Advertisement

Calcium Imaging of Neural Activity in the Olfactory System of Drosophila

  • Antonia Strutz
  • Thomas Völler
  • Thomas Riemensperger
  • André Fiala
  • Silke Sachse
Protocol
Part of the Neuromethods book series (NM, volume 72)

Abstract

Many animals are able to detect a plethora of diverse odorants using arrays of odorant receptors located on the olfactory organs. The olfactory information is subsequently encoded and processed by an overlapping, combinatorial activity of neurons forming complex neural circuits in the brain. In order to functionally dissect this neural circuitry, optical recording techniques allow visualizing spatial as well as temporal aspects of odor representations in populations of olfactory neurons. The fruit fly Drosophila melanogaster has emerged as a highly suitable model system for olfactory research as it allows for the combination of genetic, molecular and physiological analyses. Genes of interest can be ectopically expressed in target regions using different binary transcriptional systems. Thereby, fluorescent calcium indicators can be expressed to monitor neuronal activity in genetically defined subsets of neurons. In this chapter we describe various available genetically encoded calcium sensors (GECIs) and the binary transcriptional systems available for Drosophila to express these GECIs in olfactory neurons. We will explain step-by-step methods for fly brain preparation, introduce different odor application devices, and describe the components needed using a widefield or two-photon imaging system including data acquisition and analysis. Overall, this review provides a guideline for optically monitoring the spatiotemporal neuronal activity evoked by odorants in the Drosophila brain.

Key words

Drosophila melanogaster Genetically encoded calcium indicators Binary transcriptional systems Cameleon G-CaMP Olfaction Optical recording Two-photon imaging Antennal lobe Mushroom body Insect brain 

Notes

Acknowledgments

This work was supported by the Federal Ministry of Education and Research (BMBF research group to S.S.), the Max Planck Society (to S.S. and A.S.), and by the Deutsche Forschungsgemeinschaft (GRK 1156 to T.V., SFB 554 to A.F. and T.R., SPP 1392 “Integrative Analysis of Olfaction” to S.S. and A.F.). We are grateful to Erich Buchner and Bill S. Hansson for support.

References

  1. 1.
    Vosshall LB, Stocker RF (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505–533PubMedGoogle Scholar
  2. 2.
    Liang L, Luo L (2010) The olfactory circuit of the fruit fly Drosophila melanogaster. Sci China Life Sci 53:472–484PubMedGoogle Scholar
  3. 3.
    Arora K, Rodrigues V, Joshi S, Shanbhag S, Siddiqi O (1987) A gene affecting the specificity of the chemosensory neurons of Drosophila. Nature 330:62–63PubMedGoogle Scholar
  4. 4.
    Ayer RK Jr, Carlson J (1991) acj6: a gene affecting olfactory physiology and behavior in Drosophila. Proc Natl Acad Sci USA 88:5467–5471PubMedGoogle Scholar
  5. 5.
    Ayyub C, Paranjape J, Rodrigues V, Siddiqi O (1990) Genetics of olfactory behavior in Drosophila melanogaster. J Neurogenet 6:243–262PubMedGoogle Scholar
  6. 6.
    Carlson J (1991) Olfaction in Drosophila: genetic and molecular analysis. Trends Neurosci 14:520–524PubMedGoogle Scholar
  7. 7.
    Stocker RF, Lienhard MC, Borst A, Fischbach KF (1990) Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262:9–34PubMedGoogle Scholar
  8. 8.
    Stocker RF, Singh RN, Schorderet M, Siddiqi O (1983) Projection patterns of different types of antennal sensilla in the antennal glomeruli of Drosophila melanogaster. Cell Tissue Res 232:237–248PubMedGoogle Scholar
  9. 9.
    de Bruyne M, Clyne PJ, Carlson JR (1999) Odor coding in a model olfactory organ: the Drosophila maxillary palp. J Neurosci 19:4520–4532PubMedGoogle Scholar
  10. 10.
    de Bruyne M, Foster K, Carlson JR (2001) Odor coding in the Drosophila antenna. Neuron 30:537–552PubMedGoogle Scholar
  11. 11.
    Hallem EA, Carlson JR (2006) Coding of odors by a receptor repertoire. Cell 125:143–160PubMedGoogle Scholar
  12. 12.
    Hallem EA, Ho MG, Carlson JR (2004) The molecular basis of odor coding in the Drosophila antenna. Cell 117:965–979PubMedGoogle Scholar
  13. 13.
    Bhandawat V, Olsen SR, Gouwens NW, Schlief ML, Wilson RI (2007) Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations. Nat Neurosci 10:1474–1482PubMedGoogle Scholar
  14. 14.
    Chou Y-H, Spletter ML, Yaksi E, Leong JCS, Wilson RI, Luo L (2010) Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat Neurosci 13:439–449PubMedGoogle Scholar
  15. 15.
    Olsen SR, Bhandawat V, Wilson RI (2007) Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54:89–103PubMedGoogle Scholar
  16. 16.
    Wilson RI, Turner GC, Laurent G (2004) Transformation of olfactory representations in the Drosophila antennal lobe. Science 303:366–370PubMedGoogle Scholar
  17. 17.
    Seki Y, Rybak J, Wicher D, Sachse S, Hansson BS (2010) Physiological and morphological characterization of local interneurons in the Drosophila antennal lobe. J Neurophysiol 104:1007–1019PubMedGoogle Scholar
  18. 18.
    Miyawaki A (2003) Fluorescence imaging of physiological activity in complex systems using GFP-based probes. Curr Opin Neurobiol 13:591–596PubMedGoogle Scholar
  19. 19.
    Shanbhag SR, Mueller B, Steinbrecht RA (2000) Atlas of olfactory organs of Drosophila melanogaster. 2. Internal organization and cellular architecture of olfactory sensilla. Arthr Struct Dev 29:211–229Google Scholar
  20. 20.
    Shanbhag SR, Singh K, Singh RN (1995) Fine structure and primary sensory projections of sensilla located in the sacculus of the antenna of Drosophila melanogaster. Cell Tissue Res 282:237–249PubMedGoogle Scholar
  21. 21.
    Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22:327–338PubMedGoogle Scholar
  22. 22.
    Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535–1547PubMedGoogle Scholar
  23. 23.
    Fishilevich E, Vosshall LB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15:1548–1553PubMedGoogle Scholar
  24. 24.
    Vosshall LB (2001) The molecular logic of olfaction in Drosophila. Chem Senses 26:207–213PubMedGoogle Scholar
  25. 25.
    Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725–736PubMedGoogle Scholar
  26. 26.
    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 43:703–714PubMedGoogle Scholar
  27. 27.
    Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4:e20PubMedGoogle Scholar
  28. 28.
    Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002–1006PubMedGoogle Scholar
  29. 29.
    Abuin L, Bargeton B, Ulbrich MH, Isacoff EY, Kellenberger S, Benton R (2011) Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69:44–60PubMedGoogle Scholar
  30. 30.
    Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB (2009) Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136:149–162PubMedGoogle Scholar
  31. 31.
    Wicher D, Schafer R, Bauernfeind R, Stensmyr MC, Heller R, Heinemann SH, Hansson BS (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452:1007–1011PubMedGoogle Scholar
  32. 32.
    Gao Q, Yuan B, Chess A (2000) Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat Neurosci 3:780–785PubMedGoogle Scholar
  33. 33.
    Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102:147–159PubMedGoogle Scholar
  34. 34.
    Fiala A, Spall T, Diegelmann S, Eisermann B, Sachse S, Devaud JM, Buchner E, Galizia CG (2002) Genetically expressed Cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons. Curr Biol 12:1877–1884PubMedGoogle Scholar
  35. 35.
    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 112:271–282PubMedGoogle Scholar
  36. 36.
    Marin EC, Jefferis GSXE, Komiyama T, Zhu H, Luo L (2002) Representation of the glomerular olfactory map in the Drosophila brain. Cell 109:243–255PubMedGoogle Scholar
  37. 37.
    Wong AM, Wang JW, Axel R (2002) Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109:229–241PubMedGoogle Scholar
  38. 38.
    Shang Y, Claridge-Chang A, Sjulson L, Pypaert M, Miesenböck G (2007) Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128:601–612PubMedGoogle Scholar
  39. 39.
    Yaksi E, Wilson RI (2010) Electrical coupling between olfactory glomeruli. Neuron 67:1034–1047PubMedGoogle Scholar
  40. 40.
    Huang J, Zhang W, Qiao W, Hu A, Wang Z (2010) Functional connectivity and selective odor responses of excitatory local interneurons in Drosophila antennal lobe. Neuron 67:1021–1033PubMedGoogle Scholar
  41. 41.
    Dacks AM, Green DS, Root CM, Nighorn AJ, Wang JW (2009) Serotonin modulates olfactory processing in the antennal lobe of Drosophila. J Neurogenet 23:366–377PubMedGoogle Scholar
  42. 42.
    Busch S, Selcho M, Ito K, Tanimoto H (2009) A map of octopaminergic neurons in the Drosophila brain. J Comp Neurol 513:643–667PubMedGoogle Scholar
  43. 43.
    Carlsson MA, Diesner M, Schachtner J, Nässel DR (2010) Multiple neuropeptides in the Drosophila antennal lobe suggest complex modulatory circuits. J Comp Neurol 518:3359–3380PubMedGoogle Scholar
  44. 44.
    Yu D, Ponomarev A, Davis RL (2004) Altered representation of the spatial code for odors after olfactory classical conditioning; memory trace formation by synaptic recruitment. Neuron 42:437–449PubMedGoogle Scholar
  45. 45.
    Lin HH, Lin CY, Chiang AS (2007) Internal representations of smell in the Drosophila brain. J Biomed Sci 14:453–459PubMedGoogle Scholar
  46. 46.
    Tanaka NK, Awasaki T, Shimada T, Ito K (2004) Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr Biol 14:449–457PubMedGoogle Scholar
  47. 47.
    Busto GU, Cervantes-Sandoval I, Davis RL (2010) Olfactory learning in Drosophila. Physiology 25:338–346PubMedGoogle Scholar
  48. 48.
    Fiala A (2007) Olfaction and olfactory learning in Drosophila: recent progress. Curr Opin Neurobiol 17:720–726PubMedGoogle Scholar
  49. 49.
    Heisenberg M (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4:266–275PubMedGoogle Scholar
  50. 50.
    Keene AC, Waddell S (2007) Drosophila olfactory memory: single genes to complex neural circuits. Nat Rev Neurosci 8:341–354PubMedGoogle Scholar
  51. 51.
    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 23:156–172PubMedGoogle Scholar
  52. 52.
    Luo SX, Axel R, Abbott LF (2010) Generating sparse and selective third-order responses in the olfactory system of the fly. Proc Natl Acad Sci 107:10713–10718PubMedGoogle Scholar
  53. 53.
    Turner GC, Bazhenov M, Laurent G (2008) Olfactory representations by Drosophila mushroom body neurons. J Neurophysiol 99:734–746PubMedGoogle Scholar
  54. 54.
    Rodrigues V (1988) Spatial coding of olfactory information in the antennal lobe of Drosophila melanogaster. Brain Res 453:299–307PubMedGoogle Scholar
  55. 55.
    Rodrigues V, Buchner E (1984) (3H)2-deoxyglucose mapping of odor-induced neuronal activity in the antennal lobes of Drosophila melanogaster. Brain Res 324:374–378PubMedGoogle Scholar
  56. 56.
    Martin J-R, Rogers KL, Chagneau C, Brûlet P (2007) In vivo bioluminescence imaging of Ca2+ signalling in the brain of Drosophila. PLoS One 2:e275PubMedGoogle Scholar
  57. 57.
    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 388:882–887PubMedGoogle Scholar
  58. 58.
    Romoser VA, Hinkle PM, Persechini A (1997) Detection in living cells of Ca2+-dependent changes in the fluorescence emission of an indicator composed of two green fluorescent protein variants linked by a calmodulin-binding sequence. J Biol Chem 272:13270–13274PubMedGoogle Scholar
  59. 59.
    Nakai J, Ohkura M, Imoto K (2001) A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat Biotechnol 19:137–141PubMedGoogle Scholar
  60. 60.
    Hasan MT, Friedrich RW, Euler T, Larkum ME, Giese G, Both M, Duebel J, Waters J, Bujard H, Griesbeck O, Tsien RY, Nagai T, Miyawaki A, Denk W (2004) Functional fluorescent Ca2+ indicator proteins in transgenic mice under TET control. PLoS Biol 2:e163PubMedGoogle Scholar
  61. 61.
    Pologruto TA, Yasuda R, Svoboda K (2004) Monitoring neural activity and (Ca2+) with genetically encoded Ca2+ indicators. J Neurosci 24:9572–9579PubMedGoogle Scholar
  62. 62.
    Hendel T, Mank M, Schnell B, Griesbeck O, Borst A, Reiff DF (2008) Fluorescence changes of genetic calcium indicators and OGB-1 correlated with neural activity and calcium in vivo and in vitro. J Neurosci 28:7399–7411PubMedGoogle Scholar
  63. 63.
    Reiff DF, Ihring A, Guerrero G, Isacoff EY, Joesch M, Nakai J, Borst A (2005) In vivo performance of genetically encoded indicators of neural activity in flies. J Neurosci 25:4766–4778PubMedGoogle Scholar
  64. 64.
    Kamikouchi A, Wiek R, Effertz T, Gopfert MC, Fiala A (2010) Transcuticular optical imaging of stimulus-evoked neural activities in the Drosophila peripheral nervous system. Nat Protoc 5:1229–1235PubMedGoogle Scholar
  65. 65.
    Kamikouchi A, Inagaki HK, Effertz T, Hendrich O, Fiala A, Gopfert MC, Ito K (2009) The neural basis of Drosophila gravity-sensing and hearing. Nature 458:165–171PubMedGoogle Scholar
  66. 66.
    Fischer JA, Giniger E, Maniatis T, Ptashne M (1988) GAL4 activates transcription in Drosophila. Nature 332:853–856PubMedGoogle Scholar
  67. 67.
    Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415PubMedGoogle Scholar
  68. 68.
    Miyawaki A, Griesbeck O, Heim R, Tsien RY (1999) Dynamic and quantitative Ca2+ measurements using improved Cameleons. Proc Natl Acad Sci 96:2135–2140PubMedGoogle Scholar
  69. 69.
    Stocker RF, Heimbeck G, Gendre N, de Belle JS (1997) Neuroblast ablation in Drosophila P(GAL4) lines reveals origins of olfactory interneurons. J Neurobiol 32:443–456PubMedGoogle Scholar
  70. 70.
    Wang Y, Guo HF, Pologruto TA, Hannan F, Hakker I, Svoboda K, Zhong Y (2004) Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2+ imaging. J Neurosci 24:6507–6514PubMedGoogle Scholar
  71. 71.
    Golic KG, Lindquist S (1989) The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59:499–509PubMedGoogle Scholar
  72. 72.
    Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451–461PubMedGoogle Scholar
  73. 73.
    Lai S-L, Lee T (2006) Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat Neurosci 9:703–709PubMedGoogle Scholar
  74. 74.
    Brent R, Ptashne M (1985) A eukaryotic transcriptional activator bearing the DNA specificity of a prokaryotic repressor. Cell 43:729–736PubMedGoogle Scholar
  75. 75.
    Triezenberg SJ, Kingsbury RC, McKnight SL (1988) Functional dissection of VP16, the trans-activator of herpes simplex virus immediate early gene expression. Genes Dev 2:718–729PubMedGoogle Scholar
  76. 76.
    Lai S-L (2007) Neural diversity in the Drosophila olfactory circuitry: a dissertation. GSBS dissertations, University of Massachusetts Medical SchoolGoogle Scholar
  77. 77.
    Potter CJ, Tasic B, Russler EV, Liang L, Luo L (2010) The Q system: a repressible binary system for transgene expression, lineage tracing, and mosaic analysis. Cell 141:536–548PubMedGoogle Scholar
  78. 78.
    Denk W, Strickler J, Webb W (1990) Two-photon laser scanning fluorescence microscopy. Science 248:73–76PubMedGoogle Scholar
  79. 79.
    Estes PS, Roos J, van der Bliek A, Kelly RB, Krishnan KS, Ramaswami M (1996) Traffic of dynamin within individual Drosophila synaptic boutons relative to compartment-specific markers. J Neurosci 16:5443–5456PubMedGoogle Scholar
  80. 80.
    Fiala A, Spall T (2003) In vivo calcium imaging of brain activity in Drosophila by transgenic Cameleon expression. Sci STKE 174:l6Google Scholar
  81. 81.
    Pelz D, Roeske T, Syed Z, de Bruyne M, Galizia CG (2006) The molecular receptive range of an olfactory receptor in vivo (Drosophila melanogaster Or22a). J Neurobiol 66:1544–1563PubMedGoogle Scholar
  82. 82.
    Sachse S, Rueckert E, Keller A, Okada R, Tanaka NK, Ito K, Vosshall LB (2007) Activity-dependent plasticity in an olfactory circuit. Neuron 56:838–850PubMedGoogle Scholar
  83. 83.
    Silbering AF, Galizia CG (2007) Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J Neurosci 27:11966–11977PubMedGoogle Scholar
  84. 84.
    Sachse S, Galizia CG (2003) The coding of odour-intensity in the honeybee antennal lobe: local computation optimizes odour representation. Eur J Neurosci 18:2119–2132PubMedGoogle Scholar
  85. 85.
    Olsson SB, Kuebler LS, Veit D, Steck K, Schmidt A, Knaden M, Hansson BS (2011) A novel multicomponent stimulus device for use in olfactory experiments. J Neurosci Methods 195:1–9PubMedGoogle Scholar
  86. 86.
    Vetter RS, Sage AE, Justus KA, Cardé RT, Galizia CG (2006) Temporal integrity of an airborne odor stimulus is greatly affected by physical aspects of the odor delivery system. Chem Senses 31:59–369Google Scholar
  87. 87.
    Galizia CG, Vetter RS (2004) Optical methods for analyzing odor-evoked activity in the insect brain. In: Christensen TA (ed) Advances in insect sensory neuroscience. CRC Press, Boca Raton, pp 349–392Google Scholar
  88. 88.
    Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF (1999) Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 405:543–552PubMedGoogle Scholar
  89. 89.
    Truong K, Sawano A, Mizuno H, Hama H, Tong KI, Mal TK, Miyawaki A, Ikura M (2001) FRET-based in vivo Ca2+ imaging by a new calmodulin-GFP fusion molecule. Nat Struct Mol Biol 8:1069–1073Google Scholar
  90. 90.
    Mank M, Reiff DF, Heim N, Friedrich MW, Borst A, Griesbeck O (2006) A FRET-based calcium biosensor with fast signal kinetics and high fluorescence change. Biophys J 90:1790–1796PubMedGoogle Scholar
  91. 91.
    Ohkura M, Matsuzaki M, Kasai H, Imoto K, Nakai J (2005) Genetically encoded bright Ca2+ probe applicable for dynamic Ca2+ imaging of dendritic spines. Anal Chem 77:5861–5869PubMedGoogle Scholar
  92. 92.
    Nagai T, Yamada S, Tominaga T, Ichikawa M, Miyawaki A (2004) Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci 101:10554–10559PubMedGoogle Scholar
  93. 93.
    Mank M, Santos AF, Direnberger S, Mrsic-Flogel TD, Hofer SB, Stein V, Hendel T, Reiff DF, Levelt C, Borst A, Bonhoeffer T, Hubener M, Griesbeck O (2008) A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat Methods 5:805–811PubMedGoogle Scholar
  94. 94.
    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 6:875–881PubMedGoogle Scholar
  95. 95.
    Denk W, Svoboda K (1997) Photon upmanship: why multiphoton imaging is more than a gimmick. Neuron 18:351–357PubMedGoogle Scholar
  96. 96.
    Diegelmann S, Fiala A, Leibold C, Spall T, Buchner E (2002) Transgenic flies expressing the fluorescence calcium sensor Cameleon 2.1 under UAS control. Genesis 34:95–98PubMedGoogle Scholar
  97. 97.
    Asahina K, Louis M, Piccinotti S, Vosshall L (2009) A circuit supporting concentration-invariant odor perceptiokn in Drosophila. J Biol 8:9PubMedGoogle Scholar
  98. 98.
    Baird GS, Zacharias DA, Tsien RY (1999) Circular permutation and receptor insertion within green fluorescent proteins. Proc Natl Acad Sci 96:11241–11246PubMedGoogle Scholar
  99. 99.
    Griesbeck O, Baird GS, Campbell RE, Zacharias DA, Tsien RY (2001) Reducing the environmental sensitivity of yellow fluorescent protein. J Biol Chem 276:29188–29194PubMedGoogle Scholar
  100. 100.
    Yu D, Baird GS, Tsien RY, Davis RL (2003) Detection of calcium transients in Drosophila mushroom body neurons with Camgaroo reporters. J Neurosci 23:64–72PubMedGoogle Scholar
  101. 101.
    Ma J, Ptashne M (1987) A new class of yeast transcriptional activators. Cell 51:113–119PubMedGoogle Scholar
  102. 102.
    Root CM, Masuyama K, Green DS, Enell LE, Nässel DR, Lee C-H, Wang JW (2008) A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59:311–321PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Antonia Strutz
    • 1
  • Thomas Völler
    • 2
  • Thomas Riemensperger
    • 3
  • André Fiala
    • 4
  • Silke Sachse
    • 1
  1. 1.Department of Evolutionary NeuroethologyMax Planck Institute for Chemical EcologyJenaGermany
  2. 2.Neurobiology and GeneticsJulius-Maximilians-University of WuerzburgWuerzburgGermany
  3. 3.Molecular Neurobiology of Behaviour, Johann-Friedrich-Blumenbach-InstituteGeorg-August-University of GoettingenGoettingenGermany
  4. 4.Molecular Neurobiology of Behaviour, Johann-Friedrich-Blumenbach-InstituteGeorg-August- University of GoettingenGoettingenGermany

Personalised recommendations