Journal of Biological Physics

, Volume 34, Issue 3–4, pp 441–457 | Cite as

Giant Glial Cell: New Insight Through Mechanism-Based Modeling

  • D. E. Postnov
  • L. S. Ryazanova
  • N. A. Brazhe
  • A. R. Brazhe
  • G. V. Maximov
  • E. Mosekilde
  • O. V. Sosnovtseva
Original Paper

Abstract

The paper describes a detailed mechanism-based model of a tripartite synapse consisting of P- and R-neurons together with a giant glial cell in the ganglia of the medical leech (Hirudo medicinalis), which is a useful object for experimental studies in situ. We describe the two main pathways of the glial cell activation: (1) via IP3 production and Ca2 +  release from the endoplasmic reticulum and (2) via increase of the extracellular potassium concentration, glia depolarization, and opening of voltage-dependent Ca2 +  channels. We suggest that the second pathway is the more significant for establishing the positive feedback in glutamate release that is critical for the self-sustained activity of the postsynaptic neuron. This mechanism differs from the mechanisms of the astrocyte-neuron signaling previously reported.

Keywords

Tripartite synapse Glia Neuron Modeling 

Notes

Acknowledgements

This work was partly supported by the European Union through the Network of Excellence BioSim (contract no. LSHB-CT-2004-005137). N. B. and A. B. acknowledge support from Lundbeck foundation. O. S. acknowledges support from Forskningsrådet for Natur og Univers (Skou stipendium). We are grateful to Ljudmila Erokhova for useful discussions.

References

  1. 1.
    Haydon, P.G.: Glia: listening and talking to the synapse. Nat. Rev. 2, 185–193 (2001)CrossRefGoogle Scholar
  2. 2.
    Fields, R.D., Stevens-Graham, B.: New insights into neuron–glia communication. Science 298, 556–562 (2002)CrossRefADSGoogle Scholar
  3. 3.
    Bonvento, G., Giaume, C., Lorenceau, J.: Neuron–glia interactions: from physiology to behavior. J. Physiol. 96, 167–168 (2002)Google Scholar
  4. 4.
    Nedergaard, M.: Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science 263, 1768–1771 (1994)CrossRefADSGoogle Scholar
  5. 5.
    Wiencken, A.E., Casagrande, V.A.: Endothelial nitric oxide synthase (eNOS) in astrocytes: another source of nitric oxide in neocortex. Glia 26, 280–290 (1999)CrossRefGoogle Scholar
  6. 6.
    Nedergaard, M., Ransom, B., Goldman, S.A.: New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci. 26, 523–530 (2003)CrossRefGoogle Scholar
  7. 7.
    Nadkarni, S., Jung, P.: Spontaneous oscillations of dressed neurons: a new mechanism for epilepsy? Phys. Rev. Lett. 91, 268101 (2003)CrossRefADSGoogle Scholar
  8. 8.
    Postnov. D.E., Ryazanova L.S., Sosnovtseva O.V.: Functional modeling of neural-glia interaction. Biosystems 89, 84–91 (2007)CrossRefGoogle Scholar
  9. 9.
    Kuffler, S.W., Potter, D.D.: Glia in the leech central nervous system: physiological properties and neuron–glia relationship. J. Neurophysiol. 27, 290–320 (1964)Google Scholar
  10. 10.
    Nicholls, J.G., Martin, A.R., Wallace, B.G., Fuchs, P.A.: From Neuron to Brain: A Cellular and Molecular Approach to the Function of the Nervous System, 4th edn. Sinauer Associates, Sunderland MA (2001)Google Scholar
  11. 11.
    Postnov, D.E., Ryazanova, L.S., Mosekilde, E., Sosnovtseva, O.V.: Neural synchronization via potassium signaling. Int. J. Neural Syst. 16, 99–109 (2006)CrossRefGoogle Scholar
  12. 12.
    Postnov, D.E., Ryazanova, L.S., Zhirin, R.A., Mosekilde, E., Sosnovtseva, O.V.: Noise controlled synchronization in potassium coupled neural models. Int. J. Neural Syst. 17, 105–113 (2007)CrossRefGoogle Scholar
  13. 13.
    Coggeshall, R.E., Fawcett, D.W.: The fine structre of the central nervous system of the leech, Hirudo medicinalis, J. Neurophysiol. 27, 229–289 (1964)Google Scholar
  14. 14.
    Deitmer, J.W., Rose, C.R., Munch, T., Schmidt, J., Nett, W., Schneider, N.-P., Lohr, C.: Leech glial cell: functional role in a simple nervous system. Glia 28, 175–182 (1999)CrossRefGoogle Scholar
  15. 15.
    Dierkis, P.W., Hochstrate P., Schlue, W.R.: Distribution and functional properties of glutamate receptors in the leech central nervous system. J. Neurophysiol. 75, 2312–2321 (1996)Google Scholar
  16. 16.
    Hochstrate P., Piel C., Schlue, W.R.: Effect of extracellular K +  on the intracellular free Ca2 +  concentration in leech glial cells and Retzius neurons. Brain Res. 696, 231–241 (1995)CrossRefGoogle Scholar
  17. 17.
    Dorner, R., Ballanyi, K., Schulue, W.R.: Glutaminergic responses of neuropile glial cells and Retzius neurones in the leech central nervous system. Brain Res. 16, 111–116 (1990)CrossRefGoogle Scholar
  18. 18.
    Munsch, T., Deitmer, J.W.: Calcuim transients in identified leech glia cells in situ evoked by high potassium concentration and 5-hydroxytryptamine. J. Exp. Biol. 167, 251–265 (1992)Google Scholar
  19. 19.
    Lohr, C., Deitmer, J.W.: Intracellular Ca2 +  release mediated by metabotropic glutamate receptor activation in the leech giant glial cell. J. Exp. Biol. 200, 2565–2573 (1997)Google Scholar
  20. 20.
    Brune T., Deitmer, J.W.: Intracellular acidification and Ca2 +  transients in cultured rat cerebellar astrocytes evoked by glutamate agonist and noradrenaline. Glia 14, 153–161 (1995)CrossRefGoogle Scholar
  21. 21.
    Di Garbo, A., Barbi, M., Chillemi, S., Alloisio, S., Nobile, M.: Calcium signalling in astrocytes and modulation of neural activity. Biosystems 89, 74–83 (2007)CrossRefGoogle Scholar
  22. 22.
    Parpura, V., Basarsky, T.A., Liu, F., Jeftinija, K., Jeftinija, S., Haydon, P.G.: Glutamate-mediated astrocyte-neuron signalling. Nature 369, 744–747 (1994)CrossRefADSGoogle Scholar
  23. 23.
    Nadkarni, S., Jung, P.: Modeling synaptic transmission of the tripartite synapse. Phys. Biol. 4, 1–9 (2007)CrossRefADSGoogle Scholar
  24. 24.
    Nadkarni, S., Jung, P.: Dressed neurons: modeling neural-glia interactions. Phys. Biol. 1, 35–41 (2004)CrossRefADSGoogle Scholar
  25. 25.
    Wuttke, W.A.: Mechanism of potassium uptake in neuropile glial cell in the central nervous system of the leech. J. Neurophysiol. 63, 1089–1097 (1990)Google Scholar
  26. 26.
    Dietzel, I.D., Drapeau, P., Nicholls, J.G.: Voltage dependence of 5-hydroxytryptamine release at a synapse between identified leech neurons in culture. J. Physiol. 372, 192–205 (1986)Google Scholar
  27. 27.
    Stewart, R.R., Adams, W.B., Nicholls, J.G.: Presynaptic calcium currents and facilitation of serotonin release at synapses between cultured leech neurons. J. Exp. Biol. 144, 1–12 (1989)Google Scholar
  28. 28.
    Hill, B.: Ion Channels of Excitable Membrains, 3rd edn. Sinauer Associates, Sunderland MA (2001)Google Scholar

Copyright information

© Springer Science + Business Media B.V. 2008

Authors and Affiliations

  • D. E. Postnov
    • 1
  • L. S. Ryazanova
    • 1
  • N. A. Brazhe
    • 2
    • 3
  • A. R. Brazhe
    • 2
    • 3
  • G. V. Maximov
    • 2
  • E. Mosekilde
    • 3
  • O. V. Sosnovtseva
    • 3
  1. 1.Physics DepartmentSaratov State UniversitySaratovRussia
  2. 2.Biophysics Department, Biological FacultyMoscow State UniversityMoscowRussia
  3. 3.Department of PhysicsTechnical University of DenmarkKongens LyngbyDenmark

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