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. 1987 Jul 1;90(1):95–125. doi: 10.1085/jgp.90.1.95

Patch-clamp studies of isolated mouse olfactory receptor neurons

PMCID: PMC2228861  PMID: 2442298

Abstract

Olfactory receptor neurons isolated from embryonic, neonatal, and adult mice were studied using the patch-clamp technique. Several distinct types of ion channels were characterized in patches of membrane from the neuronal soma and the dendritic knob of receptor neurons, including a 130-pS Ca++-activated K+ channel with voltage-dependent kinetics, an 80-pS Ca++-activated K+ channel with voltage-insensitive kinetics, a 25- pS K+ channel with properties similar to inward rectifiers, and a 40-pS K+ channel that was activated and then inactivated by rapid depolarization. Evidence of large-conductance (greater than 200 pS) Cl- channels, which were Ca++ insensitive and increasingly active at depolarizing membrane potentials, and voltage-activated Ca++ channels (16 pS) was also obtained. From K+ channel activity recorded from cell- attached patches, the intracellular [Ca++] was inferred to be below 0.1 microM, and the membrane potential was inferred to be approximately -50 mV. The receptor neurons had high input resistances, and action potentials could be elicited by picoampere amounts of depolarizing current. The receptor neurons responded to applied odorant molecules and to forskolin with increases in membrane conductance. These results provide a description of the membrane properties of olfactory receptor neurons and a basis for understanding their electrical activity and response to odorants.

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Selected References

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  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. Ashmore J. F., Meech R. W. Ionic basis of membrane potential in outer hair cells of guinea pig cochlea. Nature. 1986 Jul 24;322(6077):368–371. doi: 10.1038/322368a0. [DOI] [PubMed] [Google Scholar]
  3. Barrett J. N., Magleby K. L., Pallotta B. S. Properties of single calcium-activated potassium channels in cultured rat muscle. J Physiol. 1982 Oct;331:211–230. doi: 10.1113/jphysiol.1982.sp014370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bechem M., Glitsch H. G., Pott L. Properties of an inward rectifying K channel in the membrane of guinea-pig atrial cardioballs. Pflugers Arch. 1983 Nov;399(3):186–193. doi: 10.1007/BF00656713. [DOI] [PubMed] [Google Scholar]
  5. Blair L. A., Dionne V. E. Developmental acquisition of Ca2+-sensitivity by K+ channels in spinal neurones. Nature. 1985 May 23;315(6017):329–331. doi: 10.1038/315329a0. [DOI] [PubMed] [Google Scholar]
  6. Blatz A. L., Magleby K. L. Correcting single channel data for missed events. Biophys J. 1986 May;49(5):967–980. doi: 10.1016/S0006-3495(86)83725-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Blatz A. L., Magleby K. L. Single chloride-selective channels active at resting membrane potentials in cultured rat skeletal muscle. Biophys J. 1985 Jan;47(1):119–123. doi: 10.1016/S0006-3495(85)83884-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Blatz A. L., Magleby K. L. Single voltage-dependent chloride-selective channels of large conductance in cultured rat muscle. Biophys J. 1983 Aug;43(2):237–241. doi: 10.1016/S0006-3495(83)84344-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brown A. M., Camerer H., Kunze D. L., Lux H. D. Similarity of unitary Ca2+ currents in three different species. Nature. 1982 Sep 9;299(5879):156–158. doi: 10.1038/299156a0. [DOI] [PubMed] [Google Scholar]
  10. Ebihara L., Speers W. C. Ionic channels in a line of embryonal carcinoma cells induced to undergo neuronal differentiation. Biophys J. 1984 Dec;46(6):827–830. doi: 10.1016/S0006-3495(84)84081-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ewald D. A., Williams A., Levitan I. B. Modulation of single Ca2+-dependent K+-channel activity by protein phosphorylation. Nature. 1985 Jun 6;315(6019):503–506. doi: 10.1038/315503a0. [DOI] [PubMed] [Google Scholar]
  12. Findlay I., Dunne M. J., Petersen O. H. High-conductance K+ channel in pancreatic islet cells can be activated and inactivated by internal calcium. J Membr Biol. 1985;83(1-2):169–175. doi: 10.1007/BF01868748. [DOI] [PubMed] [Google Scholar]
  13. Gallin E. K. Calcium- and voltage-activated potassium channels in human macrophages. Biophys J. 1984 Dec;46(6):821–825. doi: 10.1016/S0006-3495(84)84080-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gardner P. I. Single-channel recordings of three K+-selective currents in cultured chick ciliary ganglion neurons. J Neurosci. 1986 Jul;6(7):2106–2116. doi: 10.1523/JNEUROSCI.06-07-02106.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Gesteland R. C., Yancey R. A., Farbman A. I. Development of olfactory receptor neuron selectivity in the rat fetus. Neuroscience. 1982;7(12):3127–3136. doi: 10.1016/0306-4522(82)90235-4. [DOI] [PubMed] [Google Scholar]
  17. Getchell T. V. Analysis of unitary spikes recorded extracellularly from frog olfactory receptor cells and axons. J Physiol. 1973 Nov;234(3):533–551. doi: 10.1113/jphysiol.1973.sp010359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Getchell T. V. Unitary responses in frog olfactory epithelium to sterically related molecules at low concentrations. J Gen Physiol. 1974 Aug;64(2):241–261. [PMC free article] [PubMed] [Google Scholar]
  19. HODGKIN A. L., KATZ B. The effect of sodium ions on the electrical activity of giant axon of the squid. J Physiol. 1949 Mar 1;108(1):37–77. doi: 10.1113/jphysiol.1949.sp004310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Hunter M., Lopes A. G., Boulpaep E. L., Giebisch G. H. Single channel recordings of calcium-activated potassium channels in the apical membrane of rabbit cortical collecting tubules. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4237–4239. doi: 10.1073/pnas.81.13.4237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kandel E. R., Tauc L. Anomalous rectification in the metacerebral giant cells and its consequences for synaptic transmission. J Physiol. 1966 Mar;183(2):287–304. doi: 10.1113/jphysiol.1966.sp007867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kurihara K., Koyama N. High activity of adenyl cyclase in olfactory and gustatory organs. Biochem Biophys Res Commun. 1972 Jul 11;48(1):30–34. doi: 10.1016/0006-291x(72)90339-7. [DOI] [PubMed] [Google Scholar]
  24. Leibowitz M. D., Dionne V. E. Single-channel acetylcholine receptor kinetics. Biophys J. 1984 Jan;45(1):153–163. doi: 10.1016/S0006-3495(84)84144-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Levitan I. B. Phosphorylation of ion channels. J Membr Biol. 1985;87(3):177–190. doi: 10.1007/BF01871217. [DOI] [PubMed] [Google Scholar]
  26. Lidow M. S., Menco B. P. Observations on axonemes and membranes of olfactory and respiratory cilia in frogs and rats using tannic acid-supplemented fixation and photographic rotation. J Ultrastruct Res. 1984 Jan;86(1):18–30. doi: 10.1016/s0022-5320(84)90092-3. [DOI] [PubMed] [Google Scholar]
  27. Magleby K. L., Pallotta B. S. Calcium dependence of open and shut interval distributions from calcium-activated potassium channels in cultured rat muscle. J Physiol. 1983 Nov;344:585–604. doi: 10.1113/jphysiol.1983.sp014957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Marty A. Ca-dependent K channels with large unitary conductance in chromaffin cell membranes. Nature. 1981 Jun 11;291(5815):497–500. doi: 10.1038/291497a0. [DOI] [PubMed] [Google Scholar]
  29. Marty A., Tan Y. P., Trautmann A. Three types of calcium-dependent channel in rat lacrimal glands. J Physiol. 1984 Dec;357:293–325. doi: 10.1113/jphysiol.1984.sp015501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Masukawa L. M., Hedlund B., Shepherd G. M. Electrophysiological properties of identified cells in the in vitro olfactory epithelium of the tiger salamander. J Neurosci. 1985 Jan;5(1):128–135. doi: 10.1523/JNEUROSCI.05-01-00128.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Masukawa L. M., Kauer J. S., Shepherd G. M. Intracellular recordings from two cell types in an in vitro preparation of the salamander olfactory epithelium. Neurosci Lett. 1983 Jan 31;35(1):59–64. doi: 10.1016/0304-3940(83)90527-x. [DOI] [PubMed] [Google Scholar]
  32. Menevse A., Dodd G., Poynder T. M. Evidence for the specific involvement of cyclic AMP in the olfactory transduction mechanism. Biochem Biophys Res Commun. 1977 Jul 25;77(2):671–677. doi: 10.1016/s0006-291x(77)80031-4. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Nelson P. G., Frank K. Anomalous rectification in cat spinal motoneurons and effect of polarizing currents on excitatory postsynaptic potential. J Neurophysiol. 1967 Sep;30(5):1097–1113. doi: 10.1152/jn.1967.30.5.1097. [DOI] [PubMed] [Google Scholar]
  35. Owen J. D. The determination of the stability constant for calcium-EGTA. Biochim Biophys Acta. 1976 Nov 18;451(1):321–325. doi: 10.1016/0304-4165(76)90282-8. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Pallotta B. S., Magleby K. L., Barrett J. N. Single channel recordings of Ca2+-activated K+ currents in rat muscle cell culture. Nature. 1981 Oct 8;293(5832):471–474. doi: 10.1038/293471a0. [DOI] [PubMed] [Google Scholar]
  38. Petersen O. H., Maruyama Y. Calcium-activated potassium channels and their role in secretion. Nature. 1984 Feb 23;307(5953):693–696. doi: 10.1038/307693a0. [DOI] [PubMed] [Google Scholar]
  39. Rafols J. A., Getchell T. V. Morphological relations between the receptor neurons, sustentacular cells and Schwann cells in the olfactory mucosa of the salamander. Anat Rec. 1983 May;206(1):87–101. doi: 10.1002/ar.1092060111. [DOI] [PubMed] [Google Scholar]
  40. Roux B., Sauvé R. A general solution to the time interval omission problem applied to single channel analysis. Biophys J. 1985 Jul;48(1):149–158. doi: 10.1016/S0006-3495(85)83768-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sakmann B., Trube G. Conductance properties of single inwardly rectifying potassium channels in ventricular cells from guinea-pig heart. J Physiol. 1984 Feb;347:641–657. doi: 10.1113/jphysiol.1984.sp015088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Schwarze W., Kolb H. A. Voltage-dependent kinetics of an anionic channel of large unit conductance in macrophages and myotube membranes. Pflugers Arch. 1984 Nov;402(3):281–291. doi: 10.1007/BF00585511. [DOI] [PubMed] [Google Scholar]
  43. Seamon K. B., Daly J. W. Forskolin: a unique diterpene activator of cyclic AMP-generating systems. J Cyclic Nucleotide Res. 1981;7(4):201–224. [PubMed] [Google Scholar]
  44. 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]
  45. Standen N. B., Stanfield P. R., Ward T. A. Properties of single potassium channels in vesicles formed from the sarcolemma of frog skeletal muscle. J Physiol. 1985 Jul;364:339–358. doi: 10.1113/jphysiol.1985.sp015749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Strong J. A. Modulation of potassium current kinetics in bag cell neurons of Aplysia by an activator of adenylate cyclase. J Neurosci. 1984 Nov;4(11):2772–2783. doi: 10.1523/JNEUROSCI.04-11-02772.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Takagi S. F., Wyse G. A., Yajima T. Anion permeability of the olfactory receptive membrane. J Gen Physiol. 1966 Nov;50(2):473–489. doi: 10.1085/jgp.50.2.473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. 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]
  49. 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]
  50. Trube G., Hescheler J. Inward-rectifying channels in isolated patches of the heart cell membrane: ATP-dependence and comparison with cell-attached patches. Pflugers Arch. 1984 Jun;401(2):178–184. doi: 10.1007/BF00583879. [DOI] [PubMed] [Google Scholar]
  51. Vodyanoy V., Murphy R. B. Single-channel fluctuations in bimolecular lipid membranes induced by rat olfactory epithelial homogenates. Science. 1983 May 13;220(4598):717–719. doi: 10.1126/science.6301014. [DOI] [PubMed] [Google Scholar]
  52. Wong B. S., Lecar H., Adler M. Single calcium-dependent potassium channels in clonal anterior pituitary cells. Biophys J. 1982 Sep;39(3):313–317. doi: 10.1016/S0006-3495(82)84522-0. [DOI] [PMC free article] [PubMed] [Google Scholar]

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