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Chemical signals and vomeronasal system function in axolotls (Ambystoma mexicanum)

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Chemical Signals in Vertebrates 10

Conclusions

We are studying the anatomy and physiology of the olfactory and vomeronasal systems in axolotls with the goal of determining the behavioral functions of these two chemosensory systems in aquatic amphibians. Our anatomical studies demonstrate that the vomeronasal epithelium of axolotls is much like that of other tetrapods. Other studies indicate that the projections from the olfactory and vomeronasal epithelia into the central nervous system are separate through several synapses, suggesting that these chemosensory systems serve different functions. Our electrophysiological experiments have not revealed striking differences in odorant responsivity between the olfactory and vomeronasal epithelia, but we are just beginning to work in this area and cannot draw yet strong conclusions about the relative quality or strength of odorant responses in these sensory epithelia. We have begun to show that odorant cues play a role in both foraging and in social behavior in axolotls; we hope that by combining neurobiological and behavior studies, we will be able to fully understand the ways in which chemosensory stimuli are processed to mediate behavior in axolotls. Given that separate olfactory and vomeronasal systems are present in amphibians and in amniotes, the vomeronasal system must have been present in the last common ancestor of these two groups, and this animal is now thought to have been fully aquatic (Panchen, 1991; Lebedev and Coates, 1995). An understanding of the function of the vomeronasal system in aquatic amphibians may help shed light on the factors that led to the evolutionary origin of the vomeronasal system.

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References

  • Akopian, A., 2000, Neuromodulation of ligand-and voltage-gated channels in the amphibian retina, Microsc. Res. Tech. 50:403–410.

    Article  PubMed  CAS  Google Scholar 

  • Anton, W., 1911, Die Nasenhtihle der Perennibranchiaten, Morphol. Jahrb. 44:179–199.

    Google Scholar 

  • Armstrong, J. B., Duhon, S. T., and Malacinski, G. M., 1989, Raising the axolotl in captivity, in: Developmental Biology of the Axolotl, J. B. Armstrong and G. M. Malacinski, eds., Oxford University Press, New York, pp. 220–227.

    Google Scholar 

  • Arnold, S. J., 1976, Sexual behavior, sexual interference and sexual defense in the salamanders Ambystoma maculatum, Ambystoma tigrinum and Plethodonjordani, Z. Tierpsychol. 42:247–300.

    Google Scholar 

  • Asano-Miyoshi, M., Suda, T., Yasuoka, A., Osima, S., Yamashita, S., Abe, K., and Emori, Y., 2000, Random expression of main and vomeronasal olfactory receptor genes in immature and mature olfactory epithelia of Fugu rubripes, J. Biochem. 127:915–924.

    PubMed  CAS  Google Scholar 

  • Ashmore, J. F., Geleoc, G. S., and Harbott, L., 2000, Molecular mechanisms of sound amplification in the mammalian cochlea, Proc. Natl. Acad. Sci. U. S. A. 97:11759–11764.

    Article  PubMed  CAS  Google Scholar 

  • Bhatnagar, K. P., 1980, The chiropteran vomeronasal organ: Its relevance to the phylogeny of bats, in: Proceedings of the Fifth International Bat Research Conference, D. E. Wilson and A. L. Gardner, eds., Texas Tech Press, Lubbock, TX, pp. 289–315.

    Google Scholar 

  • 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. U. S. A. 95:11987–11992.

    Article  PubMed  CAS  Google Scholar 

  • Cohen-Tannoudji, J., Lavenet, C., Locatelli, A., Tillet, Y., and Signoret, J., 1989, Non-involvement of the accessory olfactory system in the LH response of anoestrous ewes to male odour, J. Reprod. Fert. 86: 135–144.

    Article  CAS  Google Scholar 

  • David, R. S., and Jaeger, R. G., 1981, Prey location through chemical cues by a terrestrial salamander, Copeia 1981:435–440.

    Article  Google Scholar 

  • Dorries, K. M., Adkins-Regan, E., and Halpern, B. P., 1997, Sensitivity and behavioral responses to the pheromone, androstenone, are not mediated by the vomeronasal organ in the pig, Brain Behav. Evol. 49: 52–63.

    Google Scholar 

  • Eisthen, H. L., 1992, Phylogeny of the vomeronasal system and of receptor cell types in the olfactory and vomeronasal epithelia of vertebrates, Micr. Res. Tech. 23:1–21.

    Article  CAS  Google Scholar 

  • Eisthen, H. L., 1997, Evolution of vertebrate olfactory systems, Brain Behav. Evol. 50: 222–233.

    PubMed  CAS  Google Scholar 

  • Eisthen, H. L., 2000, Presence of the vomeronasal system in aquatic salamanders, Phil. Trans. Roy. Soc. (London) 355:1209–1213.

    Article  CAS  Google Scholar 

  • Eisthen, H. L., Sengelaub, D. R., Schroeder, D. M., and Alberts, J. R., 1994, Anatomy and forebrain projections of the olfactory and vomeronasal organs in axolotls (Ambystoma mexicanum), Brain Behav. Evol. 44: 108–124.

    PubMed  CAS  Google Scholar 

  • Farbman, A. I., and Gesteland, R. C., 1974, Fine structure of the olfactory epithelium in the mud puppy, Necturus maculosus, Am. J. Anat. 139:227–244.

    Article  PubMed  CAS  Google Scholar 

  • Firestein, S., and Werblin, F., 1987, Gated currents in isolated olfactory receptor neurons of the larval tiger salamander, Proc. Natl. Acad. Sci. U. S. A. 84:6292–6296.

    Article  PubMed  CAS  Google Scholar 

  • Firestein, S., and Werblin, F., 1989, Odor-induced membrane currents in vertebrate olfactory receptor neurons, Science 244:79–82.

    Article  PubMed  CAS  Google Scholar 

  • Halpern, M., and Kubie, J. L., 1980, Chemical access to the vomeronasal organs of garter snakes, Physiol. Behav. 24:367–371.

    Article  PubMed  CAS  Google Scholar 

  • Halpern, M., Kubie, J. L., 1984, The role of the ophidian vomeronasal system in species-typical behavior, Trends Neurosci. 7:472–477.

    Article  Google Scholar 

  • Halpern, M., and Martinez-Marcos, A., 2003, Structure and function of the vomeronasal system: An update, Prog. Neurobiol. 70:245–318.

    Article  PubMed  CAS  Google Scholar 

  • Herrick, C. J., 1927, The amphibian forebrain IV: The cerebral hemispheres of Amblystoma, J. Comp. Neurol. Psychol. 43:231–325.

    Google Scholar 

  • Herrick, C. J., 1933, The amphibian forebrain IV: Necturus, J. Comp. Neurol. 58:1–288.

    Article  Google Scholar 

  • Herrick, C. J., 1948, The Brain of the Tiger Salamander, University of Chicago Press, Chicago.

    Google Scholar 

  • Hofmann, M. H., and Meyer, D. L., 1992, Peripheral origin of olfactory nerve fibers by-passing the olfactory bulb in Xenopus laevis, Brain Res. 589:161–163.

    Article  PubMed  CAS  Google Scholar 

  • Houck, L. D., and Reagan, N. L., 1990, Male courtship pheromones increase female receptivity in a plethodontid salamander, Anim. Behav. 39:729–734.

    Article  Google Scholar 

  • Kauer, J. S., 2002, On the scents of smell in the salamander, Nature 417:336–342.

    Article  PubMed  CAS  Google Scholar 

  • Kauer, J. S., and Moulton, D. G., 1974, Responses of olfactory bulb neurones to odour stimulation of small nasal areas in the salamander, J. Physiol. 243:717–737.

    PubMed  CAS  Google Scholar 

  • Kikuyama, S., Toyoda, F., Ohmiya, Y., Matsuda, K., Tanaka, S., and Hayashi, H., 1995, Sodefrin: A female-attracting peptide pheromone in newt cloacal glands, Science 267:1643–1645.

    Article  PubMed  CAS  Google Scholar 

  • Kokoros, J. J., and Northcutt, R. G., 1977, Telencephalic afferents of the tiger salamander Ambystoma tigrinum tigrinum (Green), J. Comp. Neurol. 173:613–628.

    Article  PubMed  CAS  Google Scholar 

  • Lebedev, O. A., and Coates, M. I., 1995, The postcranial skeleton of the Devonian tetrapod Tulerpeton curtum Lebedev, Zool. J. Linn. Soc. 114:307–348.

    Article  Google Scholar 

  • Liman, E. R., and Corey, D. P., 1996, Electrophysiological characterization of chemosensory neurons from the mouse vomeronasal organ, J. Neurosci. 16:4625–4637.

    PubMed  CAS  Google Scholar 

  • Lindquist, S. B., and Bachmann, M. D., 1982, The role of visual and olfactory cues in the prey catching behavior of the tiger salamander, Ambystoma tigrinum, Copeia 1982:81–90.

    Article  Google Scholar 

  • Lowell, W. R., and Flanigan, W. F., Jr., 1980, Marine mammal chemoreception, Mamm. Rev. 10: 53–59.

    Google Scholar 

  • Mackay-Sim, A., Duvall, D., and Graves, B. M., 1985, The West Indian manatee (Trichechus manatus) lacks a vomeronasal organ, Brain Behav. Evol. 27:186–194.

    PubMed  CAS  Google Scholar 

  • Mackay-Sim, A., and Kubie, J. L., 1981, The salamander nose: A model system for the study for the study of spatial coding of olfactory quality, Chem. Senses 6:249–257.

    Google Scholar 

  • Mackay-Sim, A., Shaman, P., and Moulton, D. G., 1982, Topographic coding of olfactory quality: Odorant-specific patterns of epithelial responsivity in the salamander, J. Neurophysiol. 48:584–596.

    PubMed  CAS  Google Scholar 

  • Münz, H., Claas, B., and Fritzsch, B., 1984, Electroreceptive and mechanoreceptive units in the lateral line of the axolotl Ambystoma mexicanum, J. Comp. Physiol. A 154:33–44.

    Article  Google Scholar 

  • Nevison, C. M., Armstrong, S., Beynon, R. J., Humphries, R. E., and Hurst, J. L., 2003, The ownership signature in mouse scent marks is involatile, Proc. R. Soc. Lond. B Biol. Sci. 270:1957–1963.

    Article  CAS  Google Scholar 

  • Oelschläger, H. A., and Buhl, E. H., 1985, Development and rudimentation of the peripheral olfactory system in the harbor porpoise Phocoena phocoena (Mammalia: Cetacea), J. Morph. 184:351–360.

    Article  Google Scholar 

  • Panchen, A. L., 1991, The early tetrapods: Classification and the shapes of cladograms, in: Origins of the Higher Groups of Tetrapods: Controversy and Consensus, H.-P. Schultze and L. Trueb, eds., Cornell University Press, Ithaca, NY, pp. 100–144.

    Google Scholar 

  • Park, D., and Eisthen, H. L., 2003, Gonadotropin releasing hormone (GnRH) modulates odorant responses in the peripheral olfactory system of axolotls, J. Neurophysiol. 90:731–738.

    Article  PubMed  CAS  Google Scholar 

  • Park, D., McGuire, J. M., Majchrzak, A. L., Ziobro, J. M., and Eisthen, H. L., 2004, Discrimination of conspecific sex and reproductive condition using chemical cues in axolotls (Ambystoma mexicanum), J. Comp. Physiol. A., in press.

    Google Scholar 

  • Park, D., and Propper, C. R., 2002, The olfactory organ is activated by a repelling pheromone in the red-spotted newt Notophthalmus viridescens, Korean J. Biol. Sci. 6:233–237.

    Google Scholar 

  • Park, D., Zawacki, S. R., and Eisthen, H. L., 2003, Olfactory signal modulation by molluscan cardioexcitatory tetrapeptide (FMRFamide) in axolotls (Ambystoma mexicanum), Chem. Senses 28:339–348.

    Article  PubMed  CAS  Google Scholar 

  • Parsons, T. S., 1959, Nasal anatomy and the phylogeny of reptiles, Evolution 13:175–187.

    Article  Google Scholar 

  • Parsons, T. S., 1967, Evolution of the nasal structures in the lower tetrapods, Am. Zool. 7: 397–413.

    Google Scholar 

  • Parsons, T. S., 1970, The origin of Jacobson’s organ. Forma Functio 3:105–111.

    Google Scholar 

  • Placyk, J. S., Jr., and Graves, B. M., 2002, Prey detection by vomeronasal chemoreception in a plethodontid salamander, J. Chem. Ecol. 28:1017–1036.

    Article  PubMed  CAS  Google Scholar 

  • Rollmann, S. M., Houck, L. D., and Feldhoff, R. C., 1999, Proteinaceous pheromone affecting female receptivity in a terrestrial salamander, Science 285:1907–1909.

    Article  PubMed  CAS  Google Scholar 

  • Sam, M., Vora, S., Malnic, B., Ma, W., Novotny, M. V., and Buck, L.B., 2001, Odorants may arouse instinctive behaviors, Nature 412:142.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt, A., and Roth, G. 1990, Central olfactory and vomeronasal pathways in salamanders, J. Hirnforsch. 31:543–553.

    PubMed  CAS  Google Scholar 

  • Seydel, O., 1895, fiber die Nasenhflhle und das Jacobson’sche Organ der Amphibien: Eine vergleichend-anatomische Untersuchung, Morphol. Jahrb. 23:453–543.

    Google Scholar 

  • Shaffer, H. B., 1993, Phylogenetics of model organisms: The laboratory axolotl, Ambystoma mexicanum, Syst. Biol. 42:508–522.

    Article  Google Scholar 

  • Shepherd, G. M., 1985, Are there labeled lines in the olfactory pathway?, in: Taste, Olfaction, and the Central Nervous System, D. W. Pfaff, Rockefeller University Press, New York, pp. 307–321.

    Google Scholar 

  • Shoop, C. R., 1960, The breeding habits of the mole salamander, Ambystoma talpoideum (Holbrook), in Southeastern Louisiana, Tulane Stud. Zool. Bot. 8:65–82.

    Google Scholar 

  • Singer, A. G., 1991, A chemistry of mammalian pheromones, J. Steroid Biochem. Mol. Biol. 39: 627–632.

    Article  PubMed  CAS  Google Scholar 

  • Smith, T. D., Bhatnagar, K. P., Shimp, K. L., Kinzinger, J. H., Bonar, C. J., Burrows, A. M., Mooney, M. P., and Siegel, M. I., 2002, Histological definition of the vomeronasal organ in humans and chimpanzees, with a comparison to other primates, Anat. Rec. 267:166–176.

    Article  PubMed  Google Scholar 

  • Smith, T. D., Siegel, M. I., and Bhatnagar, K. P., 2001, Reappraisal of the vomeronasal system of catarrhine primates: Ontogeny, morphology, functionality, and persisting questions, Anat. Rec. 265:176–192.

    Article  PubMed  CAS  Google Scholar 

  • Szabo, T., Blähser, S., Denizot, J.-P., and Ravaille-Véron, M., 1991, Projection olfactive primaire extrabulbaire chez certaines poissons t6l6ost6ens, C. R. Acad. Sci. Paris 312:555–560.

    PubMed  CAS  Google Scholar 

  • Toyoda, F., Hayakawa, Y., Ichikawa, M., and Kikuyama, S., 1999, Olfactory responses to a female-attracting pheromone in the newt, Cynops pyrrhogaster, in: R. E. Johnston, D. Müller-Schwarze, and P. W. Sorensen, eds., Advances in Chemical Signals in Vertebrates, Kluwer Academic / Plenum, New York, pp.607–615.

    Google Scholar 

  • Verrell, P. A., 1982, The sexual behavior of the red-spotted newt, Notophthalmus viridescens (Amphibia: Urodela: Salamandridae), Anim. Behav. 30:1224–1236.

    Article  Google Scholar 

  • Wabnitz, P. A., Bowie, J. H., Tyler, M. J., Wallace, J. C., and Smith, B. P., 1999, Aquatic sex pheromone from a male tree frog, Nature 401:444–445.

    Article  PubMed  CAS  Google Scholar 

  • Wirsig-Wiechmann, C. R., Houck, L. D., Feldhoff, P. W., and Feldhoff, R. C., 2002, Pheromonal activation of vomeronasal neurons in plethodontid salamanders. Brain Res. 952:335–344.

    Article  PubMed  CAS  Google Scholar 

  • Wysocki, C. J., Wellington, J. L., and Beauchamp, G. K., 1980, Access of urinary nonvolatiles to the mammalian vomeronasal organ, Science 207:781–783.

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto, N., and Ito, H., 2000, Afferent sources to the ganglion of the terminal nerve in teleosts, J. Comp. Neurol. 428:355–375.

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto, K., Kawai, Y., Hayashi, T., Ohe, Y., Hayashi, H., Toyoda, F., Kawahara, G., Iwata, T., and Kikuyama, S., 2000, Silefrin, a sodefrin-like pheromone in the abdominal gland of the sword-tailed newt, Cynops ensicauda, FEBS Lett. 472:267–270.

    Article  PubMed  CAS  Google Scholar 

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Eisthen, H.L., Park, D. (2005). Chemical signals and vomeronasal system function in axolotls (Ambystoma mexicanum). In: Mason, R.T., LeMaster, M.P., Müller-Schwarze, D. (eds) Chemical Signals in Vertebrates 10. Springer, Boston, MA . https://doi.org/10.1007/0-387-25160-X_26

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