Optical calcium imaging in the nervous system of Drosophila melanogaster

Biochimica et Biophysica Acta - General Subjects

Volumn 1820, Issue 8, 2012, Pages 1169-1178

  Riemensperger, Thomas ^a   Pech, Ulrike ^a   Dipt, Shubham ^a   Fiala, André ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Calcium sensor protein; Drosophila; Genetically encoded fluorescence sensor; Neuronal processing; Optical calcium imaging

Indexed keywords

CALCIUM ION; GENETICALLY ENCODED CALCIUM SENSOR; GREEN FLUORESCENT PROTEIN; NEURONAL CALCIUM SENSOR; UNCLASSIFIED DRUG;

AUDITORY STIMULATION; BINARY GENE EXPRESSION SYSTEM; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; CALCIUM BINDING; CALCIUM CELL LEVEL; CELL MEMBRANE DEPOLARIZATION; DNA SEQUENCE; DROSOPHILA MELANOGASTER; FLUORESCENCE IMAGING; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION SYSTEM; GENE SEQUENCE; GUSTATORY RECEPTOR GENE; MOLECULAR GENETICS; MOLECULAR IMAGING; NERVE CELL PLASTICITY; NONHUMAN; OLFACTORY SYSTEM; OPTICAL CALCIUM IMAGING; PRIORITY JOURNAL; RECEPTOR GENE; REVIEW; SENSORY RECEPTOR; SENSORY STIMULATION; TRANSGENIC ANIMAL; UPSTREAM ACTIVATOR SEQUENCE; VISUAL STIMULATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BRAIN; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; DROSOPHILA MELANOGASTER; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; LARVA; OLFACTORY PERCEPTION; RECOMBINANT FUSION PROTEINS;

DROSOPHILA MELANOGASTER;

EID: 84862121585     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2012.02.013     Document Type: Review

References (131)

1. G.M. Rubin Drosophila melanogaster as an experimental organism Science 240 1988 1453 1459
2. K.F. Fischbach, and M. Heisenberg Structural brain mutant of Drosophila melanogaster with reduced cell number in the medulla cortex and with normal optomotor yaw response Proc. Natl. Acad. Sci. U. S. A. 78 1981 1105 1109 (Pubitemid 11102168)
3. M. Heisenberg, A. Borst, S. Wagner, and D. Byers Drosophila mushroom body mutants are deficient in olfactory learning J. Neurogenet. 2 1985 1 30 (Pubitemid 15148068)
4. R. Strauss, and M. Heisenberg A higher control center of locomotor behavior in the Drosophila brain J. Neurosci. 13 1993 1852 1861 (Pubitemid 23113400)
5. K.S. Broadie Synaptogenesis in Drosophila: coupling genetics and electrophysiology J. Physiol. Paris 88 1994 123 139 (Pubitemid 24311393)
6. P. Clyne, A. Grant, R. O'Connell, and J.R. Carlson Odorant response of individual sensilla on the Drosophila antenna Invert. Neurosci. 3 1997 127 135 (Pubitemid 28433009)
7. R.I. Wilson, G.C. Turner, and G. Laurent Transformation of olfactory representations in the Drosophila antennal lobe Science 303 2004 366 370 (Pubitemid 38095775)
8. A. Fiala Olfaction and olfactory learning in Drosophila: recent progress Curr. Opin. Neurobiol. 17 2007 720 726
9. C. Montell A taste of the Drosophila gustatory receptors Curr. Opin. Neurobiol. 19 2009 345 353
10. A. Borst Drosophila's view on insect vision Curr. Biol. 19 2009 36 47
11. N. Peschel, and C. Helfrich-Förster Setting the clock - by nature: circadian rhythm in the fruitfly Drosophila melanogaster FEBS Lett. 585 2011 1435 1442
12. D.R. Nässel, and A.M. Winther Drosophila neuropeptides in regulation of physiology and behavior Prog. Neurobiol. 92 2010 42 104
13. E. Buchner, S. Buchner, and R. Hengstenberg 2-Deoxy-d-glucose maps movement-specific nervous activity in the second visual ganglion of Drosophila Science 205 1997 687 688
14. E. Buchner, and S. Buchner Mapping stimulus-induced nervous activity in small brains by [3H]2-deoxy-d-glucose Cell Tissue Res. 211 1980 51 64 (Pubitemid 11231944)
15. V. Rodrigues, and E. Buchner [3H]2-deoxyglucose mapping of odor-induced neuronal activity in the antennal lobes of Drosophila melanogaster Brain Res. 324 1984 374 378 (Pubitemid 15195976)
16. K.J. Venken, J.H. Simpson, and H.J. Bellen Genetic manipulation of genes and cells in the nervous system of the fruit fly Neuron 72 2011 202 230
17. A.E. Palmer, and R.Y. Tsien Measuring calcium signaling using genetically targetable fluorescent indicators Nat. Protoc. 1 2006 1057 1065
18. M. Mank, and O. Griesbeck Genetically encoded calcium indicators Chem. Rev. 108 2008 1550 1564 (Pubitemid 351796397)
19. S.A. Hires, L. Tian, and L.L. Looger Reporting neural activity with genetically encoded calcium indicators Brain Cell Biol. 36 2008 69 86
20. G. Miesenböck, D.A. De Angelis, and J.E. Rothman Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins Nature 394 1998 192 195 (Pubitemid 28325974)
21. A.Y. Ting, K.H. Kain, R.L. Klemke, and R.Y. Tsien Genetically encoded fluorescent reporters of protein tyrosine kinase activities in living cells Proc. Natl. Acad. Sci. U. S. A. 98 2001 15003 15008 (Pubitemid 34013959)
22. J. Zhang, Y. Ma, S.S. Taylor, and R.Y. Tsien Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering Proc. Natl. Acad. Sci. U. S. A. 98 2001 14997 15002 (Pubitemid 34013958)
23. M. Sato, T. Ozawa, K. Inukai, T. Asano, and Y. Umezawa Fluorescent indicators for imaging protein phosphorylation in single living cells Nat. Biotechnol. 20 2002 287 294 (Pubitemid 34205423)
24. J.D. Violin, J. Zhang, R.Y. Tsien, and A.C. Newton A genetically encoded fluorescent reporter reveals oscillatory phosphorylation by protein kinase C J. Cell Biol. 161 2003 899 909 (Pubitemid 36718423)
25. D. Willoughby, and D.M. Cooper Live-cell imaging of cAMP dynamics Nat. Methods 5 2008 29 36
26. H. Mutoh, A. Perron, W. Akemann, Y. Iwamoto, and T. Knöpfel Optogenetic monitoring of membrane potentials Exp. Physiol. 96 2011 13 18
27. M.J. Berridge Neuronal calcium signaling Neuron 21 1998 13 26 (Pubitemid 28355688)
28. 2+ based on green fluorescent proteins and calmodulin Nature 388 1997 882 887 (Pubitemid 27377061)
29. 2+-dependent changes in the fluorescence emission of an indicator composed of two green fluorescent protein variants linked by a calmodulin-binding sequence. A new class of fluorescent indicators J. Biol. Chem. 272 1997 13270 13274 (Pubitemid 27216756)
30. A. Fiala, T. Spall, S. Diegelmann, B. Eisermann, S. Sachse, J.M. Devaud, E. Buchner, and C.G. Galizia Genetically expressed cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons Curr. Biol. 12 2002 1877 1884 (Pubitemid 35273910)
31. N. Heim, and O. Griesbeck Genetically encoded indicators of cellular calcium dynamics based on troponin C and green fluorescent protein J. Biol. Chem. 279 2004 14280 14286 (Pubitemid 38468968)
32. G.S. Baird, D.A. Zacharias, and R.Y. Tsien Circular permutation and receptor insertion within green fluorescent proteins Proc. Natl. Acad. Sci. U. S. A. 96 1999 11241 11246 (Pubitemid 29487365)
33. 2+ Proc. Natl. Acad. Sci. U. S. A. 98 2001 3197 3202 (Pubitemid 32220822)
34. 2+) probe composed of a single green fluorescent protein Nat. Biotechnol. 19 2001 137 141 (Pubitemid 32144441)
35. 2+ measurements using improved cameleons Proc. Natl. Acad. Sci. U. S. A. 96 1999 2135 2140 (Pubitemid 29117880)
36. O. Griesbeck, G.S. Baird, R.E. Campbell, D.A. Zacharias, and R.Y. Tsien Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications J. Biol. Chem. 276 2001 29188 29194
37. 2+ analyzed with an improved genetically encoded fluorescent sensor Proc. Natl. Acad. Sci. U. S. A. 101 2004 17404 17409 (Pubitemid 39657417)
38. 2+) by circularly permuted yellow fluorescent proteins Proc. Natl. Acad. Sci. U. S. A. 101 2004 10554 10559 (Pubitemid 38955780)
39. 2+ indicators based on computationally redesigned calmodulin-peptide pairs Chem. Biol. 13 2006 521 530 (Pubitemid 43729506)
40. 2+ imaging by a new calmodulin-GFP fusion molecule Nat. Struct. Biol. 8 2001 1069 1073 (Pubitemid 33101629)
41. 2+) indicators, yellow Cameleon-Nano Nat. Methods 7 2010 729 732
42. M. Mank, D.F. Reiff, N. Heim, M.W. Friedrich, A. Borst, and O. Griesbeck A FRET-based calcium biosensor with fast signal kinetics and high fluorescence change Biophys. J. 90 2006 1790 1796
43. N. Heim, O. Garaschuk, M.W. Friedrich, M. Mank, R.I. Milos, Y. Kovalchuk, A. Konnerth, and O. Griesbeck Improved calcium imaging in transgenic mice expressing a troponin C-based biosensor Nat. Methods 4 2007 127 129 (Pubitemid 46454679)
44. M. Mank, A.F. Santos, S. Direnberger, T.D. Mrsic-Flogel, S.B. Hofer, V. Stein, T. Hendel, D.F. Reiff, C. Levelt, A. Borst, T. Bonhoeffer, M. Hübener, and O. Griesbeck A genetically encoded calcium indicator for chronic in vivo two-photon imaging Nat. Methods 5 2008 805 811
45. 2+ imaging of dendritic spines Anal. Chem. 77 2005 5861 5869 (Pubitemid 41324284)
46. 2+ indicator GCaMP2 Proc. Natl. Acad. Sci. U. S. A. 103 2006 4753 4758
47. L. Tian, S.A. Hires, T. Mao, D. Huber, M.E. Chiappe, S.H. Chalasani, L. Petreanu, J. Akerboom, S.A. McKinney, E.R. Schreiter, C.I. Bargmann, V. Jayaraman, K. Svoboda, and L.L. Looger Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators Nat. Methods 6 2009 875 881
48. A. Muto, M. Ohkura, T. Kotani, S. Higashijima, J. Nakai, and K. Kawakami Genetic visualization with an improved GCaMP calcium indicator reveals spatiotemporal activation of the spinal motor neurons in zebrafish Proc. Natl. Acad. Sci. U. S. A. 108 2011 5425 5430
49. D.F. Reiff, A. Ihring, G. Guerrero, E.Y. Isacoff, M. Joesch, J. Nakai, and A. Borst In vivo performance of genetically encoded indicators of neural activity in flies J. Neurosci. 25 2005 4766 4778 (Pubitemid 40664125)
50. T. Hendel, M. Mank, B. Schnell, O. Griesbeck, A. Borst, and D.F. Reiff Fluorescence changes of genetic calcium indicators and OGB-1 correlated with neural activity and calcium in vivo and in vitro J. Neurosci. 28 2008 7399 7411
51. A. Fiala, and T. Spall In vivo calcium imaging of brain activity in Drosophila by transgenic cameleon expression Sci. STKE 174 2003 PL6
52. A. Kamikouchi, R. Wiek, T. Effertz, M.C. Göpfert, and A. Fiala Transcuticular optical imaging of stimulus-evoked neural activities in the Drosophila peripheral nervous system Nat. Protoc. 5 2010 1229 1235
53. M.D. Adams The genome sequence of Drosophila melanogaster Science 287 2000 2185 2195 (Pubitemid 30177013)
54. G.M. Rubin, and A.C. Spradling Genetic transformation of Drosophila with transposable element vectors Science 218 1982 348 353 (Pubitemid 12037603)
55. J.A. Fischer, E. Giniger, T. Maniatis, and M. Ptashne GAL4 activates transcription in Drosophila Nature 332 1988 853 856
56. A.H. Brand, and N. Perrimon Targeted gene expression as a means of altering cell fates and generating dominant phenotypes Development 118 1993 401 415 (Pubitemid 23214028)
57. http://flystocks.bio.indiana.edu/.
58. http://www.dgrc.kit.ac.jp/en/index.html.
59. J.B. Duffy GAL4 system in Drosophila: a fly geneticist's Swiss army knife Genesis 34 2002 1 15
60. B.D. Pfeiffer, T.T. Ngo, K.L. Hibbard, C. Murphy, A. Jenett, J.W. Truman, and G.M. Rubin Refinement of tools for targeted gene expression in Drosophila Genetics 186 2010 735 755
61. D. Szüts, and M. Bienz LexA chimeras reveal the function of Drosophila Fos as a context-dependent transcriptional activator Proc. Natl. Acad. Sci. U. S. A. 97 2000 5351 5356 (Pubitemid 30313722)
62. S.L. Lai, and T. Lee Genetic mosaic with dual binary transcriptional systems in Drosophila Nat. Neurosci. 9 2006 703 709 (Pubitemid 44012270)
63. C.J. Potter, B. Tasic, E.V. Russler, L. Liang, and L. Luo The Q system: a repressible binary system for transgene expression, lineage tracing, and mosaic analysis Cell 141 2010 536 548
64. C.J. Potter, and L. Luo Using the Q system in Drosophila melanogaster Nat. Protoc. 6 2011 1105 1120
65. T. Lee, and L. Luo Mosaic analysis with a repressible neurotechnique cell marker for studies of gene function in neuronal morphogenesis Neuron 22 1999 451 461 (Pubitemid 29159845)
66. D.F. Reiff, P.R. Thiel, and C.M. Schuster Differential regulation of active zone density during long-term strengthening of Drosophila neuromuscular junctions J. Neurosci. 22 2002 9399 9409 (Pubitemid 35356183)
67. P.J. Clyne, C.G. Warr, M.R. Freeman, D. Lessing, J. Kim, and J.R. Carlson A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila Neuron 22 1999 327 338 (Pubitemid 29109666)
68. L.B. Vosshall, H. Amrein, P.S. Morozov, A. Rzhetsky, and R. Axel A spatial map of olfactory receptor expression in the Drosophila antenna Cell 96 1999 725 736 (Pubitemid 29122814)
69. R. Benton, K.S. Vannice, C. Gomez-Diaz, and L.B. Vosshall Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila Cell 136 2009 149 162
70. P.J. Clyne, C.G. Warr, and J.R. Carlson Candidate taste receptors in Drosophila Science 287 2000 1830 1834 (Pubitemid 30143969)
71. K. Scott, R. Brady Jr., A. Cravchik, P. Morozov, A. Rzhetsky, C. Zuker, and R. Axel A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila Cell 104 2001 661 673 (Pubitemid 32241017)
72. W.D. Tracey Jr., R.I. Wilson, G. Laurent, and S. Benzer painless, a Drosophila gene essential for nociception Cell 113 2003 261 273 (Pubitemid 36514976)
73. Y. Lee, Y. Lee, J. Lee, S. Bang, S. Hyun, J. Kang, S.T. Hong, E. Bae, B.K. Kaang, and J. Kim Pyrexia is a new thermal transient receptor potential channel endowing tolerance to high temperatures in Drosophila melanogaster Nat. Genet. 37 2005 305 310 (Pubitemid 41716259)
74. M. Rosenzweig, K.M. Brennan, T.D. Tayler, P.O. Phelps, A. Patapoutian, and P.A. Garrity The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis Genes Dev. 19 2005 419 424 (Pubitemid 40256272)
75. M. Rosenzweig, K. Kang, and P.A. Garrity Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster Proc. Natl. Acad. Sci. U. S. A. 2008 14668 14673
76. F.N. Hamada, M. Rosenzweig, K. Kang, S.R. Pulver, A. Ghezzi, T.J. Jegla, and P.A. Garrity An internal thermal sensor controlling temperature preference in Drosophila Nature 454 2008 217 220 (Pubitemid 351969888)
77. M. Gallio, T.A. Ofstad, L.J. Macpherson, J.W. Wang, and C.S. Zuker The coding of temperature in the Drosophila brain Cell 144 2011 614 624
78. A. Kamikouchi, T. Shimada, and K. Ito Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster J. Comp. Neurol. 499 2006 317 356 (Pubitemid 44571933)
79. A. Kamikouchi, H.K. Inagaki, T. Effertz, O. Hendrich, A. Fiala, M.C. Göpfert, and K. Ito The neural basis of Drosophila gravity-sensing and hearing Nature 458 2009 165 171
80. S. Yorozu, A. Wong, B.J. Fischer, H. Dankert, M.J. Kernan, A. Kamikouchi, K. Ito, and D.J. Anderson Distinct sensory representations of wind and near-field sound in the Drosophila brain Nature 458 2009 201 205
81. T. Effertz, R. Wiek, and M.C. Göpfert NompC TRP channel is essential for Drosophila sound receptor function Curr. Biol. 21 2011 592 597
82. L.B. Vosshall, and R.F. Stocker Molecular architecture of smell and taste in Drosophila Annu. Rev. Neurosci. 30 2007 505 533 (Pubitemid 47218766)
83. C.G. Galizia, and S. Sachse Odor coding in insects A. Menini, The Neurobiology of Olfaction 2010 CRC Press Boca Raton (FL) chapter 2
84. J.W. Wang, A.M. Wong, J. Flores, L.B. Vosshall, and R. Axel Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain Cell 112 2003 271 282 (Pubitemid 36144115)
85. J. Joerges, A. Kuettner, C.G. Galizia, and R. Menzel Representations of odors and odor mixtures visualized in the honeybee brain Nature 387 1997 285 288 (Pubitemid 27220763)
86. C.G. Galizia, R. Menzel, and B. Hölldobler Optical imaging of odor-evoked glomerular activity patterns in the antennal lobes of the ant Camponotus rufipes Naturwissenschaften 86 1999 533 537 (Pubitemid 29533687)
87. C.G. Galizia, S. Sachse, and H. Mustaparta Calcium responses to pheromones and plant odours in the antennal lobe of the male and female moth Heliothis virescens J. Comp. Physiol. A 186 2000 1049 1063
88. A.F. Silbering, and C.G. Galizia Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions J. Neurosci. 27 2007 11966 11977 (Pubitemid 350072114)
89. A.F. Silbering, R. Okada, K. Ito, and C.G. Galizia Olfactory information processing in the Drosophila antennal lobe: anything goes? J. Neurosci. 28 2008 13075 13087
90. T. Niewalda, T. Völler, C. Eschbach, J. Ehmer, W.C. Chou, M. Timme, A. Fiala, and B. Gerber A combined perceptual, physico-chemical, and imaging approach to 'odour-distances' suggests a categorizing function of the Drosophila antennal lobe PLoS One 6 2011 e24300
91. S. Sachse, E. Rueckert, A. Keller, R. Okada, N.K. Tanaka, K. Ito, and L.B. Vosshall Activity-dependent plasticity in an olfactory circuit Neuron 56 2007 838 850 (Pubitemid 350181354)
92. E.A. Hallem, A. Dahanukar, and J.R. Carlson Insect odor and taste receptors Annu. Rev. Entomol. 51 2006 113 135 (Pubitemid 43107817)
93. S. Marella, W. Fischler, P. Kong, S. Asgarian, E. Rueckert, and K. Scott Imaging taste responses in the fly brain reveals a functional map of taste category and behavior Neuron 49 2006 285 295 (Pubitemid 43089644)
94. M. Hiroi, N. Meunier, F. Marion-Poll, and T. Tanimura Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila J. Neurobiol. 61 2004 333 342 (Pubitemid 39546359)
95. A. Dahanukar, Y.T. Lei, J.Y. Kwon, and J.R. Carlson Two Gr genes underlie sugar reception in Drosophila Neuron 56 2007 503 516 (Pubitemid 350026272)
96. L.A. Weiss, A. Dahanukar, J.Y. Kwon, D. Banerjee, and J.R. Carlson The molecular and cellular basis of bitter taste in Drosophila Neuron 69 2011 258 272
97. P. Cameron, M. Hiroi, J. Ngai, and K. Scott The molecular basis for water taste in Drosophila Nature 465 2010 91 95
98. W. Fischler, P. Kong, S. Marella, and K. Scott The detection of carbonation by the Drosophila gustatory system Nature 448 2007 1054 1057 (Pubitemid 47345591)
99. D.F. Reiff, J. Plett, M. Mank, O. Griesbeck, and A. Borst Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila Nat. Neurosci. 13 2010 973 978
100. Y. Wang, A. Mamiya, A.S. Chiang, and Y. Zhong Imaging of an early memory trace in the Drosophila mushroom body J. Neurosci. 28 2008 4368 4376
101. D. Yu, D.B. Akalal, and R.L. Davis Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning Neuron 52 2006 845 855 (Pubitemid 44828452)
102. D.B. Akalal, D. Yu, and R.L. Davis A late-phase, long-term memory trace forms in the γ neurons of Drosophila mushroom bodies after olfactory classical conditioning J. Neurosci. 30 2010 16699 16708
103. K.S. Honegger, R.A. Campbell, and G.C. Turner Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body J. Neurosci. 31 2011 11772 11785
104. M. Heisenberg Mushroom body memoir: from maps to models Nat. Rev. Neurosci. 4 2003 266 275 (Pubitemid 37271372)
105. G.U. Busto, I. Cervantes-Sandoval, and R.L. Davis Olfactory learning in Drosophila Physiology (Bethesda) 25 2010 338 346
106. G.C. Turner, M. Bazhenov, and G. Laurent Olfactory representations by Drosophila mushroom body neurons J. Neurophysiol. 99 2008 734 746 (Pubitemid 351253231)
107. S.X. Luo, R. Axel, and L.F. Abbott Generating sparse and selective third-order responses in the olfactory system of the fly Proc. Natl. Acad. Sci. U. S. A. 107 2010 10713 10718
108. T. Tully, and W.G. Quinn Classical conditioning and retention in normal and mutant Drosophila melanogaster J. Comp. Physiol. A 157 1985 263 277
109. T. Riemensperger, T. Völler, P. Stock, E. Buchner, and A. Fiala Punishment prediction by dopaminergic neurons in Drosophila Curr. Biol. 15 2005 1953 1960 (Pubitemid 41566144)
110. D. Yu, A.C. Keene, A. Srivatsan, S. Waddell, and R.L. Davis Drosophila DPM neurons form a delayed and branch-specific memory trace after olfactory classical conditioning Cell 123 2005 945 957 (Pubitemid 41721038)
111. J. Séjourné, P.Y. Plaçais, Y. Aso, I. Siwanowicz, S. Trannoy, V. Thoma, S.R. Tedjakumala, G.M. Rubin, P. Tchénio, K. Ito, G. Isabel, H. Tanimoto, and T. Preat Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila Nat. Neurosci. 14 2011 903 910
112. S. Diegelmann, A. Fiala, C. Leibold, T. Spall, and E. Buchner Transgenic flies expressing the fluorescence calcium sensor Cameleon 2.1 under UAS control Genesis 34 2002 95 98
113. R.F. Stocker, G. Heimbeck, N. Gendre, and J.S. de Belle Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons J. Neurobiol. 32 1997 443 456 (Pubitemid 27172931)
114. B.D. Pfeiffer, A. Jenett, A.S. Hammonds, T.T. Ngo, S. Misra, C. Murphy, A. Scully, J.W. Carlson, K.H. Wan, T.R. Laverty, C. Mungall, R. Svirskas, J.T. Kadonaga, C.Q. Doe, M.B. Eisen, S.E. Celniker, and G.M. Rubin Tools for neuroanatomy and neurogenetics in Drosophila Proc. Natl. Acad. Sci. U. S. A. 105 2008 9715 9720 (Pubitemid 352031366)
115. T. Kuner, and G.J. Augustine A genetically encoded ratiometric indicator for chloride: capturing chloride transients in cultured hippocampal neurons Neuron 27 2000 447 459
116. O. Markova, M. Mukhtarov, E. Real, Y. Jacob, and P. Bregestovski Genetically encoded chloride indicator with improved sensitivity J. Neurosci. Methods 170 2008 67 76
117. S. Diegelmann, M. Bate, and M. Landgraf Gateway cloning vectors for the LexA-based binary expression system in Drosophila Fly (Austin) 2 2008 236 239
118. D. Pelz, T. Roeske, Z. Syed, M. de Bruyne, and C.G. Galizia The molecular receptive range of an olfactory receptor in vivo (Drosophila melanogaster Or22a) J. Neurobiol. 66 2006 1544 1563 (Pubitemid 46005367)
119. D. Yu, G.S. Baird, R.Y. Tsien, and R.L. Davis Detection of calcium transients in Drosophila mushroom body neurons with camgaroo reporters J. Neurosci. 23 2003 64 72 (Pubitemid 36050405)
120. V. Tsydzik, and N.J. Wright Dopamine modulation of the in vivo acetylcholine response in the Drosophila mushroom body Dev. Neurobiol. 69 2009 705 714
121. 2+ imaging J. Neurosci. 24 2004 6507 6514 (Pubitemid 38971698)
122. G.S. Suh, A.M. Wong, A.C. Hergarden, J.W. Wang, A.F. Simon, S. Benzer, R. Axel, and D.J. Anderson A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila Nature 431 2004 854 859 (Pubitemid 39434082)
123. V. Jayaraman, and G. Laurent Evaluating a genetically encoded optical sensor of neural activity using electrophysiology in intact adult fruit flies Front. Neural Circuits 1 2007 1 9
124. C.M. Root, J.L. Semmelhack, A.M. Wong, J. Flores, and J.W. Wang Propagation of olfactory information in Drosophila Proc. Natl. Acad. Sci. U. S. A. 104 2007 11826 11831 (Pubitemid 47175097)
125. C.M. Root, K. Masuyama, D.S. Green, L.E. Enell, D.R. Nässel, C.H. Lee, and J.W. Wang A presynaptic gain control mechanism fine-tunes olfactory behavior Neuron 59 2008 311 321 (Pubitemid 352033691)
126. K. Asahina, M. Louis, S. Piccinotti, and L.B. Vosshall A circuit supporting concentration-invariant odor perception in Drosophila J. Biol. 8 2009 9
127. M. Ai, S. Min, Y. Grosjean, C. Leblanc, R. Bell, R. Benton, and G.S. Suh Acid sensing by the Drosophila olfactory system Nature 468 2010 691 695
128. X. Liu, and R.L. Davis The GABAergic anterior paired lateral neuron suppresses and is suppressed by olfactory learning Nat. Neurosci. 12 2009 53 59
129. G. Agarwal, and E. Isacoff Specializations of a pheromonal glomerulus in the Drosophila olfactory system J. Neurophysiol. 105 2011 1711 1721
130. J.D. Seelig, M.E. Chiappe, G.K. Lott, A. Dutta, J.E. Osborne, M.B. Reiser, and V. Jayaraman Two-photon calcium imaging from head-fixed Drosophila during optomotor walking behavior Nat. Methods 7 2010 535 540
131. M.E. Chiappe, J.D. Seelig, M.B. Reiser, and V. Jayaraman Walking modulates speed sensitivity in Drosophila motion vision Curr. Biol. 20 2010 1470 1475