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Stochastic Modeling of Spreading Cortical Depression

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Stochastic Biomathematical Models

Part of the book series: Lecture Notes in Mathematics ((LNMBIOS,volume 2058))

Abstract

The nonlinear wave phenomenon of cortical spreading depression (SD), which occurs in many brain structures, has mathematical similarities to neuronal spiking but on very different space and time scales. Its properties and previous modeling are briefly reviewed. A model consisting of a 6-component reaction–diffusion system in two space dimensions is described. With 3-parameter Poisson process sources of potassium ions representing extrusions due to the random firings of neurons, the model takes the form of a multi-component set of nonlinear stochastic partial differential equations. Assuming that in a restricted small area the sources have greater strength than background, the probability of an SD wave is found as a function of the patch size. Also investigated is the probability of elicitation of SD through the occurrence of a patch with compromised metabolic activity, as may occur by virtue of an infarct after stroke. The analysis proceeds in terms of the effect of relative decreases in the strength of ATP-dependent sodium–potassium exchange pump.

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References

  1. Basarsky, T.A., Feighan, D., MacVicar, B.A.: Glutamate release through volume-activated channels during spreading depression. J. Neurosci. 19, 6439–6445 (1999)

    Google Scholar 

  2. Boissel, J.P., Ribba, B., Grenier, E., Chapuisat, G., Dronne, M.A.: Modelling methodology in physiopathology. Prog. Biophys. Molec. Biol. 97, 28–39 (2008)

    Google Scholar 

  3. Bonthius, D.J., Stringer, J.L., Lothman, E.W., Steward, O.: Spreading depression and reverberatory seizures induce the upregulation of mRNA for glial fibrillary acidic protein. Brain Res. 645, 215–224 (1994)

    Google Scholar 

  4. Broberg, M., Pope, K.J., Nilsson, M., Wallace, A., Wilson, J., Willoughby, J.O.: Preseizure increased gamma electroencephalographic activity has no effect on extracellular potassium or calcium. J. Neurosci. Res. 85, 906–918 (2007)

    Google Scholar 

  5. Chapuisat, G.: Discussion of a simple model of spreading depressions. ESAIM Proc. 18, 87–98 (2007)

    Google Scholar 

  6. Chapuisat, G., Dronneb, M.A., Grenier, E., Hommel, M., Gilquin, H., Boissel, J.P.: A global phenomenological model of ischemic stroke with stress on spreading depressions. Prog. Biophys. Molec. Biol. 97, 4–27 (2008)

    Google Scholar 

  7. Cucchiara, B., Detre, J.: Migraine and circle of Willis anomalies. Med. Hypoth. 70, 860–865 (2008)

    Google Scholar 

  8. Cui, Y., Katoaka, Y., Inui, T., Mochizuki, T., Onoe, H., Matsumura, K., Urade, Y., Yamada, H., Watanabe, Y.: Up-regulated neuronal COX-2 expression after cortical spreading depression is involved in non-REM sleep induction in rats. J. Neurosci. Res. 86, 929–936 (2008)

    Google Scholar 

  9. Dahlem, M.A., Schneider, F.M., Schöll, E.: Efficient control of transient wave forms to prevent spreading depolarizations. J. Theor. Biol. 251, 202–209 (2008)

    Google Scholar 

  10. Dahlem, M.A., Schneider, F.M., Schöll, E.: Failure of feedback as a putative common mechanism of spreading depolarizations in migraine and stroke. Chaos 18, 026,110 (2008)

    Google Scholar 

  11. Fabricius, M., Fuhr, S., Willumsen, L., Dreier, J.P., Bhatia, R., Boutelle, M.G., Hartings, J.A., Bullock, R., Strong, A.J., Lauritzen, M.: Association of seizures with cortical spreading depression and perinfarct depolarisations in the acutely injured human brain. Clin. Neurophysiol. 119, 1973–1984 (2008)

    Google Scholar 

  12. Fossier, P., Tauc, L., Baux, G.: Calcium transients and neurotransmitter release at an identified synapse. Trends Neurosci. 22, 161–166 (1999)

    Google Scholar 

  13. Garay, R.P., Garrahan, P.J.: The interaction of sodium and potassium with the sodium pump in red cells. J. Physiol. 231, 297–325 (1973)

    Google Scholar 

  14. Gardner-Medwin, A.R.: Possible roles of vertebrate neuroglia in potassium dynamics, spreading depression and migraine. J. Exp. Biol. 95, 111–127 (1981)

    Google Scholar 

  15. Gass, A., Ay, H., Szabo, K., Koroshetz, W.J.: Diffusion-weighted MRI for the small stuff: the details of acute cerebral ischaemia. Lancet Neurol. 3, 39–45 (2004)

    Google Scholar 

  16. Gorgi, A.: Spreading depression: a review of the clinical relevance. Brain Res. Rev. 38, 33–60 (2001)

    Google Scholar 

  17. Hadjikhani, N., Sanchez Del Rio, M., Wu, O., Schwartz, D., Bakker, D., Fischl, B., Kwong, K.K., Cutrer, F.M., Rosen, B.R., Tootell, R.B., Sorensen, A.G., Moskowitz, M.A.: Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc. Natl. Acad. Sci. 98, 4687–4692 (2001)

    Google Scholar 

  18. Heidelberger, R., Heinemann, C., Neher, E., Matthews, G.: Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371, 513–515 (1994)

    Google Scholar 

  19. Herreras, O.: Electrical prodromals of spreading depression void grafsteins potassium hypothesis. J. Neurophysiol. 94, 3656 (2005)

    Google Scholar 

  20. Hossman, K.A.: Cerebral ischemia: models, methods and outcomes. Neuropharmacology 55, 257–270 (2007)

    Google Scholar 

  21. Kager, H., Wadman, W.J., Somjen, G.G.: Simulated seizures and spreading depression in a neuron model incorporating interstitial space and ion concentrations. J. Neurophysiol. 84, 495,512 (2000)

    Google Scholar 

  22. Koester, H.J., Sakmann, B.: Calcium dynamics associated with action potentials in single nerve terminals of pyramidal cells in layer 2/3 of the young rat neocortex. J. Physiol. 529, 625–646 (2000)

    Google Scholar 

  23. Kramer, M.A., Szeri, A.J., Sleigh, J.W., Kirsch, H.E.: Mechanisms of seizure propagation in a cortical model. J. Comput. Neurosci. 22, 63–80 (2007)

    Google Scholar 

  24. Larrosa, B., Pastor, J., López-Aguado, L., Herreras, O.: A role for glutamate and glia in the fast network oscillations preceding spreading depression. Neuroscience 141, 1057–1068 (2006)

    Google Scholar 

  25. Lauritzen, M.: Pathophysiology of the migraine aura: the spreading depression theory. Brain 117, 191–210 (1994)

    Google Scholar 

  26. Leão, A.A.P.: Spreading depression of activity in the cerebral cortex. Neurophysiology 7, 359–390 (1944)

    Google Scholar 

  27. Leão, A.A.P., Morison, R.S.: Propagation of spreading cortical depression. J. Neurophysiol. 8, 33–45 (1945)

    Google Scholar 

  28. Makarova, J., Ibarz, J.M., Canals, S., Herreras, O.: A steady-state model of spreading depression predicts the importance of an unknown conductance in specific dendritic domains. Biophys. J. 92, 4216–4232 (2007)

    Google Scholar 

  29. Makarova, J., Makarov, V.A., Herreras, O.: Generation of sustained field potentials by gradients of polarization within single neurons: a macroscopic model of spreading depression. J. Neurophysiol. 103, 2446–2457 (2010)

    Google Scholar 

  30. Mayevsky, A., Doron, A., Manor, T., Meilin, S., Zarchin, N., Ouaknine, G.E.: Cortical spreading depression recorded from the human brain. Brain Res. 740, 268–274 (1996)

    Google Scholar 

  31. Milner, P.M.: Note on a possible correspondence between the scotomas of migraine and spreading depression of leĂŁo. Electroencephalogr. Clin. Neurophysiol. 10, 705 (1958)

    Google Scholar 

  32. Obrenovitch, T.P., Zilkha, E.: Inhibition of cortical spreading depression by L-701,324, a novel antagonist at the glycine site of the N-methyl-D-aspartate receptor complex. Br. J. Pharmacol. 117, 931–937 (1996)

    Google Scholar 

  33. Rodgers, C.I., Armstrong, G.A.B., Robertson, R.M.: Coma in response to environmental stress in the locust: a model for cortical spreading depression. J. Insect. Physiol. 56, 980–990 (2010)

    Google Scholar 

  34. Rovira, A., Grivé, E., Rovira, A., Alvarez-Sabin, J.: Distribution territories and causative mechanisms of ischemic stroke. Eur. Radiol. 15, 416–426 (2005)

    Google Scholar 

  35. Schiller, J., Helmchen, F., Sakmann, B.: Spatial profile of dendritic calcium transients evoked by action potentials in rat neocortical pyramidal neurones. J. Physiol. 487, 583–600 (1995)

    Google Scholar 

  36. Schock, S.C., Munyao, N., Yakubchyk, Y., Sabourin, L.A., Hakim, A.M., Ventureyra, E.C., Thompson, C.S.: Cortical spreading depression releases ATP into the extracellular space and purinergic receptor activation contributes to the induction of ischemic tolerance. Brain Res. 1168, 129–138 (2007)

    Google Scholar 

  37. Shapiro, B.E.: Osmotic forces and gap junctions in spreading depression: a computational model. J. Comp. Neurosci. 10, 99–120 (2001)

    Google Scholar 

  38. Somjen, G.G.: Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol. Rev. 81, 1065–1096 (2001)

    Google Scholar 

  39. Somjen, G.G., Kager, H., Wadman, W.J.: Calcium sensitive nonselective cation current promotes seizure-like discharges and spreading depression in a model neuron. J. Comp. Neurosci. 26, 139–147 (2009)

    Google Scholar 

  40. Teixeira, H.Z., Alvarenga, D.J., Almeida, A.C.G., Rodrigues, A.M., Duarte, M.A.: Parallelization of the electrodiffusion mechanism of the computational model of spreading depression. Computational Science and Engineering, Proceedings of 11th International Conference 2008, IEEE Conference publications. DOI: 10.1109/CSE.2008.12 pp. 261–266 (2008)

    Google Scholar 

  41. Torok, T.L.: Electrogenic Na + /Ca2 + -exchange of nerve and muscle cells. Prog. Neurobiol. 82, 287–347 (2007)

    Google Scholar 

  42. Tuckwell, H.C.: Predictions and properties of a model of potssium and calcium ion movements during spreading cortical depression. Int. J. Neurosci. 10, 145–165 (1980)

    Google Scholar 

  43. Tuckwell, H.C.: Mathematical modeling of spreading cortical depression: spiral and reverberating waves. Am. Inst. Phys. Conf. Proc. 1028, 46–64 (2008)

    Google Scholar 

  44. Tuckwell, H.C., Hermansen, C.L.: Ion and transmitter movements during spreading cortical depression. Int. J. Neurosci. 12, 109–135 (1981)

    Google Scholar 

  45. Tuckwell, H.C., Miura, R.M.: A mathematical model for spreading cortical depression. Biophys. J. 23, 257–276 (1978)

    Google Scholar 

  46. Van Harreveld, A.: Two mechanisms for spreading depression in the chicken retina. J. Neurobiol. 9, 419–431 (1978)

    Google Scholar 

  47. Yingst, D.R., Davis, J., Schiebinger, R.: Effects of extracellular calcium and potassium on the sodium pump of rat adrenal glomerulosa cells. Am. J. Physiol. Cell Physiol. 280, C119–C125 (2001)

    Google Scholar 

  48. Zoremba, N., Homola, A., Rossaint, R., Syková, E.: Brain metabolism and extracellular space diffusion parameters during and after transient global hypoxia in the rat cortex. Exp. Neurol. 203, 34–41 (2007)

    Google Scholar 

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Correspondence to Henry C. Tuckwell .

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Tuckwell, H.C. (2013). Stochastic Modeling of Spreading Cortical Depression. In: Bachar, M., Batzel, J., Ditlevsen, S. (eds) Stochastic Biomathematical Models. Lecture Notes in Mathematics(), vol 2058. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-32157-3_8

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