Olfactory information processing in the Drosophila antennal lobe: Anything goes?

Journal of Neuroscience

Volumn 28, Issue 49, 2008, Pages 13075-13087

  Silbering, Ana F ^a,b,d   Okada, Ryuichi ^c,e   Ito, Kei ^c   Galizia, C Giovanni ^b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b UNIVERSITY OF KONSTANZ   (Germany)

^c UNIVERSITY OF TOKYO   (Japan)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

^e TOKUSHIMA BUNRI UNIVERSITY   (Japan)

Author keywords

Antennal lobe network; Calcium imaging; Drosophila melanogaster; Local neurons; Odor concentration; Olfactory processing

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTENNA; ARTICLE; CELL POPULATION; DROSOPHILA MELANOGASTER; ELECTROENCEPHALOGRAM; FEMALE; NERVE CELL NETWORK; NONHUMAN; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; SENSORY NERVE CELL; ACTION POTENTIAL; ANIMAL; BRAIN; CALCIUM SIGNALING; CYTOLOGY; DOSE RESPONSE; DROSOPHILA; DRUG EFFECT; INTERNEURON; METABOLISM; ODOR; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; CYCLIC AMP;

ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; BRAIN; CALCIUM SIGNALING; CYCLIC AMP; DOSE-RESPONSE RELATIONSHIP, DRUG; DROSOPHILA; FEMALE; GAMMA-AMINOBUTYRIC ACID; INTERNEURONS; NERVE NET; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; SMELL; SYNAPTIC TRANSMISSION;

EID: 58149396904     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2973-08.2008     Document Type: Article

References (46)

1. Bhagavan S, Smith BH (1997) Olfactory conditioning in the honeybee Apis mellifera: effects of odor intensity. Physiol Behav 61:107-117.
2. Boeckh J, Tolbert LP (1993) Synaptic organization and development of the antennal lobe in insects. Microsc Res Tech 24:260-280.
3. Borst A (1983) Computation of olfactory signals in Drosophila melanogaster. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 152:373-383.
4. Charpak S, Mertz J, Beaurepaire E, Moreaux L, Delaney K (2001) Odor-evoked calcium signals in dendrites of rat mitral cells. Proc Natl Acad Sci U S A 98:1230-1234.
5. Christensen TA, Waldrop BR, Harrow ID, Hildebrand JG (1993) Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 173:385-399.
6. Christensen TA, Waldrop BR, Hildebrand JG (1998a) GABAergic mechanisms that shape the temporal response to odors in moth olfactory projection neurons. Ann N Y Acad Sci 855:475-481.
7. Christensen TA, Waldrop BR, Hildebrand JG (1998b) Multitasking in the olfactory system: context-dependent responses to odors reveal dual GABA-regulated coding mechanisms in single olfactory projection neurons. J Neurosci 18:5999-6008.
8. Cleland TA, Johnson BA, Leon M, Linster C (2007) Relational representation in the olfactory system. Proc Natl Acad Sci U S A 104:1953-1958.
9. Ditzen M, Evers JF, Galizia CG (2003) Odor similarity does not influence the time needed for odor processing. Chem Senses 28:781-789.
10. 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 16:5443-5456.
11. Galán RF, Sachse S, Galizia CG, Herz AV (2004) Odor-driven attractor dynamics in the antennal lobe allow for simple and rapid olfactory pattern classification. Neural Comput 16:999-1012.
12. Galizia CG, Kimmerle B (2004) Physiological and morphological characterization of honeybee olfactory neurons combining electrophysiology, calcium imaging and confocal microscopy. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190:21-38.
13. Galizia CG, Vetter RS (2004) Optical methods for analyzing odor-evoked activity in the insect brain. In: Methods in insect sensory neuroscience (Christensen TA, ed), pp 349-392. Boca Raton, FL: CRC.
14. Jordán MJ, Tandon K, Shaw PE, Goodner KL (2001) Aromatic profile of aqueous banana essence and banana fruit by gas chromatography-mass spectrometry (GC-MS) and gas chromatography-olfactometry (GC-O). J Agric Food Chem 49:4813-4817.
15. Kurtz R, Warzecha AK, Egelhaaf M (2001) Transfer of visual motion information via graded synapses operates linearly in the natural activity range. J Neurosci 21:6957-6966.
16. 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 405:543-552.
17. Laughlin SB (1989) The role of sensory adaptation in the retina. J Exp Biol 146:39-62.
18. Laurent G (1997) Olfactory processing: maps, time and codes. Curr Opin Neurobiol 7:547-553.
19. Linster C, Sachse S, Galizia CG (2005) Computational modeling suggests that response properties rather than spatial position determine connectivity between olfactory glomeruli. J Neurophysiol 93:3410-3417.
20. Markova O, Mukhtarov M, Real E, Jacob Y, Bregestovski P (2008) Genetically encoded chloride indicator with improved sensitivity. J Neurosci Methods 170:67-76.
21. Miesenböck G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192-195.
22. 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.
23. 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.
24. Olsen SR, Wilson RI (2008) Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452:956-960.
25. Olsen SR, Bhandawat V, Wilson RI (2007) Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54:89-103.
26. Pelz C, Gerber B, Menzel R (1997) Odorant intensity as a determinant for olfactory conditioning in honeybees: roles in discrimination, overshadowing and memory consolidation. J Exp Biol 200:837-847.
27. 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 66:1544-1563.
28. Root CM, Semmelhack JL, Wong AM, Flores J, Wang JW (2007) Propagation of olfactory information in Drosophila. Proc Natl Acad Sci U S A 104:11826-11831.
29. Sachse S, Galizia CG (2002) Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87:1106-1117.
30. Sachse S, Galizia CG (2003) The coding of odour-intensity in the honeybee antennal lobe: local computation optimizes odour representation. Eur J Neurosci 18:2119-2132.
31. Sachse S, Galizia CG (2006) Topography and dynamics of the olfactory system. In: Microcircuits: the interface between neurons and global brain function (Grillner S, Graybiel AM, eds), pp 251-274. Cambridge, MA: Dahlem UP-MIT.
32. Sachse S, Peele P, Silbering AF, Gühmann M, Galizia CG (2006) Role of histamine as a putative inhibitory transmitter in the honeybee antennal lobe. Front Zool 3:22.
33. Sachse S, Rueckert E, Keller A, Okada R, Tanaka NK, Ito K, Vosshall LB (2007) Activity-dependent plasticity in an olfactory circuit. Neuron 56:838-850.
34. Schmuker M, Schneider G (2007) Processing and classification of chemical data inspired by insect olfaction. Proc Natl Acad Sci U S A 104:20285-20289.
35. 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 128:601-612.
36. Silbering AF, Galizia CG (2007) Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J Neurosci 27:11966-11977.
37. Stocker RF (1994) The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275:3-26.
38. Stopfer M, Jayaraman V, Laurent G (2003) Intensity versus identity coding in an olfactory system. Neuron 39:991-1004.
39. Svoboda K, Denk W, Kleinfeld D, Tank DW (1997) In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385:161-165.
40. Tanaka NK, Tanimoto H, Ito K (2008) Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 508:711-755.
41. Venables WN, Ripley BD (2002) Classification. In: Modern applied statistics with S, pp 331-352. New York: Springer.
42. Wachowiak M, Shipley MT (2006) Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin Cell Dev Biol 17:411-423.
43. 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.
44. Wilson RI, Mainen ZF (2006) Early events in olfactory processing. Annu Rev Neurosci 29:163-201.
45. Wilson RI, Turner GC, Laurent G (2004) Transformation of olfactory representations in the Drosophila antennal lobe. Science 303:366-370.
46. Xia S, Tully T (2007) Segregation of odor identity and intensity during odor discrimination in Drosophila mushroom body. PLoS Biol 5:e264.