3D atlas describing the ontogenic evolution of the primary olfactory projections in the olfactory bulb of Xenopus laevis

Journal of Comparative Neurology

Volumn 489, Issue 4, 2005, Pages 403-424

  Gaudin, Arnaud ^a   Gascuel, Jean ^a  

^a CENTRE DES SCIENCES DU GOÛT ET DE L ALIMENTATION   (France)

Author keywords

3D imaging; Confocal microscopy; Developmental biology; Neuroanatomy; Olfaction; Olfactory bulb; Olfactory receptor neurons

Indexed keywords

ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; EVOLUTION; NEUROANATOMY; NONHUMAN; OLFACTORY BULB; OLFACTORY NERVOUS SYSTEM; OLFACTORY RECEPTOR; ONTOGENY; PRIORITY JOURNAL; THREE DIMENSIONAL IMAGING; XENOPUS LAEVIS;

ANIMALS; BRAIN MAPPING; CARBOCYANINES; FEMALE; FLUORESCENT DYES; GROWTH CONES; LARVA; LECTINS; MALE; METAMORPHOSIS, BIOLOGICAL; MICROSCOPY, CONFOCAL; OLFACTORY BULB; OLFACTORY NERVE; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; XENOPUS LAEVIS;

EID: 23044515879     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20655     Document Type: Article

References (89)

1. Altner H. 1962. Untersuchungen über Leistungen und Bau der Nase des südafrikanischen Krallenfrosches Xenopus laevis (Daudin, 1803). Z vergl Physiol 45:272-306.
2. Anadon R, Manso MJ, Rodriguez-Moldes I, Becerra M. 1995. Neurons of the olfactory organ projecting to the caudal telencephalon and hypothalamus: a carbocyanine-dye labeling study in the brown trout (Teleostei). Neurosci Lett 191:157-160.
3. Argo S, Weth F, Korsching SL. 2003. Analysis of penetrance and expressivity during ontogenesis supports a stochastic choice of zebrafish odorant receptors from predetermined groups of receptor genes. Eur J Neurosci 17:833-843.
4. Baier H, Korsching S. 1994. Olfactory glomeruli in the zebrafish form an invariant pattern and are identifiable across animals. J Neurosci 14:219-230.
5. Barnea G, O'Donnell S, Mancia F, Sun X, Nemes A, Mendelsohn M, Axel R. 2004. Odorant receptor on axon termini in the brain. Science 304:1468.
6. Becerra M, Manso MJ, Rodriguez-Moldes I, Anadon R. 1994. Primary olfactory fibers project to the ventral telencephalon and preoptic region in trout (Salmo trutta): a developmental immunocytochemical study. J Comp Neurol 342:131-143.
7. Belluscio L, Katz LC. 2001. Symmetry, stereotypy, and topography of odorant representations in mouse olfactory bulbs. J Neurosci 21:2113-2122.
8. Bozza TC, Kauer JS. 1998. Odorant response properties of convergent olfactory receptor neurons. J Neurosci 18:4560-4569.
9. Bozza T, Feinstein P, Zheng C, Mombaerts P. 2002. Odorant receptor expression defines functional units in the mouse olfactory system. J Neurosci 22:3033-3043.
10. Buck L, Axel R. 1991. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175-187.
11. Burd G. 1991. Development of the olfactory nerve in the African clawed frog, Xenopus laevis. 1. Normal development. J Comp Neurol 304:123-134.
12. Burd G. 1992. Development of the olfactory nerve in the African clawed frog, Xenopus laevis. II. Effects of hypothyroidism. J Comp Neurol 315:255-263.
13. Chambille I, Masson C, Rospars C. 1980. The deutocerebrum of the cockroach Blaberus craniifer Burm. Spatial organization of the sensory glomeruli. J Neurobiol 11:135-157.
14. Czesnik D, Rössler W, Kirchner F, Gennerich A, Schild D. 2003. Neuronal representation of odourants in the olfactory bulb of Xenopus laevis tadpoles. Eur J Neurosci 17:113-118.
15. Eisthen HL, Northcutt RG. 1996. Silver lampreys (Ichthyomyzon unicuspis) lack a gonadotropin-releasing hormone- and FMRFamideimmunoreactive terminal nerve. J Comp Neurol 370:159-172.
16. Feinstein P, Mombaerts P. 2004. A contextual model for axonal sorting into glomeruli in the mouse olfactory system. Cell 117:817-831.
17. Freitag J, Krieger J, Strotmann J, Breer H. 1995. Two classes of olfactory receptors in Xenopus laevis. Neuron 15:1383-1392.
18. Freitag J, Ludwig G, Andreini I, Rössler P, Breer H. 1998. Olfactory receptors in aquatic and terrestrial vertebrates. J Comp Physiol 183:635-650.
19. Friedrich RW, Korsching SI. 1997. Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 18:737-752.
20. Fritsch G. 1878. Untersuchungen über den feineren Bau des fischgehirns mit besonderer Berücksichtigung der Homologien bei anderren Wirbeltierklassen. Berlin: Verlag der Gutmann'schen Buchhandlung.
21. Fritz A, Gorlick DL, Burd GD. 1996. Neurogenesis in the olfactory bulb of the frog Xenopus laevis shows unique patterns during embryonic development and metamorphosis. Int J Dev Neurosci 14:931-943.
22. Frontini A, Zaidi AU, Hua H, Wolak TP, Greer CA, Kafitz KW, Li W, Zielinski B. 2003. Glomerular territories in the olfactory bulb from the larval stage of the sea lamprey Petromyzon marinus. J Comp Neurol 465:27-37.
23. 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.
24. Higgs DM, Burd GD. 2001. Neuronal turnover in the Xenopus laevis olfactory epithelium during metamorphosis. J Comp Neurol 433:124-130.
25. Hildebrand JG, Shepherd GM. 1997. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595-631.
26. Hofmann MH, Bleckmann H. 1999. Effect of temperature and calcium on transneuronal diffusion of DiI in fixed brain preparations. J Neurosci Meth 88:27-31.
27. Hofmann MH, Meyer DL. 1989a. Central projections of the nervus terminalis in four species of amphibians. Brain Behav Evol 34:301-307.
28. Hofmann MH, Meyer DL. 1989b. The nervus terminalis in larval and adult Xenopus laevis. Brain Res 498:167-169.
29. Hofmann MH, Meyer DL. 1991. Functional subdivisions of the olfactory system correlate with lectin-binding properties in Xenopus. Brain Res 654:344-347.
30. Hofmann MH, Meyer DL. 1992. Peripheral origin of olfactory fibers bypassing the olfactory bulb in Xenopus laevis. Brain Res 589:161-163.
31. Honkanen T, Ekstrom P. 1990. An immunocytochemical study of the olfactory projections in the three-spined stickleback (Gasterosteus aculeatus L.). J Comp Neurol 292:65-72.
32. Huesa G, Anadon R, Yanez J. 2000. Olfactory projections in a chondrostean fish, Acipenser baeri: an experimental study. J Comp Neurol 428:145-158.
33. Joerges J, Küttner A, Galizia G, Menzel R. 1997. Representation of odors and odors mixtures visualized in the honeybee brain. Nature 387:285-288.
34. Kashiwayanagi M, Shimano K, Kurihara K. 1996. Existence of multiple receptors in single neurons: responses of single bullfrog olfactory neurons to many cAMP-dependent and independent odorants. Brain Res 738:222-228.
35. Kauer JS, White J. 2001. Imaging and coding in the olfactory system. Annu Rev Neurosci 24:963-979.
36. Key B, Giorgi PP. 1986. Selective binding of soybean agglutinin to the olfactory system of Xenopus. Neuroscience 18:507-515.
37. Korsching SI. 2001. Odor maps in the brain: spatial aspect of odor representation in sensory surface and olfactory bulb. Cell Mol Life Sci 58:520-530.
38. Koza JM, Wirsig-Wiechmann CR. 2001. A subpopulation of nervus terminalis neurons projects to the olfactory mucosa in Xenopus laevis. J Neurosci Res 66:8-15.
39. Manzini I, Schild D. 2004. Classes of narrowing selectivity of olfactory receptor neurons of Xenopus laevis tadpoles. J Gen Physiol 123:99-107.
40. Manzini I, Rössler W, Schild D. 2002. cAMP-independent responses of olfactory neurons in Xenopus laevis tadpoles and their projection onto olfactory bulb neurons. J Physiol 545:475-484.
41. Masson C, Mustaparta H. 1990. Chemical information processing in the olfactory system of insects. Physiol Rev 70:199-245.
42. Menini A, Lagostena L, Boccaccio A. 2004. Olfaction: from odorant molecules to the olfactory cortex. News Physiol Sci 19:101-104.
43. Meyer DL, Jadhao AG, Bhargava S, Kicliter E. 1996. Bulbar representation of the "water-nose" during Xenopus ontogeny. Neurosci Lett 220:109-112.
44. Mezler M, Konzelmann S, Freitag J, Rössler P, Breer H. 1999. Expression of olfactory receptors during development in Xenopus laevis. J Exp Biol 202:365-376.
45. Mezler M, Fleischer J, Breer H. 2001a. Characteristic features and ligand specificity of the two receptor classes from Xenopus laevis. J Exp Biol 204:2987-2997.
46. Mezler M, Fleischer J, Conzelmann S, Korchi A, Widmayer P, Breer H, Boekhoff L. 2001b. Identification of a non mammalian Golf subtype: functional role in olfactory signaling of airborne odorants in Xenopus laevis. J Comp Neurol 439:400-410.
47. Mombaerts P. 1996. Targeting olfaction. Curr Opin Neurobiol 6:481-486.
48. Mombaerts P. 2004. Odorant receptor gene choice in olfactory sensory neurons: the one receptor-one neuron hypothesis revisited. Curr Opin Neurobiol 14:31-36.
49. Nezlin LP, Schild D. 2000. Structure of the olfactory bulb in tadpoles of Xenopus laevis. Cell Tissue Res 302:21-29.
50. Nezlin LP, Heermann S, Schild D, Rössler W. 2003. Organization of glomeruli in the main olfactory bulb of Xenopus laevis tadpoles. J Comp Neurol 464:257-268.
51. Nieuwkoop PD, Faber J. 1956. Normal table of development of Xenopus laevis (Daudin). Amsterdam: North-Holland.
52. Ochse W. 1948. Die Zucht des südafrikanischen Krallenfrosches Xenopus laevis, Daudin. Gynaecologia 126:57-77.
53. Oland LA, Tolbert LP. 1996. Multiple factors shape development of olfactory glomeruli: insights from an insect model system. J Neurobiol 30:92-109.
54. Parisot-Millery J, Briand L, Bézirard V, Richard-Parpaillon L, Pernollet JC, Gascuel J. 2004. A new OBP (olfactory binding protein) XLaeOBP identified in the aerial olfactory system of Xenopus laevis ana Xenopus tropicalis. FENS Forum 2004. Poster reference A193.10.
55. Pasterkamp RJ, De Winter F, Holtmaat AJ, Verhaagen J. 1998. Evidence for a role of the chemorepellent semaphorin III and its receptor neuropilin-1 in the regeneration of primary olfactory axons. J Neurosci 18:9962-9976.
56. Pinelli C, D'Aniello B, Polese G, Rastogi RK. 2004. Extrabulbar olfactory system and nervus terminalis FMRFamide immunoreactive components in Xenopus laevis ontogenesis. J Chem Neuroanat 28:37-46.
57. Rawson NE, Eberwine J, Dotson R, Jackson J, Ulrich P, Restrepo D. 2000. Expression of mRNAs encoding for two different olfactory receptor neurons. J Neurochem 75:185-195.
58. Reiss JO, Burd GD. 1996. Metamorphic remodeling of the primary olfactory projection in Xenopus: developmental independance of projections from olfactory neuron subclasses. J Neurobiol 32:213-222.
59. Reiss JO, Burd GD. 1997. Cellular and molecular interactions in the development of the Xenopus olfactory system. Semin Cell Dev Biol 8:171-179.
60. Renzi MJ, Wexler TL, Raper JA. 2000. Olfactory sensory axons expression a dominant-negative semaphoring receptor enter the CNS early and overshoot their target. Neuron 28:437-447.
61. 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.
62. Riddle D, Wong L, Oakley B. 1993. Lectin identification of olfactory receptor neuron subclasses with segregated central projections. J Neurosci 13:3018-3033.
63. Rospars JP. 1983. Invariance and sex-specific variation of the glomerular organization in the antennal lobe of a moth Manestra Brassicae and a butterfly Pieris brassicae. J Comp Neurol 220:80-96.
64. Rössler P, Mezler M, Breer H. 1998. Two olfactory marker proteins in Xenopus laevis. J Comp Neurol 395:273-280.
65. Rubin BD, Katz LC. 1999. Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron 23:499-511.
66. Saito S, Taniguchi K. 2000. Expression patterns of glycoconjugates in the three distinctive olfactory pathways of the clawed frog Xenopus laevis. J Vet Med Sci 62:153-159.
67. Satoda M, Takagi S, Ohta K, Hirata T, Fujisawa H. 1995. Differential expression of two cell surface proteins, neuropilin and plexin, in Xenopus olfactory axon subclasses. J Neurosci 15:942-955.
68. Schild D, Manzini I. 2004. Cascades of response vectors of olfactory receptor neurons in Xenopus laevis tadpoles. Eur J Neurosci 20:2111-2123.
69. Schober A, Meyer DL, Von Bartheld CS. 1994. Central projections of the nervus terminalis and the nervus praeopticus in the lungfish brain revealed by nitric oxide synthase. J Comp Neurol 349:1-19.
70. Schwanzel-Fukuda M, Silverman AJ. 1980. The nervus terminalis of the guinea pig: a new luteinizing hormone-releasing hormone (LHRH) neuronal system. J Comp Neurol 191:213-225.
71. Singer MS, Shepherd GM, Greer CA. 1995. Olfactory receptors guide axons. Nature 377:19-20.
72. St John JA, Pasquale EB, Key B. 2002. EphA receptor and Ephrin-A ligands exhibit highly regulated spatial and temporal expression patterns in the developing olfactory system. Dev Brain Res 138:1-14.
73. Strotmann J, Conzelmann S, Beck A, Feinstein P, Breer H, Mombaerts P. 2000. Local permutation in the glomerular array of the mouse olfactory bulb. J Neurosci 20:6927-6938.
74. Suzuki K, Taniguchi K, Syuto B. 1999. Characterization of olfactory receptor organs in Xenopus laevis Daudin. Anat Rec 255:420-427.
75. Szabo T, Blahser S, Denizot JP, Ravaille-Veron M. 1987. High substance P-like immunoreactivity (SPLI) in the olfactory and electrosensory cells of gymnotid fish. Neurosci Lett 81:245-249.
76. Szabo T, Blahser S, Denizot JP, Ravaille-Veron M. 1991. [Extrabulbar olfactory projection in teleost fishes]. R Acad Sci III 312:555-560.
77. 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.
78. Tobias M, Barnard C, O'Hagan R, Horng SH, Rand M, Kelley D. 2004. Vocal communication between male Xenopus laevis. Anim Behav 67:353-365.
79. Tsuboi A, Yoshihara S, Yamazaki N, Kasai H, Asai-Tsuboi H, Komatsu M, Serizawa S, Ishii T, Matsuda Y, Nagawa F, Sakano H. 1999. Olfactory neurons expressing closely related linked and homologous odorant receptor genes tend to project their axons to neighboring glomeruli in the olfactory bulb. J Neurosci 19:8409-8418.
80. Uchida N, Takahashi YK, Tanifuji M, Mori K. 2000. Odor maps in the mammalian olfactory bulb: domains organization and odorant structural features. Nat Neurosci 3:1035-1043.
81. Vassalli A, Rothman A, Feinstein P, Zapotocky M, Mombaerts P. 2002. Minigenes impart odorant receptor-specific axon guidance in the olfactory bulb. Neuron 35:681-696.
82. Vassar R, Chao SK, Sitcheran R, Nunez JM, Vosshall LB, Axel R. 1994. Topographic organization of sensory projections to the olfactory bulb. Cell 79:981-991.
83. Vogler C, Schild D. 1999. Inhibitory and excitatory responses of olfactory receptor neurons of Xenopus laevis tadpoles to stimulation with amino acids. J Exp Biol 202:997-1003.
84. Vosshall LB, Wong AM, Axel R. 2000. An olfactory sensory map in the fly brain. Cell 102:147-159.
85. Wachowiak M, Cohen LB, Zochowski MR. 2002. Distributed and concentration-invariant spatial representations of odorants by receptor neuron input to the turtle olfactory bulb. J Neurophysiol 87:1035-1045.
86. Weiss G. 1986. Die Struktur des Geruchsorgans und des Telencephalons beim südafrikanischen Krallenfrosch, Xenopus laevis (Daudin) und ihre Veränderung während der Metamorphose. PhD Dissertation, Universität Regensburg, Germany.
87. Yoshihara Y, Kawasaki M, Tamada A, Fujita H, Hayashi H, Kagamiyama H, Mori K. 1997. OCAM: a new member of the neural cell adhesion molecule family related to zone-to-zone projection of olfactory and vomeronasal axons. J Neurosci 17:5830-5842.
88. Yu CR, Power J, Barnea G, O'Donnell S, Brown HE, Osborne J, Axel R, Gogos JA. 2004. Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42:553-566.
89. Zhao H, Reed RR. 2001. X inactivation of the OCNC1 channel gene reveals a role for the activity dependent competition of the olfactory system. Cell 104:651-660.