Properties, Projections, and Tuning of Teleost Olfactory Receptor Neurons

Journal of Chemical Ecology

Volumn 39, Issue 4, 2013, Pages 451-464

  Bazáes, Alejandra ^a   Olivares, Jesús ^a   Schmachtenberg, Oliver ^a  

^a UNIVERSIDAD DE VALPARAÍSO   (Chile)

Author keywords

Crypt cell; Fish; Odorant receptor; Olfaction; Pheromone; Smell

Indexed keywords

AVOIDANCE REACTION; CELL ORGANELLE; CILIATE; FEEDING BEHAVIOR; MOLECULAR ANALYSIS; ODOR; OLFACTORY CUE; PHEROMONE; REPRODUCTION; TELEOST;

PISCES; TELEOSTEI;

PHEROMONE;

ANIMAL; ANIMAL BEHAVIOR; FISH; METABOLISM; ODOR; OLFACTORY BULB; OLFACTORY RECEPTOR; PATHOLOGY; PHYSIOLOGY; REVIEW; TELENCEPHALON;

ANIMALS; BEHAVIOR, ANIMAL; FISHES; OLFACTORY BULB; OLFACTORY RECEPTOR NEURONS; PHEROMONES; RECEPTORS, ODORANT; SMELL; TELENCEPHALON;

EID: 84876127576     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-013-0268-1     Document Type: Review

References (140)

1. Baier, H. and Korsching, S. 1994. Olfactory glomeruli in the zebrafish form an invariant pattern and are identifiable across animals. J. Neurosci. 14: 219-230.
2. Bazaes, A. and Schmachtenberg, O. 2012. Odorant tuning of olfactory crypt cells from juvenile and adult rainbow trout. J. Exp. Biol. 215: 1740-1748.
3. Belanger, R. M., Smith, C. M., Corkum, L. D., and Zielinski, B. S. 2003. Morphology and histochemistry of the peripheral olfactory organ in the round goby, Neogobius melanostomus (Teleostei: Gobiidae). J. Morphol. 257: 62-71.
4. Belanger, R. M., Pachkowski, M. D., and Stacey, N. E. 2010. Methyltestosterone-induced changes in electro-olfactogram responses and courtship behaviors of cyprinids. Chem. Senses 35: 65-74.
5. Bettini, S., Lazzari, M., Ciani, F., and Franceschini, V. 2009. Immunohistochemical and histochemical characteristics of the olfactory system of the guppy, Poecilia reticulata (Teleostei, Poecilidae). Anat. Rec. (Hoboken) 292: 1569-1576.
6. Bettini, S., Lazzari, M., and Franceschini, V. 2012. Quantitative analysis of crypt cell population during postnatal development of the olfactory organ of the guppy, Poecilia reticulata (Teleostei, Poecilidae), from birth to sexual maturity. J. Exp. Biol. 215: 2711-2715.
7. Brown, E. N. and Smith, R. J. F. 1998. Acquired predator recognition in juvenile rainbow trout (Oncorhynchus mykiss): Conditioning hatchery-reared fish to recognize chemical cues of a predator. Can. J. Fish. Aquat. Sci. 55: 611-617.
8. Buck, L. and Axel, R. 1991. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65: 175-187.
9. Cao, Y., Oh, B. C., and Stryer, L. 1998. Cloning and localization of two multigene receptor families in goldfish olfactory epithelium. Proc. Natl. Acad. Sci USA 95: 11987-11992.
10. Caprio, J. and Byrd Jr., R. P. 1984. Electrophysiological evidence for acidic, basic, and neutral amino acid olfactory receptor sites in the catfish. J. Gen. Physiol. 84: 403-422.
11. Chivers, D. P., Wisenden, B. D., Hindman, C. J., Michalak, T. A., Kusch, R. C., Kaminskyj, S. G., Jack, K. L., Ferrari, M. C., Pollock, R. J., Halbgewachs, C. F., et al. 2007. Epidermal 'alarm substance' cells of fishes maintained by non-alarm functions: Possible defence against pathogens, parasites and UVB radiation. Proc. Biol. Sci. 274: 2611-2619.
12. Colombo, L., Marconato, A., Colombo, P., and Friso, C. 1980. Endocrinology of teleost reproduction: A testicular steroid pheromone in the black goby, Gobius jozo L. Boll. Zool. 47: 355-364.
13. Defraipont, M. and Sorensen, P. W. 1993. Exposure to the pheromone 17α, 20β-dihydroxy-4-pregnen-3-one enhances the behavioural spawning success, sperm production and sperm motility of male goldfish. Anim. Behav. 46: 245-256.
14. Doldan, M. J., Cid, P., Mantilla, L., and de Miguel Villegas, E. 2011. Development of the olfactory system in turbot (Psetta maxima L.). J. Chem. Neuroanat. 41: 148-157.
15. Døving, K. B. and Lastein, S. 2009. The alarm reaction in fishes-odorants, modulations of responses, neural pathways. Ann. N. Y. Acad. Sci. 1170: 413-423.
16. Døving, K. B. and Selset, R. 1980. Behavior patterns in cod released by electrical stimulation of olfactory tract bundlets. Science 207: 559-560.
17. Døving, K. B., Selset, R., and Thommesen, G. 1980. Olfactory sensitivity to bile acids in salmonid fishes. Acta Physiol. Scand. 108: 123-131.
18. Døving, K. B., Hansson, K. A., Backstrom, T., and Hamdani, E. H. 2011. Visualizing a set of olfactory sensory neurons responding to a bile salt. J. Exp. Biol. 214: 80-87.
19. Eisthen, H. L. 2004. The goldfish knows: Olfactory receptor cell morphology predicts receptor gene expression. J. Comp. Neurol. 477: 341-346.
20. Erickson, J. and Caprio, J. 1984. The spatial distribution of ciliated and microvillous olfactory receptor neurons in the channel catfish is not matched by a differential specificity to amino acid and bile salt stimuli. Chem. Senses 9: 127-141.
21. Evans, R. E., Zielinski, B., and Hara, T. J. 1982. Development and regeneration of the olfactory organ in rainbow trout, pp. 15-38, in Τ. J. Hara (ed.), Chemoreception in Fishes. Elsevier, Amsterdam.
22. Ferrando, S., Bottaro, M., Gallus, L., Girosi, L., Vacchi, M., and Tagliafierro, G. 2006. Observations of crypt neuron-like cells in the olfactory epithelium of a cartilaginous fish. Neurosci. Lett. 403: 280-282.
23. Finger, T. E. 1975. The distribution of the olfactory tracts in the bullhead catfish, Ictalurus nebulosus. J. Comp. Neurol. 161: 125-141.
24. Friedrich, R. W. and Korsching, S. I. 1998. Chemotopic, combinatorial, and noncombinatorial odorant representations in the olfactory bulb revealed using a voltage-sensitive axon tracer. J. Neurosci. 18: 9977-9988.
25. Fuss, S. H. and Korsching, S. I. 2001. Odorant feature detection: activity mapping of structure response relationships in the zebrafish olfactory bulb. J. Neurosci. 21: 8396-8407.
26. Gayoso, J. A., Castro, A., Anadon, R., and Manso, M. J. 2011. Differential bulbar and extrabulbar projections of diverse olfactory receptor neuron populations in the adult zebrafish (Danio rerio). J. Comp. Neurol. 519: 247-276.
27. Gayoso, J. A., Castro, A., Anadon, R., and Manso, M. J. 2012. Crypt cells of the zebrafish Danio rerio mainly project to the dorsomedial glomerular field of the olfactory bulb. Chem. Senses 37: 357-369.
28. Giaquinto, P. C. and Hara, T. J. 2008. Discrimination of bile acids by the rainbow trout olfactory system: Evidence as potential pheromone. Biol. Res. 41: 33-42.
29. Hagey, L. R., Møller, P. R., Hofmann, A. F., and Krasowski, M. D. 2010. Diversity of bile salts in fish and amphibians: Evolution of a complex biochemical pathway. Physiol. Biochem. Zool. 83: 308-321.
30. Halpern, M. and Martinez-Marcos, A. 2003. Structure and function of the vomeronasal system: An update. Prog. Neurobiol. 70: 245-318.
31. Hamdani, E. H. and Døving, K. B. 2002. The alarm reaction in crucian carp is mediated by olfactory neurons with long dendrites. Chem. Senses 27: 395-398.
32. Hamdani, E. H. and Døving, K. B. 2003. Sensitivity and selectivity of neurons in the medial region of the olfactory bulb to skin extract from conspecifics in crucian carp, Carassius carassius. Chem. Senses 28: 181-189.
33. Hamdani, E. H. and Døving, K. 2005. Functional organization of the olfactory system in fish, pp. 221-255, in B. G. Kapoor, F. Ladich, S. Collin, and W. G. Raschi (eds.), Communication in Fish. Oxford & IBH Publishing Co. Pvt. Ltd, New Delhi.
34. Hamdani, E. H. and Døving, K. B. 2006. Specific projection of the sensory crypt cells in the olfactory system in crucian carp, Carassius carassius. Chem. Senses 31: 63-67.
35. Hamdani, E. H. and Døving, K. B. 2007. The functional organization of the fish olfactory system. Prog. Neurobiol. 82: 80-86.
36. Hamdani, E. H., Stabell, O. B., Alexander, G., and Døving, K. B. 2000. Alarm reaction in the crucian carp is mediated by the medial bundle of the medial olfactory tract. Chem. Senses 25: 103-109.
37. Hamdani, E. H., Alexander, G., and Døving, K. B. 2001a. Projection of sensory neurons with microvilli to the lateral olfactory tract indicates their participation in feeding behaviour in crucian carp. Chem. Senses 26: 1139-1144.
38. Hamdani, E. H., Kasumyan, A., and Døving, K. B. 2001b. Is feeding behaviour in crucian carp mediated by the lateral olfactory tract? Chem. Senses 26: 1133-1138.
39. Hamdani, E. H., Lastein, S., Gregersen, F., and Døving, K. B. 2008. Seasonal variations in olfactory sensory neurons-fish sensitivity to sex pheromones explained? Chem. Senses 33: 119-123.
40. Hansen, A. and Finger, T. E. 2000. Phyletic distribution of crypt-type olfactory receptor neurons in fishes. Brain. Behav. Evol. 55: 100-110.
41. Hansen, A. and Zielinski, B. S. 2005. Diversity in the olfactory epithelium of bony fishes: development, lamellar arrangement, sensory neuron cell types and transduction components. J. Neurocytol. 34: 183-208.
42. Hansen, A., Eller, P., Finger, T. E., and Zeiske, E. 1997. The crypt cell: A microvillous ciliated olfactory receptor cell in teleost fishes. Chem. Senses 22: 694-695.
43. Hansen, A., Zippel, H. P., Sorensen, P. W., and Caprio, J. 1999. Ultrastructure of the olfactory epithelium in intact, axotomized, and bulbectomized goldfish, Carassius auratus. Microsc. Res. Tech. 45: 325-338.
44. Hansen, A., Rolen, S. H., Anderson, K., Morita, Y., Caprio, J., and Finger, T. E. 2003. Correlation between olfactory receptor cell type and function in the channel catfish. J. Neurosci. 23: 9328-9339.
45. Hansen, A., Anderson, K. T., and Finger, T. E. 2004. Differential distribution of olfactory receptor neurons in goldfish: Structural and molecular correlates. J. Comp. Neurol. 477: 347-359.
46. Hara, T. J. 1994. Olfaction and gustation in fish: An overview. Acta Physiol. Scand. 152: 207-217.
47. Hara T. J. 2011. Gustation, pp. 45-96, in T. J. Hara, B. S. Zielinski (eds.) Sensory Systems Neuroscience. Fish Physiology. Series 25, Academic Press, San Diego, CA, USA, 2006.
48. Hara, T. J. and Zhang, C. 1998. Topographic bulbar projections and dual neural pathways of the primary olfactory neurons in salmonid fishes. Neuroscience 82: 301-313.
49. Hashiguchi, Y. and Nishida, M. 2007. Evolution of trace amine associated receptor (TAAR) gene family in vertebrates: Lineage-specific expansions and degradations of a second class of vertebrate chemosensory receptors expressed in the olfactory epithelium. Mol. Biol. Evol. 24: 2099-2107.
50. Hashiguchi, Y., Furuta, Y., and Nishida, M. 2008. Evolutionary patterns and selective pressures of odorant/pheromone receptor gene families in teleost fishes. PLoS One 3: e4083.
51. Hubbard, P. C., Barata, E. N., and Canario, A. V. 2003. Olfactory sensitivity of the gilthead seabream (Sparus auratus L) to conspecific body fluids. J. Chem. Ecol. 29: 2481-2498.
52. Hussain, A., Saraiva, L. R., and Korsching, S. I. 2009. Positive Darwinian selection and the birth of an olfactory receptor clade in teleosts. Proc. Natl. Acad. Sci. USA 106: 4313-4318.
53. Jones, D. T. and Reed, R. R. 1989. Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science 244: 790-795.
54. Kang, J. and Caprio, J. 1995. In vivo responses of single olfactory receptor neurons in the channel catfish, Ictalurus punctatus. J. Neurophysiol. 73: 172-177.
55. Kobayashi, M., Sorensen, P. W., and Stacey, N. 2002. Hormonal and pheromonal control of spawning behavior in the goldfish. Fish Physiol. Biochem. 26: 71-84.
56. Koide, T., Miyasaka, N., Morimoto, K., Asakawa, K., Urasaki, A., Kawakami, K., and Yoshihara, Y. 2009. Olfactory neural circuitry for attraction to amino acids revealed by transposon-mediated gene trap approach in zebrafish. Proc. Natl. Acad. Sci. USA 106: 9884-9889.
57. Korsching, S. 2009. The molecular evolution of teleost olfactory receptor gene families. Results Probl. Cell Differ. 47: 37-55.
58. Kudo, H., Doi, Y., Ueda, H., and Kaeriyama, M. 2009. Molecular characterization and histochemical demonstration of salmon olfactory marker protein in the olfactory epithelium of lacustrine sockeye salmon (Oncorhynchus nerka). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 154: 142-150.
59. Laberge, F. and Hara, T. J. 2001. Neurobiology of fish olfaction: A review. Brain Res. Brain Res. Rev. 36: 46-59.
60. Lambert, J. G., Hurk, R., Schoonen, W. G., Resink, J. W., and Oordt, P. G. 1986. Gonadal steroidogenesis and the possible role of steroid glucuronides as sex pheromones in two species of teleosts. Fish Physiol. Biochem. 2: 101-107.
61. Lastein, S., Hamdani, E. H., and Døving, K. B. 2006. Gender distinction in neural discrimination of sex pheromones in the olfactory bulb of crucian carp, Carassius carassius. Chem. Senses 31: 69-77.
62. Li, W., Scott, A. P., Siefkes, M. J., Yan, H., Liu, Q., Yun, S. S., and Gage, D. A. 2002. Bile Acid secreted by male sea lamprey that acts as a sex pheromone. Science 296: 138-141.
63. Li, J., Mack, J. A., Souren, M., Yaksi, E., Higashijima, S., Mione, M., Fetcho, J. R., and Friedrich, R. W. 2005. Early development of functional spatial maps in the zebrafish olfactory bulb. J. Neurosci. 25: 5784-5795.
64. Liberles, S. D. 2009. Trace amine-associated receptors are olfactory receptors in vertebrates. Ann. N. Y. Acad. Sci. 1170: 168-172.
65. Liberles, S. D. and Buck, L. B. 2006. A second class of chemosensory receptors in the olfactory epithelium. Nature 442: 645-650.
66. Lim, H. and Sorensen, P. W. 2011. Polar metabolites synergize the activity of prostaglandin F2alpha in a species-specific hormonal sex pheromone released by ovulated common carp. J. Chem. Ecol. 37: 695-704.
67. Lipschitz, D. L. and Michel, W. C. 2002. Amino acid odorants stimulate microvillar sensory neurons. Chem. Senses 27: 277-286.
68. Margolis, F. L. 1972. A brain protein unique to the olfactory bulb. Proc. Natl. Acad. Sci. USA 69: 1221-1224.
69. Mathuru, A. S., Kibat, C., Cheong, W. F., Shui, G., Wenk, M. R., Friedrich, R. W., and Jesuthasan, S. 2012. Chondroitin fragments are odorants that trigger fear behavior in fish. Curr. Biol. 22: 538-544.
70. Meredith, T. L., Caprio, J., and Kajiura, S. M. 2012. Sensitivity and specificity of the olfactory epithelia of two elasmobranch species to bile salts. J. Exp. Biol. 215: 2660-2667.
71. Michel, W. C. and Derbidge, D. S. 1997. Evidence of distinct amino acid and bile salt receptors in the olfactory system of the zebrafish, Danio rerio. Brain Res. 764: 179-187.
72. Michel, W. C., Sanderson, M. J., Olson, J. K., and Lipschitz, D. L. 2003. Evidence of a novel transduction pathway mediating detection of polyamines by the zebrafish olfactory system. J. Exp. Biol. 206: 1697-1706.
73. Miklavc, P. and Valentinčič, T. 2012. Chemotopy of amino acids on the olfactory bulb predicts olfactory discrimination capabilities of zebrafish Danio rerio. Chem. Senses 37: 65-75.
74. Miyasaka, N., Morimoto, K., Tsubokawa, T., Higashijima, S., Okamoto, H., and Yoshihara, Y. 2009. From the olfactory bulb to higher brain centers: Genetic visualization of secondary olfactory pathways in zebrafish. J. Neurosci. 29: 4756-4767.
75. Ngai, J., Dowling, M. M., Buck, L., Axel, R., and Chess, A. 1993. The family of genes encoding odorant receptors in the channel catfish. Cell 72: 657-666.
76. Nieuwenhuys, R. 2011. The development and general morphology of the telencephalon of actinopterygian fishes: Synopsis, documentation and commentary. Brain Struct. Funct. 215: 141-157.
77. Nieuwenhuys, R., Ten donkelaar, H. J., and Nicholson, C. 1998. Holosteans and teleosts, pp. 759-938, in The Central Nervous System of Vertebrates, Chapter 15, Volume 2. Springer-Verlag, Berlin and Heidelberg.
78. Nikonov, A. A. and Caprio, J. 2001. Electrophysiological evidence for a chemotopy of biologically relevant odors in the olfactory bulb of the channel catfish. J. Neurophysiol. 86: 1869-1876.
79. Nikonov, A. A. and Caprio, J. 2007a. Highly specific olfactory receptor neurons for types of amino acids in the channel catfish. J. Neurophysiol. 98: 1909-1918.
80. Nikonov, A. A. and Caprio, J. 2007b. Responses of olfactory forebrain units to amino acids in the channel catfish. J. Neurophysiol. 97: 2490-2498.
81. Nikonov, A. A., Finger, T. E., and Caprio, J. 2005. Beyond the olfactory bulb: An odotopic map in the forebrain. Proc. Natl. Acad. Sci. USA 102: 18688-18693.
82. Ogawa, K. and Caprio, J. 2010. Major differences in the proportion of amino acid fiber types transmitting taste information from oral and extraoral regions in the channel catfish. J. Neurophysiol. 103: 2062-2073.
83. Oka, Y. and Korsching, S. I. 2011. Shared and unique G alpha proteins in the zebrafish versus mammalian senses of taste and smell. Chem. Senses 36: 357-365.
84. Oka, Y., Saraiva, L. R., and Korsching, S. I. 2011. Crypt neurons express a single V1R-related ora gene. Chem. Senses 37: 219-227.
85. Pankhurst, N. W., Hilder, P. I., and Pankhurst, P. M. 1999. Reproductive condition and behavior in relation to plasma levels of gonadal steroids in the spiny damselfish Acanthochromis polyacanthus. Gen. Comp. Endocrinol. 115: 53-69.
86. Parra, K. V., Adrian Jr., J. C., and Gerlai, R. 2009. The synthetic substance hypoxanthine 3-N-oxide elicits alarm reactions in zebrafish (Danio rerio). Behav. Brain Res. 205: 336-341.
87. Pfister, P. and Rodriguez, I. 2005. Olfactory expression of a single and highly variable V1r pheromone receptor-like gene in fish species. Proc. Natl. Acad. Sci. USA 102: 5489-5494.
88. Poling, K. R., Fraser, E. J., and Sorensen, P. W. 2001. The three steroidal components of the goldfish preovulatory pheromone signal evoke different behaviors in males. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 129: 645-651.
89. Polkinghorne, C. N., Olson, J. M., Galaher, D. G., and Sorensen, P. W. 2001. Larval sea lamprey release two unique bile acids to the water at a rate sufficient to produce detectable riverine pheromone plumes. Fish Physiol. Biochem. 24: 15-30.
90. Pottinger, T. G. and Moore, A. 1997. Characterization of putative steroid receptors in the membrane, cytosol and nuclear fractions from the olfactory tissue of brown and rainbow trout. Fish Physiol. Biochem. 16: 45-63.
91. Poulin, R., Marcogliese, D. J., and McLaughlin, J. D. 1999. Skin-penetrating parasites and the release of alarm substances in juvenile rainbow trout. J. Fish Biol. 55: 47-53.
92. Resink, J. W., Schoonen, W. G., Albers, P. C., File, D. M., Notenboom, C. D., van den Hurk, R., and van Oordt, P. G. 1989. The chemical nature of sex attracting pheromones from seminal vesicle of Africa catfish, Clarias gariepinus. Aquaculture 83: 137-151.
93. Riddle, D. R., Wong, L. D., and Oakley, B. 1993. Lectin identification of olfactory receptor neuron subclasses with segregated central projections. J. Neurosci. 13: 3018-3033.
94. Rolen, S. H., Sorensen, P. W., Mattson, D., and Caprio, J. 2003. Polyamines as olfactory stimuli in the goldfish Carassius auratus. J. Exp. Biol. 206: 1683-1696.
95. Sandulescu, C. M., Teow, R. Y., Hale, M. E., and Zhang, C. 2011. Onset and dynamic expression of S100 proteins in the olfactory organ and the lateral line system in zebrafish development. Brain Res. 1383: 120-127.
96. Sato, K. and Suzuki, N. 2000. The contribution of a Ca(2+)-activated Cl(-) conductance to amino-acid-induced inward current responses of ciliated olfactory neurons of the rainbow trout. J. Exp. Biol. 203: 253-262.
97. Sato, K. and Suzuki, N. 2001. Whole-cell response characteristics of ciliated and microvillous olfactory receptor neurons to amino acids, pheromone candidates and urine in rainbow trout. Chem. Senses 26: 1145-1156.
98. Sato, Y., Miyasaka, N., and Yoshihara, Y. 2005. Mutually exclusive glomerular innervation by two distinct types of olfactory sensory neurons revealed in transgenic zebrafish. J. Neurosci. 25: 4889-4897.
99. Satou, M., Oka, Y., Kusunoki, M., Matsushima, T., Kato, M., Fujita, I., and Ueda, K. 1984. Telencephalic and preoptic areas integrate sexual behavior in hime salmon (landlocked red salmon, Oncorhynchus nerka): Results of electrical brain stimulation experiments. Physiol. Behav. 33: 441-447.
100. Schmachtenberg, O. 2006. Histological and electrophysiological properties of crypt cells from the olfactory epithelium of the marine teleost Trachurus symmetricus. J. Comp. Neurol. 495: 113-121.
101. Schmachtenberg, O. and Bacigalupo, J. 2004. Olfactory transduction in ciliated receptor neurons of the Cabinza grunt, Isacia conceptionis (Teleostei: Haemulidae). Eur. J. Neurosci. 20: 3378-3386.
102. Shoji, T., Ueda, H., Ohgami, T., Sakamoto, T., Katsuragi, Y., Yamauchi, K., and Kurihara, K. 2000. Amino acids dissolved in stream water as possible home stream odorants for masu salmon. Chem. Senses 25: 533-540.
103. Sorensen, P. W. and Caprio, J. 1998. Chemoreception, pp. 375-405, in D. H. Evens (ed.), The Physiology of Fishes. CRC LLC, New York.
104. Sorensen, P. W. and Scott, A. P. 1994. The evolution of hormonal sex pheromones in teleost fish: poor correlation between the pattern of steroid release by goldfish and olfactory sensitivity suggests that these cues evolved as a result of chemical spying rather than signal specialization. Acta Physiol. Scand. 152: 191-205.
105. Sorensen, P. W., Hara, T. J., and Stacey, N. E. 1987. Extreme olfactory sensitivity of mature and gonadally-regressed goldfish to a potent steroidal pheromone, 17α, 20β-dihydroxy-4-pregnen-3-one. J. Comp. Physiol. A 160: 305-313.
106. Sorensen, P. W., Hara, T. J., Stacey, N. E., and Goetz, F. W. 1988. F prostaglandins function as potent olfactory stimulants that comprise the postovulatory female sex pheromone in goldfish. Biol. Reprod. 39: 1039-1050.
107. Sorensen, P. W., Stacey, N. E., and Chamberlain, K. J. 1989. Differing behavioral and endocrinological effects of two female sex pheromones on male goldfish. Horm. Behav. 23: 317-332.
108. Sorensen, P. W., Hara, T. J., Stacey, N. E., and Dulka, J. G. 1990. Extreme olfactory specificity of the male goldfish to the preovulatory steroidal pheromone 17α, 20β-dihydroxy-4-pregnen-3-one. J. Comp. Physiol. A 166: 373-383.
109. Sorensen, P. W., Hara, T. J., and Stacey, N. E. 1991. Sex pheromones selectively stimulate the medial olfactory tracts of male goldfish. Brain Res. 558: 343-347.
110. Sorensen, P. W., Scott, A. P., Stacey, N. E., and Bowdin, L. 1995. Sulfated 17α, 20β-dihydroxy-4-pregnen-3-one functions as a potent and specific olfactory stimulant with pheromonal actions in the goldfish. Gen. Comp. Endocrinol. 100: 128-142.
111. Sorensen, P. W., Scott, A. P., and Kihslinger, R. L. 2000. How common hormonal metabolites function as relatively specific pheromones in the goldfish, pp. 125-129, in B. Norberg, O. S. Kjesbu, G. L. Taranger, E. Andersson, and S. O. Stefansson (eds.), Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. Bergen, Norway.
112. Sorensen, P. W., Pinillos, M., and Scott, A. P. 2005. Sexually mature male goldfish release large quantities of androstenedione into the water where it functions as a pheromone. Gen. Comp. Endocrinol. 140: 164-175.
113. Speca, D. J., Lin, D. M., Sorensen, P. W., Isacoff, E. Y., Ngai, J., and Dittman, A. H. 1999. Functional identification of a goldfish odorant receptor. Neuron 23: 487-498.
114. Speedie, N. and Gerlai, R. 2008. Alarm substance induced behavioral responses in zebrafish (Danio rerio). Behav. Brain Res. 188: 168-177.
115. Spence, R., Gerlach, G., Lawrence, C., and Smith, C. 2008. The behaviour and ecology of the zebrafish, Danio rerio. Biol. Rev. Camb. Philos. Soc. 83: 13-34.
116. Stabell, O. 1984. Homing and olfaction in salmonids: A critical review with special reference to the Atlantic salmon. Biol. Rev. Camb. Philos. Soc. 59: 333-388.
117. Stacey, N. E. and Kyle, A. L. 1983. Effects of olfactory tract lesions on sexual and feeding behavior in the goldfish. Physiol. Behav. 30: 621-628.
118. Stacey, N. and Sorensen, P. W. 2005. Reproductive pheromones. Behav. Physiol. Fish 24: 359-412.
119. Stacey, N. and Sorensen, P. W. 2009. Hormonal pheromones in fish. Chapter 18, pp. 639-681, in D. W. Pfaff, A. P. Arnold, A. M. Etgen, S. E. Fahrbach, and R. T. Rubin (eds.), Hormones, Brain and Behavior, 2nd ed., Vol. 1. Elsevier Press, San Diego.
120. Sutterlin, A. M. and Sutterlin, N. 1971. Electrical responses of the olfactory epithelium of Atlantic salmon (Salmo salar). J. Fish. Res. Board Can. 29: 565-572.
121. Suzuki, N. and Tucker, D. 1971. Amino acids as olfactory stimuli in freshwater catfish, Ictalurus catus (Linn). Comp. Biochem. Physiol. A Comp. Physiol. 40: 399-404.
122. Thommesen, G. 1978. The spatial distribution of odour induced potentials in the olfactory bulb of char and trout (Salmonidae). Acta Physiol. Scand. 102: 205-217.
123. Thommesen, G. 1983. Morphology, distribution, and specificity of olfactory receptor cells in salmonid fishes. Acta Physiol. Scand. 117: 241-249.
124. Valentinčič, T., Lamb, C. F., and Caprio, J. 1999. Expression of a reflex biting/snapping response to amino acids prior to first exogenous feeding in salmonid alevins. Physiol. Behav. 67: 567-572.
125. Valentinčič, T., Kralj, J., Stenovec, M., Koce, A., and Caprio, J. 2000. The behavioral detection of binary mixtures of amino acids and their individual components by catfish. J. Exp. Biol. 203: 3307-3317.
126. van den Hurk, R. and Lambert, J. G. D. 1983. Ovarian steroid glucuronides function as sex pheromones for male zebrafish, Brachydanio rerio. Canad. J. Zool. 61: 2381-2387.
127. van den Hurk, R., Schoonen, W. G., van Zoelen, G. A., and Lambert, J. G. 1987. The biosynthesis of steroid glucuronides in the testis of the zebrafish, Brachydanio rerio, and their pheromonal function as ovulation inducers. Gen. Comp. Endocrinol. 68: 179-188.
128. Vielma, A., Ardiles, A., Delgado, L., and Schmachtenberg, O. 2008. The elusive crypt olfactory receptor neuron: evidence for its stimulation by amino acids and cAMP pathway agonists. J. Exp. Biol. 211: 2417-2422.
129. von Bartheld, C. S., Meyer, D. L., Fiebig, E., and Ebbesson, S. O. 1984. Central connections of the olfactory bulb in the goldfish, Carassius auratus. Cell Tissue Res. 238: 475-487.
130. von Frisch, K. 1938. Zur psychologie des fisch-schwarmes. Naturwissenschaften 26: 601-606.
131. von Rekowski, C. and Zippel, H. P. 1993. In goldfish the qualitative discriminative ability for odors rapidly returns after bilateral nerve axotomy and lateral olfactory tract transection. Brain Res. 618: 338-340.
132. Weltzien, F. A., Hoglund, E., Hamdani, E. H., and Døving, K. B. 2003. Does the lateral bundle of the medial olfactory tract mediate reproductive behavior in male crucian carp? Chem. Senses 28: 293-300.
133. Whitlock, K. E. 2006. The sense of scents: Olfactory behaviors in the zebrafish. Zebrafish 3: 203-213.
134. Wisby, W. J. and Hasler, A. D. 1954. Effect of olfactory occlusion on migrating silver salmon (Oncorhynchus kisutch). J. Fish. Res. Board Can. 11: 472-478.
135. Yaksi, E., Von Saint Paul, F., Niessing, J., Bundschuh, S. T., and Friedrich, R. W. 2009. Transformation of odor representations in target areas of the olfactory bulb. Nat. Neurosci. 12: 474-482.
136. Yamamoto, Y. and Ueda, H. 2009. Behavioral responses by migratory chum salmon to amino acids in natal stream water. Zoolog Sci 26: 778-782.
137. Yambe, H., Kitamura, S., Kamio, M., Yamada, M., Matsunaga, S., Fusetani, N., and Yamazaki, F. 2006. L-Kynurenine, an amino acid identified as a sex pheromone in the urine of ovulated female masu salmon. Proc. Natl. Acad. Sci. USA 103: 15370-15374.
138. Zeiske, E., Theisen, B., and Breucker, H. 1992. Structure, development, and evolutionary aspects of the peripheral olfactory system, pp. 13-39, in T. J. Hara (ed.), Fish Chemoreception. Chapman and Hall, London.
139. Zhang, C. and Hara, T. J. 2009. Lake char (Salvelinus namaycush) olfactory neurons are highly sensitive and specific to bile acids. J. Comp. Physiol. A 195: 203-215.
140. Zhang, C., Brown, S. B., and Hara, T. J. 2001. Biochemical and physiological evidence that bile acids produced and released by lake char (Salvelinus namaycush) function as chemical signals. J. Comp. Physiol. B 171: 161-171.