CAS  Google Scholar 

  116. Brown MR, Crim JW, Arata RC, Cai HN, Chun C, Shen P (1999) Identification of a Drosophila brain-gut peptide related to the neuropeptide Y family. Peptides 20:1035–1042

    PubMed  CAS  Google Scholar 

  117. Shen P, Cai HN (2001) Drosophila neuropeptide F mediates integration of chemosensory stimulation and conditioning of the nervous system by food. J Neurobiol 47:16–25

    PubMed  CAS  Google Scholar 

  118. Wu Q, Zhao Z, Shen P (2005) Regulation of aversion to noxious food by Drosophila neuropeptide Y- and insulin-like systems. Nat Neurosci 8:1350–1355

    PubMed  CAS  Google Scholar 

  119. Wu Q, Zhang Y, Xu J, Shen P (2005) Regulation of hunger-driven behaviors by neural ribosomal S6 kinase in Drosophila. Proc Natl Acad Sci U S A 102:13289–13294

    PubMed  CAS  Google Scholar 

  120. Vosshall LB, Stocker RF (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505–533

    PubMed  CAS  Google Scholar 

  121. Gerber B, Stocker RF, Tanimura T, Thum AS (2009) Smelling, tasting, learning: Drosophila as a study case. Results Probl Cell Differ 47:139–185

    PubMed  CAS  Google Scholar 

  122. Carvalho GB, Kapahi P, Anderson DJ, Benzer S (2006) Allocrine modulation of feeding behavior by the sex peptide of Drosophila. Curr Biol 16:692–696

    PubMed  CAS  Google Scholar 

  123. Prasad NG, Shakarad M, Anitha D, Rajamani M, Joshi A (2001) Correlated responses to selection for faster development and early reproduction in Drosophila: the evolution of larval traits. Evolution 55:1363–1372

    PubMed  CAS  Google Scholar 

  124. Amrein H, Thorne N (2005) Gustatory perception and behavior in Drosophila melanogaster. Curr Biol 15:R673–R684

    PubMed  CAS  Google Scholar 

  125. Wong R, Piper MD, Wertheim B, Partridge L (2009) Quantification of food intake in Drosophila. PLoS One 4:e6063

    PubMed  Google Scholar 

  126. Shiraiwa T, Carlson JR (2007) Proboscis extension response (PER) assay in Drosophila. J Vis Exp 3:193

    PubMed  Google Scholar 

  127. Marella S, Fischler M, Kong P, Asgarian S, Reukhert E, Scott K (2006) Imaging taste response in the fly brain reveals a functional map of taste category and behavior. Neuron 49:285–295

    PubMed  CAS  Google Scholar 

  128. Serway CN, Kaufman RR, Strauss R, de Belle JS (2009) Mushroom bodies enhance initial motor activity in Drosophila. J Neurogenet 23:173–184

    PubMed  Google Scholar 

  129. Strauss R (2002) The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12:633–638

    PubMed  CAS  Google Scholar 

  130. Fry SN, Rohrseitz N, Straw AD, Dickinson MH (2008) TrackFly: virtual reality for a behavioral system analysis in free-flying fruit flies. J Neurosci Methods 171:110–117

    PubMed  Google Scholar 

  131. Straw AD, Lee S, Dickinson MH (2010) Visual control of altitude in flying Drosophila. Curr Biol 20:1550–1556

    PubMed  CAS  Google Scholar 

  132. Straw AD, Branson K, Neumann TR, Dickinson MH (2011) Multi-camera real-time three-dimensional tracking of multiple flying animals. J R Soc Interface 8:395–409

    PubMed  Google Scholar 

  133. Frye MA (2007) Behavioral neurobiology: a vibrating gyroscope controls fly steering maneuvers. Curr Biol 17:R134–R136

    PubMed  CAS  Google Scholar 

  134. Borst A, Haag J, Reiff DF (2010) Fly motion vision. Annu Rev Neurosci 33:49–70

    PubMed  CAS  Google Scholar 

  135. Gotz KG (1980) Visual guidance in Drosophila. Basic Life Sci 16:391–407

    PubMed  CAS  Google Scholar 

  136. Martin JR (2004) A portrait of locomotor behaviour in Drosophila determined by a video-tracking paradigm. Behav Processes 67: 207–219

    PubMed  Google Scholar 

  137. Robie AA, Straw AD, Dickinson MH (2010) Object preference by walking fruit flies, Drosophila melanogaster, is mediated by vision and graviperception. J Exp Biol 213:2494–2506

    PubMed  Google Scholar 

  138. Valente D, Golani I, Mitra PP (2007) Analysis of the trajectory of Drosophila melanogaster in a circular open field arena. PLoS One 2:e1083

    PubMed  Google Scholar 

  139. Strauss R (1998) Automatische Diagnose genetisch bedingter Laufanomalien der Fliege Drosophila bei freier Bewegung in realer und virtueller Umgebung. Forsch Wiss Rechnen GWDG-Bericht Nr 51:53–78

    Google Scholar 

  140. Pick S, Strauss R (2005) Goal-driven behavioral adaptations in gap-climbing Drosophila. Curr Biol 15:1473–1478

    PubMed  CAS  Google Scholar 

  141. Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703–714

    PubMed  CAS  Google Scholar 

  142. Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4:e20

    PubMed  Google Scholar 

  143. Wang JW, Wong AM, Flores J, Vosshall LB, Axel R (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112:271–282

    PubMed  CAS  Google Scholar 

  144. Anholt RR, Lyman RF, Mackay TF (1996) Effects of single P-element insertions on olfactory behavior in Drosophila melanogaster. Genetics 143:293–301

    PubMed  CAS  Google Scholar 

  145. Tully T, Preat T, Boynton SC, Del Vecchio M (1994) Genetic dissection of consolidated memory in Drosophila. Cell 79:35–47

    PubMed  CAS  Google Scholar 

  146. DeZazzo J, Tully T (1995) Dissection of memory formation: from behavioral pharmacology to molecular genetics. Trends Neurosci 18:212–218

    PubMed  CAS  Google Scholar 

  147. Dubnau J, Chiang AS, Tully T (2003) Neural substrates of memory: from synapse to system. J Neurobiol 54:238–253

    PubMed  CAS  Google Scholar 

  148. Isabel G, Pascual A, Preat T (2004) Exclusive consolidated memory phases in Drosophila. Science 304:1024–1027

    PubMed  CAS  Google Scholar 

  149. Joiner MA, Griffith LC (1999) Mapping of the anatomical circuit of CaM kinase-dependent courtship conditioning in Drosophila. Learn Mem 6:177–192

    PubMed  CAS  Google Scholar 

  150. Liu L, Wolf R, Ernst R, Heisenberg M (1999) Context generalization in Drosophila visual learning requires the mushroom bodies. Nature 400:753–756

    PubMed  CAS  Google Scholar 

  151. Putz G, Heisenberg M (2002) Memories in Drosophila heat-box learning. Learn Mem 9:349–359

    PubMed  Google Scholar 

  152. Chiang AS, Blum A, Barditch J, Chen YH, Chiu SL, Regulski M, Armstrong JD, Tully T, Dubnau J (2004) radish encodes a phospholipase-A2 and defines a neural circuit involved in anesthesia-resistant memory. Curr Biol 14:263–272

    PubMed  CAS  Google Scholar 

  153. Xia S, Miyashita T, Fu TF, Lin WY, Wu CL, Pyzocha L, Lin IR, Saitoe M, Tully T, Chiang AS (2005) NMDA receptors mediate olfactory learning and memory in Drosophila. Curr Biol 15:603–615

    PubMed  CAS  Google Scholar 

  154. Skoulakis EM, Grammenoudi S (2006) Dunces and da Vincis: the genetics of learning and memory in Drosophila. Cell Mol Life Sci 63:975–988

    PubMed  CAS  Google Scholar 

  155. Dudai Y, Jan YN, Byers D, Quinn WG, Benzer S (1976) Dunce, a mutant of Drosophila deficient in learning. Proc Natl Acad Sci U S A 73:1684–1688

    PubMed  CAS  Google Scholar 

  156. Livingstone MS, Sziber PP, Quinn WG (1984) Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant. Cell 37:205–215

    PubMed  CAS  Google Scholar 

  157. Levin LR, Han PL, Hwang PM, Feinstein PG, Davis RL, Reed RR (1992) The Drosophila learning and memory gene rutabaga encodes a Ca2+/calmodulin-responsive adenylyl cyclase. Cell 68:479–489

    PubMed  CAS  Google Scholar 

  158. Tempel BL, Livingstone MS, Quinn WG (1984) Mutations in the dopa decarboxylase gene affect learning in Drosophila. Proc Natl Acad Sci U S A 81:3577–3581

    PubMed  CAS  Google Scholar 

  159. Choi KW, Smith RF, Buratowski RM, Quinn WG (1991) Deficient protein kinase C activity in turnip, a Drosophila learning mutant. J Biol Chem 266:15999–16006

    PubMed  CAS  Google Scholar 

  160. Chapman PF, Frenguelli BG, Smith A, Chen CM, Silva AJ (1995) The alpha-Ca2+/calmodulin kinase II: a bidirectional modulator of presynaptic plasticity. Neuron 14:591–597

    PubMed  CAS  Google Scholar 

  161. Grotewiel MS, Beck CD, Wu KH, Zhu XR, Davis RL (1998) Integrin-mediated short-term memory in Drosophila. Nature 391:455–460

    PubMed  CAS  Google Scholar 

  162. Cheng Y, Endo K, Wu K, Rodan AR, Heberlein U, Davis RL (2001) Drosophila fasciclinII is required for the formation of odor memories and for normal sensitivity to alcohol. Cell 105:757–768

    PubMed  CAS  Google Scholar 

  163. Dubnau J, Chiang AS, Grady L, Barditch J, Gossweiler S, McNeil J, Smith P, Buldoc F, Scott R, Certa U, Broger C, Tully T (2003) The staufen/pumilio pathway is involved in Drosophila long-term memory. Curr Biol 13:286–296

    PubMed  CAS  Google Scholar 

  164. Schwaerzel M, Monstirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23:10495–10502

    PubMed  CAS  Google Scholar 

  165. Godenschwege TA, Reisch D, Diegelmann S, Eberle K, Funk N, Heisenberg M, Hoppe V, Hoppe J, Klagges BR, Martin JR, Nikitina EA, Putz G, Reifegerste R, Reisch N, Rister J, Schaupp M, Scholz H, Schwärzel M, Werner U, Zars TD, Buchner S, Buchner E (2004) Flies lacking all synapsins are unexpectedly healthy but are impaired in complex behaviour. Eur J Neurosci 20:611–622

    PubMed  Google Scholar 

  166. Presente A, Boyles RS, Serway CN, de Belle JS, Andres AJ (2004) Notch is required for long-term memory in Drosophila. Proc Natl Acad Sci U S A 101:1764–1768

    PubMed  CAS  Google Scholar 

  167. Stocker RF (1994) The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275:3–26

    PubMed  CAS  Google Scholar 

  168. Stocker RF (2001) Drosophila as a focus in olfactory research: mapping of olfactory sensilla by fine structure, odor specificity, odorant receptor expression, and central connectivity. Microsc Res Tech 55:284–296

    PubMed  CAS  Google Scholar 

  169. Gerber B, Stocker RF (2007) The Drosophila larva as a model for studying chemosensation and chemosensory learning: a review. Chem Senses 32:65–89

    PubMed  CAS  Google Scholar 

  170. Aceves-Pina EO, Quinn WG (1979) Learning in normal and mutant Drosophila larvae. Science 206:93–96

    PubMed  CAS  Google Scholar 

  171. Scherer S, Stocker RF, Gerber B (2003) Olfactory learning in individually assayed Drosophila larvae. Learn Mem 10:217–225

    PubMed  Google Scholar 

  172. Gerber B, Scherer S, Neuser K, Michels B, Hendel T, Stocker RF, Heisenberg M (2004) Visual learning in individually assayed Drosophila larvae. J Exp Biol 207:179–188

    PubMed  CAS  Google Scholar 

  173. Hendel T, Michels B, Neuser K, Schipanski A, Kaun K, Sokolowski MB, Marohn F, Michel R, Heisenberg M, Gerber B (2005) 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

    Google Scholar 

  174. Michels B, Diegelmann S, Tanimoto H, Schwenkert I, Buchner E, Gerber B (2005) A role for synapsin in associative learning: the Drosophila larva as a study case. Learn Mem 12:224–231

    PubMed  Google Scholar 

  175. Yarali A, Hendel T, Gerber B (2006) Olfactory learning and behaviour are ‘insulated’ against visual processing in larval Drosophila. J Comp Physiol A 192:1133–1145

    Google Scholar 

  176. Quinn WG, Harris WA, Benzer S (1974) Conditioned behavior in Drosophila melanogaster. Proc Natl Acad Sci U S A 71:708–712

    PubMed  CAS  Google Scholar 

  177. Jellies JA (1981) Associative olfactory conditioning in Drosophila melanogaster and memory retention through metamorphosis. Master thesis, Illinois State University, Illinois

    Google Scholar 

  178. Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A 157:263–277

    PubMed  CAS  Google Scholar 

  179. Quinn WG, Sziber PP, Booker R (1979) The Drosophila memory mutant amnesiac. Nature 277:212–214

    PubMed  CAS  Google Scholar 

  180. Tempel BL, Bonini N, Dawson DR, Quinn WG (1983) Reward learning in normal and mutant Drosophila. Proc Natl Acad Sci U S A 80:1482–1486

    PubMed  CAS  Google Scholar 

  181. Keene AC, Krashes MJ, Leung B, Bernard JA, Waddell S (2006) Drosophila dorsal paired medial neurons provide a general mechanism for memory consolidation. Curr Biol 16:1524–1530

    PubMed  CAS  Google Scholar 

  182. Krashes MJ, Waddell S (2008) Rapid consolidation to a radish and protein synthesis-dependent long-term memory after single-session appetitive olfactory conditioning in Drosophila. J Neurosci 28:3103–3113

    PubMed  CAS  Google Scholar 

  183. Medioni J, Vaysse G (1975) [Conditional suppression of a reflex in Drosophila ­melanogaster: acquisition and extinction]. C R Seances Soc Biol Fil 169:1386–1391

    PubMed  CAS  Google Scholar 

  184. DeJianne D, McGuire TR, Pruzan-Hotchkiss A (1985) Conditioned suppression of proboscis extension in Drosophila melanogaster. J Comp Psychol 99:74–80

    PubMed  CAS  Google Scholar 

  185. Chabaud MA, Devaud JM, Pham-Delegue MH, Preat T, Kaiser L (2006) Olfactory conditioning of proboscis activity in Drosophila melanogaster. J Comp Physiol A 192:1335–1348

    Google Scholar 

  186. Dill M, Wolf R, Heisenberg M (1993) Visual pattern recognition in Drosophila involves retinotopic matching. Nature 365:751–753

    PubMed  CAS  Google Scholar 

  187. Guo A, Gotz KG (1997) Association of visual objects and olfactory cues in Drosophila. Learn Mem 4:192–204

    PubMed  CAS  Google Scholar 

  188. Xia S, Liu L, Feng C, Guo A (1997) Memory consolidation in Drosophila operant visual learning. Learn Mem 4:205–218

    PubMed  CAS  Google Scholar 

  189. Wolf R, Wittig T, Liu L, Wustmann G, Eyding D, Heisenberg M (1998) Drosophila mushroom bodies are dispensable for visual, tactile, and motor learning. Learn Mem 5:166–178

    PubMed  CAS  Google Scholar 

  190. Brembs B, Heisenberg M (2000) The operant and the classical in conditioned orientation of Drosophila melanogaster at the flight simulator. Learn Mem 7:104–115

    PubMed  CAS  Google Scholar 

  191. Strauss R, Pichler J (1998) Persistence of orientation toward a temporarily invisible landmark in Drosophila melanogaster. J Comp Physiol A 182:411–423

    PubMed  CAS  Google Scholar 

  192. Neuser K, Triphan T, Mronz M, Poeck B, Strauss R (2008) Analysis of a spatial orientation memory in Drosophila. Nature 453:1244–1247

    PubMed  CAS  Google Scholar 

  193. Wustmann G, Heisenberg M (1997) Behavioral manipulation of retrieval in a spatial memory task for Drosophila melanogaster. Learn Mem 4:328–336

    PubMed  CAS  Google Scholar 

  194. Gailey DA, Jackson FR, Siegel RW (1984) Conditioning mutations in Drosophila melanogaster affect an experience-dependent behavioral modification in courting males. Genetics 106:613–623

    PubMed  CAS  Google Scholar 

  195. Ejima A, Smith BP, Lucas C, Levine JD, Griffith LC (2005) Sequential learning of pheromonal cues modulates memory consolidation in trainer-specific associative courtship conditioning. Curr Biol 15:194–206

    PubMed  CAS  Google Scholar 

  196. McBride SM, Giuliani G, Choi C, Krause P, Correale D, Watson K, Baker G, Siwicki KK (1999) Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster. Neuron 24:967–977

    PubMed  CAS  Google Scholar 

  197. Toma DP, White KP, Hirsch J, Greenspan RJ (2002) Identification of genes involved in Drosophila melanogaster geotaxis, a complex behavioral trait. Nat Genet 31:349–353

    PubMed  CAS  Google Scholar 

  198. Mertens I, Vandingenen A, Johnson EC, Shafer OT, Li W, Trigg JS, De Loof A, Schoofs L, Taghert PH (2005) PDF receptor signaling in Drosophila contributes to both circadian and geotactic behaviors. Neuron 48:213–219

    PubMed  CAS  Google Scholar 

  199. Hirsch J (1959) Studies in experimental behavior genetics. II. Individual differences in geotaxis as a function of chromosome variations in synthesized Drosophila populations. J Comp Physiol Psychol 52:304–308

    PubMed  CAS  Google Scholar 

  200. Gong Z (2009) Behavioral dissection of Drosophila larval phototaxis. Biochem Biophys Res Commun 382:395–399

    PubMed  CAS  Google Scholar 

  201. Gong Z, Liu J, Guo C, Zhou Y, Teng Y, Liu L (2010) Two pairs of neurons in the central brain control Drosophila innate light preference. Science 330:499–502

    PubMed  CAS  Google Scholar 

  202. Xiang Y, Yuan Q, Vogt N, Looger LL, Jan LY, Jan YN (2010) Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 468:921–926

    PubMed  CAS  Google Scholar 

  203. Sawin-McCormack EP, Sokolowski MB, Campos AR (1995) Characterization and genetic analysis of Drosophila melanogaster photobehavior during larval development. J Neurogenet 10:119–135

    PubMed  CAS  Google Scholar 

  204. Hadlern NM (1964) Genetic influence on phototaxis in Drosophila melanogaster. Biol Bull 126:264–273

    Google Scholar 

  205. Rein K, Zöckler M, Mader MT, Grübel C, Heisenberg M (2002) The Drosophila standard brain. Curr Biol 12:227–231

    PubMed  CAS  Google Scholar 

  206. Cachero S, Ostrovsky AD, Yu JY, Dickson BJ, Jefferis GSXE (2010) Sexual dimorphism in the fly brain. Curr Biol 20:1589–1601

    PubMed  CAS  Google Scholar 

  207. Chiang AS, Lin CY, Chuang CC, Chang HM, Hsieh CH, Yeh CW, Shih CT, Wu JJ, Wang GT, Chen YC, Wu CC, Chen GY, Ching YT, Lee PC, Lin CY, Lin HH, Wu CC, Hsu HW, Huang YA, Chen JY, Chian HJ, Lu CF, Ni RF, Yeh CY, Hwang JK (2011) Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr Biol 21:1–11

    PubMed  CAS  Google Scholar 

  208. Yu JY, Kanai MI, Demir E, Jefferis GSXE, Dickson BJ (2010) Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr Biol 20:1602–1614

    PubMed  CAS  Google Scholar 

  209. Fujita SC, Zipursky SL, Benzer S, Ferrus A, Shotwell SL (1982) Monoclonal antibodies against the Drosophila nervous system. Proc Natl Acad Sci U S A 79:7929–7933

    PubMed  CAS  Google Scholar 

  210. Hofbauer A (1991) A library of monoclonal antibodies against the brain of Drosophila ­melanogaster. Professorial Dissertation, University of Würzburg, Germany

    Google Scholar 

  211. Hofbauer A, Ebel T, Waltenspiel B, Oswald P, Y-c C, Halder P, Biskup S, Lewandrowski U, Winkler C, Sickmann A, Buchner S, Buchner E (2009) The Wuerzburg hybridoma library against Drosophila brain. J Neurogenet 23:78–91

    PubMed  CAS  Google Scholar 

  212. Goodman CS, Bastiani MJ, Doe CQ, du Lac S, Helfand SL, Kuwada JY, Thomas JB (1984) Cell recognition during neuronal development. Science 225:1271–1279

    PubMed  CAS  Google Scholar 

  213. Zipursky SL, Venkatesh TR, Benzer S (1985) From monoclonal antibody to gene for a neuron-specific glycoprotein in Drosophila. Proc Natl Acad Sci U S A 82:1855–1859

    PubMed  CAS  Google Scholar 

  214. Pfeiffer BD, Jenett A, Hammonds AS, Ngo T-TB, Misra S, Murphy C, Scully A, Carlson JW, Wan KH, Laverty TR, Mungall C, Svirskas R, Kadonaga JT, Doe CQ, Eisen MB, Celniker SE, Rubin GM (2008) Tools for neuroanatomy and neurogenetics in Drosophila. Proc Natl Acad Sci U S A 105:9715–9720

    PubMed  CAS  Google Scholar 

  215. Estes PS, Ho GL, Narayanan R, Ramaswami M (2000) Synaptic localization and restricted diffusion of a Drosophila neuronal synaptobrevin-green fluorescent protein chimera in vivo. J Neurogenet 13:233–255

    PubMed  CAS  Google Scholar 

  216. Zhang YQ, Rodesch CK, Broadie K (2002) Living synaptic vesicle marker: synaptotagmin-GFP. Genesis 34:142–145

    PubMed  CAS  Google Scholar 

  217. Andersen R, Li Y, Resseguie M, Brenman JE (2005) Calcium/calmodulin-dependent protein kinase II alters structural plasticity and cytoskeletal dynamics in Drosophila. J Neurosci 25:8878–8888

    PubMed  CAS  Google Scholar 

  218. Diagana TT, Thomas U, Prokopenko SN, Xiao B, Worley PF, Thomas JB (2002) Mutation of Drosophila homer disrupts control of locomotor activity and behavioral plasticity. J Neurosci 22:428–436

    PubMed  CAS  Google Scholar 

  219. Wang J, Ma X, Yang JS, Zheng X, Zugates CT, Lee CH, Lee T (2004) Transmembrane/juxtamembrane domain-dependent Dscam distribution and function during mushroom body neuronal morphogenesis. Neuron 43:663–672

    PubMed  CAS  Google Scholar 

  220. Nicolaï LJ, Ramaekers A, Raemaekers T, Drozdzecki A, Mauss AS, Yan J, Landgraf M, Annaert W, Hassan BA (2010) Genetically encoded dendritic marker sheds light on neuronal connectivity in Drosophila. Proc Natl Acad Sci U S A 107:20553–20558

    PubMed  Google Scholar 

  221. Yoshihara Y, Mizuno T, Nakahira M, Kawasaki M, Watanabe Y, Kagamiyama H, Jishage K, Ueda O, Suzuki H, Tabuchi K, Sawamoto K, Okano H, Noda T, Mori K (1999) A genetic approach to visualization of multisynaptic neural pathways using plant lectin transgene. Neuron 22:33–41

    PubMed  CAS  Google Scholar 

  222. Pfeiffer BD, Ngo TT, Hibbard KL, Murphy C, Jenett A, Truman JW, Rubin GM (2010) Refinement of tools for targeted gene expression in Drosophila. Genetics 186:735–755

    PubMed  CAS  Google Scholar 

  223. Luan H, Peabody NC, Vinson CR, White BH (2006) Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron 52:425–436

    PubMed  CAS  Google Scholar 

  224. Lai SL, Lee T (2006) Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat Neurosci 9:703–709

    PubMed  CAS  Google Scholar 

  225. Potter CJ, Tasic B, Russler EV, Liang L, Luo L (2010) The Q system: a repressible system for transgene expression, lineage tracing, and mosaic analysis. Cell 141:536–548

    PubMed  CAS  Google Scholar 

  226. Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451–461

    PubMed  CAS  Google Scholar 

  227. Choi CM, Vilain S, Langen M, Van Kelst S, De Geest N, Yan J, Verstreken P, Hassan BA (2009) Conditional mutagenesis in Drosophila. Science 324:54

    PubMed  CAS  Google Scholar 

  228. Marek KW, Davis GW (2002) Transgenically encoded protein photoinactivation (FlAsH-FALI): acute inactivation of synaptotagmin I. Neuron 36:805–813

    PubMed  CAS  Google Scholar 

  229. Venken KJ, Kasprowicz J, Kuenen S, Yan J, Hassan BA, Verstreken P (2008) Recombineering-mediated tagging of Drosophila genomic constructs for in vivo localization and acute protein inactivation. Nucleic Acids Res 36:e114

    PubMed  Google Scholar 

  230. Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, Ikura M, Tsien RY (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388:882–887

    PubMed  CAS  Google Scholar 

  231. Nakai J, Ohkura M, Imoto K (2001) A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat Biotechnol 19:137–141

    PubMed  CAS  Google Scholar 

  232. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6:875–881

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patrick Callaerts .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media, LLC

About this protocol

Cite this protocol

Zwarts, L., Clements, J., Callaerts, P. (2012). Deciphering the Adult Brain: From Neuroanatomy to Behavior. In: Hassan, B. (eds) The Making and Un-Making of Neuronal Circuits in Drosophila. Neuromethods, vol 69. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-61779-830-6_1

Download citation

  • DOI: https://doi.org/10.1007/978-1-61779-830-6_1

  • Published:

  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-61779-829-0

  • Online ISBN: 978-1-61779-830-6

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics