Skip to main content
Log in

Dynamical patterns of calcium signaling in a functional model of neuron–astrocyte networks

  • Original Paper
  • Published:
Journal of Biological Physics Aims and scope Submit manuscript

Abstract

We propose a functional mathematical model for neuron-astrocyte networks. The model incorporates elements of the tripartite synapse and the spatial branching structure of coupled astrocytes. We consider glutamate-induced calcium signaling as a specific mode of excitability and transmission in astrocytic–neuronal networks. We reproduce local and global dynamical patterns observed experimentally.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Haydon, P.G.: Glia: listening and talking to the synapse. Nat. Rev. 2, 185–193 (2001)

    Article  Google Scholar 

  2. Fields, R.D., Stevens-Graham, B.: New insights into neuron–glia communication. Science 298, 556–562 (2002)

    Article  ADS  Google Scholar 

  3. Bonvento, G., Giaume, C., Lorenceau, J.: Neuron–glia interactions: from physiology to behavior. J. Physiol. 96, 167–168 (2002)

    Google Scholar 

  4. Fiacco, T.A.: Advances in understanding new roles for astrocytes in the modulation of neuronal activity. Physiol. News 72, 18–20 (2008)

    Google Scholar 

  5. Nedergaard, M.: Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science 263, 1768–1771 (1994)

    Article  ADS  Google Scholar 

  6. Carmignoto, G.: Reciprocal communication systems between astrocytes and neurons. Prog. Neurobiol. 62, 561–581 (2000)

    Article  Google Scholar 

  7. Finkbeiner, S.: Calcium waves in astrocytes—filling in the gaps. Neuron 8, 1101–1108 (1992)

    Article  Google Scholar 

  8. Dani, J.W., Chernjavsky, A., Smith, S.J.: Neuronal activity triggers calcium waves in hippocampal astrocyte network. Neuron 8, 429–440 (1992)

    Article  Google Scholar 

  9. Butt, A.M., Ransom, B.R.: Morphology of astrocytes and oligodendrocytes during development in the intact optic rat nerve. J. Comp. Neurol. 338, 141–158 (1993)

    Article  Google Scholar 

  10. Pasti, L., Pozzan, T., Carmignotto, G.: Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J. Neurosci. 17, 7817–7830 (1997)

    Google Scholar 

  11. Lee, S.H., Kim, W.T., Cornell-Bell, A.H., Sontheimer, H.: Astrocytes exhibit regional specificity in gap-junctional coupling. Glia 11, 315–325 (1994)

    Article  Google Scholar 

  12. Cornell-Bell, A.H., Sontheimer, H., Cooper, S.M., Smith, S.J.: Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247, 470–473 (1990)

    Article  ADS  Google Scholar 

  13. Newman, E.A.: Glial cell inhibition of neurons by release of ATP. J. Neurosci. 23, 1659–1666 (2003)

    Google Scholar 

  14. Fellin, T., Pascual, O., Haydon, P.G.: Astrocytes coordinate synaptic networks: balanced excitation and inhibition. Physiology 21, 208–215 (2006)

    Article  Google Scholar 

  15. Bowser, D.N., Khakh, B.S.: ATP excites interneurons and astrocytes to increase synaptic inhibition in neuronal networks. J. Neurosci. 24, 8606–8620 (2004)

    Article  Google Scholar 

  16. Koizumi, S., Fujishita, K., Tsuda, M., Shigemoto-Mogami, Y., Inoue, K.: Dynamic inhibition of excitatory synaptic transmission by astrocyte-derived ATP in hyppocampal cultures. Proc. Natl. Acad. Sci. U. S. A. 100, 11023–11028 (2003)

    Article  ADS  Google Scholar 

  17. Serrano, A., Naddjeri, N., Lacaille, J.-C., Robitaille, R.: GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. J. Neurosci. 26, 5370–5382 (2006)

    Article  Google Scholar 

  18. Hansson, E.: Could chronic pain and spread of pain sensation be induced and maintained by glial activation? Acta Physiol. (Oxf.) 187, 321–327 (2006)

    Article  Google Scholar 

  19. Fellin, T., Gomez-Gonzalo, M., Gobbo, S., Carmignoto, G., Haydon, P.G.: Astrocytic glutamate is not necessary for the generation of epileptiform neuronal activity in hippocampal slices. J. Neurosci. 26, 9312–9322 (2006)

    Article  Google Scholar 

  20. Tian, G.-F., Azmi, H., Takano, T., Xu, Q., Peng, W., Lin, J., Oberheim, NA., Lou, N., Zeilke, R., Kang, R., Nedergaard, M.: An astrocyte basis of epilepsy. Nat. Med. 11, 973–981 (2005)

    Google Scholar 

  21. Nadkarni, S., Jung, P.: Spontaneous oscillations of dressed neurons: a new mechanism for epilepsy? Phys. Rev. Lett. 91, 268101 (2003)

    Article  ADS  Google Scholar 

  22. Nadkarni, S., Jung, P.: Dressed neurons: modeling neural–glia interactions. Phys. Biol. 1, 35–41 (2004)

    Article  ADS  Google Scholar 

  23. Nadkarni, S., Jung, P.: Modeling synaptic transmission of the tripartite synapse. Phys. Biol. 4, 1–9 (2007)

    Article  ADS  Google Scholar 

  24. Nadkarni, S., Jung, P., Levine, H.: Astrocytes optimize the synaptic transmission of information. PLoS Comput. Biol. 4(5), e1000088 (2008)

    Article  MathSciNet  Google Scholar 

  25. Stamatakis, M., Mantzaris, N.V.: Modeling of ATP-mediated signal transduction and wave propagation in astrocytic cellular networks. J. Theor. Biol. 241, 649–668 (2006)

    Article  MathSciNet  Google Scholar 

  26. Bennett, M.R., Farnell, L., Gibson, W.G.: A quantitative model of purinergic junctional transmission of calcium waves in astrocyte networks. Biophys. J. 89, 2235-2250 (2005)

    Article  Google Scholar 

  27. Gibson, W.G., Farnell, L., Bennett, M.R.: A computational model relating changes in cerebral blood volume to synaptic activity in neurons. Neurocomputing 70, 1674–1679 (2007)

    Article  Google Scholar 

  28. Postnov, D.E., Ryazanova, L.S., Brazhe, N.A., Brazhe, A.R., Maximov, G.V., Mosekilde, E., Sosnovtseva, O.V.: Giant glial cell: new insight throuth mechanism-based modeling. J. Biol. Phys. 34, 441–457 (2008)

    Article  Google Scholar 

  29. Postnov, D.E., Ryazanova, L.S., Sosnovtseva, O.V.: Functional modeling of neural–glial interaction. Biosystems 89(1–3), 84–91 (2007)

    Article  Google Scholar 

  30. FitzHugh, R.A.: Impulses and physiological states in theoretical models of nerve membrane. Biophys. J. 1, 445–446 (1961)

    Article  ADS  Google Scholar 

  31. Kopell, N., Ermentrout, G.B., Whittington, M.A., Traub, R.D.: Gamma rhythms and beta rhythms have different synchronization properties. Proc. Natl. Acad. Sci. U. S. A. 97, 1867–1872 (2000)

    Article  ADS  Google Scholar 

  32. Keener, J., Sneyd, J.: Mathematical Physiology. Springer, New York (1998)

    MATH  Google Scholar 

  33. Dupont, G., Goldbeter, A.: One-pool model for Ca2+ oscillations involving Ca2+ and inositol 1,4,5-triphosphate as co-agonists for Ca2+ release. Cell Calcium 14, 311–322 (1993)

    Article  Google Scholar 

  34. Jung, P., Cornell-Bell, A., Madden, K.S., Moss, F.: Noise-induced spiral waves in astrocyte syncytia show evidence of self-organized criticality. J. Neurophysiol. 79, 1098–1101 (1998)

    Google Scholar 

  35. Zhu, X., Bergles, D.E., Nishiyama, A.: NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135, 145–157 (2008)

    Article  Google Scholar 

  36. Katyal, S., El-Khamisy, S.F., Russell, H.R., Li, Y., Ju, L., Caldecott, K.W., McKinnon, P.J.: TDP1 facilitates chromosomal single-strand break repair in neurons and is neuroprotective in vivo. EMBO J. 26, 4720–4731 (2007)

    Article  Google Scholar 

  37. Martin, A., Hofmann, H.D., Kirsch, M.: Glial reactivity in ciliary neurotrophic factor-deficient mice after optic nerve lesion. J. Neurosci. 23(13), 5416–5424 (2003)

    Google Scholar 

  38. Bushong, E.A., Martone, M.E., Ellisman, M.H.: Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development. Int. J. Dev. Neurosci. 22, 73–86 (2004)

    Article  Google Scholar 

  39. Bushong, E.A., Martone, M.E., Jones, Y.Z., Ellisman, M.H.: Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J. Neurosci. 22(1), 183–192 (2002)

    Google Scholar 

  40. Mi, H., Barres, B.A.: Purification and characterization of astrocyte precursor cells in the developing rat optic nerve. J. Neurosci. 19(3), 1049–1061 (1999)

    Google Scholar 

  41. Lee, M.Y., Deller, T., Kirsch, M., Frotscher, M., Hofmann, H.D.: Differential regulation of ciliary neurotrophic factor (CNTF) and CNTF receptor alpha expression in astrocytes and neurons of the fascia dentata after entorhinal cortex lesion. J. Neurosci. 17(3), 1137–1146 (1997)

    Google Scholar 

  42. ftp://cell.biophys.msu.ru/pub/soft/astro-net-2008-11-18.tar.gz

  43. Fellin, T., Carmignoto, G.: Neurone-to-astrocyte signaling in the brain represents a distinct multifunctional unit. J. Physiol. 559(1), 3–15 (2004)

    Article  Google Scholar 

  44. Manzoni, O.J., Manabe, T., Nikoll, R.A.: Release of adenosine by activation of NMDA receptor in the hippocampus. Science 265, 2098–2101 (1994)

    Article  ADS  Google Scholar 

  45. Ryazanova, L., Trenikhina, Y., Zhirin, R., Postnov, D.: Noise-induced firing patterns in generalized neuron model with subthreshold oscillations. Proc. SPIE 6436, 64360W (2007)

Download references

Acknowledgements

This work was partly supported by the European Commission (NoE BioSim, Contract No. 4SHB-CT-2004-005137). N.B and A.B. acknowledge support from the Lundbeck Foundation and O.S. acknowledges the Skou grant from Forskningsraadet for Natur og Univers. D.P. and R.K. acknowledge support from the RFBR grant 090201049.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. E. Postnov.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Postnov, D.E., Koreshkov, R.N., Brazhe, N.A. et al. Dynamical patterns of calcium signaling in a functional model of neuron–astrocyte networks. J Biol Phys 35, 425–445 (2009). https://doi.org/10.1007/s10867-009-9156-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10867-009-9156-x

Keywords

Navigation