Journal of Chemical Ecology

, Volume 39, Issue 4, pp 451–464 | Cite as

Properties, Projections, and Tuning of Teleost Olfactory Receptor Neurons

  • Alejandra Bazáes
  • Jesús Olivares
  • Oliver Schmachtenberg
Review Article


In many fishes, the olfactory sense participates in such vital processes as feeding, reproduction, orientation, and predator avoidance. In teleosts, these tasks are fulfilled by a single type of olfactory organ for odorant and pheromone detection, containing ciliated and microvillus receptor neurons, and olfactory crypt cells. Recently, progress was made in understanding crypt cell function with the discovery of a V1R-like odorant receptor expressed in this neuron, an analysis of crypt cell odorant tuning properties, and the dissection of crypt cell connectivity within the telecephalon. Here, we review recent findings on the molecular properties, functions, and associated neural pathways of the three types of teleost olfactory receptor neurons with special emphasis on the crypt cell, and evaluate their roles in the detection of food, social and sexual odorants.


Olfaction Smell Pheromone Crypt cell Odorant receptor Fish 



We thank Dr. John T. Caprio for a critical and expert revision of the manuscript. This work was supported by FONDECYT grants 1090343 and 1120513 and the CINV Millennium Institute.


  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.PubMedGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  16. Døving, K. B. and Selset, R. 1980. Behavior patterns in cod released by electrical stimulation of olfactory tract bundlets. Science 207:559–560.PubMedCrossRefGoogle Scholar
  17. Døving, K. B., Selset, R., and Thommesen, G. 1980. Olfactory sensitivity to bile acids in salmonid fishes. Acta Physiol. Scand. 108:123–131.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  19. Eisthen, H. L. 2004. The goldfish knows: Olfactory receptor cell morphology predicts receptor gene expression. J. Comp. Neurol. 477:341–346.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefGoogle Scholar
  23. Finger, T. E. 1975. The distribution of the olfactory tracts in the bullhead catfish, Ictalurus nebulosus. J. Comp. Neurol. 161:125–141.PubMedCrossRefGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedGoogle Scholar
  30. Halpern, M. and Martinez-Marcos, A. 2003. Structure and function of the vomeronasal system: An update. Prog. Neurobiol. 70:245–318.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  35. Hamdani, E. H. and Døving, K. B. 2007. The functional organization of the fish olfactory system. Prog. Neurobiol. 82:80–86.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  40. Hansen, A. and Finger, T. E. 2000. Phyletic distribution of crypt-type olfactory receptor neurons in fishes. Brain. Behav. Evol. 55:100–110.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  46. Hara, T. J. 1994. Olfaction and gustation in fish: An overview. Acta Physiol. Scand. 152:207–217.PubMedCrossRefGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  57. Korsching, S. 2009. The molecular evolution of teleost olfactory receptor gene families. Results Probl. Cell Differ. 47:37–55.PubMedGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  59. Laberge, F. and Hara, T. J. 2001. Neurobiology of fish olfaction: A review. Brain Res. Brain Res. Rev. 36:46–59.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  64. Liberles, S. D. 2009. Trace amine-associated receptors are olfactory receptors in vertebrates. Ann. N. Y. Acad. Sci. 1170:168–172.PubMedCrossRefGoogle Scholar
  65. Liberles, S. D. and Buck, L. B. 2006. A second class of chemosensory receptors in the olfactory epithelium. Nature 442:645–650.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  67. Lipschitz, D. L. and Michel, W. C. 2002. Amino acid odorants stimulate microvillar sensory neurons. Chem. Senses 27:277–286.PubMedCrossRefGoogle Scholar
  68. Margolis, F. L. 1972. A brain protein unique to the olfactory bulb. Proc. Natl. Acad. Sci. USA 69:1221–1224.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.Google Scholar
  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.PubMedGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  114. Speedie, N. and Gerlai, R. 2008. Alarm substance induced behavioral responses in zebrafish (Danio rerio). Behav. Brain Res. 188:168–177.PubMedCrossRefGoogle Scholar
  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.PubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  118. Stacey, N. and Sorensen, P. W. 2005. Reproductive pheromones. Behav. Physiol. Fish 24:359–412.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  123. Thommesen, G. 1983. Morphology, distribution, and specificity of olfactory receptor cells in salmonid fishes. Acta Physiol. Scand. 117:241–249.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  130. von Frisch, K. 1938. Zur psychologie des fisch-schwarmes. Naturwissenschaften 26:601–606.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  133. Whitlock, K. E. 2006. The sense of scents: Olfactory behaviors in the zebrafish. Zebrafish 3:203–213.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Alejandra Bazáes
    • 1
  • Jesús Olivares
    • 1
  • Oliver Schmachtenberg
    • 1
  1. 1.Centro Interdisciplinario de Neurociencia de Valparaíso CINV, Facultad de CienciasUniversidad de ValparaísoValparaísoChile

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