Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 1987 Oct;52(4):571–576. doi: 10.1016/S0006-3495(87)83246-0

Activity-dependent calcium transients in central nervous system myelinated axons revealed by the calcium indicator Fura-2.

V Lev-Ram 1, A Grinvald 1
PMCID: PMC1330047  PMID: 3676438

Abstract

Optical measurements from rat optic nerve, loaded with the new Ca2+ indicator Fura-2, provide the first evidence for the presence of activity-dependent fast intracellular [Ca2+] transients in mammalian central nervous system (CNS) myelinated axons. The results suggest that voltage-dependent Ca2+ channels are present in some of the myelinated axons. Optical measurements from axons stained with anterogradely transported voltage-sensitive dye suggest the presence of Ca2+-dependent potassium conductances in these axons. This report also demonstrates that Fura-2 can readily detect changes in [Ca2+] inside cells as a result of electrical activity, and establishes its suitability for measurements of intracellular Ca2+ transients in the millisecond time domain.

Full text

PDF
572

Selected References

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

  1. Ahmed Z., Connor J. A. Measurement of calcium influx under voltage clamp in molluscan neurones using the metallochromic dye arsenazo III. J Physiol. 1979 Jan;286:61–82. doi: 10.1113/jphysiol.1979.sp012607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baylor D. A., Nicholls J. G. Changes in extracellular potassium concentration produced by neuronal activity in the central nervous system of the leech. J Physiol. 1969 Aug;203(3):555–569. doi: 10.1113/jphysiol.1969.sp008879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brown J. E., Cohen L. B., De Weer P., Pinto L. H., Ross W. N., Salzberg B. M. Rapid changes in intracellular free calcium concentration. Detection by metallochromic indicator dyes in squid giant axon. Biophys J. 1975 Nov;15(11):1155–1160. doi: 10.1016/S0006-3495(75)85891-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chiu S. Y., Ritchie J. M. Evidence for the presence of potassium channels in the paranodal region of acutely demyelinated mammalian single nerve fibres. J Physiol. 1981;313:415–437. doi: 10.1113/jphysiol.1981.sp013674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Connor J. A. Digital imaging of free calcium changes and of spatial gradients in growing processes in single, mammalian central nervous system cells. Proc Natl Acad Sci U S A. 1986 Aug;83(16):6179–6183. doi: 10.1073/pnas.83.16.6179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Connors B. W., Ransom B. R., Kunis D. M., Gutnick M. J. Activity-dependent K+ accumulation in the developing rat optic nerve. Science. 1982 Jun 18;216(4552):1341–1343. doi: 10.1126/science.7079771. [DOI] [PubMed] [Google Scholar]
  7. Foster R. E., Connors B. W., Waxman S. G. Rat optic nerve: electrophysiological, pharmacological and anatomical studies during development. Brain Res. 1982 Mar;255(3):371–386. doi: 10.1016/0165-3806(82)90005-0. [DOI] [PubMed] [Google Scholar]
  8. Gorman A. L., Thomas M. V. Intracellular calcium accumulation during depolarization in a molluscan neurone. J Physiol. 1980 Nov;308:259–285. doi: 10.1113/jphysiol.1980.sp013471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Grinvald A., Fine A., Farber I. C., Hildesheim R. Fluorescence monitoring of electrical responses from small neurons and their processes. Biophys J. 1983 May;42(2):195–198. doi: 10.1016/S0006-3495(83)84386-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Grinvald A., Hildesheim R., Farber I. C., Anglister L. Improved fluorescent probes for the measurement of rapid changes in membrane potential. Biophys J. 1982 Sep;39(3):301–308. doi: 10.1016/S0006-3495(82)84520-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Grinvald A. Real-time optical mapping of neuronal activity: from single growth cones to the intact mammalian brain. Annu Rev Neurosci. 1985;8:263–305. doi: 10.1146/annurev.ne.08.030185.001403. [DOI] [PubMed] [Google Scholar]
  12. Grinvald A., Salzberg B. M., Lev-Ram V., Hildesheim R. Optical recording of synaptic potentials from processes of single neurons using intracellular potentiometric dyes. Biophys J. 1987 Apr;51(4):643–651. doi: 10.1016/S0006-3495(87)83389-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
  14. Gupta R. K., Salzberg B. M., Grinvald A., Cohen L. B., Kamino K., Lesher S., Boyle M. B., Waggoner A. S., Wang C. H. Improvements in optical methods for measuring rapid changes in membrane potential. J Membr Biol. 1981 Feb 15;58(2):123–137. doi: 10.1007/BF01870975. [DOI] [PubMed] [Google Scholar]
  15. Hagiwara S., Byerly L. Calcium channel. Annu Rev Neurosci. 1981;4:69–125. doi: 10.1146/annurev.ne.04.030181.000441. [DOI] [PubMed] [Google Scholar]
  16. Kettenmann H., Sonnhof U., Schachner M. Exclusive potassium dependence of the membrane potential in cultured mouse oligodendrocytes. J Neurosci. 1983 Mar;3(3):500–505. doi: 10.1523/JNEUROSCI.03-03-00500.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Konnerth A., Orkand R. K. Voltage-sensitive dyes measure potential changes in axons and glia of the frog optic nerve. Neurosci Lett. 1986 May 6;66(1):49–54. doi: 10.1016/0304-3940(86)90164-3. [DOI] [PubMed] [Google Scholar]
  18. Latorre R., Coronado R., Vergara C. K+ channels gated by voltage and ions. Annu Rev Physiol. 1984;46:485–495. doi: 10.1146/annurev.ph.46.030184.002413. [DOI] [PubMed] [Google Scholar]
  19. Lev-Ram V., Grinvald A. Ca2+- and K+-dependent communication between central nervous system myelinated axons and oligodendrocytes revealed by voltage-sensitive dyes. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6651–6655. doi: 10.1073/pnas.83.17.6651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. MacVicar B. A. Voltage-dependent calcium channels in glial cells. Science. 1984 Dec 14;226(4680):1345–1347. doi: 10.1126/science.6095454. [DOI] [PubMed] [Google Scholar]
  21. Murray N., Steck A. J. Impulse conduction regulates myelin basic protein phosphorylation in rat optic nerve. J Neurochem. 1984 Jul;43(1):243–248. doi: 10.1111/j.1471-4159.1984.tb06702.x. [DOI] [PubMed] [Google Scholar]
  22. Orkand R. K., Nicholls J. G., Kuffler S. W. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol. 1966 Jul;29(4):788–806. doi: 10.1152/jn.1966.29.4.788. [DOI] [PubMed] [Google Scholar]
  23. Poenie M., Alderton J., Tsien R. Y., Steinhardt R. A. Changes of free calcium levels with stages of the cell division cycle. Nature. 1985 May 9;315(6015):147–149. doi: 10.1038/315147a0. [DOI] [PubMed] [Google Scholar]
  24. Ross W. N., Stockbridge L. L., Stockbridge N. L. Regional properties of calcium entry in barnacle neurons determined with Arsenazo III and a photodiode array. J Neurosci. 1986 Apr;6(4):1148–1159. doi: 10.1523/JNEUROSCI.06-04-01148.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schnapp B., Peracchia C., Mugnaini E. The paranodal axo-glial junction in the central nervous system studied with thin sections and freeze-fracture. Neuroscience. 1976 Jun;1(3):181–190. doi: 10.1016/0306-4522(76)90075-0. [DOI] [PubMed] [Google Scholar]
  26. Simon S. M., Llinás R. R. Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys J. 1985 Sep;48(3):485–498. doi: 10.1016/S0006-3495(85)83804-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Smith K. J., Schauf C. L. Size-dependent variation of nodal properties in myelinated nerve. Nature. 1981 Sep 24;293(5830):297–299. doi: 10.1038/293297a0. [DOI] [PubMed] [Google Scholar]
  28. Stockbridge N., Ross W. N. Localized Ca2+ and calcium-activated potassium conductances in terminals of a barnacle photoreceptor. Nature. 1984 May 17;309(5965):266–268. doi: 10.1038/309266a0. [DOI] [PubMed] [Google Scholar]
  29. Waggoner A. S., Grinvald A. Mechanisms of rapid optical changes of potential sensitive dyes. Ann N Y Acad Sci. 1977 Dec 30;303:217–241. [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES