Topological reorganization of odor representations in the olfactory bulb

PLoS Biology

Volumn 5, Issue 7, 2007, Pages 1453-1473

  Yaksi, Emre ^a   Judkewitz, Benjamin ^a,c   Friedrich, Rainer W ^a,b  

^a MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; INTERNEURON; MITRAL CELL; MOUSE; NERVE CELL; NONHUMAN; ODOR; OLFACTORY BULB; SENSORY STIMULATION; SYNAPTIC MEMBRANE; ZEBRA FISH; ANIMAL; CALCIUM SIGNALING; EVOKED RESPONSE; FEEDBACK SYSTEM; GENETICS; HISTOLOGY; OLFACTORY SYSTEM; PHYSIOLOGY; TRANSGENIC ANIMAL;

DANIO RERIO;

PHOTOPROTEIN; RECOMBINANT PROTEIN; YELLOW CAMELEON 2.1;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CALCIUM SIGNALING; EVOKED POTENTIALS; FEEDBACK, BIOCHEMICAL; INTERNEURONS; LUMINESCENT PROTEINS; ODORS; OLFACTORY BULB; OLFACTORY PATHWAYS; RECOMBINANT PROTEINS; ZEBRAFISH;

EID: 34547096762     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0050178     Document Type: Article

References (85)

1. Van Essen DC, Gallant JL (1994) Neural mechanisms of form and motion processing in the primate visual system. Neuron 13: 1-10.
2. Konishi M, Takahashi TT, Wagner H, Sullivan WE, Carr CE (1988) Neurophysiological and anatomical substrates of sound localization in the owl. In: Edelman GM, Gall WE, Cowan WM, editors. Auditory function: neurobiological bases of hearing. New York: Wiley. pp. 721-745.
3. Kaas JH (1997) Topographic maps are fundamental to sensory processing. Brain Res Bull 44: 107-112.
4. Wilson RI, Mainen ZF (2006) Early events in olfactory processing. Annu Rev Neurosci 29: 163-201.
5. Araneda RC, Kini AD, Firestein S (2000) The molecular receptive range of an odorant receptor. Nature Neurosci 3: 1248-1255.
6. Stewart WB, Kauer JS, Shepherd GM (1979) Functional organization of rat olfactory bulb analysed by the 2-deoxyglucose method. J Comp Neurol 185: 715-734.
7. Rubin BD, Katz LC (1999) Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron 23: 499-511.
8. Wachowiak M, Cohen LB (2001) Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron 32: 723-735.
9. Friedrich RW, Korsching SI (1997) Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 18: 737-752.
10. Friedrich RW, Korsching SI (1998) Chemotopic, combinatorial and noncombinatorial odorant representations in the olfactory bulb revealed using a voltage-sensitive axon tracer. J Neurosci 18: 9977-9988.
11. Leon M, Johnson BA (2003) Olfactory coding in the mammalian olfactory bulb. Brain Res Brain Res Rev 42: 23-32.
12. Uchida N, Takahashi YK, Tanifuji M, Mori K (2000) Odor maps in the mammalian olfactory bulb: Domain organization and odorant structural features. Nat Neurosci 3: 1035-1043.
13. Mori K, Takahashi YK, Igarashi KM, Yamaguchi M (2006) Maps of odorant molecular features in the mammalian olfactory bulb. Physiol Rev 86: 409-433.
14. Mombaerts P (2001) How smell develops. Nat Rev Neurosci 4: 1192-1198.
15. Hallem EA, Ho MG, Carlson JR (2004) The molecular basis of odor coding in the Drosophila antenna. Cell 117: 965-979.
16. Malnic B, Hirono J, Sato T, Buck LB (1999) Combinatorial receptor codes for odors. Cell 96: 713-723.
17. Takahashi YK, Kurosaki M, Hirono S, Mori K (2004) Topographic representation of odorant molecular features in the rat olfactory bulb. J Neurophysiol 92: 2413-2427.
18. Belluscio L, Katz LC (2001) Symmetry, stereotypy, and topography of odorant representations in mouse olfactory bulbs. J Neurosci 21: 2113-2122.
19. Fuss SH, Korsching SI (2001) Odorant feature detection: Activity mapping of structure response relationships in the zebrafish olfactory bulb. J Neurosci 21: 8396-8407.
20. Xu F, Liu N, Kida I, Rothman DL, Hyder F, et al. (2003) Odor maps of aldehydes and esters revealed by functional MRI in the glomerular layer of the mouse olfactory bulb. Proc Natl Acad Sci U S A 100: 11029-11034.
21. Friedrich RW, Stopfer M (2001) Recent dynamics in olfactory population coding. Curr Opin Neurobiol 11: 468-474.
22. Andres KH (1970) Anatomy and ultrastructure of the olfactory bulb in fish, amphibia, reptiles, birds and mammals. In: Wolstenholme GEW, Knight J, editors. Ciba foundation symposium on taste and smell in vertebrates. London: Churchill Press. pp. 177-196.
23. Allison AC (1953) The morphology of the olfactory system in the vertebrates. Biol Rev 28: 195-244.
24. Aungst JL, Heyward PM, Puche AC, Karnup SV, Hayar A, et al. (2003) Centre-surround inhibition among olfactory bulb glomeruli. Nature 426: 623-629.
25. Shepherd GM, Chen WR, Greer CA (2004) Olfactory bulb. In: Shepherd GM, editor. The synaptic organization of the brain. Oxford: Oxford University Press. pp. 165-216.
26. Lowe G (2003) Electrical signaling in the olfactory bulb. Curr Opin Neurobiol 13: 476-481.
27. Adrian ED (1950) The electrical activity of the mammalian olfactory bulb. EEG Clin Neurophysiol 2: 377-388.
28. Macrides F, Chorover SL (1972) Olfactory bulb units: Activity correlated with inhalation cycles and odor quality. Science 185: 84-87.
29. Meredith M (1986) Patterned response to odor in mammalian olfactory bulb: The influence of intensity. J Neurophysiol 56: 572-597.
30. Gray CM, Skinner JE (1988) Centrifugal regulation of neuronal activity in the olfactory bulb of the waking rabbit as revealed by reversible cryogenic blockade. Exp Brain Res 69: 378-386.
31. Buonviso N, Chaput MA, Berthommier F (1992) Temporal pattern analyses in pairs of neighboring mitral cells. J Neurophysiol 68: 417-424.
32. Friedrich RW, Laurent G (2001) Dynamic optimization of odor representations in the olfactory bulb by slow temporal patterning of mitral cell activity. Science 291: 889-894.
33. Friedrich RW, Habermann CJ, Laurent G (2004) Multiplexing using synchrony in the zebrafish olfactory bulb. Nature Neurosci 7: 862-871.
34. Friedrich RW, Laurent G (2004) Dynamics of olfactory bulb input and output activity during odor stimulation in zebrafish. J Neurophysiol 91: 2658-2669.
35. Imamura K, Mataga N, Mori K (1992) Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. I. Aliphatic compounds. J Neurophysiol 68: 1986-2002.
36. Katoh K, Koshimoto H, Tani A, Mori K (1993) Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. II. Aromatic compounds. J Neurophysiol 70: 2161-2175.
37. Rinberg D, Koulakov A, Gelperin A (2006) Sparse odor coding in awake behaving mice. J Neurosci 26: 8857-8865.
38. Guthrie KM, Anderson AJ, Leon M, Gall C (1993) Odor-induced increases in c-fos mRNA expression reveal an anatomical "unit" for odor processing in olfactory bulb. Proc Natl Acad Sci U S A 90: 3329-3333.
39. Sallaz M, Jourdan F (1993) C-fos expression and 2-deoxyglucose uptake in the olfactory bulb of odour-stimulated awake rats. Neuroreport 4: 55-58.
40. Sallaz M, Jourdan F (1996) Odour-induced c-fos expression in the rat olfactory bulb: Involvement of centrifugal afferents. Brain Res 721: 66-75.
41. Edwards JG, Michel WC (2002) Odor-stimulated glutamatergic neurotransmission in the zebrafish olfactory bulb. J Comp Neurol 454: 294-309.
42. Yang X, Renken R, Hyder F, Siddeek M, Greer CA, et al. (1998) Dynamic mapping at the laminar level of odor-elicited responses in rat olfactory bulb by functional MRI. Proc Natl Acad Sci U S A 95: 7715-7720.
43. Cinelli AR, Hamilton KA, Kauer JS (1995) Salamander olfactory bulb neuronal activity observed by video rate, voltage-sensitive dye imaging. III. Spatial and temporal properties of responses evoked by odorant stimulation. J Neurophysiol 73: 2053-2071.
44. Helmchen F, Denk W (2005) Deep tissue two-photon microscopy. Nat Methods 2: 932-940.
45. Denk W, Strickler JH, Webb WW (1990) Two-photon laser scanning fluorescence microscopy. Science 248: 73-76.
46. Stosiek C, Garaschuk O, Holthoff K, Konnerth A (2003) In vivo two-photon calcium imaging of neuronal networks. Proc Natl Acad Sci U S A 100: 7319-7324.
47. 2+ imaging. Pflügers Arch 446: 766-773.
48. Kerr JN, Greenberg D, Helmchen F (2005) Imaging input and output of neocortical networks in vivo. Proc Natl Acad Sci U S A 102: 14063-14068.
49. Ohki K, Chung S, Ch'ng YH, Kara P, Reid RC (2005) Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 433: 597-603.
50. Ohki K, Chung S, Kara P, Hubener M, Bonhoeffer T, et al. (2006) Highly ordered arrangement of single neurons in orientation pinwheels. Nature 442: 925-928.
51. 2+ imaging. Nat Methods 3: 377-383.
52. Byrd CA, Brunjes PC (1995) Organization of the olfactory system in the adult zebrafish: histological, immunohistochemical, and quantitative analysis. J Comp Neurol 358: 247-259.
53. Fuller CL, Yettaw HK, Byrd CA (2006) Mitral cells in the olfactory bulb of adult zebrafish (Danio rerio): Morphology and distribution. J Comp Neurol 499: 218-230.
54. Li J, Mack JA, Souren M, Yaksi E, Higashijima S, et al. (2005) Early development of functional spatial maps in the zebrafish olfactory bulb. J Neurosci 25: 5784-5795.
55. Carr WES (1988) The molecular nature of chemical stimuli in the aquatic environment. In: Atema J, Fay RR, Popper AN, Tavolga WN, editors. Sensory biology of aquatic animals. New York: Springer. pp. 3-27.
56. Vinje WE, Gallant JL (2000) Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287: 1273-1276.
57. Uchida N, Mainen ZF (2003) Speed and accuracy of olfactory discrimination in the rat. Nat Neurosci 6: 1224-1229.
58. Abraham NM, Spors H, Carleton A, Margrie TW, Kuner T, et al. (2004) Maintaining accuracy at the expense of speed: Stimulus similarity defines odor discrimination time in mice. Neuron 44: 865-876.
59. Rinberg D, Koulakov A, Gelperin A (2006) Speed-accuracy tradeoff in olfaction. Neuron 51: 351-358.
60. Friedrich RW (2006) Mechanisms of odor discrimination: Neurophysiological and behavioral approaches. Trends Neurosci 29: 40-47.
61. Bieber SL, Smith DV (1986) Multivariate analysis of sensory data: A comparison of methods. Chem Senses 11: 19-47.
62. Reyment R, Jöreskog KG (1996) Applied factor analysis in the natural sciences. 2nd edition. Cambridge: Cambridge University Press. 371 p.
63. Murphy GJ, Glickfeld LL, Balsen Z, Isaacson JS (2004) Sensory neuron signaling to the brain: Properties of transmitter release from olfactory nerve terminals. J Neurosci 24: 3023-3030.
64. Rhein LD, Cagan RH (1983) Biochemical studies of olfaction: Binding specificity of odorants to a cilia preparation from rainbow trout olfactory rosettes. J Neurochem 41: 569-577.
65. Caprio J, Byrd RJ (1984) Electrophysiological evidence for acidic, basic, and neutral amino acid olfactory receptor sites in the catfish. J Gen Physiol 84: 403-422.
66. Ng M, Roorda RD, Lima SQ, Zemelman BV, Morcillo P, et al. (2002) Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36: 463-474.
67. Wilson RI, Turner GC, Laurent G (2004) Transformation of olfactory representations in the Drosophila antennal lobe. Science 303: 366-370.
68. Egger V, Svoboda K, Mainen ZF (2005) Dendrodendritic synaptic signals in olfactory bulb granule cells: Local spine boost and global low-threshold spike. J Neurosci 25: 3521-3530.
69. Murphy GJ, Darcy DP, Isaacson JS (2005) Intraglomerular inhibition: Signaling mechanisms of an olfactory microcircuit. Nat Neurosci 8: 354-364.
70. Pressler RT, Strowbridge BW (2006) Blanes cells mediate persistent feedforward inhibition onto granule cells in the olfactory bulb. Neuron 49: 889-904.
71. Cang J, Isaacson JS (2003) In vivo whole-cell recording of odor-evoked synaptic transmission in the rat olfactory bulb. J Neurosci 23: 4108-4116.
72. Wellis DP, Scott JW (1990) Intracellular responses of identified rat olfactory bulb interneurons to electrical and odor stimulation. J Neurophysiol 64: 932-947.
73. Luo M, Katz LC (2001) Response correlation maps of neurons in the mammalian olfactory bulb. Neuron 32: 1165-1179.
74. Hall BJ, Delaney KR (2002) Contribution of a calcium-activated non-specific conductance to NMDA receptor-mediated synaptic potentials in granule cells of the frog olfactory bulb. J Physiol 543: 819-834.
75. Margrie TW, Schaefer AT (2003) Theta oscillation coupled spike latencies yield computational vigour in a mammalian sensory system. J Physiol 546: 363-374.
76. Kapoor V, Urban NN (2006) Glomerulus-specific, long-latency activity in the olfactory bulb granule cell network. J Neurosci 26: 11709-11719.
77. Shang Y, Claridge-Chang A, Sjulson L, Pypaert M, Miesenbock G (2007) Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128: 601-612.
78. Didier A, Carleton A, Bjaalie JG, Vincent JD, Ottersen OP, et al. (2001) A dendrodendritic reciprocal synapse provides a recurrent excitatory connection in the olfactory bulb. Proc Natl Acad Sci U S A 98: 6441-6446.
79. Isaacson JS (1999) Glutamate spillover mediates excitatory transmission in the rat olfactory bulb. Neuron 23: 377-384.
80. Døving KB, Selset R, Thommesen G (1980) Olfactory sensitivity to bile acids in salmonid fishes. Acta Physiol Scand 108: 123-131.
81. Higashijima S, Masino MA, Mandel G, Fetcho JR (2003) Imaging neuronal activity during zebrafish behavior with a genetically encoded calcium indicator. J Neurophysiol 90: 3986-3997.
82. 2+ based on green fluorescent proteins and calmodulin. Nature 388: 882-887.
83. Mathieson WB, Maler L (1988) Morphological and electrophysiological properties of a novel in vitro preparation: The electrosenspry lateral line lobe brain slice. J Comp Physiol A 163: 489-506.
84. Rolls ET, Tovee MJ (1995) Sparseness of the neuronal representation of stimuli in the primate temporal visual-cortex. J Neurophysiol 73: 713-726.
85. Satou M (1990) Synaptic organization, local neuronal circuitry, and functional segregation of the teleost olfactory bulb. Prog Neurobiol 34: 115-142.