Skip to main content
SpringerLink
Log in

Olfactory Imprinting in Salmon: New Models and Approaches

  • Chapter
The Senses of Fish

Abstract

Olfactory imprinting is a specialized form of unconditioned learning in which olfactory information is acquired and then used in some specific behavioral context later in life. A key characteristics of an imprinted memory is that it is formed during a sensitive period of development. This prerequisite thus distinguishes olfactory imprinting from other types of odor learning in which only conditioned exposure to an odor stimulus is required for learning to occur. Most investigations designed to explore the mechanisms underlying olfactory imprinting have focused on mammalian species, concentrating on synaptic events at the level of the main and accessory olfactory bulbs (Hudson 1993). Recent integrative studies with salmon (Dittman et al. 1997; Nevitt et al. 1994) and rabbits (Semke et al. 1995), however, provide compelling evidence that highly specific imprinted odor memories may also be retained in the periphery, i.e., at the level of the olfactory epithelium proper. These results suggest that populations of olfactory receptor neurons may be selectively tuned to respond to odor molecules present during a hormonally linked sensitive period. A potential key to the mechanism of how these peripheral odor memories become established draws on the unique ability of olfactory receptor neurons to turn over throughout an organism’s life span (Farbman 1994). How hormonal and environmental factors work together to influence olfactory neurogenesis is not yet been rigorously addressed in the literature (Shepherd 1994), but ultimately may provide important new insights not only for basic science but for salmon conservation as well.

This chapter was first published in 1998 under the title “A New Model for Olfactory Imprinting in Salmon” in: Integrative Biology 1 (6): 215–223. It has been republished with permission from Wiley Publications.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Bowers S.M. (1988) Morphologic differences in the Atlantic salmon olfactory bulb between the parr and smolt stages of development, M.S., Yale University.

    Google Scholar 

  • Breer H., Klemm T., Boekhoff I. (1992) Nitric oxide mediated formation of cyclic GMP in the olfactory system, NeuroReport 2: 1030–1032.

    Article  Google Scholar 

  • Brennan P.A., Keverne E.B. (1997) Neural mechanisms of mammalian olfactory learning, Progress in Neurobiology (Oxford) 51: 457–481.

    Article  CAS  Google Scholar 

  • Brent A.G., Moore D.D., Larsen P.R. (1991) Thyroid hormone regulation of gene expression, Ann. Rev. Physiol. 53: 17–35.

    Article  CAS  Google Scholar 

  • Buck L., Axel R. (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition, Cell 65: 175–187.

    Article  PubMed  CAS  Google Scholar 

  • Burd G.D. (1990) Role of thyroxine in neural development of the olfactory system, in: Dovin K.B. (Eds.), The Proceedings of the Tenth International Symposium on Olfaction and Taste, GCA A.S. Press, Oslo, pp. 196–205.

    Google Scholar 

  • Burd G.D. (1991) Development of the olfactory nerve in the African clawed frog, Xenopus laevis: I. Normal development, J. Comp. Neurol. 304: 123–134.

    Article  PubMed  CAS  Google Scholar 

  • Chen Z., Pace U., Heldman J., Shapira A., Lancet D. (1986) Isolated frog olfactory cilia: a preparation of dendritic membranes from chemosensory neurons, J. Neurosci. 6: 2146–2154.

    PubMed  CAS  Google Scholar 

  • Cooper J.C., Hasler A.D. (1974) Electroencephalographic evidence for retention of olfactory cues in homing Coho salmon, Science 183: 336–338.

    Article  PubMed  CAS  Google Scholar 

  • Cooper J.C., Hasler A.D. (1976) Electrophysiological studies of morpholine-imprinted coho salmon (Oncorhynchus kisutch) and rainbow trout (Salmo gairdneri), J. Fish. Res. Board Can. 33: 688–694.

    Article  Google Scholar 

  • Courtenay S.C. (1989) Learning and Memory of Chemosensory Stimuli by Underyearling Coho Salmon, Oncorhynchus Kisutch Walbaum, Ph.D., University of British Columbia.

    Google Scholar 

  • DeGroot L.J., Refetoff S., Bernal J., Rue P.A., Coleoni A.H. (1978) Nuclear receptors for thyroid hormone, J. Endocrinol. Invest. 1: 79–88.

    PubMed  CAS  Google Scholar 

  • Denver R.J. (1998) The molecular basis of thyroid hormone-dependent central nervous system remodeling during amphibian metamorphosis, Comp. Biochem. Physiol. C 119: 219–228.

    Article  PubMed  CAS  Google Scholar 

  • Dickhoff W.W., Darling D.S., Gorbman A. (1982) Thyroid function during smoltification of salmonid fish, Gumma Symp. Endocr. 19: 45–61.

    CAS  Google Scholar 

  • Dickhoff W.W., Sullivan C. (1987) Involvement of the thyroid gland in smoltification, with special reference to metabolic and developmental processes, Am. Fish. Soc. Symp. 1: 197–210.

    Google Scholar 

  • Dittman A.H. (1994) Behavioral and Biochemical Mechanisms of Olfactory Imprinting and Homing by Coho Salmon, Ph.D., University of Washington, Seattle.

    Google Scholar 

  • Dittman A.H., Quinn T.P. (1996) Homing in Pacific salmon: mechanisms and ecological basis, J. Exp. Biol. 199: 83–91.

    PubMed  Google Scholar 

  • Dittman A.H., Quinn T.P, Dickhoff W.W., Larsen D.A. (1994) Interactions between novel water, thyroxine and olfactory imprinting in underyearling coho salmon, Oncorhynchus kisutch (Walbaum), Aquacult. Fish. Manag. 25: 157–169.

    Google Scholar 

  • Dittman A.H., Quinn T.P., Nevitt G.A. (1996) Timing of imprinting to natural and artificial odors by coho salmon (Oncorhynchus kisutch), Can. J. Fish. Aquat. Sci. 53: 434–442.

    Article  Google Scholar 

  • Dittman A.H., Quinn T.P, Nevitt G.A., Hacker B., Storm D.R. (1997) Sensitization of olfactory guanylyl cyclase to a specific imprinted odorant in coho salmon, Neuron 19: 381–389.

    Article  PubMed  CAS  Google Scholar 

  • Dodson J.J., Bitterman M.E. (1989) Compound uniqueness and the interactive role of morpholine in fish chemoreception, Biol. Behav. 14: 13–27.

    Google Scholar 

  • Farbman A.I. (1994) Developmental biology of olfactory sensory neurons, Sem. Cell Biol. 5: 3–10.

    Article  CAS  Google Scholar 

  • Fleming I.A., Gross M.R. (1992) Reproductive behavior of hatchery and wild coho salmon (Oncorhynchus kisutch): does it differ? Aquaculture 103: 101–121.

    Article  Google Scholar 

  • Fleming I.A., Gross M.R. (1994) Breeding competition in a Pacific salmon (coho:Oncorhynchus kisutch): measures of natural and sexual selection, Evolution 48: 637–657.

    Article  Google Scholar 

  • Folmar L.C., Dickhoff W.W. (1980) The parr-smolt transformation (smolitification) and seawater adaptation, Aquaculture 21: 1–37.

    Article  CAS  Google Scholar 

  • Glass C.K., Holloway J.M. (1990) Regulation of gene expression by the thyroid hormone receptor, Biochem. Biophys. Acta 1032: 157–176.

    PubMed  CAS  Google Scholar 

  • Gould F., Butcher L.L. (1989) Developing cholinergic basal forebrain neurons are sensitive to thyroid hormone, J. Neurosci. 9: 3347–3358.

    PubMed  CAS  Google Scholar 

  • Grant W.S. (1997) Genetic effects of straying of non-native fish hatchery fish into natural populations: proceedings of the workshop, U.S. Dept. Commerce, NOAA Tech Memo: NMFS-NWFSC-30 130p.

    Google Scholar 

  • Hara T.J., Brown S.B. (1979) Olfactory bulbar electrical responses of rainbow trout (Salmo gairdneri) exposed to morpholine during smoltification, J.Fish. Res. Board Can. 36: 1186–1190.

    Article  Google Scholar 

  • Hara T.J., MacDonald S., Evans R.E., Murui T., Arai S. (1984) Morpholine, bile acids and skin mucus as possible chemical cues in salmonid homing: an electrophysiological re-evaluation, in: McCleave J.D., Arnold G.P, Dodson J.D., Neill W.H. (Eds.), Mechanisms of Migration in Fishes, Plenum Publishing Corp., New York, pp. 363–378.

    Chapter  Google Scholar 

  • Hara T.J., Ueda K., Gorbman A. (1965) Electroencephalographic studies in homing salmon, Science 149: 884–885.

    Article  PubMed  CAS  Google Scholar 

  • Hara T.J., Zielinski B. (1989) Structural and functional development of the olfactory organ in teleosts, Trans. Am. Fish Soc. 118: 183–194.

    Article  Google Scholar 

  • Hasler A.D., Scholz A.T. (1983) Olfactory Imprinting and Homing in Salmon, Springer-Verlag, New York.

    Book  Google Scholar 

  • Hasler A.D., Wisby W.J. (1951) Discrimination of stream odors by fishes and relation to parent stream behavior, Am. Nat. 85: 223–238.

    Article  CAS  Google Scholar 

  • Higgs D.A., Fagerlund U.H.M., Eales J.G., McBride J.R. (1982) Application of thyroid and steroid hormones as anabolic agents in fish culture, Comp. Biochem. Physiol. 73B: 143476.

    Google Scholar 

  • Hoar W.S. (1988) The physiology of smoking in salmonids, in: Hoar W.S., Randall D.J. (Eds.), Fish Physiology, Academic Press, New York, pp. 275–343.

    Google Scholar 

  • Hoffnagle T.L., Rivizzani A.J. (1990) Stimulation of plasma thyroxine levels by novel water chemistry during smoltification in Chinook salmon (Oncorhynchus tshawytscha), Can. J. Fish. Aquat. Sci. 47: 1513–1517.

    Article  CAS  Google Scholar 

  • Hofmann M.H., Michler A., Meyer D.L. (1989) Thyroxine influences neuronal connectivity in the adult frog brain, Brain Res. 492: 389–391.

    Article  PubMed  CAS  Google Scholar 

  • Hoskins S.G., Grobstein P. (1985) Development of the ipsilateral retinothalamic projection in the frog, Xenopus laevis, J. Neurosci. 5: 930–940.

    PubMed  CAS  Google Scholar 

  • Hudson R. (1993) Olfactory imprinting, Curr. Op. Neurobiol. 3: 548–552.

    Article  PubMed  CAS  Google Scholar 

  • Iwamoto R.N. (1982) Strain-Photoperiod-Temperature Interactions in Coho Salmon: Freshwater Growth, Smoltification and Seawater Adaptation, Ph.D., University of Washington, Seattle.

    Google Scholar 

  • Jarrard H.E. (1997) Postembryonic changes in the structure of the olfactory bulb of the Chinook salmon (Oncorhynchus tshawytscha) across its life history, Brain Behav. Evol. 49: 249–260.

    Article  PubMed  CAS  Google Scholar 

  • Lin R.J., Rivas R.J., Grau E.G., Nishoka R.S., Bern H.A. (1985) Changes in plasma thyroxine following transfer of young coho salmon (Oncorhynchus kisutch) from fresh water to fresh water, Aquaculture 45: 381–382.

    Article  Google Scholar 

  • Mackay-Sim A., Beard M.D. (1987) Hypothyroidism disrupts neural development in the olfactory epithelium of adult mice, Dev. Brain. Res. 36: 190–198.

    Article  CAS  Google Scholar 

  • Meisami E., Louie J., Hudson R., Distel H. (1990) A morphometric comparison of the olfactory epithelium of newborn and weaning rabbits, Cell Tissue Res. 262: 89–97.

    Article  PubMed  CAS  Google Scholar 

  • Morin P.P., Dodson J.J., Dore F.Y. (1989) Thyroid activity concomitant with olfactory learning and heart rate changes in Atlantic salmon, Salmo salar, during smoltification, Can. J. Fish. Aquat. Sci. 46: 131–136.

    Article  CAS  Google Scholar 

  • Morin P.P., Doving S. (1992) Changes in the function of Atlantic salmon, Salmo salar, in the courses of smoltification, Can. J. Fish. Aquat. Sci. 49: 1704–1713.

    Article  Google Scholar 

  • Moyle P.B. (1998) Effects of hatcheries and hatchery fish on wild salmon and steelhead populations in California, Salmonid Restoration Conference, Santa Rosa, CA.

    Google Scholar 

  • Nevitt G.A. (1990) Olfactory Mechanisms in Two Teleost Fishes, Ph.D., University of Washington, Seattle.

    Google Scholar 

  • Nevitt G.A. (1995) A new model for olfactory imprinting in coho salmon, in: Burrows M., Matheson T., Newland PL., Schuppe H. (Eds.), Nervous Systems and Behaviour, Thieme Medical Publishers, New York, pp. 381.

    Google Scholar 

  • Nevitt G.A., Dittman A.H., Quinn T.P., Moody W.J. (1994) Evidence for a peripheral olfactory memory in imprinted salmon, Proc. Natl. Acad. Sci. (USA) 91: 4288–4292.

    Article  CAS  Google Scholar 

  • Nevitt G.A., Moody W.J. (1992) An electrophysiological characterization of ciliated olfactory receptor cells of the coho salmon Oncorhynchus kisutch, J. Exp. Biol. 166: 1–17.

    PubMed  CAS  Google Scholar 

  • Ngai J., Chess A., Dowling M.M, Necles N., Macagno E.R., Axel R. (1993) Coding of olfactory information: topography of odorant receptor expression in the catfish olfactory epithelium, Cell. Tissue Res. 72: 667–680.

    CAS  Google Scholar 

  • Oppenheimer J.H., Schwartz H.L., Mariash C.N., Kinlaw W.B., Wong N.C.W., Freake H.C. (1987) Advances in understanding of thyroid hormone action at the cellular level, Endocrine Reviews 8: 288–308.

    Article  PubMed  CAS  Google Scholar 

  • Paternostro M.A., Meisami E. (1994) Quantitative (3H) thymidine autoradiography of neurogenesis in the olfactory epithelium of developing normal, hypothyroid and hypothyroid-rehabilitated rats, Dev. Brain Res. 83: 151–162.

    Article  CAS  Google Scholar 

  • Paternostro M.A., Meisami E. (1996) Essential role of thyroid hormones in maturation of olfactory receptor neurons: an immunocytochemical study of number and cytoarchitecture of OMP-positive cells in developing rats, Int. J. Dev. Neuro. 14: 867–880.

    Article  CAS  Google Scholar 

  • Peterson N.P. (1982) Immigration of juvenile coho salmon (Oncorhynchus kisutch) into riverine ponds, Can. J. Fish. Aquat. Sci. 39: 1308–1310.

    Article  Google Scholar 

  • Quinn T.P., Dittman A.H. (1990) Pacific salmon migrations and homing: mechanisms and adaptive significance, TREE 5: 174–177.

    PubMed  CAS  Google Scholar 

  • Rami A., Patel A.J., Rabie A. (1986a) Thyroid hormone and development of the rat hippocampus: morphological alterations in granule and pyramidal cells, Neuroscience 19: 1217–1226.

    Article  PubMed  CAS  Google Scholar 

  • Rami A., Rabie A., Patel A.J. (1986b) Thyroid hormone and development of the rat hippocampus: cell acquisition in the dentate gyrus, Neuroscience 10: 1207–1216.

    Article  Google Scholar 

  • Restrepo D., Boekhoff I., Breer H. (1993) Rapid kinetic measurements of second messenger formation in olfactory cilia from channel catfish, Am. J. Physiol. 264: C906–C911.

    PubMed  CAS  Google Scholar 

  • Riddle D.R., Oakley B. (1992) Immunocytochemical identification of primary olfactory afférents in rainbow trout, J. Comp. Neurol. 324: 575–589.

    Article  PubMed  CAS  Google Scholar 

  • Sammuels H.H., Forman B.M., Ye Z.S. (1989) Regulation of gene expressed by thyroid hormone, Ann. Rev. Physiol. 51: 623–639.

    Article  Google Scholar 

  • Scholz A.T. (1980) Hormonal Regulation of Smolt Transformation and Olfactory Imprinting in Coho Salmon, Ph.D., University of Wisconsin.

    Google Scholar 

  • Scholz A.T., Gosse CK., Cooper J.C, Horrall R.M., Hasler A.D., Daly R.I, Poff R.J. (1978) Homing of rainbow trout transplanted in Lake Michigan: a comparison of three procedures used for imprinting and stocking, Trans. Am. Fish. Soc. 107: 439–443.

    Article  Google Scholar 

  • Scholz A.T, Horrall R.M, Cooper J.C, Hasler A.D. (1976) Imprinting to chemical cues: the basis for homestream selection in salmon, Science 1972: 1247–1249.

    Article  Google Scholar 

  • Semke E., Distel H., Hudson R. (1995) Specific enhancement of olfactory receptor sensitivity associated with foetal learning of food odors in the rabbit, Naturwissenschaften 82: 148–149.

    Article  PubMed  CAS  Google Scholar 

  • Shepherd G.M. (1994) Discrimination of molecular signals by the olfactory receptor neuron, Neuron 13: 771–790.

    Article  PubMed  CAS  Google Scholar 

  • Shimizu M., Ueda H., Kawamura H., Shimazaki K., Yamauchi K. (1995) Electrophoretic changes in olfactory system proteins in masu salmon during parr-smolt transformation, J. Fish. Biol. 47: 1044–1054.

    Article  CAS  Google Scholar 

  • Sklar P.B., Anholt R.H, Snyder S.H. (1986) The odorant-sensitive adenylate cyclase of olfactory receptor cells: differential stimulation by distinct classes of odorants, J. Biol. Chem. 261: 15538–15543.

    PubMed  CAS  Google Scholar 

  • Sutterlin A.M., Gray R. (1973) Chemical basis of homing for Atlantic salmon (Salmo salar) to a hatchery, J. Fish. Res. Board Can. 30: 985–989.

    CAS  Google Scholar 

  • Tilson M.B., Scholz A.T., White R.J., Galloway H. (1994) Thyroid-induced chemical imprinting in early life stages and assessment of smoltification in kokanee salmon hatcheries 1993 Annual Report, prepared for Bonneville Power Administration, Portland, Oregon.

    Google Scholar 

  • Tilson M.B., Scholz A.T., White R.J., Henderickson J.L. (1995) Artificial imprinting and smoltification in juvenile kokanee salmon: implications for operating Lake Roosevelt kokanee salmon hatcheries 1994 Annual Report, prepared for Bonneville Power Administration, Portland, Oregon.

    Google Scholar 

  • Ueda K., Hara T.J., Gorbman A. (1967) Electroencephalographic studies on olfactory discrimination in adult spawning salmon, Comp. Biochem. Physiol. 21: 133–143.

    Article  PubMed  CAS  Google Scholar 

  • Varnavskaya N.V., Wood C.C., Everett R.J., Wilmot R.L., Varnavsky VS., Midanaya V.V., Quinn T.P. (1994) Genetic differentiation of subpopulations of sockeye salmon (Oncorhynchus nerka) within lakes of Alaska, British Columbia, and Kamchatka, Russia, Can. J. Fish. Aquat. Sci. 51: 147–157.

    Article  CAS  Google Scholar 

  • Wang H.W., Wysocki C.J., Gold G.H. (1993) Induction of olfactory receptor sensitivity in mice, Chem. Senses 18: 647.

    Article  Google Scholar 

  • Wood C.C. (1995) Life history variation and population structure in sockeye salmon, Amer. Fish. Soc. Symp. 17: 195–216.

    Google Scholar 

  • Youngson A.F., Simpson T.H. (1984) Changes in serum thyroxine levels during smoking in captive and wild Atlantic salmon, Salmo salar, J. Fish. Biol. 24: 29–39.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Section of Neurobiology, Physiology and Behavior, University of California, Davis, CA, U.S.A.

    Gabrielle Nevitt

  2. National Marine Fisheries Service, Northwest Fisheries Science Center, Seattle, WA, U.S.A.

    Andrew Dittman

Authors
  1. Gabrielle Nevitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrew Dittman
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Institute for Zoology, Neuroethology/Sensory Ecology, Universität Bonn, Endenicher Allee 11-13, 53115, Bonn, Germany

    Gerhard von der Emde

  2. Institute for Zoology, Universität Bonn, Poppelsdorfer Schloss, D-53115, Bonn, Germany

    Joachim Mogdans

  3. 58, Manohar Enclave, Balwant Nagar Extension, Gwalior, 474002, M.P., India

    B. G. Kapoor

Rights and permissions

Reprints and permissions

Copyright information

© 2004 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Nevitt, G., Dittman, A. (2004). Olfactory Imprinting in Salmon: New Models and Approaches. In: von der Emde, G., Mogdans, J., Kapoor, B.G. (eds) The Senses of Fish. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1060-3_5

Download citation

  • DOI: https://doi.org/10.1007/978-94-007-1060-3_5

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-3779-2

  • Online ISBN: 978-94-007-1060-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation