Advertisement

Nasal Chemical Senses in Snakes

  • Mimi Halpern
Part of the NATO Advanced Science Institutes Series book series (NSSA, volume 56)

Abstract

Most terrestrial vertebrates possess at least two nasal chemoreceptive organs: the main olfactory apparatus, which consists of the sensory epithelium lining the posterior and dorsal aspects of the nasal cavity, and the vomeronasal organ, a medially located pouch or sac lying along the nasal septum which is also lined with a sensory epithelium. Whereas considerable attention has, in the past, been devoted to the anatomy, physiology and functional significance of the olfactory system, until very recently relatively little attention has been directed to unraveling the mysteries of the vomeronasal organ.

Keywords

Olfactory Bulb Olfactory System Main Olfactory Bulb Vomeronasal Organ Garter Snake 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allison, A.C., 1953, The morphology of the olfactory system in the vertebrates. Biol. Rev., 28:195–244.CrossRefGoogle Scholar
  2. Altner, H., and Kolnberger, I., 1975, The application of transmission electron microscopy on the study of the olfactory epithelium of vertebrates, in “Methods of Olfactory Research”, D.G. Moulton, A. Turk and J.W. Johnston, Jr., eds., Academic Press, London.Google Scholar
  3. Bard, P., and Mountcastle, V.B., 1948, Some forebrain mechanisms involved in expression of rage with special reference to suppression of angry behavior. Res. Publ. Ass. Nerv. Ment. Dis., 27:362–404.Google Scholar
  4. Bellairs, A., 1959, Reproduction in lizards and snakes. New Biol., 30:73–90.Google Scholar
  5. Blanchard, F.M., and Blanchard, F.C., 1941, Mating of the garter snake Thamnophis sirtalis sirtalis (Linnaeus). Mich. Acad, of Sci., Arts and Letters, Papers., 27:215–234.Google Scholar
  6. Bodian, D., 1936, A method for staining nerve fibers and nerve endings in mounted paraffin sections. Anat. Rec, 65:89–97.CrossRefGoogle Scholar
  7. Bodian, D., 1937, The stain of paraffin sections of nervous tissue with activated protargol: The role of fixatives. Anat. Rec, 69:153–162.CrossRefGoogle Scholar
  8. Bogert, C.M., 1941, Sensory cues used by rattlesnakes in their recognition of ophidian enemies. Ann. New York Acad. Sci., 41:329–343.CrossRefGoogle Scholar
  9. Broadwell, R.D., 1975, Olfactory relationships of the telencephalon and diencephalon in the rabbit I: An autoradiographic study of the efferent connections of the main and accessory olfactory bulbs. J. Comp. Neurol., 163:329–346.PubMedCrossRefGoogle Scholar
  10. Burghardt, G.M., 1966, Stimulus control of the prey attack response in naive garter snakes. Psychonom. Sci., 4:37–38.Google Scholar
  11. Burghardt, G.M., 1970, Chemical perception in reptiles, in “Advances in Chemoreception” Vol.1: Communication by chemical signals, J.W. Johnston, Jr., D.R. Moulton and A. Turk, eds., Appleton-Century-Crofts, New York.Google Scholar
  12. Burghardt, G.M., 1977a, Of iguanas and dinosaurs: Social behavior and communication in neonate reptiles. Amer. Zool., 17:177–190.Google Scholar
  13. Burghardt, G.M., 1977b, The ontogeny, evolution, and stimulus control of feeding in humans and reptiles, in “The Chemical Senses and Nutrition”, M.R. Kare and O. Maller, eds., Academic Press, New York.Google Scholar
  14. Burghardt, G.M., 1980, Behavioral and stimulus correlates of vomeronasal functioning in reptiles: feeding, grouping, sex, and tongue use, in “Chemical Signals Vertebrates and Aquatic Invertebrates”, D. Müller-Schwarze and R.M. Silverstein, eds., Plenum Press, New York.Google Scholar
  15. Burghardt, G.M., and Hess, E.H., 1968, Factors influencing the chemical release of prey attack in newborn snakes. J. Comp. Physiol. Psychol., 66:289–295.PubMedCrossRefGoogle Scholar
  16. Burghardt, G.M., and Pruitt, G.H., 1975, The role of the tongue and senses in feeding of naive and experienced garter snakes. Physiol. Behav., 14:185–194.PubMedCrossRefGoogle Scholar
  17. Cowles, R.B., 1938, Unusual defense postures assumed by rattlesnakes. Copeia, 1938:13–16.CrossRefGoogle Scholar
  18. Cowles, R.B., and Phelan, R.L., 1958, Olfaction in rattlesnakes. Copeia, 1958:77–83.CrossRefGoogle Scholar
  19. Davis, B. J., Macrides, F., Youngs, W.M., Schneider, S.P., and Rosene, D.L., 1978, Efferents and centrifugal afferents to the main and accessory olfactory bulbs in the hamster. Brain Res. Bull., 3:59–72.PubMedCrossRefGoogle Scholar
  20. De01mos, J.S., and Ingram, W.R., 1972, The projection field of the stria terminalis in the rat brain, An experimental study. J. Comp. Neurol., 146:303–334.CrossRefGoogle Scholar
  21. DeOlmos, J.S., Hardy, H., and Heimer, L., 1978, The afferent connections of the main and accessory olfactory bulb informations in the rat: An experimental HRP-study. J. Comp. Neurol., 181: 213–244.CrossRefGoogle Scholar
  22. Devine, M.C., 1976, Species discrimination in mate selection by free-living male garter snakes and experimental evidence for the role of pheromones. Herp. Rev., 7: (Abstract).Google Scholar
  23. Dundee, H., and Miller, M.C.III., 1968, Aggregative behavior and habitat conditioning by the prairie ringneck snake Diadophis punctatus arnyi. Tulane Studies in Zool. Bot., 15:41–58.Google Scholar
  24. Fink, R.P. and Heimer, L., 1967, Two methods for selective silver impregnation of degeneration axons and their synaptic endings in the central nervous system. Brain Res., 4:369–374.PubMedCrossRefGoogle Scholar
  25. Gabe, M., and St.Girons, H., 1976, Contribution a la morphologie comparee des fosses nasales et de leure annexes chez les lepidosorienes. Mem. Muse. Nat. D’Histoire Naturelle (Serie A), 98:1–87.Google Scholar
  26. Gamble, H.J., 1952, An experimental study of the secondary olfactory connections in Lacerta viridis. J. Anat., 86:180–196.PubMedGoogle Scholar
  27. Garstka, W.R., and Crews, D., 1981, Female sex pheromone in the skin and circulation of a garter snake. Science, 214:681–683.PubMedCrossRefGoogle Scholar
  28. Geldard, F.A., 1972, “The Human Senses”, John Wiley and Sons, Inc., New York.Google Scholar
  29. Haberly, L.B., and Price, J.L., 1978a, Association and commissural fiber systems of the olfactory cortex of the rat I: Systems originating in the piriform cortex and adjacent areas. J. Comp. Neurol., 178:711–740.PubMedCrossRefGoogle Scholar
  30. Haberly, L.B., and Price, J, L., 1978b, Association and commissural fiber systems of the olfactory cortex of the rat II: Systems originating in the olfactory peduncle. J. Comp. Neurol., 181:781–808.PubMedCrossRefGoogle Scholar
  31. Halpern, M., 1974, An experimental demonstration of the fornix system in a snake. Soc. Neurosci. 4th Ann. Meeting.Google Scholar
  32. Halpern, M., 1976a, The efferent connections of the olfactory bulb and accessory olfactory bulb in the snakes Thamnophis sirtalis and Thamnophis radix. J. Morphol., 150:553–578.PubMedGoogle Scholar
  33. Halpern, M., 1976b, Efferent connections of the lateral and dorsal cortices of snakes of the genus Thamnophis. Anat. Rec, 184:421.Google Scholar
  34. Halpern, M., 1980, The telencephalon of snakes, in “Comparative Neurology of the Telencephalon”, S.O.E. Ebbesson, ed., Plenum Press, New York.Google Scholar
  35. Halpern, M., and Frumin, N., 1979, Roles of the vomeronasal and olfactory systems in prey attack and feeding in adult garter snakes. Physiol. Behav., 22:1183–1189.PubMedCrossRefGoogle Scholar
  36. Halpern, M., and Kubie, J.L., 1980, Chemical access to the vomeronasal organs of garter snakes. Physiol. Behav., 24:367–371.PubMedCrossRefGoogle Scholar
  37. Halpern, M., and Silfen, R., 1974, The efferent connections of the nucleus shericus in the snake Thamnophis sirtalis. Anat. Rec, 178:368.Google Scholar
  38. Halpern, M., Heller, S., and Vagvolgyi, A., 1981, Garter snakes respond to air-borne odorants with increased tongue-flicking. East. Psychol. Ass. 52nd Ann. Meeting, New York, N.Y.Google Scholar
  39. Heimer, L., 1969, The secondary olfactory connections in mammals, reptiles and sharks. Ann. N.Y. Acad. Sci., 167:129–146.CrossRefGoogle Scholar
  40. Heller, S., and Halpern, M., 1981, Laboratory observations on conspecific and congeneric scent trailing in garter snakes (Thamnophis). Behav. Neurol. Biol., 33:372–377.CrossRefGoogle Scholar
  41. Heller, S.B., and Halpern, M., 1983a, Laboratory observations of aggregative behavior of garter snakes Thamnophis sirtalis. J. Comp. Physiol. Psychol., (in press).Google Scholar
  42. Heller, S.B., and Halpern, M., 1983b, Laboratory observations of aggregative behavior of garter snakes, Thamnophis sirtalis: The roles of the visual, olfactory and vomeronasal senses. J. Comp. Physiol. Psychol., (in press).Google Scholar
  43. Herrick, C.J., 1921, The connections of the vomeronasal nerve, accessory olfactory bulb and amygdala in amphibia. J. Comp. Neurol., 33:213–280.CrossRefGoogle Scholar
  44. Johns, M.A., Feder, H.H., Komisaruk, B.R., and Mayer, A.D., 1978, Urine-induced reflex ovulation in anovulatory rats may be a vomeronasal effect. Nature, 272:446–447.PubMedCrossRefGoogle Scholar
  45. Kahmann, H., 1932, Sinnesphysiologische Studien an Reptilien I: Experimentelle Untersuchungen über das Jakobsonsche Organ der Eidechsen und Schlangen. Zool. Jb., Abt. Allg. Zool. Physiol, d. Tiere, 51:173:238.Google Scholar
  46. Kahmann, H., 1934, Zur Chemorezeption der Schlangen (ein Nachtrag). Zool. Anz., 107:249:263.Google Scholar
  47. Kaneko, N., Debski, E.A., Wilson, M.C., and Whitten, W.K., 1980, Puberty acceleration in mice II: Evidence that the vomeronasal organ is a receptor for the primer pheromone in male mouse urine. Biol. Reprod., 22:873–878.PubMedCrossRefGoogle Scholar
  48. Krettek, J.E., and Price, J.L., 1977a, The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J. Comp. Neurol., 171:157–192.PubMedCrossRefGoogle Scholar
  49. Krettek, J.E., and Price, J.L., 1977b, Projections from the amydaloid complex to the cerebral cortex and thalamus in the rat and cat. J. Comp. Neurol., 172:687–722.PubMedCrossRefGoogle Scholar
  50. Krettek, J.E., and Price, J.L., 1978, Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J. Comp. Neurol., 178:225–254.PubMedCrossRefGoogle Scholar
  51. Kubie, J.L., 1977, “The Role of the Vomeronasal Organ in Garter Snake Prey Trainling and Courtship”, Ph.D. Thesis, School of Graduate Studies, Downstate Medical Center, New York.Google Scholar
  52. Kubie, J.L., and Halpern, M., 1975, Laboratory observations of trailing behavior in garter snakes. J. Comp. Physiol. Psychol., 89:667–674.PubMedCrossRefGoogle Scholar
  53. Kubie, J.L., and Halpern, M., 1978, Garter snake trailing behavior: Effects of varying prey extract concentration and mode of prey extract presentation. J. Comp. Physiol. Psychol., 92:362–373.PubMedCrossRefGoogle Scholar
  54. Kubie, J.L., and Halpern, M., 1979, The chemical senses involved in garter snake prey trailing. J. Comp. Physiol. Psychol., 93:648:667.Google Scholar
  55. Kubie, J.L., Cohen, J., and Halpern, M., 1978a, Shedding of estradiol benzoate treated garter snakes enhances their sexual attractiveness and the attractiveness of untreated penmates. Anim. Behav., 26:562:570.Google Scholar
  56. Kubie, J.L., Vagvolgyi, A., and Halpern, M., 1978b, The roles of the vomeronasal and olfactory systems in the courtship behavior of male garter snakes. J. Comp. Physiol. Psychol., 92:627–641.CrossRefGoogle Scholar
  57. Leonard, C.M., and Scott, J.W., 1971, Origin and distribution of the amygdalofugal pathways in the rat: An experimental neuroanatomical study. J. Comp. Neurol., 141:313–330.PubMedCrossRefGoogle Scholar
  58. Lohmann, A.H.M., 1963, The anterior olfactory lobe of the guinea pig: A descriptive and experimental study. Acta Anat., 53(Suppl.49):1–109.Google Scholar
  59. Marques, D.M., 1979, Roles of the main olfactory and vomeronasal systems in the response of the female hamster to young. Behav. Neural. Biol., 26:311–329.PubMedCrossRefGoogle Scholar
  60. McNemar, Q., 1969, “Psychological Statistics”, 4th edn., Wiley, New York.Google Scholar
  61. Meredith, M., Marques, D.M., O’Connelly, R.J., and Stern, F., 1980, Vomeronasal pump: Significance for male hamster sexual behavior. Science, 207:1224–1226.PubMedCrossRefGoogle Scholar
  62. Moncrieff, P.W., 1967, “The Chemical Senses”, 3rd edn., L.Hill, London.Google Scholar
  63. Naulleau, G., 1965, La biologie et le comportement predateur de Vipera aspis au laboratoire et dans la nature. Bull. Biol. France Belg., 99:395–524.Google Scholar
  64. Noble, G.K., 1937, The sense organs involved in the courtship of Storeria, Thamnophis and other snakes. Bull. Amer. Mus. Nat. Hist., 73:673–725.Google Scholar
  65. Noble, G.K., and Clausen, H.J., 1936, The aggregative behavior of Storeria dekayi and other snakes, with especial reference to the sense organs involved. Ecolog. Monog., 6:269–316.CrossRefGoogle Scholar
  66. Noble, G.K., and Kumpf, K.F., 1936, The function of Jacobson’s organ in lizards. J. Gen. Psychol., 48:371–382.Google Scholar
  67. Powers, J.B., and Winans, S.S., 1975, Vomeronasal organ: Critical role in mediating sexual behavior in the male hamster. Science, 187:961–963.PubMedCrossRefGoogle Scholar
  68. Powers, J.B., Fields, R.B., and Winans, S.S., 1979, Olfactory and vomeronasal system participation in male hamsters’ attraction to female vaginal secretions. Physiol. Behav., 22:77–84.PubMedCrossRefGoogle Scholar
  69. Price, J.L., 1973, An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex. J. Comp. Neurol., 150:87–108.PubMedCrossRefGoogle Scholar
  70. Raisman, G., 1972, An experimental study of the projection of the amygdala to the accessory olfactory bulb and its relationship to the concept of a dual olfactory system. Exp. Brain Res., 14:395–408.Google Scholar
  71. Reynolds, J., and Keverne, E.B., 1979, The accessory olfactory system and its role in pheromonally mediated suppression of oestrus in grouped mice. J. Reprod. Fertil., 57:31–35.PubMedCrossRefGoogle Scholar
  72. Scalia, F., and Winans, S.S., 1975, The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J. Comp. Neurol., 161:31–56.PubMedCrossRefGoogle Scholar
  73. Scalia, F., and Winans, S.S., 1976, New perspectives on the morphology of the olfactory system: Olfactory and vomeronasal pathways in mammals, in “Mammalian Olfaction, Reproductive Processes, and Behavior”, R.L. Doty, ed., Academic Press, New York.Google Scholar
  74. Sheffield, L.P., Law, Ü.M., and Burghardt, G.M., 1968, On the nature of chemical food sign stimuli for newborn garter snakes. Commun. Behav. Biol., 2:7–12.Google Scholar
  75. Ulinski, P.S., 1976, Intracortical connections in the snakes Natrix sipedon and Thamnophis sirtalis. J. Morphol., 150:463–484.PubMedGoogle Scholar
  76. Wang, R.T., and Halpern, M., 1980a, Light and electron microscopic observations on the normal structure of the vomeronasal organ of garter snakes. J. Morphol., 164:47–67.CrossRefGoogle Scholar
  77. Wang, R.T., and Halpern, M., 1980b, Scanning electron microscopic studies of the surface morphology of the vomeronasal epithelium and olfactory epithelium of garter snakes. Amer. J. Anat., 157:399–428.PubMedCrossRefGoogle Scholar
  78. Wang, R.T., and Halpern, M., 1982, Neurogenesis in the vomeronasal epithelium of adult garter snakes I: Degeneration of bipolar neurons and proliferation of undifferentiated cells following experimental vomeronasal axotomy. Brain Res., (in press).Google Scholar
  79. Wang, R.T., Kubie, J.L., and Halpern, M., 1977, Brevital Sodium: An effective anesthetic agent for performing surgery on small reptiles. Copeia, 1977:738–743.CrossRefGoogle Scholar
  80. Weideman, E., 1931, Zur Biologie der Nahrungsaufnahme europäischer Schlangen. Zool. Jb. Abt. System., Ökol. Geo. Tiere, 61:621–636.Google Scholar
  81. Wilde, W.S., 1938, The role of Jacobson’s organ in the feeding reaction of the common garter snake Thamnophis sirtalis sirtalis (Linn). J. Exp. Zool., 77:445–465.CrossRefGoogle Scholar
  82. Winans, S.S., and Powers, J.B., 1977, Olfactory and vomeronasal deafferentation of male hamsters: Histological and behavioral analyses. Brain Res., 126:325–344.PubMedCrossRefGoogle Scholar
  83. Winans, S.S., and Scalia, F., 1970, Amydaloid nucleus: New afferent input from the vomeronasal organ. Science, 170:330–332.PubMedCrossRefGoogle Scholar
  84. Wright, A.H., and Wright, A.A., 1957, “Handbook of Snakes of the United States and Canada”, Comstock Publishing Associates, Ithaca.Google Scholar

Copyright information

© Plenum Press, New York 1983

Authors and Affiliations

  • Mimi Halpern
    • 1
  1. 1.Department of Anatomy and Cell Biology Program in Biological PsychologyDownstate Medical CenterBrooklynUSA

Personalised recommendations