Skip to main content
Log in

Dual role of ryanodine-sensitive calcium stores in central neurons

  • Lectures
  • Published:
Neurophysiology Aims and scope

Abstract

The ryanodine-sensitive intracellular Ca2+ stores are known to play a major role in excitation-contraction coupling in muscles. Although these stores are also abundantly present in central neurons, their functional role in these cells remains unclear. Using fluorometric digital imaging of the intracellular Ca2+ concentration ([Ca2+] i ) in rat hippocampal slices, we investigated the dynamic properties of the ryanodine-sensitive Ca2+ stores inCA1 hippocampal pyramidal cells. We found that at rest the ryanodine-sensitive Ca2+ stores are functioning predominantly as a “sink” for Ca ions responding to an increase in [Ca2+] i with an increase in the amount of Ca ions accumulated inside the stores. If, however, [Ca2+] i increases significantly, as happens during strong neuronal discharges, the ryanodine-sensitive Ca2+ stores respond with Ca2+ release, thus acting as an amplifier of the intracellular Ca2+ signal.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. A. H. Sharp, P. S. McPherson, T. M. Dawson, et al., “Differential immunohistochemical localization of inositol 1,4,5-trisphosphate-and ryanodine-sensitive Ca2+ release channels in rat brain,”J. Neurosci.,13, 3051–3063 (1993).

    PubMed  CAS  Google Scholar 

  2. T. Furuichi, D. Furutama, Y. Hakamata, et al., “Multiple types of ryanodine receptor/Ca2+ release channels are differentially expressed in rabbit brain,”J. Neurosci.,14, 4794–485 (1994).

    PubMed  CAS  Google Scholar 

  3. J. Holliday, R. J. Adams, T. J. Sejnowski, and N. C. Spitzer, “Calcium-induced release of calcium regulates differentiation of cultured spinal neurons,”Neuron,7, 787–796 (1991).

    Article  PubMed  CAS  Google Scholar 

  4. S. Y. Hua, M. Nohmi, and K. Kuba, “Characteristics of Ca2+ release induced by Ca2+ influx in cultured bullfrog sympathetic neurons,”J. Physiol.,464, 245–272 (1993).

    PubMed  CAS  Google Scholar 

  5. I. Llano, R. DiPolo, and A. Marty, “Calcium-induced calcium release in cerebellar Purkinje cells,”Neuron,12, 663–673 (1994).

    Article  PubMed  CAS  Google Scholar 

  6. M. Kano, O. Garaschuk, A. Verkhratsky, and A. Konnerth, “Ryanodine receptor-mediated intracellular calcium release in rat cerebellar Purkinje neurons,”J. Physiol.,487, 1–16 (1995).

    PubMed  CAS  Google Scholar 

  7. A. Shmigol, A. Verkhratsky, and G. Isenberg, “Calcium-induced calcium release in rat sensory neurons,”J. Physiol.,489, 627–636 (1995).

    PubMed  CAS  Google Scholar 

  8. A. Fabiato, “Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum,”Am. J. Physiol.,245, C1–14 (1983).

    PubMed  CAS  Google Scholar 

  9. M. Nabauer, G. Callewaert, L. Cleemann, and M. Morad, “Regulation of calcium release is gated by calcium current, not gating charge, in cardiac myocytes,”Science,244, 800–803 (1989).

    PubMed  CAS  Google Scholar 

  10. S. Alford, B. G. Frenguelli, J. G. Schofield, and G. L. Collingridge, “Characterization of Ca2+ signals induced in hippocampalCA1 neurons by the synaptic activation of NMDA receptors,”J. Physiol.,469, 693–716 (1993).

    PubMed  CAS  Google Scholar 

  11. R. J. Miller, “Neuronal Ca2+: getting it up and keeping it up,”Trends Neurosci.,15, 317–319 (1992).

    Article  PubMed  CAS  Google Scholar 

  12. A. Schiegg, W. Gerstner, R. Ritz, and J. L. van Hemmen, “Intracellular Ca2+ stores can account for the time course of LTP induction: a model of Ca2+ dynamics in dendritic spines,”J. Neurophysiol.,74 1046–1055 (1995).

    PubMed  CAS  Google Scholar 

  13. Y. Wang, J. Wu, M. J. Rowan, and R. Anwyl, “Ryanodine produces a low frequency stimulation-induced NMDA receptor-independent long-term potentiation in the rat dentate gyrusin vitro,”J. Physiol.,495, 755–767 (1996).

    PubMed  CAS  Google Scholar 

  14. A. Shmigol, S. Kirischuk, P. Kostyuk, and A. Verkhratsky, “Different properties of caffeine-sensitive Ca2+ stores in peripheral and central mammalian neurons,”Pflügers Arch.,426, 174–176 (1994).

    Article  PubMed  CAS  Google Scholar 

  15. J. R. Brorson, D. Bleakman, S. J. Gibbons, and R. J. Miller, “The properties of intracellular calcium stores in cultured rat cerebellar neurons,”J. Neurosci.,11, 4024–4043 (1991).

    PubMed  CAS  Google Scholar 

  16. P. B. Simpson, R. A. Challiss, and S. R. Nahorski, “Neuronal Ca2+ stores: activation and function,”Trends Neurosci,18, 299–306 (1995).

    Article  PubMed  CAS  Google Scholar 

  17. D. D. Friel and R. W. Tsien, “A caffeine- and ryanodine-sensitive Ca2+ store in bullfrog sympathetic neurons modulates effects of Ca2+ entry on [Ca2+] i ,”J. Physiol.,450, 217–246 (1992).

    PubMed  CAS  Google Scholar 

  18. H. Markram, P. J. Helm, and B. Sakmann, “Dendritic calcium transients evoked by single back-propagating action potentials in rat neocortical pyramidal neurons,”J. Physiol.,485, 1–20 (1995).

    PubMed  CAS  Google Scholar 

  19. O. Garaschuk, R. Schneggenburger, C. Schirra, et al., “Fractional Ca2+ currents through somatic and dendritic glutamate receptor channels of rat hippocampalCA1 pyramidal neurons,”J. Physiol.,491, 757–772 (1996).

    PubMed  CAS  Google Scholar 

  20. F. A. Edwards, A. Konnerth, B. Sakmann, and T. Takahashi, “A thin slice preparation for patch clamp recordings from neurons of the mammalian central nervous system,”Pflügers Arch.,414, 600–612 (1989).

    Article  PubMed  CAS  Google Scholar 

  21. J. Eilers, R. Schneggenburger, and A. Konnerth “Patch clamp and calcium imaging in brain slices,” in:Single Channel Recording, B. Sakmann and E. Neher (eds.), Plenum Publishing Co., New York (1995), pp. 213–229.

    Google Scholar 

  22. O. Garaschuk and A. Konnerth, “Quantitative calcium imaging in brain slices,” in:Imaging Living Cells, R. Rizzuto and C. Fasolato (eds.), Landes/Springer, Austin (in press).

  23. E. Neher, “Combined fura-2 and patch clamp measurements in rat perioneal mast cells,” in:Neuromuscular Junction, L. Sellin, R. Libelius, and S. Thesleff (eds.), Elsevier, Amsterdam (1989). pp. 65–76.

    Google Scholar 

  24. O. Garaschuk, Y. Yaary, and A. Konnerth, “Release and sequestration of calcium by ryanodine-sensitive stores in rat hippocampal neurons,”J. Physiol.,502, 13–30 (1997).

    Article  PubMed  CAS  Google Scholar 

  25. K. J. Seymour-Laurent and M. E. Barish, “Inositol 1,4,5-trisphosphate and ryanodine receptor distributions and patterns of acetylcholine- and caffeine-induced calcium release in cultured mouse hippocampal neurons,”J. Neurosci,15, 2592–2608 (1995).

    PubMed  CAS  Google Scholar 

  26. T. Pozzan, R. Rizzuto, P. Volpe, and J. Meldolesi, “Molecular and cellular physiology of intracellular calcium stores,”Physiol. Rev.,74, 595–636 (1994).

    PubMed  CAS  Google Scholar 

  27. A. Shmigol, P. Kostyuk, and A. Verkhratsky, “Role of caffeine-sensitive Ca2+ stores in Ca2+ signal termination in adult mouse DRG neurons,”NeuroReport,5, 2073–2076 (1994).

    PubMed  CAS  Google Scholar 

  28. V. Henzi and A. B. MacDermott, “Characteristics and function of Ca2+-and inositol 1,4,5-trisphosphate-releasable stores of Ca2+ in neurons,”Neuroscience,46, 251–273 (1992).

    Article  PubMed  CAS  Google Scholar 

  29. A. Shmigol, N. Svichar, P. Kostyuk, and A. verkhratsky, “Gradual caffeine-induced Ca2+ release in mouse dorsal root ganglion neurons is controlled by cytoplasmic and luminal Ca2+,”Neuroscience,73, 1061–1067 (1996).

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Garaschuk, O., Konnerth, A. Dual role of ryanodine-sensitive calcium stores in central neurons. Neurophysiology 29, 199–204 (1997). https://doi.org/10.1007/BF02461229

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02461229

Keywords

Navigation