Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2+ imaging

Journal of Neuroscience

Volumn 24, Issue 29, 2004, Pages 6507-6514

  Wang, Yalin ^a   Guo, Hui Fu ^a   Pologruto, Thomas A ^a,b   Hannan, Frances ^a   Hakker, Inessa ^a   Svoboda, Karel ^a,b   Zhong, Yi ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

Calcium imaging; G CaMP; Kenyon cell; Mushroom body; Odor; Stereotype; Two photon

Indexed keywords

BENZALDEHYDE; CALCIUM ION; GREEN FLUORESCENT PROTEIN;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; DROSOPHILA; FLUORESCENCE MICROSCOPY; IMAGE RECONSTRUCTION; KENYON CELL; MUSHROOM BODY; NERVE CELL; NONHUMAN; ODOR; OLFACTORY NERVOUS SYSTEM; PRIORITY JOURNAL; STEREOTYPY; THREE DIMENSIONAL IMAGING;

ANIMALS; CALCIUM; DROSOPHILA; GREEN FLUORESCENT PROTEINS; LUMINESCENT AGENTS; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; MUSHROOM BODIES; NEURONS; ODORS;

EID: 3242753324     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3727-03.2004     Document Type: Article

References (50)

1. Bicker G, Kreissl S (1994) Calcium imaging reveals nicotinic acetylcholine receptors on cultured mushroom body neurons. J Neurophysiol 71:808-810.
2. Bozza TC, Mombaerts P (2001) Olfactory coding: revealing intrinsic representations of odors. Curr Biol 11:R687-R690.
3. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
4. Buck LB (2000) The molecular architecture of odor and pheromone sensing in mammals. Cell 100:611-618.
5. Chess A, Simon I, Cedar H, Axel R (1994) Allelic inactivation regulates olfactory receptor gene expression. Cell 78:823-834.
6. 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 22:327-338.
7. s signaling in Drosophila mushroom bodies. Science 274:2104-2107.
8. de Bruyne M, Foster K, Carlson JR (2001) Odor coding in the Drosophila antenna. Neuron 30:537-552.
9. Denk W, Svoboda K (1997) Photon upmanship: why multiphoton imaging is more than a gimmick. Neuron 18:351-357.
10. Galizia CG, Sachse S, Rappert A, Menzel R (1999) The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat Neurosci 2:473-478.
11. Gao Q, Yuan B, Chess A (2000) Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat Neurosci 3:780-785.
12. Goldberg F, Grunewald B, Rosenboom H, Menzel R (1999) Nicotinic acetylcholine currents of cultured Kenyon cells from the mushroom bodies of the honey bee Aapis mellifera. J Physiol (Lond) 514:759-768.
13. Gorczyca MG, Hall JC (1987) Immunohistochemical localization of choline acetyltransferase during development and in Chats mutants of Drosophila melanogaster. J Neurosci 7:1361-1369.
14. Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595-631.
15. Jefferis GS, Marin EC, Stocker RF, Luo L (2001) Target neuron prespecification in the olfactory map of Drosophila. Nature 414:204-208.
16. Johnson BA, Woo CC, Leon M (1998) Spatial coding of odorant features in the glomerular layer of the rat olfactory bulb. J Comp Neurol 393:457-471.
17. Kauer JS, White J (2001) Imaging and coding in the olfactory system. Annu Rev Neurosci 24:963-979.
18. Korsching S (2002) Olfactory maps and odor images. Curt Opin Neurobiol 12:387-392.
19. Lendvai B, Stern EA, Chen B, Svoboda K (2000) Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404:876-881.
20. Malnic B, Hirono J, Sato T, Buck LB (1999) Combinatorial receptor codes for odors. Cell 96:713-723.
21. Maravall M, Mainen ZF, Sabatini BL, Svoboda K (2000) Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys J 78:2655-2667.
22. Marin EC, Jefferis GS, Komiyama T, Zhu H, Luo L (2002) Representation of the glomerular olfactory map in the Drosophila brain. Cell 109:243-255.
23. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R (1996) Visualizing an olfactory sensory map. Cell 87:675-686.
24. 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.
25. Nemitz JW, Goldberg SJ (1983) Neuronal responses of rat pyriform cortex to odor stimulation: an extracellular and intracellular study. J Neurophysiol 49:188-203.
26. Oleskevich S (1999) Cholinergic synaptic transmission in insect mushroom bodies in vitro. J Neurophysiol 82:1091-1096.
27. Perez-Orive J, Mazor O, Turner GC, Cassenaer S, Wilson RI, Laurent G (2002) Oscillations and sparsening of odor representations in the mushroom body. Science 297:359-365.
28. Pologruto TA, Sabatini BL, Svoboda K (2003) ScanImage: flexible software for operating laser scanning microscopes. Biomed Eng Online 2:13.
29. Rein K, Zockler M, Mader MT, Grubel C, Heisenberg M (2002) The Drosophila standard brain. Curr Biol 12:227-231.
30. Ressler KJ, Sullivan SL, Buck LB (1994) Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79:1245-1255.
31. Rodrigues V (1988) Spatial coding of olfactory information in the antennal lobe of Drosophila melanogaster. Brain Res 453:299-307.
32. Rubin BD, Katz LC (1999) Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron 23:499-511.
33. Schoenbaum G, Eichenbaum H (1995) Information coding in the rodent prefrontal cortex. I. Single-neuron activity in orbitofrontal cortex compared with that in pyriform cortex. J Neurophysiol 74:733-750.
34. Skoulakis E, Acevedo S (2003) Characterization of a novel non-associative behavior, "protection from habituation," defined by D14-3-3zeta mutants.
35. Spradling AC, Rubin GM (1982) Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218:341-347.
36. 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 232:237-248.
37. Stopfer M, Jayaraman V, Laurent G (2003) Intensity versus identity coding in an olfactory system. Neuron 39:991-1004.
38. Su H, O'Dowd DK (2003) Fast synaptic currents in Drosophila mushroom body Kenyon cells are mediated by alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors and picrotoxin-sensitive GABA receptors. J Neurosci 23:9246-9253.
39. Svoboda K, Denk W, Kleinfeld D, Tank DW (1997) In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385:161-165.
40. Technau G, Heisenberg M (1982) Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature 295:405-407.
41. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725-736.
42. Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102:147-159.
43. Wachowiak M, Cohen LB (2001) Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron 32:723-735.
44. 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.
45. Wang Y, Wright NJ, Guo H, Xie Z, Svoboda K, Malinow R, Smith DP, Zhong Y (2001) Genetic manipulation of the odor-evoked distributed neural activity in the Drosophila mushroom body. Neuron 29:267-276.
46. Wicher D, Penzlin H (1997) Ca2+ currents in central insect neurons: electrophysiological and pharmacological properties. J Neurophysiol 77:186-199.
47. Wong AM, Wang JW, Axel R (2002) Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109:229-241.
48. Yasuyama K, Meinertzhagen IA, Schurmann FW (2002) Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J Comp Neurol 445:211-226.
49. Yu D, Baird GS, Tsien RY, Davis RL (2003) Detection of calcium transients in Drosophila mushroom body neurons with camgaroo reporters. J Neurosci 23:64-72.
50. Zou Z, Horowitz LF, Montmayeur JP, Snapper S, Buck LB (2001) Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Nature 414:173-179.