New Insights on Temporal Lobe Epilepsy Based on Plasticity-Related Network Changes and High-Order Statistics

  • Erika Reime Kinjo
  • Pedro Xavier Royero Rodríguez
  • Bianca Araújo dos Santos
  • Guilherme Shigueto Vilar Higa
  • Mariana Sacrini Ayres Ferraz
  • Christian Schmeltzer
  • Sten Rüdiger
  • Alexandre Hiroaki Kihara
Article

Abstract

Epilepsy is a disorder of the brain characterized by the predisposition to generate recurrent unprovoked seizures, which involves reshaping of neuronal circuitries based on intense neuronal activity. In this review, we first detailed the regulation of plasticity-associated genes, such as ARC, GAP-43, PSD-95, synapsin, and synaptophysin. Indeed, reshaping of neuronal connectivity after the primary, acute epileptogenesis event increases the excitability of the temporal lobe. Herein, we also discussed the heterogeneity of neuronal populations regarding the number of synaptic connections, which in the theoretical field is commonly referred as degree. Employing integrate-and-fire neuronal model, we determined that in addition to increased synaptic strength, degree correlations might play essential and unsuspected roles in the control of network activity. Indeed, assortativity, which can be described as a condition where high-degree correlations are observed, increases the excitability of neural networks. In this review, we summarized recent topics in the field, and data were discussed according to newly developed or unusual tools, as provided by mathematical graph analysis and high-order statistics. With this, we were able to present new foundations for the pathological activity observed in temporal lobe epilepsy.

Keywords

Epileptogenesis Status epilepticus Neuronal plasticity Assortativity Degree correlations Networks TLE 

Notes

Acknowledgements

AHK is grateful for grants from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2014/16711-6, 2011/50151-0, 2015/50122-0) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 308608/2014-3), Brazil. SR acknowledges support from the DFG-IRTG 1740/2.

References

  1. 1.
    Buckmaster PS (2014) Does mossy fiber sprouting give rise to the epileptic state? In: Scharfman HE, Buckmaster PS (eds) issues in Clinical Epileptology: A view from the bench. Adv Exp Med Biol 813. Springer Netherlands:161–168. doi: 10.1007/978-94-017-8914-1_13 CrossRefPubMedGoogle Scholar
  2. 2.
    O’Dell CM, Das A, Gt W, Ray SK, Banik NL (2012) Understanding the basic mechanisms underlying seizures in mesial temporal lobe epilepsy and possible therapeutic targets: a review. J Neurosci Res 90(5):913–924. doi: 10.1002/jnr.22829 CrossRefPubMedGoogle Scholar
  3. 3.
    Dixit AB, Banerjee J, Srivastava A, Tripathi M, Sarkar C, Kakkar A, Jain M, Chandra PS (2016) RNA-seq analysis of hippocampal tissues reveals novel candidate genes for drug refractory epilepsy in patients with MTLE-HS. Genomics 107(5):178–188. doi: 10.1016/j.ygeno.2016.04.001 CrossRefPubMedGoogle Scholar
  4. 4.
    Vieira AS, de Matos AH, do Canto AM, Rocha CS, Carvalho BS, Pascoal VD, Norwood B, Bauer S et al (2016) RNA sequencing reveals region-specific molecular mechanisms associated with epileptogenesis in a model of classical hippocampal sclerosis. Scientific reports 6:22416. doi: 10.1038/srep22416 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Hunt RF, Boychuk JA, Smith BN (2013) Neural circuit mechanisms of post-traumatic epilepsy. Front Cell Neurosci 7:89. doi: 10.3389/fncel.2013.00089 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Buckmaster PS, Lew FH (2011) Rapamycin suppresses mossy fiber sprouting but not seizure frequency in a mouse model of temporal lobe epilepsy. J Neurosci 31(6):2337–2347. doi: 10.1523/JNEUROSCI.4852-10.2011 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Heng K, Haney MM, Buckmaster PS (2013) High-dose rapamycin blocks mossy fiber sprouting but not seizures in a mouse model of temporal lobe epilepsy. Epilepsia 54(9):1535–1541. doi: 10.1111/epi.12246 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Wuarin JP, Dudek FE (1996) Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainate-treated epileptic rats. J Neurosci 16(14):4438–4448PubMedGoogle Scholar
  9. 9.
    Lynch M, Sutula T (2000) Recurrent excitatory connectivity in the dentate gyrus of kindled and kainic acid-treated rats. J Neurophysiol 83(2):693–704PubMedGoogle Scholar
  10. 10.
    Winokur RS, Kubal T, Liu D, Davis SF, Smith BN (2004) Recurrent excitation in the dentate gyrus of a murine model of temporal lobe epilepsy. Epilepsy Res 58(2–3):93–105. doi: 10.1016/j.eplepsyres.2004.01.002 CrossRefPubMedGoogle Scholar
  11. 11.
    Blumcke I, Thom M, Aronica E, Armstrong DD, Bartolomei F, Bernasconi A, Bernasconi N, Bien CG et al (2013) International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: a task force report from the ILAE commission on diagnostic methods. Epilepsia 54(7):1315–1329. doi: 10.1111/epi.12220 CrossRefPubMedGoogle Scholar
  12. 12.
    Schoene-Bake JC, Keller SS, Niehusmann P, Volmering E, Elger C, Deppe M, Weber B (2014) In vivo mapping of hippocampal subfields in mesial temporal lobe epilepsy: relation to histopathology. Hum Brain Mapp 35(9):4718–4728. doi: 10.1002/hbm.22506 CrossRefPubMedGoogle Scholar
  13. 13.
    Buckmaster PS, Dudek FE (1997) Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J Comp Neurol 385(3):385–404CrossRefPubMedGoogle Scholar
  14. 14.
    Sutula TP (2004) Mechanisms of epilepsy progression: current theories and perspectives from neuroplasticity in adulthood and development. Epilepsy Res 60(2–3):161–171. doi: 10.1016/j.eplepsyres.2004.07.001 CrossRefPubMedGoogle Scholar
  15. 15.
    Tauck DL, Nadler JV (1985) Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 5(4):1016–1022PubMedGoogle Scholar
  16. 16.
    Rao MS, Hattiangady B, Reddy DS, Shetty AK (2006) Hippocampal neurodegeneration, spontaneous seizures, and mossy fiber sprouting in the F344 rat model of temporal lobe epilepsy. J Neurosci Res 83(6):1088–1105. doi: 10.1002/jnr.20802 CrossRefPubMedGoogle Scholar
  17. 17.
    Dingledine R, Varvel NH, Dudek FE (2014) When and how do seizures kill neurons, and is cell death relevant to epileptogenesis? Adv Exp Med Biol 813:109–122. doi: 10.1007/978-94-017-8914-1_9 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6(4):347–470. doi: 10.1002/(SICI)1098-1063(1996)6:4<347::AID-HIPO1>3.0.CO;2-I CrossRefPubMedGoogle Scholar
  19. 19.
    Sperk G, Wieser R, Widmann R, Singer EA (1986) Kainic acid induced seizures: changes in somatostatin, substance P and neurotensin. Neuroscience 17(4):1117–1126CrossRefPubMedGoogle Scholar
  20. 20.
    Shetty AK, Turner DA (1995) Intracerebroventricular kainic acid administration in adult rat alters hippocampal calbindin and non-phosphorylated neurofilament expression. J Comp Neurol 363(4):581–599. doi: 10.1002/cne.903630406 CrossRefPubMedGoogle Scholar
  21. 21.
    Shetty AK, Turner DA (2001) Glutamic acid decarboxylase-67-positive hippocampal interneurons undergo a permanent reduction in number following kainic acid-induced degeneration of CA3 pyramidal neurons. Exp Neurol 169(2):276–297. doi: 10.1006/exnr.2001.7668 CrossRefPubMedGoogle Scholar
  22. 22.
    Janz P, Savanthrapadian S, Haussler U, Kilias A, Nestel S, Kretz O, Kirsch M, Bartos M et al (2016) Synaptic remodeling of entorhinal input contributes to an aberrant hippocampal network in temporal lobe epilepsy. Cereb Cortex. doi: 10.1093/cercor/bhw093
  23. 23.
    Kinjo ER, Higa GS, Morya E, Valle AC, Kihara AH, Britto LR (2014) Reciprocal regulation of epileptiform neuronal oscillations and electrical synapses in the rat hippocampus. PLoS One 9(10):e109149. doi: 10.1371/journal.pone.0109149 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Haussler U, Rinas K, Kilias A, Egert U, Haas CA (2016) Mossy fiber sprouting and pyramidal cell dispersion in the hippocampal CA2 region in a mouse model of temporal lobe epilepsy. Hippocampus 26(5):577–588. doi: 10.1002/hipo.22543 CrossRefPubMedGoogle Scholar
  25. 25.
    Morimoto K, Fahnestock M, Racine RJ (2004) Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog Neurobiol 73(1):1–60. doi: 10.1016/j.pneurobio.2004.03.009 CrossRefPubMedGoogle Scholar
  26. 26.
    Morimoto K, Sato K, Sato S, Yamada N, Hayabara T (1998) Time-dependent changes in rat hippocampal synapsin I mRNA expression during long-term potentiation. Brain Res 783(1):57–62CrossRefPubMedGoogle Scholar
  27. 27.
    Suemaru S, Sato K, Morimoto K, Yamada N, Sato T, Kuroda S (2000) Increment of synapsin I immunoreactivity in the hippocampus of the rat kindling model of epilepsy. Neuroreport 11(6):1319–1322CrossRefPubMedGoogle Scholar
  28. 28.
    Mitsuya K, Nitta N, Suzuki F (2009) Persistent zinc depletion in the mossy fiber terminals in the intrahippocampal kainate mouse model of mesial temporal lobe epilepsy. Epilepsia 50(8):1979–1990. doi: 10.1111/j.1528-1167.2009.02055.x CrossRefPubMedGoogle Scholar
  29. 29.
    Li S, Reinprecht I, Fahnestock M, Racine RJ (2002) Activity-dependent changes in synaptophysin immunoreactivity in hippocampus, piriform cortex, and entorhinal cortex of the rat. Neuroscience 115(4):1221–1229CrossRefPubMedGoogle Scholar
  30. 30.
    Jiang Q, Wang J, Wu X, Jiang Y (2007) Alterations of NR2B and PSD-95 expression after early-life epileptiform discharges in developing neurons. Int J Dev Neurosci 25(3):165–170. doi: 10.1016/j.ijdevneu.2007.02.001 CrossRefPubMedGoogle Scholar
  31. 31.
    Sun QJ, Duan RS, Wang AH, Shang W, Zhang T, Zhang XQ, Chi ZF (2009) Alterations of NR2B and PSD-95 expression in hippocampus of kainic acid-exposed rats with behavioural deficits. Behav Brain Res 201(2):292–299. doi: 10.1016/j.bbr.2009.02.027 CrossRefPubMedGoogle Scholar
  32. 32.
    Frasca A, Aalbers M, Frigerio F, Fiordaliso F, Salio M, Gobbi M, Cagnotto A, Gardoni F et al (2011) Misplaced NMDA receptors in epileptogenesis contribute to excitotoxicity. Neurobiol Dis 43(2):507–515. doi: 10.1016/j.nbd.2011.04.024 CrossRefPubMedGoogle Scholar
  33. 33.
    Meberg PJ, Gall CM, Routtenberg A (1993) Induction of F1/GAP-43 gene expression in hippocampal granule cells after seizures [corrected]. Brain Res Mol Brain Res 17(3–4):295–299CrossRefPubMedGoogle Scholar
  34. 34.
    Bendotti C, Baldessari S, Pende M, Southgate T, Guglielmetti F, Samanin R (1997) Relationship between GAP-43 expression in the dentate gyrus and synaptic reorganization of hippocampal mossy fibres in rats treated with kainic acid. Eur J Neurosci 9(1):93–101CrossRefPubMedGoogle Scholar
  35. 35.
    Rekart JL, Routtenberg A (2010) Overexpression of GAP-43 reveals unexpected properties of hippocampal mossy fibers. Hippocampus 20(1):46–57. doi: 10.1002/hipo.20668 PubMedPubMedCentralGoogle Scholar
  36. 36.
    Lyford GL, Yamagata K, Kaufmann WE, Barnes CA, Sanders LK, Copeland NG, Gilbert DJ, Jenkins NA et al (1995) Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14(2):433–445CrossRefPubMedGoogle Scholar
  37. 37.
    Akiyama K, Ishikawa M, Saito A (2008) mRNA expression of activity-regulated cytoskeleton-associated protein (arc) in the amygdala-kindled rats. Brain Res 1189:236–246. doi: 10.1016/j.brainres.2007.10.102 CrossRefPubMedGoogle Scholar
  38. 38.
    Christensen KV, Leffers H, Watson WP, Sanchez C, Kallunki P, Egebjerg J (2010) Levetiracetam attenuates hippocampal expression of synaptic plasticity-related immediate early and late response genes in amygdala-kindled rats. BMC Neurosci 11:9. doi: 10.1186/1471-2202-11-9 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Szyndler J, Maciejak P, Wislowska-Stanek A, Lehner M, Plaznik A (2013) Changes in the Egr1 and arc expression in brain structures of pentylenetetrazole-kindled rats. Pharmacological reports : PR 65(2):368–378CrossRefPubMedGoogle Scholar
  40. 40.
    Gangarossa G, Di Benedetto M, O’Sullivan GJ, Dunleavy M, Alcacer C, Bonito-Oliva A, Henshall DC, Waddington JL et al (2011) Convulsant doses of a dopamine D1 receptor agonist result in Erk-dependent increases in Zif268 and arc/Arg3.1 expression in mouse dentate gyrus. PLoS One 6(5):e19415. doi: 10.1371/journal.pone.0019415 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Engel J Jr, Thompson PM, Stern JM, Staba RJ, Bragin A, Mody I (2013) Connectomics and epilepsy. Curr Opin Neurol 26(2):186–194. doi: 10.1097/WCO.0b013e32835ee5b8 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10(3):186–198. doi: 10.1038/nrn2575 CrossRefPubMedGoogle Scholar
  43. 43.
    De Vico FF, Richiardi J, Chavez M, Achard S (2014) Graph analysis of functional brain networks: practical issues in translational neuroscience. Philos Trans R Soc Lond Ser B Biol Sci 369(1653). doi: 10.1098/rstb.2013.0521
  44. 44.
    Pessoa L (2014) Understanding brain networks and brain organization. Physics of life reviews 11(3):400–435. doi: 10.1016/j.plrev.2014.03.005 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Stam CJ (2014) Modern network science of neurological disorders. Nat Rev Neurosci 15(10):683–695. doi: 10.1038/nrn3801 CrossRefPubMedGoogle Scholar
  46. 46.
    Bullmore ET, Bassett DS (2011) Brain graphs: graphical models of the human brain connectome. Annu Rev Clin Psychol 7:113–140. doi: 10.1146/annurev-clinpsy-040510-143934 CrossRefPubMedGoogle Scholar
  47. 47.
    Bernhardt BC, Chen Z, He Y, Evans AC, Bernasconi N (2011) Graph-theoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. Cereb Cortex 21(9):2147–2157. doi: 10.1093/cercor/bhq291 CrossRefPubMedGoogle Scholar
  48. 48.
    van Diessen E, Diederen SJ, Braun KP, Jansen FE, Stam CJ (2013) Functional and structural brain networks in epilepsy: what have we learned? Epilepsia 54(11):1855–1865. doi: 10.1111/epi.12350 CrossRefPubMedGoogle Scholar
  49. 49.
    Kramer MA, Cash SS (2012) Epilepsy as a disorder of cortical network organization. Neuroscientist 18(4):360–372. doi: 10.1177/1073858411422754 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Bassett DS, Bullmore E, Verchinski BA, Mattay VS, Weinberger DR, Meyer-Lindenberg A (2008) Hierarchical organization of human cortical networks in health and schizophrenia. J Neurosci 28(37):9239–9248. doi: 10.1523/JNEUROSCI.1929-08.2008 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Bialonski S, Lehnertz K (2013) Assortative mixing in functional brain networks during epileptic seizures. Chaos 23(3):033139. doi: 10.1063/1.4821915 CrossRefPubMedGoogle Scholar
  52. 52.
    Agosta F, Sala S, Valsasina P, Meani A, Canu E, Magnani G, Cappa SF, Scola E et al (2013) Brain network connectivity assessed using graph theory in frontotemporal dementia. Neurology 81(2):134–143. doi: 10.1212/WNL.0b013e31829a33f8 CrossRefPubMedGoogle Scholar
  53. 53.
    Agosta F, Galantucci S, Valsasina P, Canu E, Meani A, Marcone A, Magnani G, Falini A et al (2014) Disrupted brain connectome in semantic variant of primary progressive aphasia. Neurobiol Aging 35(11):2646–2655. doi: 10.1016/j.neurobiolaging.2014.05.017 CrossRefPubMedGoogle Scholar
  54. 54.
    Kramer MA, Eden UT, Lepage KQ, Kolaczyk ED, Bianchi MT, Cash SS (2011) Emergence of persistent networks in long-term intracranial EEG recordings. J Neurosci 31(44):15757–15767. doi: 10.1523/JNEUROSCI.2287-11.2011 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    de Haan W, Pijnenburg YA, Strijers RL, van der Made Y, van der Flier WM, Scheltens P, Stam CJ (2009) Functional neural network analysis in frontotemporal dementia and Alzheimer’s disease using EEG and graph theory. BMC Neurosci 10:101. doi: 10.1186/1471-2202-10-101 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Kuhnert MT, Elger CE, Lehnertz K (2010) Long-term variability of global statistical properties of epileptic brain networks. Chaos 20(4):043126. doi: 10.1063/1.3504998 CrossRefPubMedGoogle Scholar
  57. 57.
    Chiang S, Haneef Z (2014) Graph theory findings in the pathophysiology of temporal lobe epilepsy. Clin Neurophysiol 125(7):1295–1305. doi: 10.1016/j.clinph.2014.04.004 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Albert R, Jeong H, Barabasi AL (2000) Error and attack tolerance of complex networks. Nature 406(6794):378–382. doi: 10.1038/35019019 CrossRefPubMedGoogle Scholar
  59. 59.
    Achard S, Bullmore E (2007) Efficiency and cost of economical brain functional networks. PLoS Comput Biol 3(2):e17. doi: 10.1371/journal.pcbi.0030017 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Netoff TI, Clewley R, Arno S, Keck T, White JA (2004) Epilepsy in small-world networks. J Neurosci 24(37):8075–8083. doi: 10.1523/JNEUROSCI.1509-04.2004 CrossRefPubMedGoogle Scholar
  61. 61.
    Percha B, Dzakpasu R, Zochowski M, Parent J (2005) Transition from local to global phase synchrony in small world neural network and its possible implications for epilepsy. Phys Rev E Stat Nonlinear Soft Matter Phys 72(3 Pt 1):031909. doi: 10.1103/PhysRevE.72.031909 CrossRefGoogle Scholar
  62. 62.
    Dyhrfjeld-Johnsen J, Santhakumar V, Morgan RJ, Huerta R, Tsimring L, Soltesz I (2007) Topological determinants of epileptogenesis in large-scale structural and functional models of the dentate gyrus derived from experimental data. J Neurophysiol 97(2):1566–1587. doi: 10.1152/jn.00950.2006 CrossRefPubMedGoogle Scholar
  63. 63.
    Horstmann MT, Bialonski S, Noennig N, Mai H, Prusseit J, Wellmer J, Hinrichs H, Lehnertz K (2010) State dependent properties of epileptic brain networks: comparative graph-theoretical analyses of simultaneously recorded EEG and MEG. Clin Neurophysiol 121(2):172–185. doi: 10.1016/j.clinph.2009.10.013 CrossRefPubMedGoogle Scholar
  64. 64.
    van Dellen E, Douw L, Baayen JC, Heimans JJ, Ponten SC, Vandertop WP, Velis DN, Stam CJ et al (2009) Long-term effects of temporal lobe epilepsy on local neural networks: a graph theoretical analysis of corticography recordings. PLoS One 4(11):e8081. doi: 10.1371/journal.pone.0008081 CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Sun DA, Sombati S, DeLorenzo RJ (2001) Glutamate injury-induced epileptogenesis in hippocampal neurons: an in vitro model of stroke-induced “epilepsy”. Stroke 32(10):2344–2350CrossRefPubMedGoogle Scholar
  66. 66.
    Vaessen MJ, Jansen JF, Vlooswijk MC, Hofman PA, Majoie HJ, Aldenkamp AP, Backes WH (2012) White matter network abnormalities are associated with cognitive decline in chronic epilepsy. Cereb Cortex 22(9):2139–2147. doi: 10.1093/cercor/bhr298 CrossRefPubMedGoogle Scholar
  67. 67.
    Newman ME (2002) Assortative mixing in networks. Phys Rev Lett 89(20):208701. doi: 10.1103/PhysRevLett.89.208701 CrossRefPubMedGoogle Scholar
  68. 68.
    Foster JG, Foster DV, Grassberger P, Paczuski M (2010) Edge direction and the structure of networks. Proc Natl Acad Sci U S A 107(24):10815–10820. doi: 10.1073/pnas.0912671107 CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Ponten SC, Bartolomei F, Stam CJ (2007) Small-world networks and epilepsy: graph theoretical analysis of intracerebrally recorded mesial temporal lobe seizures. Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology 118(4):918–927. doi: 10.1016/j.clinph.2006.12.002 CrossRefGoogle Scholar
  70. 70.
    Kramer MA, Kolaczyk ED, Kirsch HE (2008) Emergent network topology at seizure onset in humans. Epilepsy Res 79(2–3):173–186. doi: 10.1016/j.eplepsyres.2008.02.002 CrossRefPubMedGoogle Scholar
  71. 71.
    Schindler KA, Bialonski S, Horstmann MT, Elger CE, Lehnertz K (2008) Evolving functional network properties and synchronizability during human epileptic seizures. Chaos 18(3):033119. doi: 10.1063/1.2966112 CrossRefPubMedGoogle Scholar
  72. 72.
    Braun U, Plichta MM, Esslinger C, Sauer C, Haddad L, Grimm O, Mier D, Mohnke S et al (2012) Test-retest reliability of resting-state connectivity network characteristics using fMRI and graph theoretical measures. NeuroImage 59(2):1404–1412. doi: 10.1016/j.neuroimage.2011.08.044 CrossRefPubMedGoogle Scholar
  73. 73.
    Jalili M, Knyazeva MG (2011) Constructing brain functional networks from EEG: partial and unpartial correlations. J Integr Neurosci 10(2):213–232. doi: 10.1142/S0219635211002725 CrossRefPubMedGoogle Scholar
  74. 74.
    Geier C, Lehnertz K, Bialonski S (2015) Time-dependent degree-degree correlations in epileptic brain networks: from assortative to dissortative mixing. Front Hum Neurosci 9:462. doi: 10.3389/fnhum.2015.00462 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Newman ME (2003) Mixing patterns in networks. Phys Rev E Stat Nonlinear Soft Matter Phys 67(2 Pt 2):026126. doi: 10.1103/PhysRevE.67.026126 CrossRefGoogle Scholar
  76. 76.
    Motter AE, Zhou C, Kurths J (2005) Network synchronization, diffusion, and the paradox of heterogeneity. Phys Rev E Stat Nonlinear Soft Matter Phys 71(1 Pt 2):016116. doi: 10.1103/PhysRevE.71.016116 CrossRefGoogle Scholar
  77. 77.
    Kinjo ER, Higa GS, Santos BA, de Sousa E, Damico MV, Walter LT, Morya E, Valle AC et al (2016) Pilocarpine-induced seizures trigger differential regulation of microRNA-stability related genes in rat hippocampal neurons. Scientific reports 6:20969. doi: 10.1038/srep20969 CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    de Lanerolle NC, Kim JH, Robbins RJ, Spencer DD (1989) Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res 495(2):387–395CrossRefPubMedGoogle Scholar
  79. 79.
    Babb TL, Kupfer WR, Pretorius JK, Crandall PH, Levesque MF (1991) Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience 42(2):351–363CrossRefPubMedGoogle Scholar
  80. 80.
    Wuarin JP, Dudek FE (2001) Excitatory synaptic input to granule cells increases with time after kainate treatment. J Neurophysiol 85(3):1067–1077PubMedGoogle Scholar
  81. 81.
    Cavazos JE, Zhang P, Qazi R, Sutula TP (2003) Ultrastructural features of sprouted mossy fiber synapses in kindled and kainic acid-treated rats. J Comp Neurol 458(3):272–292. doi: 10.1002/cne.10581 CrossRefPubMedGoogle Scholar
  82. 82.
    Simmons ML, Terman GW, Chavkin C (1997) Spontaneous excitatory currents and kappa-opioid receptor inhibition in dentate gyrus are increased in the rat pilocarpine model of temporal lobe epilepsy. J Neurophysiol 78(4):1860–1868PubMedGoogle Scholar
  83. 83.
    Okazaki MM, Molnar P, Nadler JV (1999) Recurrent mossy fiber pathway in rat dentate gyrus: synaptic currents evoked in presence and absence of seizure-induced growth. J Neurophysiol 81(4):1645–1660PubMedGoogle Scholar
  84. 84.
    Meconi A, Lui E, Marrone DF (2015) Sustained arc expression in adult-generated granule cells. Neurosci Lett 603:66–70. doi: 10.1016/j.neulet.2015.07.029 CrossRefPubMedGoogle Scholar
  85. 85.
    Perez Y, Morin F, Beaulieu C, Lacaille JC (1996) Axonal sprouting of CA1 pyramidal cells in hyperexcitable hippocampal slices of kainate-treated rats. Eur J Neurosci 8(4):736–748CrossRefPubMedGoogle Scholar
  86. 86.
    Lehmann TN, Gabriel S, Kovacs R, Eilers A, Kivi A, Schulze K, Lanksch WR, Meencke HJ et al (2000) Alterations of neuronal connectivity in area CA1 of hippocampal slices from temporal lobe epilepsy patients and from pilocarpine-treated epileptic rats. Epilepsia 41(Suppl 6):S190–S194CrossRefPubMedGoogle Scholar
  87. 87.
    McKinney RA, Debanne D, Gahwiler BH, Thompson SM (1997) Lesion-induced axonal sprouting and hyperexcitability in the hippocampus in vitro: implications for the genesis of posttraumatic epilepsy. Nat Med 3(9):990–996CrossRefPubMedGoogle Scholar
  88. 88.
    Le Duigou C, Simonnet J, Telenczuk MT, Fricker D, Miles R (2014) Recurrent synapses and circuits in the CA3 region of the hippocampus: an associative network. Front Cell Neurosci 7:262. doi: 10.3389/fncel.2013.00262 CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Case M, Soltesz I (2011) Computational modeling of epilepsy. Epilepsia 52(Suppl 8):12–15. doi: 10.1111/j.1528-1167.2011.03225.x CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Schmeltzer C, Kihara AH, Sokolov IM, Rudiger S (2015) Degree correlations optimize neuronal network sensitivity to sub-threshold stimuli. PLoS One 10(6):e0121794. doi: 10.1371/journal.pone.0121794 CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Hall D, Kuhlmann L (2013) Mechanisms of seizure propagation in 2-dimensional centre-surround recurrent networks. PLoS One 8(8):e71369. doi: 10.1371/journal.pone.0071369 CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Ursino M, La Cara GE (2006) Travelling waves and EEG patterns during epileptic seizure: analysis with an integrate-and-fire neural network. J Theor Biol 242(1):171–187. doi: 10.1016/j.jtbi.2006.02.012 CrossRefPubMedGoogle Scholar
  93. 93.
    Sporns O, Honey CJ, Kotter R (2007) Identification and classification of hubs in brain networks. PLoS One 2(10):e1049. doi: 10.1371/journal.pone.0001049 CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Tomov P, Pena RF, Roque AC, Zaks MA (2016) Mechanisms of self-sustained oscillatory states in hierarchical modular networks with mixtures of electrophysiological cell types. Front Comput Neurosci 10:23. doi: 10.3389/fncom.2016.00023 CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Jiang X, Lachance M, Rossignol E (2016) Involvement of cortical fast-spiking parvalbumin-positive basket cells in epilepsy. Prog Brain Res 226:81–126. doi: 10.1016/bs.pbr.2016.04.012 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Erika Reime Kinjo
    • 1
  • Pedro Xavier Royero Rodríguez
    • 1
  • Bianca Araújo dos Santos
    • 1
  • Guilherme Shigueto Vilar Higa
    • 1
    • 2
  • Mariana Sacrini Ayres Ferraz
    • 1
  • Christian Schmeltzer
    • 1
    • 3
  • Sten Rüdiger
    • 3
  • Alexandre Hiroaki Kihara
    • 1
    • 2
  1. 1.Laboratório de Neurogenética, Centro de Matemática, Computação e CogniçãoUniversidade Federal do ABCSão Bernardo do CampoBrazil
  2. 2.Departamento de Fisiologia e Biofísica, Instituto de Ciências BiomédicasUniversidade de São PauloSão PauloBrazil
  3. 3.Institute of PhysicsHumboldt University at BerlinBerlinGermany

Personalised recommendations