Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations

Nature Neuroscience

Volumn 10, Issue 11, 2007, Pages 1474-1482

  Bhandawat, Vikas ^a   Olsen, Shawn R ^a   Gouwens, Nathan W ^a   Schlief, Michelle L ^a   Wilson, Rachel I ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DROSOPHILA MELANOGASTER; FEMALE; NERVE CELL; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RELIABILITY; SPIKE; VERTEBRATE;

ACTION POTENTIALS; ANIMALS; DISCRIMINATION (PSYCHOLOGY); DROSOPHILA; NONLINEAR DYNAMICS; ODORS; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; PATCH-CLAMP TECHNIQUES; REPRODUCIBILITY OF RESULTS; SENSE ORGANS; SMELL;

EID: 35548945012     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1976     Document Type: Article

References (48)

1. Bargmann, C.I. Comparative chemosensation from receptors to ecology. Nature 444, 295-301 (2006).
2. Mombaerts, P. Genes and ligands for odorant, vomeronasal and taste receptors. Nat. Rev. Neurosci. 5, 263-278 (2004).
3. Laissue, P.P. et al. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J. Comp. Neurol. 405, 543-552 (1999).
4. Hallem, E.A. & Carlson, J.R. The odor coding system of Drosophila. Trends Genet. 20, 453-459 (2004).
5. Couto, A., Alenius, M. & Dickson, B.J. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15, 1535-1547 (2005).
6. Fishilevich, E. & Vosshall, L.B. Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15, 1548-1553 (2005).
7. Stopfer, M. & Laurent, G. Short-term memory in olfactory network dynamics. Nature 402, 664-668 (1999).
8. Bazhenov, M., Stopfer, M., Sejnowski, T.J. & Laurent, G. Fast odor learning improves reliability of odor responses in the locust antennal lobe. Neuron 46, 483-492 (2005).
9. Derby, C.D. & Ache, B.W. Quality coding of a complex odorant in an invertebrate. J. Neurophysiol. 51, 906-924 (1984).
10. Mathews, D.F. Response patterns of single neurons in the tortoise olfactory epithelium and olfactory bulb. J. Gen. Physiol. 60, 166-180 (1972).
11. Duchamp, A. Electrophysiological responses of olfactory bulb interneurons to odor stimuli in the frog. A comparison with receptor cells. Chem. Senses 7, 191-210 (1982).
12. Ng, M. et al. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36, 463-474 (2002).
13. Wang, J.W., Wong, A.M., Flores, J., Vosshall, L.B. & Axel, R. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112, 271-282 (2003).
14. Wilson, R.I., Turner, G.C. & Laurent, G. Transformation of olfactory representations in the Drosophila antennal lobe. Science 303, 366-370 (2004).
15. 2+ indicators. J. Neurosci. 24, 9572-9579 (2004).
16. Sankaranarayanan, S. & Ryan, T.A. Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nat. Cell Biol. 2, 197-204 (2000).
17. Shadlen, M.N. & Newsome, W.T. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J. Neurosci. 18, 3870-3896 (1998).
18. Kara, P., Reinagel, P. & Reid, R.C. Low response variability in simultaneously recorded retinal, thalamic, and cortical neurons. Neuron 27, 635-646 (2000).
19. Vogel, A., Hennig, R.M. & Ronacher, B. Increase of neuronal response variability at higher processing levels as revealed by simultaneous recordings. J. Neurophysiol. 93, 3548-3559 (2005).
20. Stocker, R.F., Heimbeck, G., Gendre, N. & de Belle, J.S. Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J. Neurobiol. 32, 443-456 (1997).
21. de Bruyne, M., Clyne, P.J. & Carlson, J.R. Odor coding in a model olfactory organ: the Drosophila maxillary palp. J. Neurosci. 19, 4520-4532 (1999).
22. de Bruyne, M., Foster, K. & Carlson, J.R. Odor coding in the Drosophila antenna. Neuron 30, 537-552 (2001).
23. Budick, S.A. & Dickinson, M.H. Free-flight responses of Drosophila melanogaster to attractive odors. J. Exp. Biol. 209, 3001-3017 (2006).
24. Hallem, E.A. & Carlson, J.R. Coding of odors by a receptor repertoire. Cell 125, 143-160 (2006).
25. Hallem, E.A., Ho, M.G. & Carlson, J.R. The molecular basis of odor coding in the Drosophila antenna. Cell 117, 965-979 (2004).
26. Olsen, S.R., Bhandawat, V. & Wilson, R.I. Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54, 89-103 (2007).
27. Shang, Y., Claridge-Chang, A., Sjulson, L., Pypaert, M. & Miesenbock, G. Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128, 601-612 (2007).
28. Laughlin, S. A simple coding procedure enhances a neuron's information capacity. Z. Naturforsch. [C] 36, 910-912 (1981).
29. Perez-Orive, J. et al. Oscillations and sparsening of odor representations in the mushroom body. Science 297, 359-365 (2002).
30. Marin, E.C., Jefferis, G.S., Komiyama, T., Zhu, H. & Luo, L. Representation of the glomerular olfactory map in the Drosophila brain. Cell 109, 243-255 (2002).
31. Wong, A.M., Wang, J.W. & Axel, R. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109, 229-241 (2002).
32. Tanaka, N.K., Awasaki, T., Shimada, T. & Ito, K. Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr. Biol. 14, 449-457 (2004).
33. Simoncelli, E.P. Vision and the statistics of the visual environment. Curr. Opin. Neurobiol. 13, 144-149 (2003).
34. Shadlen, M.N. & Newsome, W.T. Noise, neural codes and cortical organization. Curr. Opin. Neurobiol. 4, 569-579 (1994).
35. Berry, M.J., Warland, D.K. & Meister, M. The structure and precision of retinal spike trains. Proc. Natl. Acad. Sci. USA 94, 5411-5416 (1997).
36. Alonso, J.M., Usrey, W.M. & Reid, R.C. Rules of connectivity between geniculate cells and simple cells in cat primary visual cortex. J. Neurosci. 21, 4002-4015 (2001).
37. Berry, M.J. II & Meister, M. Refractoriness and neural precision. J. Neurosci. 18, 2200-2211 (1998).
38. Shanbhag, S.R., Muller, B. & Steinbrecht, R.A. Atlas of olfactory organs of Drosophila melanogaster. 1. Types, external organization, innervation, and distribution of olfactory sensilla. Int. J. Insect Morphol. Embryol. 28, 377-397 (1999).
39. Armstrong-Gold, C.E. & Rieke, F. Bandpass filtering at the rod to second-order cell synapse in salamander (Ambystoma tigrinum) retina. J. Neurosci. 23, 3796-3806 (2003).
40. Stopfer, M., Jayaraman, V. & Laurent, G. Intensity versus identity coding in an olfactory system. Neuron 39, 991-1004 (2003).
41. Mazor, O. & Laurent, G. Transient dynamics vs. fixed points in odor representations by locust antennal lobe projection neurons. Neuron 48, 661-673 (2005).
42. Laughlin, S.B., Howard, J. & Blakeslee, B. Synaptic limitations to contrast coding in the retina of the blowfly Calliphora. Proc. R. Soc. Lond. B 231, 437-467 (1987).
43. Laurent, G. Olfactory network dynamics and the coding of multidimensional signals. Nat. Rev. Neurosci. 3, 884-895 (2002).
44. Schlief, M.L. & Wilson, R.I. Olfactory processing and behavior downstream from highly selective receptor neurons. Nat. Neurosci. 10, 623-630 (2007).
45. Nozawa, M. & Nei, M. Evolutionary dynamics of olfactory receptor genes in Drosophila species. Proc. Natl. Acad. Sci. USA 104, 7122-7127 (2007).
46. Wilson, R.I. & Laurent, G. Role of GABAergic inhibition in shaping odor-evoked spatio-temporal patterns in the Drosophila antennal lobe. J. Neurosci. 25, 9069-9079 (2005).
47. Wachowiak, M. et al. Inhibition of olfactory receptor neuron input to olfactory bulb glomeruli mediated by suppression of presynaptic calcium influx. J. Neurophysiol. 94, 2700-2712 (2005).
48. Vinje, W.E. & Gallant, J.L. Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287, 1273-1276 (2000).