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Genetic Pathways to Circuit Understanding in Drosophila

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Neural Tracing Methods

Part of the book series: Neuromethods ((NM,volume 92))

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Abstract

Genetic tools enable a diverse array of experimental approaches to dissect the relationships between brain function and behavior. Many genetic tools have been developed for use in the fruit fly, Drosophila melanogaster, making it a powerful model system due to its rich behavioral repertoire on one hand and, on the other, the accessible size and scale of its highly stereotyped nervous system. The stereotypy of the fly brain, in particular, makes it possible to interrogate, in essence, the same cell types—genetically, morphologically, physiologically, molecularly, and behaviorally—across individual flies. In this chapter, we describe how genetic tools can be used to target specific cell types in the fly. We then illustrate how these tools can be used to measure or manipulate a cell type’s activity, thereby shedding light on that cell type’s function within an intact circuit. Finally, we describe how tools that directly manipulate genes in a cell-type-specific manner can be used to identify the molecular and cellular mechanisms underlying each cell’s function.

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References

  1. Akerboom J et al (2009) Crystal structures of the GCaMP calcium sensor reveal the mechanism of fluorescence signal change and aid rational design. J Biol Chem 284(10):6455–6464

    CAS  PubMed Central  PubMed  Google Scholar 

  2. Akerboom J et al (2013) Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front Mol Neurosci 6:2

    CAS  PubMed Central  PubMed  Google Scholar 

  3. Akerboom J et al (2012) Optimization of a GCaMP calcium indicator for neural activity imaging. J Neurosci 32(40):13819–13840

    CAS  PubMed Central  PubMed  Google Scholar 

  4. Alekseyenko OV et al (2013) Single dopaminergic neurons that modulate aggression in Drosophila. Proc Natl Acad Sci U S A 110(15):6151–6156

    CAS  PubMed Central  PubMed  Google Scholar 

  5. Asahina K et al (2014) Tachykinin-expressing neurons control male-specific aggressive arousal in Drosophila. Cell 156(1–2):221–235

    CAS  PubMed  Google Scholar 

  6. Baines R et al (2001) Altered electrical properties in Drosophila neurons developing without synaptic transmission. J Neurosci 21(5):1523–1531

    CAS  PubMed  Google Scholar 

  7. Bausenwein B, Fischbach K-F (1992) Activity labeling patterns in the medulla of Drosophila melanogaster caused by motion stimuli. Cell Tissue Res 270(1):25–35

    CAS  PubMed  Google Scholar 

  8. Bausenwein B, Müller NR, Heisenberg M (1994) Behavior-dependent activity labeling in the central complex of Drosophila during controlled visual stimulation. J Comp Neurol 340(2):255–268

    CAS  PubMed  Google Scholar 

  9. Bellen HJ et al (2011) The Drosophila gene disruption project: progress using transposons with distinctive site specificities. Genetics 188(3):731–743

    CAS  PubMed Central  PubMed  Google Scholar 

  10. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118(2):401–415

    CAS  PubMed  Google Scholar 

  11. Cajal R (1909) Histologie du système nerveux de l’homme et des vertébrés

    Google Scholar 

  12. Campos-Ortega JA, Jfirgens G, Hofbauer A (1979) Cell Clones and Pattern Formation : Studies on sevenless, a Mutant of Drosophila melanogaster. Wilhelm Roux’s Arch 50:27–50

    Google Scholar 

  13. Cao G et al (2013) Genetically targeted optical electrophysiology in intact neural circuits. Cell 154(4):904–913

    CAS  PubMed  Google Scholar 

  14. Chan C et al (2011) Article Systematic Discovery of Rab GTPases with Synaptic Functions in Drosophila. Curr Biol 21(20):1704–1715

    CAS  PubMed Central  PubMed  Google Scholar 

  15. Chen C-C et al (2012) Visualizing long-term memory formation in two neurons of the Drosophila brain. Science (NY) 335(6069):678–685

    CAS  Google Scholar 

  16. Chen T-W et al (2013) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499(7458):295–300

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Chiang A-S et al (2011) Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr Biol 21(1):1–11

    CAS  PubMed  Google Scholar 

  18. Clark D et al (2011) Defining the computational structure of the motion detector in Drosophila. Neuron 70(6):1165–1177

    CAS  PubMed Central  PubMed  Google Scholar 

  19. Cox RT, Spradling AC (2003) A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 130(8):1579–1590

    CAS  PubMed  Google Scholar 

  20. Datta SR et al (2008) The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 452(7186):473–477

    CAS  PubMed  Google Scholar 

  21. Davis I et al (1995) A Nuclear GFP That marks Nuclei in Living Drosophila Embryos: Maternal Supply Overcomes a Delay in the Appearance of Zygotic Fluorescence. Dev Biol 170(2):726–729

    CAS  PubMed  Google Scholar 

  22. Denk W, Strickler J, Watt W (1990) Two-Photon Laser Scanning Fluorescence Microscopy. Science 248:73–76

    CAS  PubMed  Google Scholar 

  23. Dietzl G et al (2007) ARTICLES A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448:151–156

    CAS  PubMed  Google Scholar 

  24. Dudai Y, Jan Y (1976) dunce, a mutant of Drosophila deficient in learning. Proc Natl Acad Sci U S A 73(5):1684–1688

    CAS  PubMed Central  PubMed  Google Scholar 

  25. Estes PS et al (2000) Synaptic localization and restricted diffusion of a drosophila neuronal synaptobrevin - Green fluorescent protein Chimera in vivo. J Neurogenet 1(4):233–255

    Google Scholar 

  26. Fan P et al (2013) Genetic and neural mechanisms that inhibit Drosophila from mating with other species. Cell 154(1):89–102

    CAS  PubMed  Google Scholar 

  27. Feinberg EH et al (2008) Neurotechnique GFP reconstitution across synaptic partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 57:353–363

    CAS  PubMed  Google Scholar 

  28. Fiala A et al (2002) Genetically Expressed Cameleon in Drosophila melanogaster Is Used to Visualize Olfactory Information in Projection Neurons. Curr Biol 12(02):1877–1884, http://www.sciencedirect.com/science/article/pii/S0960982202012393

  29. Fire A et al (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391(February):806–811

    CAS  PubMed  Google Scholar 

  30. Fischbach K-F, Dittrich APM (1989) The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res 258:441–475

    Google Scholar 

  31. Fişek M, Wilson RI (2014) Stereotyped connectivity and computations in higher-order olfactory neurons. Nat Neurosci 17(2):280–288

    PubMed  Google Scholar 

  32. Ghosh I et al (2000) Antiparallel leucine zipper-directed protein reassembly: application to the green fluorescent protein department of molecular biophysics and biochemistry the dissection and subsequent reassembly of a protein from peptidic fragments provides an avenue for. Mol Biol Cell 11:5658–5659

    Google Scholar 

  33. Gohl DM et al (2011) A versatile in vivo system for directed dissection of gene expression patterns. Nat Methods 8(3):231–237

    CAS  PubMed Central  PubMed  Google Scholar 

  34. Gonzalez-Bellido PT et al (2009) Overexpressing temperature-sensitive dynamin decelerates phototransduction and bundles microtubules in Drosophila photoreceptors. J Neurosci 29(45):14199–14210

    CAS  PubMed Central  PubMed  Google Scholar 

  35. Gordon MD, Scott K (2009) Motor control in a Drosophila taste circuit. Neuron 61(3):373–384

    CAS  PubMed Central  PubMed  Google Scholar 

  36. Grueber WB et al (2007) Projections of Drosophila multidendritic neurons in the central nervous system: links with peripheral dendrite morphology. Development (Camb) 134(1):55–64

    CAS  Google Scholar 

  37. Hadjieconomou D et al (2011) Flybow: genetic multicolor cell labeling for neural circuit analysis in Drosophila melanogaster. Nat Methods 8(3)

    Google Scholar 

  38. Haikala V et al (2013) Optogenetic Control of Fly Optomotor Responses. J Neurosci 33(34):13927–13934

    CAS  PubMed  Google Scholar 

  39. Hakeda-Suzuki S et al (2011) Golden Goal collaborates with Flamingo in conferring synaptic-layer specificity in the visual system. Nat Neurosci 14(3):314–323

    CAS  PubMed  Google Scholar 

  40. Hall JC (1978) Courtship among males due to a male-sterile mutation in Drosophila melanogaster. Behav Genet 8(2):125–141

    CAS  PubMed  Google Scholar 

  41. Hamada FN et al (2008) An internal thermal sensor controlling temperature preference in Drosophila. Nature 454(7201):217–220

    CAS  PubMed Central  PubMed  Google Scholar 

  42. Hampel S et al (2011) Drosophila Brainbow: a recombinase-based fluorescence labeling technique to subdivide neural expression patterns. Nat Methods 8(3):253–259

    CAS  PubMed Central  PubMed  Google Scholar 

  43. Han C, Jan LY, Jan Y-N (2011) Enhancer-driven membrane markers for analysis of nonautonomous mechanisms reveal neuron-glia interactions in Drosophila. Proc Natl Acad Sci U S A 108(23):9673–9678

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Häsemeyer M et al (2009) Sensory neurons in the Drosophila genital tract regulate female reproductive behavior. Neuron 61(4):511–518

    PubMed  Google Scholar 

  45. Heim N, Griesbeck O (2004) Genetically encoded indicators of cellular calcium dynamics based on troponin C and green fluorescent protein. J Biol Chem 279(14):14280–14286

    CAS  PubMed  Google Scholar 

  46. Hiesinger PR et al (1999) Neuropil pattern formation and regulation of cell adhesion molecules in Drosophila optic lobe development depend on synaptobrevin. J Neurosci 19(17):7548–7556

    CAS  PubMed  Google Scholar 

  47. Horn C et al (2003) piggyBac-based insertional mutagensis and functional insect genomics. Genetics 163(2):647–661

    CAS  PubMed Central  PubMed  Google Scholar 

  48. Hotta Y, Benzer S (1970) Genetic Dissection of the Drosophila Nervous System by Means of Mosaics. Proc Natl Acad Sci U S A 67(3):1156–1163

    CAS  PubMed Central  PubMed  Google Scholar 

  49. Ignell R et al (2009) Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila. Proc Natl Acad Sci U S A 106(31):13070–13075

    CAS  PubMed Central  PubMed  Google Scholar 

  50. Inada K et al (2011) Optical dissection of neural circuits responsible for Drosophila larval locomotion with halorhodopsin. PLoS One 6(12):29019

    Google Scholar 

  51. Jefferis G et al (2001) Target neuron prespecification in the olfactory map of Drosophila. Nature 414(November):204–208

    CAS  PubMed  Google Scholar 

  52. Joesch M et al (2010) ON and OFF pathways in Drosophila motion vision. Nature 468(7321):300–304

    CAS  PubMed  Google Scholar 

  53. Katsov AY, Clandinin TR (2008) Motion processing streams in Drosophila are behaviorally specialized. Neuron 59(2):322–335

    CAS  PubMed Central  PubMed  Google Scholar 

  54. Kennerdell JR, Carthew RW (2000) Heritable gene silencing in Drosophila using double-stranded RNA. Nat Biotechnol 18(8):896–898

    CAS  PubMed  Google Scholar 

  55. Kim J et al (2012) mGRASP enables mapping mammalian synaptic connectivity with light microscopy. Nat Methods 9(1):96–102

    CAS  Google Scholar 

  56. Kim WJ, Jan LY, Jan YN (2013) A PDF/NPF Neuropeptide Signaling Circuitry of Male Drosophila melanogaster Controls Rival-Induced Prolonged Mating. Neuron 80(5):1190–1205

    CAS  PubMed  Google Scholar 

  57. Kimura K-I et al (2008) Fruitless and doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron 59(5):759–769

    CAS  PubMed  Google Scholar 

  58. Kimura K-I et al (2005) Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain. Nature 438(7065):229–233

    CAS  PubMed  Google Scholar 

  59. Kitamoto T (2000) Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. Science (Abstract)

    Google Scholar 

  60. Konopka RJ, Benzer S (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A 68(9):2112–2116

    CAS  PubMed Central  PubMed  Google Scholar 

  61. Lai S-L, Lee T (2006) Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat Neurosci 9(5):703–709

    CAS  PubMed  Google Scholar 

  62. Lee T et al (2000) Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron 25(2):307–316

    CAS  PubMed  Google Scholar 

  63. Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22(3):451–461

    CAS  PubMed  Google Scholar 

  64. Lewandoski M (2001) Conditional control of gene expression in the mouse. Nat Rev Genet 2(10):743–755

    CAS  PubMed  Google Scholar 

  65. Lima SQ, Miesenböck G (2005) Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121(1):141–152

    CAS  PubMed  Google Scholar 

  66. Liu C et al (2012) A subset of dopamine neurons signals reward for odour memory in Drosophila. Nature 488(7412):512–516

    CAS  PubMed  Google Scholar 

  67. Liu G et al (2006) Distinct memory traces for two visual features in the Drosophila brain. Nature 439(7076):551–556

    CAS  PubMed  Google Scholar 

  68. Livet J et al (2007) Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450(7166):56–62

    CAS  PubMed  Google Scholar 

  69. Maisak MS et al (2013) A directional tuning map of Drosophila elementary motion detectors. Nature 500(7461):212–216

    CAS  PubMed  Google Scholar 

  70. Mank M et al (2008) A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat Methods 5(9):805–811

    CAS  PubMed  Google Scholar 

  71. Manoli DS et al (2005) Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436(7049):395–400

    CAS  PubMed  Google Scholar 

  72. Marella S, Mann K, Scott K (2012) Dopaminergic modulation of sucrose acceptance behavior in Drosophila. Neuron 73(5):941–950

    CAS  PubMed Central  PubMed  Google Scholar 

  73. Meinertzhagen I, O’Neil SD (1991) Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J Comp Neurol 305(2):232–263

    CAS  PubMed  Google Scholar 

  74. Mellert DJ, Truman JW (2012) Transvection is common throughout the Drosophila genome. Genetics 191(4):1129–1141

    CAS  PubMed Central  PubMed  Google Scholar 

  75. Melom JE, Littleton JT (2013) Mutation of a NCKX eliminates glial microdomain calcium oscillations and enhances seizure susceptibility. J Neurosci 33(3):1169–1178

    CAS  PubMed Central  PubMed  Google Scholar 

  76. Miesenböck G, Angelis DD, Rothman J (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394(July):192–195

    PubMed  Google Scholar 

  77. Miller M et al (2009) TU-tagging: cell type specific RNA isolation from intact complex tissues. Nat Methods 6(6):439–441

    CAS  PubMed Central  PubMed  Google Scholar 

  78. Minsky M (1961) Microscopy Apparatus., p.US Patent 3,013,467

    Google Scholar 

  79. Miyawaki A et al (1997) Letters to nature fluorescent indicators for Ca 2+ based on green fluorescent proteins and calmodulin. Nature 388:882–887

    CAS  PubMed  Google Scholar 

  80. Morante J, Desplan C (2008) The color-vision circuit in the medulla of Drosophila. Curr Biol 18(8):553–565

    CAS  PubMed Central  PubMed  Google Scholar 

  81. Mosca TJ et al (2005) Dissection of synaptic excitability phenotypes by using a dominant-negative Shaker K + channel subunit. Proc Natl Acad Sci U S A 102(9):3477–3482

    CAS  PubMed Central  PubMed  Google Scholar 

  82. Muzumdar MD et al (2007) A global double-fluorescent Cre reporter mouse. Genesis 605(September):593–605

    Google Scholar 

  83. 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(2):137–141

    CAS  PubMed  Google Scholar 

  84. Ni J-Q et al (2009) A Drosophila resource of transgenic RNAi lines for neurogenetics. Genetics 182(4):1089–1100

    CAS  PubMed Central  PubMed  Google Scholar 

  85. Nitabach MN et al (2008) Electrical Hyperexcitation of Lateral Ventral Pacemaker Neurons Desynchronizes Downstream Circadian Oscillators in the fly circadian circuit and induces multiple behavioral periods. J Neurosci 26(2):479–489

    Google Scholar 

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

    PubMed Central  PubMed  Google Scholar 

  87. Otsuna H, Ito KEI (2006) Systematic analysis of the visual projection neurons of Drosophila melanogaster. I Lobula-Specific Pathways. J Comp Neurol 497:928–958

    PubMed  Google Scholar 

  88. Peled ES, Isacoff EY (2011) Optical quantal analysis of synaptic transmission in wild-type and rab3-mutant Drosophila motor axons. Nat Neurosci 14(4):519–526

    CAS  PubMed  Google Scholar 

  89. Pfeiffer BD et al (2008) Tools for neuroanatomy and neurogenetics in Drosophila. Proc Natl Acad Sci U S A 105(28):9715–9720

    CAS  PubMed Central  PubMed  Google Scholar 

  90. Pfeiffer BD, Truman JW, Rubin GM (2012) Using translational enhancers to increase transgene expression in Drosophila. Proc Natl Acad Sci U S A 109(17):6626–6631

    CAS  PubMed Central  PubMed  Google Scholar 

  91. von Philipsborn AC et al (2011) Article Neuronal Control of Drosophila Courtship Song. Neuron 69(3):509–522

    CAS  PubMed  Google Scholar 

  92. Pielage J et al (2008) A presynaptic giant ankyrin stabilizes the NMJ through regulation of presynaptic microtubules and transsynaptic cell adhesion. Neuron 58(2):195–209

    CAS  PubMed Central  PubMed  Google Scholar 

  93. Pilling AD et al (2006) Kinesin-1 and dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. PLoS One 17(4):2057–2068

    CAS  Google Scholar 

  94. Potter C et al (2010) The Q System : A Repressible Binary System for Transgene Expression, Lineage Tracing, and Mosaic Analysis. Cell 141(3):536–548

    CAS  PubMed Central  PubMed  Google Scholar 

  95. Reiff DF, Thiel PR, Schuster CM (2002) Differential regulation of active zone density during long-term strengthening of Drosophila neuromuscular junctions. J Neurosci 22(21):9399–9409

    CAS  PubMed  Google Scholar 

  96. Root CM et al (2009) A Presynaptic Gain Control Mechanism Fine-Tunes Olfactory Behavior. Neuron 59(2):311–321

    Google Scholar 

  97. Rust MJ, Bates M, Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3(10):793–795

    CAS  PubMed Central  PubMed  Google Scholar 

  98. Ruta V et al (2010) sensory input to descending output. Nature 468(7324):686–690

    CAS  PubMed  Google Scholar 

  99. Schnell B et al (2012) Columnar cells necessary for motion responses of wide-field visual interneurons in Drosophila. J Comp Physiol

    Google Scholar 

  100. Schroll C et al (2006) Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr Biol 16(17):1741–1747

    CAS  PubMed  Google Scholar 

  101. Siddiqi O, Seymour B (1976) Neurophysiological defects in temperature-sensitive paralytic mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A 73(9):3253–3257

    CAS  PubMed Central  PubMed  Google Scholar 

  102. Silies M et al (2013) Modular Use of Peripheral Input Channels Tunes Motion-Detecting Circuitry. Neuron 79(1):111–127

    CAS  PubMed Central  PubMed  Google Scholar 

  103. Stocker R et al (1990) Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262:9–34

    CAS  PubMed  Google Scholar 

  104. Stockinger P, Kvitsiani D, Rotkopf S et al (2005) Neural circuitry that governs Drosophila male courtship behavior. Cell 121(5):795–807

    CAS  PubMed  Google Scholar 

  105. Strausfeld NJ (1976) Atlas of an insect brain. Springer-Verlag, New York

    Google Scholar 

  106. Sun XR et al (2013) Fast GCaMPs for improved tracking of neuronal activity. Nat Commun 4:2170

    PubMed  Google Scholar 

  107. Suzuki DT, Grigliatti T, Williamson R (1971) A mutation ( parats) causing reversible adult paralysis. Proc Natl Acad Sci U S A 68(5):890–893

    CAS  PubMed Central  PubMed  Google Scholar 

  108. Sweeney ST et al (1995) Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14(2):341–351

    CAS  PubMed  Google Scholar 

  109. Takemura S et al (2013) A visual motion detection circuit suggested by Drosophila connectomics. Nature 500(7461):175–181

    CAS  PubMed Central  PubMed  Google Scholar 

  110. Takemura S et al (2011) Cholinergic circuits integrate neighboring visual signals in a Drosophila motion detection pathway. Curr Biol 21(24):2077–2084

    CAS  PubMed Central  PubMed  Google Scholar 

  111. Takemura S-Y, Lu Z, Meinertzhagen I (2008) Synaptic circuits of the Drosophila optic lobe: the input terminals to the medulla. J Comp Neurol 509(5):493–513

    PubMed Central  PubMed  Google Scholar 

  112. Thestrup T et al (2014) Optimized ratiometric calcium sensors for functional in vivo imaging of neurons and T lymphocytes. Nat Methods 11(2):175–182

    CAS  PubMed  Google Scholar 

  113. Tian L et al (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6(12):875–881

    CAS  PubMed Central  PubMed  Google Scholar 

  114. Ting C-Y (2014) Photoreceptor-derived activin promotes dendritic termination and restricts the receptive fields of first-order interneurons in Drosophila. Neuron pp 1–17

    Google Scholar 

  115. Tuthill JC et al (2013) Contributions of the 12 neuron classes in the fly lamina to motion vision. Neuron 79(1):128–140

    CAS  PubMed Central  PubMed  Google Scholar 

  116. De Vries SEJ, Clandinin TR (2012) Loom-sensitive neurons link computation to action in the Drosophila visual system. Curr Biol 22(5):353–362

    PubMed Central  PubMed  Google Scholar 

  117. Wang JW et al (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112(2):271–282

    CAS  PubMed  Google Scholar 

  118. Wang Q et al (2008) Structural basis for calcium sensing by GCaMP2. Structure (Lond 1993) 16(12):1817–1827

    CAS  Google Scholar 

  119. White BH et al (2001) Targeted attenuation of electrical activity in Drosophila using a genetically modified K(+) channel. Neuron 31(5):699–711

    CAS  PubMed  Google Scholar 

  120. Wong AM, Wang JW, Axel R (2002) Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109(2):229–241

    CAS  PubMed  Google Scholar 

  121. Wu C-L et al (2013) An octopamine-mushroom body circuit modulates the formation of anesthesia-resistant memory in Drosophila. Curr Biol 23(23):2346–2354

    CAS  PubMed  Google Scholar 

  122. Xu T, Rubin GM (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development (Camb) 117(4):1223–1237

    CAS  Google Scholar 

  123. Yang C-H et al (2009) Control of the postmating behavioral switch in Drosophila females by internal sensory neurons. Neuron 61(4):519–526

    CAS  PubMed Central  PubMed  Google Scholar 

  124. Yang Z, Edenberg HJ, Davis RL (2005) Isolation of mRNA from specific tissues of Drosophila by mRNA tagging. Nucleic Acids Res 33(17):e148

    PubMed Central  PubMed  Google Scholar 

  125. Yapici N et al (2008) A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 451(7174):33–37

    PubMed  Google Scholar 

  126. Yu JY et al (2010) Article Cellular Organization of the Neural Circuit that Drives Drosophila Courtship Behavior. Curr Biol 20(18):1602–1614

    CAS  PubMed  Google Scholar 

  127. Zars T (2000) Localization of a Short-Term Memory in Drosophila. Science 288(5466):672–675

    CAS  PubMed  Google Scholar 

  128. Zhang YQ, Rodesch CK, Broadie K (2002) Living synaptic vesicle marker: synaptotagmin-GFP. Genesis (NY) 34(1–2):142–145

    CAS  Google Scholar 

  129. Zhao Y et al (2011) An expanded palette of genetically encoded Ca2+ indicators. Science 1888(2011)

    Google Scholar 

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Authors and Affiliations

  1. Department of Neurobiology, Stanford University, 299 W. Campus Drive, Stanford, CA, 94305, USA

    Jennifer J. Esch, Yvette E. Fisher, Jonathan C. S. Leong & Thomas R. Clandinin

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  1. Jennifer J. Esch
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  2. Yvette E. Fisher
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  3. Jonathan C. S. Leong
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  4. Thomas R. Clandinin
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Correspondence to Thomas R. Clandinin .

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  1. Baylor College of Medicine, Houston, Texas, USA

    Benjamin R. Arenkiel

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Esch, J.J., Fisher, Y.E., Leong, J.C.S., Clandinin, T.R. (2015). Genetic Pathways to Circuit Understanding in Drosophila. In: Arenkiel, B. (eds) Neural Tracing Methods. Neuromethods, vol 92. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-1963-5_12

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