Abstract
The remarkable homing ability of salmon relies on olfactory cues, but its cellular basis is unknown. To test the role of peripheral olfactory receptors in odorant memory retention, we imprinted coho salmon (Oncorhynchus kisutch) to micromolar concentrations of phenyl ethyl alcohol during parr-smolt transformation. The following year, we measured phenyl ethyl alcohol responses in the peripheral receptor cells using patch clamp. Cells from imprinted fish showed increased sensitivity to phenyl ethyl alcohol compared either to cells from naive fish or to sensitivity to another behaviorally important odorant (L-serine). Field experiments verified an increased behavioral preference for phenyl ethyl alcohol by imprinted salmon as adults. Thus, some component of the imprinted olfactory homestream memory appears to be retained peripherally.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Brennan P., Kaba H., Keverne E. B. Olfactory recognition: a simple memory system. Science. 1990 Nov 30;250(4985):1223–1226. doi: 10.1126/science.2147078. [DOI] [PubMed] [Google Scholar]
- Brent G. A., Moore D. D., Larsen P. R. Thyroid hormone regulation of gene expression. Annu Rev Physiol. 1991;53:17–35. doi: 10.1146/annurev.ph.53.030191.000313. [DOI] [PubMed] [Google Scholar]
- Buck L., Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 1991 Apr 5;65(1):175–187. doi: 10.1016/0092-8674(91)90418-x. [DOI] [PubMed] [Google Scholar]
- Burd G. D. Development of the olfactory nerve in the African clawed frog, Xenopus laevis: I. Normal development. J Comp Neurol. 1991 Feb 1;304(1):123–134. doi: 10.1002/cne.903040109. [DOI] [PubMed] [Google Scholar]
- Cooper J. C., Hasler A. D. Electroencephalographic evidence for retention of olfactory cues in homing coho salmon. Science. 1974 Jan 25;183(4122):336–338. doi: 10.1126/science.183.4122.336. [DOI] [PubMed] [Google Scholar]
- Dionne V. E. Chemosensory responses in isolated olfactory receptor neurons from Necturus maculosus. J Gen Physiol. 1992 Mar;99(3):415–433. doi: 10.1085/jgp.99.3.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Farbman A. I. Olfactory neurogenesis: genetic or environmental controls? Trends Neurosci. 1990 Sep;13(9):362–365. doi: 10.1016/0166-2236(90)90017-5. [DOI] [PubMed] [Google Scholar]
- Glass C. K., Holloway J. M. Regulation of gene expression by the thyroid hormone receptor. Biochim Biophys Acta. 1990 Dec 11;1032(2-3):157–176. doi: 10.1016/0304-419x(90)90002-i. [DOI] [PubMed] [Google Scholar]
- Gould E., Butcher L. L. Developing cholinergic basal forebrain neurons are sensitive to thyroid hormone. J Neurosci. 1989 Sep;9(9):3347–3358. doi: 10.1523/JNEUROSCI.09-09-03347.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
- Hill D. L., Przekop P. R., Jr Influences of dietary sodium on functional taste receptor development: a sensitive period. Science. 1988 Sep 30;241(4874):1826–1828. doi: 10.1126/science.3175625. [DOI] [PubMed] [Google Scholar]
- Hofmann M. H., Michler A., Meyer D. L. Thyroxine influences neuronal connectivity in the adult frog brain. Brain Res. 1989 Jul 17;492(1-2):389–391. doi: 10.1016/0006-8993(89)90926-8. [DOI] [PubMed] [Google Scholar]
- Hoskins S. G., Grobstein P. Development of the ipsilateral retinothalamic projection in the frog Xenopus laevis. III. The role of thyroxine. J Neurosci. 1985 Apr;5(4):930–940. doi: 10.1523/JNEUROSCI.05-04-00930.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hudson R. Olfactory imprinting. Curr Opin Neurobiol. 1993 Aug;3(4):548–552. doi: 10.1016/0959-4388(93)90054-3. [DOI] [PubMed] [Google Scholar]
- IDLER D. R., FAGERLUND U. H., MAYOH H. Olfactory perception in migrating salmon. I. L-serine, a salmon repellent in mammalian skin. J Gen Physiol. 1956 Jul 20;39(6):889–892. doi: 10.1085/jgp.39.6.889. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kostyuk P. G. Calcium ionic channels in electrically excitable membrane. Neuroscience. 1980;5(6):945–959. doi: 10.1016/0306-4522(80)90178-5. [DOI] [PubMed] [Google Scholar]
- Lancet D. Vertebrate olfactory reception. Annu Rev Neurosci. 1986;9:329–355. doi: 10.1146/annurev.ne.09.030186.001553. [DOI] [PubMed] [Google Scholar]
- Mackay-Sim A., Beard M. D. Hypothyroidism disrupts neural development in the olfactory epithelium of adult mice. Brain Res. 1987 Dec 1;433(2):190–198. doi: 10.1016/0165-3806(87)90023-x. [DOI] [PubMed] [Google Scholar]
- Maue R. A., Dionne V. E. Patch-clamp studies of isolated mouse olfactory receptor neurons. J Gen Physiol. 1987 Jul;90(1):95–125. doi: 10.1085/jgp.90.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nevitt G. A., Moody W. J. An electrophysiological characterization of ciliated olfactory receptor cells of the coho salmon Oncorhynchus kisutch. J Exp Biol. 1992 May;166:1–17. doi: 10.1242/jeb.166.1.1. [DOI] [PubMed] [Google Scholar]
- Ngai J., Chess A., Dowling M. M., Necles N., Macagno E. R., Axel R. Coding of olfactory information: topography of odorant receptor expression in the catfish olfactory epithelium. Cell. 1993 Mar 12;72(5):667–680. doi: 10.1016/0092-8674(93)90396-8. [DOI] [PubMed] [Google Scholar]
- Oppenheimer J. H., Schwartz H. L., Mariash C. N., Kinlaw W. B., Wong N. C., Freake H. C. Advances in our understanding of thyroid hormone action at the cellular level. Endocr Rev. 1987 Aug;8(3):288–308. doi: 10.1210/edrv-8-3-288. [DOI] [PubMed] [Google Scholar]
- Paternostro M. A., Meisami E. Lack of thyroid hormones but not their excess affects the maturation of olfactory receptor neurons: a quantitative morphologic study in the postnatal rat. Int J Dev Neurosci. 1991;9(5):439–452. doi: 10.1016/0736-5748(91)90030-p. [DOI] [PubMed] [Google Scholar]
- Paternostro M., Meisami E. Selective effects of thyroid hormonal deprivation on growth and development of olfactory receptor sheet during the early postnatal period: a morphometric and cell count study in the rat. Int J Dev Neurosci. 1989;7(3):243–255. doi: 10.1016/0736-5748(89)90029-4. [DOI] [PubMed] [Google Scholar]
- Rami A., Patel A. J., Rabié A. Thyroid hormone and development of the rat hippocampus: morphological alterations in granule and pyramidal cells. Neuroscience. 1986 Dec;19(4):1217–1226. doi: 10.1016/0306-4522(86)90135-1. [DOI] [PubMed] [Google Scholar]
- Rami A., Rabié A., Patel A. J. Thyroid hormone and development of the rat hippocampus: cell acquisition in the dentate gyrus. Neuroscience. 1986 Dec;19(4):1207–1216. doi: 10.1016/0306-4522(86)90134-x. [DOI] [PubMed] [Google Scholar]
- Riddle D. R., Oakley B. Evaluation of projection patterns in the primary olfactory system of rainbow trout. J Neurosci. 1991 Dec;11(12):3752–3762. doi: 10.1523/JNEUROSCI.11-12-03752.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Riddle D. R., Oakley B. Immunocytochemical identification of primary olfactory afferents in rainbow trout. J Comp Neurol. 1992 Oct 22;324(4):575–589. doi: 10.1002/cne.903240410. [DOI] [PubMed] [Google Scholar]
- Samuels H. H., Forman B. M., Horowitz Z. D., Ye Z. S. Regulation of gene expression by thyroid hormone. Annu Rev Physiol. 1989;51:623–639. doi: 10.1146/annurev.ph.51.030189.003203. [DOI] [PubMed] [Google Scholar]
- Scholz A. T., Horrall R. M., Cooper J. C., Hasler A. D. Imprinting to chemical cues: the basis for home stream selection in salmon. Science. 1976 Jun 18;192(4245):1247–1249. doi: 10.1126/science.1273590. [DOI] [PubMed] [Google Scholar]
- Wang H. W., Wysocki C. J., Gold G. H. Induction of olfactory receptor sensitivity in mice. Science. 1993 May 14;260(5110):998–1000. doi: 10.1126/science.8493539. [DOI] [PubMed] [Google Scholar]