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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Aug 15;92(17):7864–7868. doi: 10.1073/pnas.92.17.7864

Olfactory transduction is intrinsically noisy.

G Lowe 1, G H Gold 1
PMCID: PMC41246  PMID: 7544007

Abstract

The sources of noise that limit olfactory signal detection were investigated in dissociated rat olfactory receptor cells. Near-threshold odorant-evoked currents exhibited large random fluctuation. However, similar fluctuations were observed in the absence of applied odorants when currents were induced by elevating the intracellular cyclic AMP concentration. This suggests that the fluctuations reflect noise intrinsic to the transduction mechanism, rather than the quantal nature of an odorant stimulus. For many odorants, this intrinsic noise may preclude the reliable detection of single odorant molecules.

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Selected References

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

  1. ALLISON A. C., WARWICK R. T. T. Quantitative observations on the olfactory system of the rabbit. Brain. 1949 Jun;72(Pt 2):186–197. doi: 10.1093/brain/72.2.186. [DOI] [PubMed] [Google Scholar]
  2. Bakalyar H. A., Reed R. R. Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science. 1990 Dec 7;250(4986):1403–1406. doi: 10.1126/science.2255909. [DOI] [PubMed] [Google Scholar]
  3. Baylor D. A., Nunn B. J., Schnapf J. L. The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. J Physiol. 1984 Dec;357:575–607. doi: 10.1113/jphysiol.1984.sp015518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berg H. C., Purcell E. M. Physics of chemoreception. Biophys J. 1977 Nov;20(2):193–219. doi: 10.1016/S0006-3495(77)85544-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boekhoff I., Breer H. Termination of second messenger signaling in olfaction. Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):471–474. doi: 10.1073/pnas.89.2.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boekhoff I., Inglese J., Schleicher S., Koch W. J., Lefkowitz R. J., Breer H. Olfactory desensitization requires membrane targeting of receptor kinase mediated by beta gamma-subunits of heterotrimeric G proteins. J Biol Chem. 1994 Jan 7;269(1):37–40. [PubMed] [Google Scholar]
  7. Bond R. A., Leff P., Johnson T. D., Milano C. A., Rockman H. A., McMinn T. R., Apparsundaram S., Hyek M. F., Kenakin T. P., Allen L. F. Physiological effects of inverse agonists in transgenic mice with myocardial overexpression of the beta 2-adrenoceptor. Nature. 1995 Mar 16;374(6519):272–276. doi: 10.1038/374272a0. [DOI] [PubMed] [Google Scholar]
  8. Borisy F. F., Ronnett G. V., Cunningham A. M., Juilfs D., Beavo J., Snyder S. H. Calcium/calmodulin-activated phosphodiesterase expressed in olfactory receptor neurons. J Neurosci. 1992 Mar;12(3):915–923. doi: 10.1523/JNEUROSCI.12-03-00915.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Breer H., Boekhoff I., Tareilus E. Rapid kinetics of second messenger formation in olfactory transduction. Nature. 1990 May 3;345(6270):65–68. doi: 10.1038/345065a0. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Chen T. Y., Yau K. W. Direct modulation by Ca(2+)-calmodulin of cyclic nucleotide-activated channel of rat olfactory receptor neurons. Nature. 1994 Apr 7;368(6471):545–548. doi: 10.1038/368545a0. [DOI] [PubMed] [Google Scholar]
  12. Dawson T. M., Arriza J. L., Jaworsky D. E., Borisy F. F., Attramadal H., Lefkowitz R. J., Ronnett G. V. Beta-adrenergic receptor kinase-2 and beta-arrestin-2 as mediators of odorant-induced desensitization. Science. 1993 Feb 5;259(5096):825–829. doi: 10.1126/science.8381559. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Firestein S., Picco C., Menini A. The relation between stimulus and response in olfactory receptor cells of the tiger salamander. J Physiol. 1993 Aug;468:1–10. doi: 10.1113/jphysiol.1993.sp019756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Firestein S., Zufall F., Shepherd G. M. Single odor-sensitive channels in olfactory receptor neurons are also gated by cyclic nucleotides. J Neurosci. 1991 Nov;11(11):3565–3572. doi: 10.1523/JNEUROSCI.11-11-03565.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Frings S., Lynch J. W., Lindemann B. Properties of cyclic nucleotide-gated channels mediating olfactory transduction. Activation, selectivity, and blockage. J Gen Physiol. 1992 Jul;100(1):45–67. doi: 10.1085/jgp.100.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gold G. H., Lowe G. Single odorant molecules? Nature. 1995 Jul 6;376(6535):27–27. doi: 10.1038/376027a0. [DOI] [PubMed] [Google Scholar]
  20. Jackson M. B. Spontaneous openings of the acetylcholine receptor channel. Proc Natl Acad Sci U S A. 1984 Jun;81(12):3901–3904. doi: 10.1073/pnas.81.12.3901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jones D. T., Reed R. R. Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science. 1989 May 19;244(4906):790–795. doi: 10.1126/science.2499043. [DOI] [PubMed] [Google Scholar]
  22. Kleene S. J. Origin of the chloride current in olfactory transduction. Neuron. 1993 Jul;11(1):123–132. doi: 10.1016/0896-6273(93)90276-w. [DOI] [PubMed] [Google Scholar]
  23. Kramer R. H., Siegelbaum S. A. Intracellular Ca2+ regulates the sensitivity of cyclic nucleotide-gated channels in olfactory receptor neurons. Neuron. 1992 Nov;9(5):897–906. doi: 10.1016/0896-6273(92)90242-6. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Kurahashi T., Shibuya T. Ca2(+)-dependent adaptive properties in the solitary olfactory receptor cell of the newt. Brain Res. 1990 May 7;515(1-2):261–268. doi: 10.1016/0006-8993(90)90605-b. [DOI] [PubMed] [Google Scholar]
  26. Kurahashi T. The response induced by intracellular cyclic AMP in isolated olfactory receptor cells of the newt. J Physiol. 1990 Nov;430:355–371. doi: 10.1113/jphysiol.1990.sp018295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kurahashi T., Yau K. W. Co-existence of cationic and chloride components in odorant-induced current of vertebrate olfactory receptor cells. Nature. 1993 May 6;363(6424):71–74. doi: 10.1038/363071a0. [DOI] [PubMed] [Google Scholar]
  28. Lowe G., Gold G. H. Contribution of the ciliary cyclic nucleotide-gated conductance to olfactory transduction in the salamander. J Physiol. 1993 Mar;462:175–196. doi: 10.1113/jphysiol.1993.sp019550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lowe G., Gold G. H. Nonlinear amplification by calcium-dependent chloride channels in olfactory receptor cells. Nature. 1993 Nov 18;366(6452):283–286. doi: 10.1038/366283a0. [DOI] [PubMed] [Google Scholar]
  30. Lowe G., Nakamura T., Gold G. H. Adenylate cyclase mediates olfactory transduction for a wide variety of odorants. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5641–5645. doi: 10.1073/pnas.86.14.5641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Menini A., Picco C., Firestein S. Quantal-like current fluctuations induced by odorants in olfactory receptor cells. Nature. 1995 Feb 2;373(6513):435–437. doi: 10.1038/373435a0. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. Schleicher S., Boekhoff I., Arriza J., Lefkowitz R. J., Breer H. A beta-adrenergic receptor kinase-like enzyme is involved in olfactory signal termination. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1420–1424. doi: 10.1073/pnas.90.4.1420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Shirley S. G., Robinson C. J., Dickinson K., Aujla R., Dodd G. H. Olfactory adenylate cyclase of the rat. Stimulation by odorants and inhibition by Ca2+. Biochem J. 1986 Dec 1;240(2):605–607. doi: 10.1042/bj2400605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sklar P. B., Anholt R. R., Snyder S. H. The odorant-sensitive adenylate cyclase of olfactory receptor cells. Differential stimulation by distinct classes of odorants. J Biol Chem. 1986 Nov 25;261(33):15538–15543. [PubMed] [Google Scholar]
  37. Zufall F., Shepherd G. M., Firestein S. Inhibition of the olfactory cyclic nucleotide gated ion channel by intracellular calcium. Proc Biol Sci. 1991 Dec 23;246(1317):225–230. doi: 10.1098/rspb.1991.0148. [DOI] [PubMed] [Google Scholar]

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