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Computational Intelligence and Neuroscience
Volume 2013 (2013), Article ID 949816, 19 pages
http://dx.doi.org/10.1155/2013/949816
Research Article

Enhanced Synaptic Connectivity in the Dentate Gyrus during Epileptiform Activity: Network Simulation

1Laboratório de Neurociência Experimental e Computacional, Departamento de Engenharia de Biossistemas, Universidade Federal de São João del-Rei (UFSJ), Brazil
2Programa de Engenharia Biomédica, Universidade Federal do Rio de Janeiro (UFRJ/COPPE), Brazil
3Disciplina de Neurologia Experimental, Escola Paulista de Medicina (EPM), Universidade Federal de São Paulo (UNIFESP), Brazil
4Disciplina de Neurofisiologia e Fisiologia do Exercício, Escola Paulista de Medicina (EPM), Universidade Federal de São Paulo (UNIFESP), Brazil

Received 7 August 2012; Revised 6 December 2012; Accepted 20 December 2012

Academic Editor: Steven Bressler

Copyright © 2013 Keite Lira de Almeida França et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Engel, Seizures and Epilepsy, Edited by F. A. Davis Company, F. A. Davis Company, Philadelphia, Pa, USA, 1989.
  2. M. J. S. Fernandes, E. A. Cavalheiro, J. P. Leite, and D. S. Persike, “Temporal lobe epilepsy: cell death and molecular targets activity,” in Underlying Mechanisms of Epilepsy, F. S. Kaneez, Ed., pp. 117–134, InTech, Rijeka, Croatia, 2011.
  3. A. K. Sharma, R. Y. Reams, W. H. Jordan, M. A. Miller, H. L. Thacker, and P. W. Snyder, “Mesial temporal lobe epilepsy: pathogenesis, induced rodent models and lesions,” Toxicologic Pathology, vol. 35, no. 7, pp. 984–999, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. F. A. Guedes, O. Y. Galvis-Alonso, and J. P. Leite, “Plasticidade neuronal associada à epilepsia do lobo temporal mesial: insights a partir de Estudos em Humanos e em Modelos Animais,” Journal of Epilepsy and Clinical Neurophysiology, vol. 12, pp. 10–17, 2006.
  5. P. S. Buckmaster, G. F. Zhang, and R. Yamawaki, “Axon sprouting in a model of temporal lobe epilepsy creates a predominantly excitatory feedback circuit,” Journal of Neuroscience, vol. 22, no. 15, pp. 6650–6658, 2002. View at Scopus
  6. M. J. A. M. van Puttena, L. C. Liefaardb, M. Danhof, and R. A. Voskuyl, “Quantitative EEG analysis: a biomarker for epileptogenesis,” in Pharmacoresistance in Epilepsy-Modelling and Prediction of Disease Progression, C. Liefaard, Ed., pp. 51–67, 2008.
  7. K. Morimoto, M. Fahnestock, and R. J. Racine, “Kindling and status epilepticus models of epilepsy: rewiring the brain,” Progress in Neurobiology, vol. 73, no. 1, pp. 1–60, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. J. E. Franck, J. Pokorny, D. D. Kunkel, and P. A. Schwartzkroin, “Physiologic and morphologic characteristics of granule cell circuitry in human epileptic hippocampus,” Epilepsia, vol. 36, no. 6, pp. 543–558, 1995. View at Publisher · View at Google Scholar · View at Scopus
  9. M. M. Okazaki, P. Molnár, and J. V. Nadler, “Recurrent mossy fiber pathway in rat dentate gyrus: synaptic currents evoked in presence and absence of seizure-induced growth,” Journal of Neurophysiology, vol. 81, no. 4, pp. 1645–1660, 1999. View at Scopus
  10. J. P. Wuarin and F. E. Dudek, “Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainate-treated epileptic rats,” Journal of Neuroscience, vol. 16, no. 14, pp. 4438–4448, 1996. View at Scopus
  11. W. W. Lytton, K. M. Hellman, and T. P. Sutula, “Computer models of hippocampal circuit changes of the kindling model of epilepsy,” Artificial Intelligence in Medicine, vol. 13, no. 1-2, pp. 81–97, 1998. View at Publisher · View at Google Scholar · View at Scopus
  12. V. Santhakumar, I. Aradi, and I. Soltesz, “Role of mossy fiber sprouting and mossy cell loss in hyperexcitability: a network model of the dentate gyrus incorporating cell types and axonal topography,” Journal of Neurophysiology, vol. 93, no. 1, pp. 437–453, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. R. J. Morgan and I. Soltesz, “Nonrandom connectivity of the epileptic dentate gyrus predicts a major role for neuronal hubs in seizures,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 16, pp. 6179–6184, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. A. C. G. Almeida, A. M. Rodrigues, F. A. Scorza et al., “Mechanistic hypotheses for nonsynaptic epileptiform activity induction and its transition from the interictal to ictal state-Computational simulation,” Epilepsia, vol. 49, no. 11, pp. 1908–1924, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. W. S. McCulloch and W. Pitts, “A logical calculus of the ideas immanent in nervous activity,” The Bulletin of Mathematical Biophysics, vol. 5, no. 4, pp. 115–133, 1943. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Dyhrfjeld-Johnsen, V. Santhakumar, R. J. Morgan, R. Huerta, L. Tsimring, and I. Soltesz, “Topological determinants of epileptogenesis in large-scale structural and functional models of the dentate gyrus derived from experimental data,” Journal of Neurophysiology, vol. 97, no. 2, pp. 1566–1587, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. J. R. Wolff and G. P. Wagner, “Selforganization in synaptogenesis: interaction between the formation of excitatory and inhibitory synapses,” in Synergetics of the Brain, E. Basar, H. Flohr, H. Haken, and A. J. Mandell, Eds., pp. 50–59, Springer, Berlin, Germany, 1983.
  18. I. E. Dammasch and G. P. Wagner, “On the properties of randomly connected McCulloch-Pitts networks: differences between input-constant and input-variant networks,” Cybernetics and Systems, vol. 15, no. 1-2, pp. 91–117, 1984. View at Scopus
  19. I. E. Dammasch, G. P. Wagner, and J. R. Wolff, “Self-stabilization of neuronal networks I. The compensation algorithm for synaptogenesis,” Biological Cybernetics, vol. 54, no. 4-5, pp. 211–222, 1986. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Butz, K. Lehmann, I. E. Dammasch, and G. Teuchert-Noodt, “A theoretical network model to analyse neurogenesis and synaptogenesis in the dentate gyrus,” Neural Networks, vol. 19, no. 10, pp. 1490–1505, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. I. E. Dammasch, G. P. Wagner, and J. R. Wolff, “Self-stabilization of neuronal networks. II. Stability conditions for synaptogenesis,” Biological Cybernetics, vol. 58, no. 3, pp. 149–158, 1988. View at Scopus
  22. A. C. G. Almeida, A. M. Rodrigues, M. A. Duarte et al., “Biophysical aspects of the nonsynaptic epileptiform activity,” in Underlying Mechanisms of Epilepsy, F. S. Kaneez, Ed., pp. 189–218, InTech, Rijeka, Croatia, 2011.
  23. L. J. Cromme and I. E. Dammasch, “Compensation type algorithms for neural nets: stability and convergence,” Journal of Mathematical Biology, vol. 27, no. 3, pp. 327–340, 1989. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Lisman, “A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 23, pp. 9574–9578, 1989.
  25. J. T. Trachtenberg, B. E. Chen, G. W. Knott et al., “Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex,” Nature, vol. 420, no. 6917, pp. 788–794, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. V. De Paola, A. Holtmaat, G. Knott et al., “Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex,” Neuron, vol. 49, no. 6, pp. 861–875, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. J. E. Cavazos, G. Golarai, and T. P. Sutula, “Mossy fiber synaptic reorganization induced by kindling: time course of development, progression, and permanence,” Journal of Neuroscience, vol. 11, no. 9, pp. 2795–2803, 1991. View at Scopus
  28. B. Adams, M. Lee, M. Fahnestock, and R. J. Racine, “Long-term potentiation trains induce mossy fiber sprouting,” Brain Research, vol. 775, no. 1-2, pp. 193–197, 1997. View at Publisher · View at Google Scholar · View at Scopus
  29. U. Sayin, S. Osting, J. Hagen, P. Rutecki, and T. Sutula, “Spontaneous seizures and loss of axo-axonic and axo-somatic inhibition induced by repeated brief seizures in kindled rats,” Journal of Neuroscience, vol. 23, no. 7, pp. 2759–2768, 2003. View at Scopus
  30. H. R. Pathak, F. Weissinger, M. Terunuma et al., “Disrupted dentate granule cell chloride regulation enhances synaptic excitability during development of temporal lobe epilepsy,” Journal of Neuroscience, vol. 27, no. 51, pp. 14012–14022, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. S. W. Briggs and A. S. Galanopoulou, “Altered GABA signaling in early life epilepsies,” Neural Plasticity, vol. 2011, Article ID 527605, 16 pages, 2011. View at Publisher · View at Google Scholar
  32. I. Cohen, V. Navarro, S. Clemenceau, M. Baulac, and R. Miles, “On the origin of interictal activity in human temporal lobe epilepsy in vitro,” Science, vol. 298, no. 5597, pp. 1418–1421, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. G. Huberfeld, L. Wittner, S. Clemenceau et al., “Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy,” Journal of Neuroscience, vol. 27, no. 37, pp. 9866–9873, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. A. T. U. Schaefers, K. Grafen, G. Teuchert-Noodt, and Y. Winter, “Synaptic remodeling in the dentate gyrus, CA3, CA1, subiculum, and entorhinal cortex of mice: effects of deprived rearing and voluntary running,” Neural Plasticity, vol. 2010, Article ID 870573, 11 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. V. Santhakumar, R. Bender, M. Frotscher et al., “Granule cell hyperexcitability in the early post-traumatic rat dentate gyrus: the 'irritable mossy cell' hypothesis,” Journal of Physiology, vol. 524, no. 1, pp. 117–134, 2000. View at Scopus
  36. J. V. Nadler, “The recurrent mossy fiber pathway of the epileptic brain,” Neurochemical Research, vol. 28, no. 11, pp. 1649–1658, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. P. S. Buckmaster and F. H. Lew, “Rapamycin suppresses mossy fiber sprouting but not seizure frequency in a mouse model of temporal lobe epilepsy,” Journal of Neuroscience, vol. 31, no. 6, pp. 2337–2347, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. J. G. R. Jefferys and H. L. Haas, “Synchronized bursting of CA1 hippocampal pyramidal cells in the absence of synaptic transmission,” Nature, vol. 300, no. 5891, pp. 448–450, 1982. View at Scopus
  39. C. P. Taylor and F. E. Dudek, “Synchronous neural afterdischarges in rat hippocampal slices without active chemical synapses,” Science, vol. 218, no. 4574, pp. 810–812, 1982. View at Scopus
  40. Z. Q. Xiong and J. L. Stringer, “Sodium pump activity, not glial spatial buffering, clears potassium after epileptiform activity induced in the dentate gyrus,” Journal of Neurophysiology, vol. 83, no. 3, pp. 1443–1451, 2000. View at Scopus
  41. M. Frotscher, P. Jonas, and R. S. Sloviter, “Synapses formed by normal and abnormal hippocampal mossy fibers,” Cell and Tissue Research, vol. 326, no. 2, pp. 361–367, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. W. W. Lytton, “Computer modelling of epilepsy,” Nature Reviews Neuroscience, vol. 9, no. 8, pp. 626–637, 2008. View at Publisher · View at Google Scholar · View at Scopus