Skip to main content
NCBI home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1992 Mar 1;99(3):415–433. doi: 10.1085/jgp.99.3.415

Chemosensory responses in isolated olfactory receptor neurons from Necturus maculosus

PMCID: PMC2216604  PMID: 1588301

Abstract

Olfactory receptor neurons were isolated without enzymes from the mudpuppy, Necturus maculosus, and tested for chemosensitivity. The cells responded to odorants with changes in firing frequency and alterations in excitability that were detected with tight-seal patch electrodes using on-cell and whole-cell recording conditions. Chemosensitive cells exhibited two primary response characteristics: excitation and inhibition. Both types of primary response were observed in different cells stimulated by mixtures of amino acids as well as by the single compound L-alanine, suggesting that there may be more than one transduction pathway for some odorants. Using the normal whole-cell recording method, the chemosensitivity of competent cells washed out rapidly; a resistive whole-cell method was used to record odorant responses under current-clamp conditions. In response to chemical stimulation, excitability appeared to be modulated in several different ways in different cells: odorants induced hyperpolarizing or depolarizing receptor potentials, elicited or inhibited transient, rhythmic generator potentials, and altered excitability without changing the membrane potential or input resistance. These effects suggest that olfactory transduction is mediated through at least three different pathways with effects on four or more components of the membrane conductance. Polychotomous pathways such as these may be important for odor discrimination and for sharpening the "odor image" generated in the olfactory epithelium.

Full Text

The Full Text of this article is available as a PDF (1.4 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson P. A., Ache B. W. Voltage- and current-clamp recordings of the receptor potential in olfactory receptor cells in situ. Brain Res. 1985 Jul 15;338(2):273–280. doi: 10.1016/0006-8993(85)90157-x. [DOI] [PubMed] [Google Scholar]
  2. Anderson P. A., Hamilton K. A. Intracellular recordings from isolated salamander olfactory receptor neurons. Neuroscience. 1987 Apr;21(1):167–173. doi: 10.1016/0306-4522(87)90330-7. [DOI] [PubMed] [Google Scholar]
  3. Arzt A. H., Silver W. L., Mason J. R., Clark L. Olfactory responses of aquatic and terrestrial tiger salamanders to airborne and waterborne stimuli. J Comp Physiol A. 1986 Apr;158(4):479–487. doi: 10.1007/BF00603794. [DOI] [PubMed] [Google Scholar]
  4. Boekhoff I., Tareilus E., Strotmann J., Breer H. Rapid activation of alternative second messenger pathways in olfactory cilia from rats by different odorants. EMBO J. 1990 Aug;9(8):2453–2458. doi: 10.1002/j.1460-2075.1990.tb07422.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Firestein S., Darrow B., Shepherd G. M. Activation of the sensory current in salamander olfactory receptor neurons depends on a G protein-mediated cAMP second messenger system. Neuron. 1991 May;6(5):825–835. doi: 10.1016/0896-6273(91)90178-3. [DOI] [PubMed] [Google Scholar]
  7. Firestein S., Shepherd G. M., Werblin F. S. Time course of the membrane current underlying sensory transduction in salamander olfactory receptor neurones. J Physiol. 1990 Nov;430:135–158. doi: 10.1113/jphysiol.1990.sp018286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Firestein S., Werblin F. Odor-induced membrane currents in vertebrate-olfactory receptor neurons. Science. 1989 Apr 7;244(4900):79–82. doi: 10.1126/science.2704991. [DOI] [PubMed] [Google Scholar]
  9. Frings S., Lindemann B. Current recording from sensory cilia of olfactory receptor cells in situ. I. The neuronal response to cyclic nucleotides. J Gen Physiol. 1991 Jan;97(1):1–16. doi: 10.1085/jgp.97.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Frings S., Lindemann B. Odorant response of isolated olfactory receptor cells is blocked by amiloride. J Membr Biol. 1988 Nov;105(3):233–243. doi: 10.1007/BF01871000. [DOI] [PubMed] [Google Scholar]
  11. Frings S., Lindemann B. Single unit recording from olfactory cilia. Biophys J. 1990 May;57(5):1091–1094. doi: 10.1016/S0006-3495(90)82627-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gesteland R. C., Lettvin J. Y., Pitts W. H. Chemical transmission in the nose of the frog. J Physiol. 1965 Dec;181(3):525–559. doi: 10.1113/jphysiol.1965.sp007781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Getchell T. V. Analysis of intracellular recordings from salamander olfactory epithelium. Brain Res. 1977 Mar 11;123(2):275–286. doi: 10.1016/0006-8993(77)90479-6. [DOI] [PubMed] [Google Scholar]
  14. Getchell T. V. Functional properties of vertebrate olfactory receptor neurons. Physiol Rev. 1986 Jul;66(3):772–818. doi: 10.1152/physrev.1986.66.3.772. [DOI] [PubMed] [Google Scholar]
  15. Getchell T. V., Shepherd G. M. Responses of olfactory receptor cells to step pulses of odour at different concentrations in the salamander. J Physiol. 1978 Sep;282:521–540. doi: 10.1113/jphysiol.1978.sp012479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Horn R., Marty A. Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol. 1988 Aug;92(2):145–159. doi: 10.1085/jgp.92.2.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kashiwayanagi M., Suenaga A., Enomoto S., Kurihara K. Membrane fluidity changes of liposomes in response to various odorants. Complexity of membrane composition and variety of adsorption sites for odorants. Biophys J. 1990 Oct;58(4):887–895. doi: 10.1016/S0006-3495(90)82433-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kleene S. J., Gesteland R. C. Calcium-activated chloride conductance in frog olfactory cilia. J Neurosci. 1991 Nov;11(11):3624–3629. doi: 10.1523/JNEUROSCI.11-11-03624.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kurahashi T. Activation by odorants of cation-selective conductance in the olfactory receptor cell isolated from the newt. J Physiol. 1989 Dec;419:177–192. doi: 10.1113/jphysiol.1989.sp017868. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lerner M. R., Reagan J., Gyorgyi T., Roby A. Olfaction by melanophores: what does it mean? Proc Natl Acad Sci U S A. 1988 Jan;85(1):261–264. doi: 10.1073/pnas.85.1.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Nakamura T., Gold G. H. A cyclic nucleotide-gated conductance in olfactory receptor cilia. 1987 Jan 29-Feb 4Nature. 325(6103):442–444. doi: 10.1038/325442a0. [DOI] [PubMed] [Google Scholar]
  24. O'Connell R. J., Mozell M. M. Quantitative stimulation of frog olfactory receptors. J Neurophysiol. 1969 Jan;32(1):51–63. doi: 10.1152/jn.1969.32.1.51. [DOI] [PubMed] [Google Scholar]
  25. OTTOSON D. Analysis of the electrical activity of the olfactory epithelium. Acta Physiol Scand Suppl. 1955;35(122):1–83. [PubMed] [Google Scholar]
  26. Pace U., Hanski E., Salomon Y., Lancet D. Odorant-sensitive adenylate cyclase may mediate olfactory reception. Nature. 1985 Jul 18;316(6025):255–258. doi: 10.1038/316255a0. [DOI] [PubMed] [Google Scholar]
  27. Restrepo D., Miyamoto T., Bryant B. P., Teeter J. H. Odor stimuli trigger influx of calcium into olfactory neurons of the channel catfish. Science. 1990 Sep 7;249(4973):1166–1168. doi: 10.1126/science.2168580. [DOI] [PubMed] [Google Scholar]
  28. Schild D., Bischofberger J. Ca2+ modulates an unspecific cation conductance in olfactory cilia of Xenopus laevis. Exp Brain Res. 1991;84(1):187–194. doi: 10.1007/BF00231774. [DOI] [PubMed] [Google Scholar]
  29. Schwindt P. C., Spain W. J., Foehring R. C., Stafstrom C. E., Chubb M. C., Crill W. E. Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro. J Neurophysiol. 1988 Feb;59(2):424–449. doi: 10.1152/jn.1988.59.2.424. [DOI] [PubMed] [Google Scholar]
  30. Trotier D. A patch-clamp analysis of membrane currents in salamander olfactory receptor cells. Pflugers Arch. 1986 Dec;407(6):589–595. doi: 10.1007/BF00582636. [DOI] [PubMed] [Google Scholar]
  31. Trotier D., MacLeod P. Intracellular recordings from salamander olfactory receptor cells. Brain Res. 1983 Jun 6;268(2):225–237. doi: 10.1016/0006-8993(83)90488-2. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES