Advertisement

Acta Neuropathologica

, Volume 128, Issue 1, pp 21–37 | Cite as

Epilepsies associated with hippocampal sclerosis

  • Fernando Cendes
  • Americo C. Sakamoto
  • Roberto Spreafico
  • William Bingaman
  • Albert J. Becker
Review

Abstract

Hippocampal sclerosis (HS) is considered the most frequent neuropathological finding in patients with mesial temporal lobe epilepsy (MTLE). Hippocampal specimens of pharmacoresistant MTLE patients that underwent epilepsy surgery for seizure control reveal the characteristic pattern of segmental neuronal cell loss and concomitant astrogliosis. However, classification issues of hippocampal lesion patterns have been a matter of intense debate. International consensus classification has only recently provided significant progress for comparisons of neurosurgical and clinic-pathological series between different centers. The respective four-tiered classification system of the International League Against Epilepsy subdivides HS into three types and includes a term of “gliosis only, no-HS”. Future studies will be necessary to investigate whether each of these subtypes of HS may be related to different etiological factors or with postoperative memory and seizure outcome. Molecular studies have provided potential deeper insights into the pathogenesis of HS and MTLE on the basis of epilepsy-surgical hippocampal specimens and corresponding animal models. These include channelopathies, activation of NMDA receptors, and other conditions related to Ca2+ influx into neurons, the imbalance of Ca2+—binding proteins, acquired channelopathies that increase neuronal excitability, paraneoplastic and non-paraneoplastic inflammatory events, and epigenetic regulation promoting or facilitating hippocampal epileptogenesis. Genetic predisposition for HS is clearly suggested by the high incidence of family history in patients with HS, and by familial MTLE with HS. So far, it is clear that HS is multifactorial and there is no individual pathogenic factor either necessary or sufficient to generate this intriguing histopathological condition. The obvious variety of pathogenetic combinations underlying HS may explain the multitude of clinical presentations, different responses to clinical and surgical treatment. We believe that the stratification of neuropathological patterns can help to characterize specific clinic-pathological entities and predict the postsurgical seizure control in an improved fashion.

Keywords

Temporal lobe epilepsy Seizures Long term epilepsy Neurodegeneration Gliosis MRI Treatment Surgery Outcome 

Notes

Acknowledgments

FC’s work is supported by FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo, Brazil), Grant # 2013/07559-3. AJB’s work is supported by EuroEpinomics and DFG (SFB 1089, KFO 177), European Union EpiTarget Consortium in FP7, the Else Kröner-Fresenius and German Israeli Foundations and BonFor. RS is supported by the Italian Ministry of Health and Associazione “P: Zorzi” per le Neuroscienze.

References

  1. 1.
    Andrade-Valenca LP, Valenca MM, Velasco TR, Carlotti CG Jr, Assirati JA, Galvis-Alonso OY, Neder L, Cendes F, Leite JP (2008) Mesial temporal lobe epilepsy: clinical and neuropathologic findings of familial and sporadic forms. Epilepsia 49(6):1046–1054PubMedGoogle Scholar
  2. 2.
    Aptel H, Hilaire C, Pieraut S, Boukhaddaoui H, Mallie S, Valmier J, Scamps F (2007) The Cav3.2/alpha1H T-type Ca2 + current is a molecular determinant of excitatory effects of GABA in adult sensory neurons. Mol Cell Neurosci 36(2):293–303PubMedGoogle Scholar
  3. 3.
    Arai N, Umitsu R, Komori T, Hayashi M, Kurata K, Nagata J, Tamagawa K, Mizutani T, Oda M, Morimatsu Y (2003) Peculiar form of cerebral microdysgenesis characterized by white matter neurons with perineuronal and perivascular glial satellitosis: A study using a variety of human autopsied brains. Pathol Int 53(6):345–352PubMedGoogle Scholar
  4. 4.
    Arruda F, Cendes F, Andermann F, Dubeau F, Villemure JG, Jones-Gotman M, Poulin N, Arnold DL, Olivier A (1996) Mesial atrophy and outcome after amygdalohippocampectomy or temporal lobe removal. Ann Neurol 40(3):446–450PubMedGoogle Scholar
  5. 5.
    Barba C, Barbati G, Minotti L, Hoffmann D, Kahane P (2007) Ictal clinical and scalp-EEG findings differentiating temporal lobe epilepsies from temporal ‘plus’ epilepsies. Brain 130(Pt 7):1957–1967PubMedGoogle Scholar
  6. 6.
    Bartolomei F, Cosandier-Rimele D, McGonigal A, Aubert S, Regis J, Gavaret M, Wendling F, Chauvel P (2010) From mesial temporal lobe to temporoperisylvian seizures: a quantified study of temporal lobe seizure networks. Epilepsia 51(10):2147–2158PubMedGoogle Scholar
  7. 7.
    Becker AJ, Pitsch J, Sochivko D, Opitz T, Staniek M, Chen CC, Campbell KP, Schoch S, Yaari Y, Beck H (2008) Transcriptional upregulation of Cav3.2 mediates epileptogenesis in the pilocarpine model of epilepsy. J Neurosci 28(49):13341–13353PubMedGoogle Scholar
  8. 8.
    Bell B, Lin JJ, Seidenberg M, Hermann B (2011) The neurobiology of cognitive disorders in temporal lobe epilepsy. Nat Rev Neurol 7(3):154–164PubMedGoogle Scholar
  9. 9.
    Ben-Ari Y, Tremblay E, Riche D, Ghilini G, Naquet R (1981) Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience 6(7):1361–1391PubMedGoogle Scholar
  10. 10.
    Berg AT, Berkovic SF, Brodie MJ, Buchhalter J, Cross JH, van Boas WE, Engel J, French J, Glauser TA, Mathern GW, Moshe SL, Nordli D, Plouin P, Scheffer IE (2010) Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005-2009. Epilepsia 51(4):676–685PubMedGoogle Scholar
  11. 11.
    Berg AT, Langfitt J, Shinnar S, Vickrey BG, Sperling MR, Walczak T, Bazil C, Pacia SV, Spencer SS (2003) How long does it take for partial epilepsy to become intractable? Neurology 60(2):186–190PubMedGoogle Scholar
  12. 12.
    Berkovic SF, Howell RA, Hopper JL (1994) Familial temporal lobe epilepsy: a new syndrome with adolescent/adult onset and a benign course. In: Wolf P (ed) Epileptic seizures and syndromes. John Libbey, London, pp 259–265Google Scholar
  13. 13.
    Berkovic SF, McIntosh A, Howell RA, Mitchell A, Sheffield LJ, Hopper JL (1996) Familial temporal lobe epilepsy—a common disorder identified in twins. Ann Neurol 40(2):227–235PubMedGoogle Scholar
  14. 14.
    Berkovic SF, Scheffer IE (1998) Febrile seizures: genetics and relationship to other epilepsy syndromes. Curr Opin Neurol 11(2):129–134PubMedGoogle Scholar
  15. 15.
    Bernard C, Anderson A, Becker A, Poolos NP, Beck H, Johnston D (2004) Acquired dendritic channelopathy in temporal lobe epilepsy. Science 305(5683):532–535PubMedGoogle Scholar
  16. 16.
    Bernasconi A, Andermann F, Cendes F, Dubeau F, Andermann E, Olivier A (1998) Nocturnal temporal lobe epilepsy. Neurology 50(6):1772–1777PubMedGoogle Scholar
  17. 17.
    Bien CG, Urbach H, Schramm J, Soeder BM, Becker AJ, Voltz R, Vincent A, Elger CE (2007) Limbic encephalitis as a precipitating event in adult-onset temporal lobe epilepsy. Neurology 69(12):1236–1244PubMedGoogle Scholar
  18. 18.
    Bien CG, Vincent A, Barnett MH, Becker AJ, Blumcke I, Graus F, Jellinger KA, Reuss DE, Ribalta T, Schlegel J, Sutton I, Lassmann H, Bauer J (2012) Immunopathology of autoantibody-associated encephalitides: clues for pathogenesis. Brain 135(Pt 5):1622–1638PubMedGoogle Scholar
  19. 19.
    Bilevicius E, Yasuda CL, Silva MS, Guerreiro CA, Lopes-Cendes I, Cendes F (2010) Antiepileptic drug response in temporal lobe epilepsy: a clinical and MRI morphometry study. Neurology 75(19):1695–1701PubMedGoogle Scholar
  20. 20.
    Blumcke I, Becker AJ, Klein C, Scheiwe C, Lie AA, Beck H, Waha A, Friedl MG, Kuhn R, Emson P, Elger C, Wiestler OD (2000) Temporal lobe epilepsy associated up-regulation of metabotropic glutamate receptors: correlated changes in mGluR1 mRNA and protein expression in experimental animals and human patients. J Neuropathol Exp Neurol 59(1):1–10PubMedGoogle Scholar
  21. 21.
    Blumcke I, Coras R, Miyata H, Ozkara C (2012) Defining clinico-neuropathological subtypes of mesial temporal lobe epilepsy with hippocampal sclerosis. Brain Pathol 22(3):402–411PubMedGoogle Scholar
  22. 22.
    Blumcke I, Cross JH, Spreafico R (2013) The international consensus classification for hippocampal sclerosis: an important step towards accurate prognosis. Lancet Neurol 12(9):844–846PubMedGoogle Scholar
  23. 23.
    Blumcke I, Kistner I, Clusmann H, Schramm J, Becker AJ, Elger CE, Bien CG, Merschhemke M, Meencke HJ, Lehmann T, Buchfelder M, Weigel D, Buslei R, Stefan H, Pauli E, Hildebrandt M (2009) Towards a clinico-pathological classification of granule cell dispersion in human mesial temporal lobe epilepsies. Acta Neuropathol 117(5):535–544PubMedGoogle Scholar
  24. 24.
    Blumcke I, Pauli E, Clusmann H, Schramm J, Becker A, Elger C, Merschhemke M, Meencke HJ, Lehmann T, von Deimling A, Scheiwe C, Zentner J, Volk B, Romstock J, Stefan H, Hildebrandt M (2007) A new clinico-pathological classification system for mesial temporal sclerosis. Acta Neuropathol 113(3):235–244PubMedCentralPubMedGoogle Scholar
  25. 25.
    Blumcke I, Thom M, Aronica E, Armstrong DD, Bartolomei F, Bernasconi A, Bernasconi N, Bien CG, Cendes F, Coras R, Cross JH, Jacques TS, Kahane P, Mathern GW, Miyata H, Moshe SL, Oz B, Ozkara C, Perucca E, Sisodiya S, Wiebe S, Spreafico R (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):1315–1329PubMedGoogle Scholar
  26. 26.
    Blumcke I, Thom M, Aronica E, Armstrong DD, Vinters HV, Palmini A, Jacques TS, Avanzini G, Barkovich AJ, Battaglia G, Becker A, Cepeda C, Cendes F, Colombo N, Crino P, Cross JH, Delalande O, Dubeau F, Duncan J, Guerrini R, Kahane P, Mathern G, Najm I, Ozkara C, Raybaud C, Represa A, Roper SN, Salamon N, Schulze-Bonhage A, Tassi L, Vezzani A, Spreafico R (2011) The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc task force of the ilae diagnostic methods commission. Epilepsia 52(1):158–174PubMedCentralPubMedGoogle Scholar
  27. 27.
    Blumcke I, Thom M, Wiestler OD (2002) Ammon’s horn sclerosis: a maldevelopmental disorder associated with temporal lobe epilepsy. Brain Pathol 12(2):199–211PubMedGoogle Scholar
  28. 28.
    Bonilha L, Yasuda CL, Rorden C, Li LM, Tedeschi H, de Oliveira E, Cendes F (2007) Does resection of the medial temporal lobe improve the outcome of temporal lobe epilepsy surgery? Epilepsia 48(3):571–578PubMedGoogle Scholar
  29. 29.
    Bouchet C, Cazauvieilh JB (1825) De l’épilepsie considéré dans ses rapports avec l’aliénation mentale. Arch Gen Med 9:510–542Google Scholar
  30. 30.
    Brewster A, Bender RA, Chen Y, Dube C, Eghbal-Ahmadi M, Baram TZ (2002) Developmental febrile seizures modulate hippocampal gene expression of hyperpolarization-activated channels in an isoform- and cell-specific manner. J Neurosci 22(11):4591–4599PubMedCentralPubMedGoogle Scholar
  31. 31.
    Brockhaus A, Elger CE (1995) Complex partial seizures of temporal lobe origin in children of different age groups. Epilepsia 36(12):1173–1181PubMedGoogle Scholar
  32. 32.
    Brooks-Kayal AR, Shumate MD, Jin H, Rikhter TY, Coulter DA (1998) Selective changes in single cell GABA(A) receptor subunit expression and function in temporal lobe epilepsy. Nat Med 4(10):1166–1172PubMedGoogle Scholar
  33. 33.
    Bruton CJ (1988) The neuropathology of temporal lobe epilepsy. In: Russel G, Marley E, Williams P (eds) Maudsley monographs. Oxford University Press, London, pp 1–158Google Scholar
  34. 34.
    Cendes F (2005) Progressive hippocampal and extrahippocampal atrophy in drug resistant epilepsy. Curr Opin Neurol 18(2):173–177PubMedGoogle Scholar
  35. 35.
    Cendes F (2013) Neuroimaging in investigation of patients with epilepsy. Continuum (Minneap Minn)  19 (3 Epilepsy):623–642Google Scholar
  36. 36.
    Cendes F, Andermann F, Carpenter S, Zatorre RJ, Cashman NR (1995) Temporal lobe epilepsy caused by domoic acid intoxication: evidence for glutamate receptor-mediated excitotoxicity in humans. Ann Neurol 37(1):123–126PubMedGoogle Scholar
  37. 37.
    Cendes F, Cook MJ, Watson C, Andermann F, Fish DR, Shorvon SD, Bergin P, Free S, Dubeau F, Arnold DL (1995) Frequency and characteristics of dual pathology in patients with lesional epilepsy. Neurology 45(11):2058–2064PubMedGoogle Scholar
  38. 38.
    Cendes F, Dubeau F, Andermann F, Quesney LF, Gambardella A, Jones-Gotman M, Bizzi J, Olivier A, Gotman J, Arnold DL (1996) Significance of mesial temporal atrophy in relation to intracranial ictal and interictal stereo EEG abnormalities. Brain 119:1317–1326PubMedGoogle Scholar
  39. 39.
    Cendes F, Kahane P, Brodie MJ, Andermann F (2012) The mesio-temporal lobe epilepsy syndrome. Epileptic syndromes in infancy, childhood and adolescence, 5th edn. John Libbey Eurotext Ltd, EastleighGoogle Scholar
  40. 40.
    Cendes F, Knowlton RC, Novotny E, Li LM, Antel S, Sawrie S, Laxer KD, Arnold DL (2002) Magnetic resonance spectroscopy in epilepsy: clinical issues. Epilepsia 43(Suppl 1):32–39Google Scholar
  41. 41.
    Cendes F, Li LM, Andermann F, Watson C, Fish DR, Shorvon SD, Dubeau F, Arnold DL (1999) Dual pathology and its clinical relevance. Adv Neurol 81:153–164PubMedGoogle Scholar
  42. 42.
    Chen K, Aradi I, Thon N, Eghbal-Ahmadi M, Baram TZ, Soltesz I (2001) Persistently modified h-channels after complex febrile seizures convert the seizure-induced enhancement of inhibition to hyperexcitability. Nat Med 7(3):331–337PubMedCentralPubMedGoogle Scholar
  43. 43.
    Choi D, Na DG, Byun HS, Suh YL, Kim SE, Ro DW, Chung IG, Hong SC, Hong SB (1999) White-matter change in mesial temporal sclerosis: correlation of MRI with PET, pathology, and clinical features. Epilepsia 40(11):1634–1641PubMedGoogle Scholar
  44. 44.
    Coan AC, Cendes F (2013) Epilepsy as progressive disorders: what is the evidence that can guide our clinical decisions and how can neuroimaging help? Epilepsy Behav: E&B 26(3):313–321Google Scholar
  45. 45.
    Coan AC, Cendes F (2013) Understanding the spectrum of temporal lobe epilepsy: contributions for the development of individualized therapies. Expert Rev Neurother 13(12):1383–1394PubMedGoogle Scholar
  46. 46.
    Coan AC, Kubota B, Bergo FP, Campos BM, Cendes F (2014) 3T MRI quantification of hippocampal volume and signal in mesial temporal lobe epilepsy improves detection of hippocampal sclerosis. AJNR Am J Neuroradiol 35(1):77–83 Google Scholar
  47. 47.
    da Costa Neves RS, Jardim AP, Caboclo LO, Lancellotti C, Marinho TF, Hamad AP, Marinho M, Centeno R, Cavalheiro EA, Scorza CA, Targas Yacubian EM (2013) Granule cell dispersion is not a predictor of surgical outcome in temporal lobe epilepsy with mesial temporal sclerosis. Clin Neuropathol 32(1):24–30PubMedGoogle Scholar
  48. 48.
    de Lanerolle NC, Kim JH, Williamson A, Spencer SS, Zaveri HP, Eid T, Spencer DD (2003) A retrospective analysis of hippocampal pathology in human temporal lobe epilepsy: evidence for distinctive patient subcategories. Epilepsia 44(5):677–687PubMedGoogle Scholar
  49. 49.
    de Tisi J, Bell GS, Peacock JL, McEvoy AW, Harkness WF, Sander JW, Duncan JS (2011) The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: a cohort study. Lancet 378(9800):1388–1395PubMedGoogle Scholar
  50. 50.
    Dyhrfjeld-Johnsen J, Morgan RJ, Foldy C, Soltesz I (2008) Upregulated H-current in hyperexcitable CA1 dendrites after febrile seizures. Front Cell Neurosci 2:2PubMedCentralPubMedGoogle Scholar
  51. 51.
    Emery JA, Roper SN, Rojiani AM (1997) White matter neuronal heterotopia in temporal lobe epilepsy: a morphometric and immunohistochemical study. J Neuropathol Exp Neurol 56(12):1276–1282PubMedGoogle Scholar
  52. 52.
    Engel J Jr, McDermott MP, Wiebe S, Langfitt JT, Stern JM, Dewar S, Sperling MR, Gardiner I, Erba G, Fried I, Jacobs M, Vinters HV, Mintzer S, Kieburtz K, Early Randomized Surgical Epilepsy Trial Study G (2012) Early surgical therapy for drug-resistant temporal lobe epilepsy: a randomized trial. JAMA: J Am Med Assoc 307(9):922–930Google Scholar
  53. 53.
    Engel J Jr, Wiebe S, French J, Sperling M, Williamson P, Spencer D, Gumnit R, Zahn C, Westbrook E, Enos B, Quality Standards Subcommittee of the American Academy of N, American Epilepsy S, American Association of Neurological S (2003) Practice parameter: temporal lobe and localized neocortical resections for epilepsy: report of the Quality Standards Subcommittee of the American Academy of Neurology, in association with the American Epilepsy Society and the American Association of Neurological Surgeons. Neurology 60(4):538–547PubMedGoogle Scholar
  54. 54.
    Fauser S, Essang C, Altenmuller DM, Staack A, Steinhoff BJ, Strobl K, Bast T, Schubert-Bast S, Doostkam S, Zentner J, Schulze-Bonhage A (2013) Is there evidence for clinical differences related to the new classification of temporal lobe cortical dysplasia? Epilepsia 54(5):909–917PubMedGoogle Scholar
  55. 55.
    Frick A, Magee J, Johnston D (2004) LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat Neurosci 7(2):126–135PubMedGoogle Scholar
  56. 56.
    Gambardella A, Reutens DC, Andermann F, Cendes F, Gloor P, Dubeau F, Olivier A (1994) Late-onset drop attacks in temporal lobe epilepsy: a reevaluation of the concept of temporal lobe syncope. Neurology 44(6):1074–1078PubMedGoogle Scholar
  57. 57.
    Garbelli R, Meroni A, Magnaghi G, Beolchi MS, Ferrario A, Tassi L, Bramerio M, Spreafico R (2006) Architectural (Type IA) focal cortical dysplasia and parvalbumin immunostaining in temporal lobe epilepsy. Epilepsia 47(6):1074–1078PubMedGoogle Scholar
  58. 58.
    Garbelli R, Milesi G, Medici V, Villani F, Didato G, Deleo F, D’Incerti L, Morbin M, Mazzoleni G, Giovagnoli AR, Parente A, Zucca I, Mastropietro A, Spreafico R (2012) Blurring in patients with temporal lobe epilepsy: clinical, high-field imaging and ultrastructural study. Brain 135(Pt 8):2337–2349PubMedGoogle Scholar
  59. 59.
    Gargaro AC, Sakamoto AC, Bianchin MM, Geraldi Cde V, Scorsi-Rosset S, Coimbra ER, Carlotti CG Jr, Assirati JA, Velasco TR (2013) Atypical neuropsychological profiles and cognitive outcome in mesial temporal lobe epilepsy. Epilepsy Behav: E&B 27(3):461–469Google Scholar
  60. 60.
    Gloor P (1997) The temporal lobe and limbic system. Oxford University Press, New YorkGoogle Scholar
  61. 61.
    Goldberg EM, Coulter DA (2013) Mechanisms of epileptogenesis: a convergence on neural circuit dysfunction. Nat Rev Neurosci 14(5):337–349PubMedCentralPubMedGoogle Scholar
  62. 62.
    Grimminger T, Pernhorst K, Surges R, Niehusmann P, Priebe L, von Lehe M, Hoffmann P, Cichon S, Schoch S, Becker AJ (2013) Levetiracetam resistance: synaptic signatures corresponding promoter SNPs in epileptic hippocampi. Neurobiol Dis 60:115–125PubMedGoogle Scholar
  63. 63.
    Hauser WA, Annegers JF, Rocca WA (1996) Descriptive epidemiology of epilepsy—contributions of population-based studies from Rochester, Minnesota. Mayo Clin Proc 71(6):576–586PubMedGoogle Scholar
  64. 64.
    Hirsch LJ, Spencer SS, Williamson PD, Spencer DD, Mattson RH (1991) Comparison of bitemporal and unitemporal epilepsy defined by depth electroencephalography. Ann Neurol 30(3):340–346PubMedGoogle Scholar
  65. 65.
    Hoffman DA, Johnston D (1998) Downregulation of transient K + channels in dendrites of hippocampal CA1 pyramidal neurons by activation of PKA and PKC. J Neurosci 18(10):3521–3528PubMedGoogle Scholar
  66. 66.
    Hoffman DA, Magee JC, Colbert CM, Johnston D (1997) K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387(6636):869–875PubMedGoogle Scholar
  67. 67.
    Hughes EG, Peng X, Gleichman AJ, Lai M, Zhou L, Tsou R, Parsons TD, Lynch DR, Dalmau J, Balice-Gordon RJ (2010) Cellular and synaptic mechanisms of anti-NMDA receptor encephalitis. J Neurosci 30(17):5866–5875PubMedCentralPubMedGoogle Scholar
  68. 68.
    Jackson JH (1880) On a particular variety of epilepsy (“intellectual aura”), one case with symptoms of organic brain disease. Brain 11:179–207Google Scholar
  69. 69.
    Janszky J, Janszky I, Schulz R, Hoppe M, Behne F, Pannek HW, Ebner A (2005) Temporal lobe epilepsy with hippocampal sclerosis: predictors for long-term surgical outcome. Brain 128(Pt 2):395–404PubMedGoogle Scholar
  70. 70.
    Jeha LE, Najm IM, Bingaman WE, Khandwala F, Widdess-Walsh P, Morris HH, Dinner DS, Nair D, Foldvary-Schaeffer N, Prayson RA, Comair Y, O’Brien R, Bulacio J, Gupta A, Luders HO (2006) Predictors of outcome after temporal lobectomy for the treatment of intractable epilepsy. Neurology 66(12):1938–1940PubMedGoogle Scholar
  71. 71.
    Jessberger S, Nakashima K, Clemenson GD Jr, Mejia E, Mathews E, Ure K, Ogawa S, Sinton CM, Gage FH, Hsieh J (2007) Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci 27(22):5967–5975PubMedGoogle Scholar
  72. 72.
    Jimenez-Mateos EM, Engel T, Merino-Serrais P, McKiernan RC, Tanaka K, Mouri G, Sano T, O’Tuathaigh C, Waddington JL, Prenter S, Delanty N, Farrell MA, O’Brien DF, Conroy RM, Stallings RL, DeFelipe J, Henshall DC (2012) Silencing microRNA-134 produces neuroprotective and prolonged seizure-suppressive effects. Nat Med 18(7):1087–1094PubMedCentralPubMedGoogle Scholar
  73. 73.
    Jung S, Jones TD, Lugo JN Jr, Sheerin AH, Miller JW, D’Ambrosio R, Anderson AE, Poolos NP (2007) Progressive dendritic HCN channelopathy during epileptogenesis in the rat pilocarpine model of epilepsy. J Neurosci 27(47):13012–13021PubMedCentralPubMedGoogle Scholar
  74. 74.
    Kahane P, Bartolomei F (2010) Temporal lobe epilepsy and hippocampal sclerosis: lessons from depth EEG recordings. Epilepsia 51(Suppl 1):59–62PubMedGoogle Scholar
  75. 75.
    Kanner AM (2006) Epilepsy, suicidal behaviour, and depression: do they share common pathogenic mechanisms? Lancet Neurol 5(2):107–108PubMedGoogle Scholar
  76. 76.
    Keller SS, Roberts N (2008) Voxel-based morphometry of temporal lobe epilepsy: an introduction and review of the literature. Epilepsia 49(5):741–757PubMedGoogle Scholar
  77. 77.
    Kim J, Jung SC, Clemens AM, Petralia RS, Hoffman DA (2007) Regulation of dendritic excitability by activity-dependent trafficking of the A-type K+ channel subunit Kv4.2 in hippocampal neurons. Neuron 54(6):933–947PubMedCentralPubMedGoogle Scholar
  78. 78.
    Kobayashi E, D’Agostino MD, Lopes-Cendes I, Andermann E, Dubeau F, Guerreiro CA, Schenka AA, Queiroz LS, Olivier A, Cendes F, Andermann F (2003) Outcome of surgical treatment in familial mesial temporal lobe epilepsy. Epilepsia 44(8):1080–1084PubMedGoogle Scholar
  79. 79.
    Kobayashi E, D’Agostino MD, Lopes-Cendes I, Berkovic SF, Li ML, Andermann E, Andermann F, Cendes F (2003) Hippocampal atrophy and T2-weighted signal changes in familial mesial temporal lobe epilepsy. Neurology 60(3):405–409PubMedGoogle Scholar
  80. 80.
    Kobayashi E, Li LM, Lopes-Cendes I, Cendes F (2002) Magnetic resonance imaging evidence of hippocampal sclerosis in asymptomatic, first-degree relatives of patients with familial mesial temporal lobe epilepsy. Arch Neurol 59(12):1891–1894PubMedGoogle Scholar
  81. 81.
    Kobayashi E, Lopes-Cendes I, Guerreiro CA, Sousa SC, Guerreiro MM, Cendes F (2001) Seizure outcome and hippocampal atrophy in familial mesial temporal lobe epilepsy. Neurology 56(2):166–172PubMedGoogle Scholar
  82. 82.
    Kobow K, Jeske I, Hildebrandt M, Hauke J, Hahnen E, Buslei R, Buchfelder M, Weigel D, Stefan H, Kasper B, Pauli E, Blumcke I (2009) Increased reelin promoter methylation is associated with granule cell dispersion in human temporal lobe epilepsy. J Neuropathol Exp Neurol 68(4):356–364PubMedGoogle Scholar
  83. 83.
    Kobow K, Kaspi A, Harikrishnan KN, Kiese K, Ziemann M, Khurana I, Fritzsche I, Hauke J, Hahnen E, Coras R, Muhlebner A, El-Osta A, Blumcke I (2013) Deep sequencing reveals increased DNA methylation in chronic rat epilepsy. Acta Neuropathol 126(5):741–756PubMedCentralPubMedGoogle Scholar
  84. 84.
    Kovacs R, Heinemann U, Steinhauser C (2012) Mechanisms underlying blood-brain barrier dysfunction in brain pathology and epileptogenesis: role of astroglia. Epilepsia 53(Suppl 6):53–59PubMedGoogle Scholar
  85. 85.
    Krendl R, Lurger S, Baumgartner C (2008) Absolute spike frequency predicts surgical outcome in TLE with unilateral hippocampal atrophy. Neurology 71(6):413–418PubMedGoogle Scholar
  86. 86.
    Kubova H, Lukasiuk K, Pitkanen A (2012) New insight on the mechanisms of epileptogenesis in the developing brain. Adv Tech Stand Neurosurg 39:3–44PubMedGoogle Scholar
  87. 87.
    Kwan P, Arzimanoglou A, Berg AT, Brodie MJ, Allen Hauser W, Mathern G, Moshe SL, Perucca E, Wiebe S, French J (2010) Definition of drug resistant epilepsy: consensus proposal by the ad hoc Task Force of the ILAE Commission on Therapeutic Strategies. Epilepsia 51(6):1069–1077PubMedGoogle Scholar
  88. 88.
    Kwan P, Brodie MJ (2000) Early identification of refractory epilepsy. N Engl J Med 342(5):314–319PubMedGoogle Scholar
  89. 89.
    Kwan P, Brodie MJ (2004) Drug treatment of epilepsy: when does it fail and how to optimize its use? CNS Spectr 9(2):110–119PubMedGoogle Scholar
  90. 90.
    Labate A, Gambardella A, Andermann E, Aguglia U, Cendes F, Berkovic SF, Andermann F (2011) Benign mesial temporal lobe epilepsy. Nat Rev Neurol 7(4):237–240PubMedGoogle Scholar
  91. 91.
    Lai M, Hughes EG, Peng X, Zhou L, Gleichman AJ, Shu H, Mata S, Kremens D, Vitaliani R, Geschwind MD, Bataller L, Kalb RG, Davis R, Graus F, Lynch DR, Balice-Gordon R, Dalmau J (2009) AMPA receptor antibodies in limbic encephalitis alter synaptic receptor location. Ann Neurol 65(4):424–434PubMedCentralPubMedGoogle Scholar
  92. 92.
    Lai M, Huijbers MG, Lancaster E, Graus F, Bataller L, Balice-Gordon R, Cowell JK, Dalmau J (2010) Investigation of LGI1 as the antigen in limbic encephalitis previously attributed to potassium channels: a case series. Lancet Neurol 9(8):776–785PubMedCentralPubMedGoogle Scholar
  93. 93.
    Lalic T, Pettingill P, Vincent A, Capogna M (2011) Human limbic encephalitis serum enhances hippocampal mossy fiber-CA3 pyramidal cell synaptic transmission. Epilepsia 52(1):121–131PubMedGoogle Scholar
  94. 94.
    Landré E, Turak B, Chassoux F, Chagot D, Gagnepain JP, Chodkiewicz JP (2001) Postural disturbances and changes in facial expression during temporo-limbic seizures in children. In: Avanzini G, Beaumanoir A, Mira L (eds) Limbic seizures in children. John Libbey & Company Ltd, London, pp 105–114Google Scholar
  95. 95.
    Li LM, Cendes F, Andermann F, Watson C, Fish DR, Cook MJ, Dubeau F, Duncan JS, Shorvon SD, Berkovic SF, Free S, Olivier A, Harkness W, Arnold DL (1999) Surgical outcome in patients with epilepsy and dual pathology. Brain 122(Pt 5):799–805PubMedGoogle Scholar
  96. 96.
    Lie AA, Becker A, Behle K, Beck H, Malitschek B, Conn PJ, Kuhn R, Nitsch R, Plaschke M, Schramm J, Elger CE, Wiestler OD, Blumcke I (2000) Up-regulation of the metabotropic glutamate receptor mGluR4 in hippocampal neurons with reduced seizure vulnerability. Ann Neurol 47(1):26–35PubMedGoogle Scholar
  97. 97.
    Lukasiuk K, Pitkanen A (2012) Molecular basis of acquired epileptogenesis. Handb Clin Neurol 107:3–12PubMedGoogle Scholar
  98. 98.
    Malmgren K, Thom M (2012) Hippocampal sclerosis–origins and imaging. Epilepsia 53(Suppl 4):19–33PubMedGoogle Scholar
  99. 99.
    Marcelin B, Chauviere L, Becker A, Migliore M, Esclapez M, Bernard C (2009) h channel-dependent deficit of theta oscillation resonance and phase shift in temporal lobe epilepsy. Neurobiol Dis 33(3):436–447PubMedGoogle Scholar
  100. 100.
    Margerison JH, Corsellis JA (1966) Epilepsy and the temporal lobes. A clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain 89:499–530PubMedGoogle Scholar
  101. 101.
    Maroso M, Balosso S, Ravizza T, Liu J, Aronica E, Iyer AM, Rossetti C, Molteni M, Casalgrandi M, Manfredi AA, Bianchi ME, Vezzani A (2010) Toll-like receptor 4 and high-mobility group box-1 are involved in ictogenesis and can be targeted to reduce seizures. Nat Med 16(4):413–419PubMedGoogle Scholar
  102. 102.
    Mathern GW, Kuhlman PA, Mendoza D, Pretorius JK (1997) Human fascia dentata anatomy and hippocampal neuron densities differ depending on the epileptic syndrome and age at first seizure. J Neuropathol Exp Neurol 56(2):199–212PubMedGoogle Scholar
  103. 103.
    McIntosh AM, Kalnins RM, Mitchell LA, Fabinyi GC, Briellmann RS, Berkovic SF (2004) Temporal lobectomy: long-term seizure outcome, late recurrence and risks for seizure recurrence. Brain 127(Pt 9):2018–2030PubMedGoogle Scholar
  104. 104.
    Meencke HJ (2009) Clinical neuropathology of the epilepsies in the 100 years of the ILAE (1909–2009). Epilepsia 50(Suppl 3):8–16PubMedGoogle Scholar
  105. 105.
    Meroni A, Galli C, Bramerio M, Tassi L, Colombo N, Cossu M, Lo Russo G, Garbelli R, Spreafico R (2009) Nodular heterotopia: a neuropathological study of 24 patients undergoing surgery for drug-resistant epilepsy. Epilepsia 50(1):116–124PubMedGoogle Scholar
  106. 106.
    Mitchell LA, Jackson GD, Kalnins RM, Saling MM, Fitt GJ, Ashpole RD, Berkovic SF (1999) Anterior temporal abnormality in temporal lobe epilepsy: a quantitative MRI and histopathologic study. Neurology 52(2):327–336PubMedGoogle Scholar
  107. 107.
    Mohamed A, Wyllie E, Ruggieri P, Kotagal P, Babb T, Hilbig A, Wylie C, Ying Z, Staugaitis S, Najm I, Bulacio J, Foldvary N, Luders H, Bingaman W (2001) Temporal lobe epilepsy due to hippocampal sclerosis in pediatric candidates for epilepsy surgery. Neurology 56(12):1643–1649PubMedGoogle Scholar
  108. 108.
    Morita ME, Yasuda CL, Betting LE, Pacagnella D, Conz L, Barbosa PH, Maurer-Morelli CV, Costa AL, Kobayashi E, Lopes-Cendes I, Cendes F (2012) MRI and EEG as long-term seizure outcome predictors in familial mesial temporal lobe epilepsy. Neurology 79(24):2349–2354PubMedGoogle Scholar
  109. 109.
    Nobili L, Cossu M, Mai R, Tassi L, Cardinale F, Castana L, Citterio A, Sartori I, Lo Russo G, Francione S (2004) Sleep-related hyperkinetic seizures of temporal lobe origin. Neurology 62(3):482–485PubMedGoogle Scholar
  110. 110.
    O’Brien TJ, So EL, Mullan BP, Hauser MF, Brinkmann BH, Bohnen NI, Hanson D, Cascino GD, Jack CR Jr, Sharbrough FW (1998) Subtraction ictal SPECT co-registered to MRI improves clinical usefulness of SPECT in localizing the surgical seizure focus. Neurology 50(2):445–454PubMedGoogle Scholar
  111. 111.
    Palmini A, Najm I, Avanzini G, Babb T, Guerrini R, Foldvary-Schaefer N, Jackson G, Luders HO, Prayson R, Spreafico R, Vinters HV (2004) Terminology and classification of the cortical dysplasias. Neurology 62(6 Suppl 3):S2–S8PubMedGoogle Scholar
  112. 112.
    Pathak HR, Weissinger F, Terunuma M, Carlson GC, Hsu FC, Moss SJ, Coulter DA (2007) Disrupted dentate granule cell chloride regulation enhances synaptic excitability during development of temporal lobe epilepsy. J Neurosci 27(51):14012–14022PubMedCentralPubMedGoogle Scholar
  113. 113.
    Pitkanen A, Lukasiuk K (2011) Mechanisms of epileptogenesis and potential treatment targets. Lancet Neurol 10(2):173–186PubMedGoogle Scholar
  114. 114.
    Pitsch J, Opitz T, Borm V, Woitecki A, Staniek M, Beck H, Becker AJ, Schoch S (2012) The presynaptic active zone protein RIM1alpha controls epileptogenesis following status epilepticus. J Neurosci 32(36):12384–12395PubMedGoogle Scholar
  115. 115.
    Sagar HJ, Oxbury JM (1987) Hippocampal neuron loss in temporal lobe epilepsy: correlation with early childhood convulsions. Ann Neurol 22:334–340PubMedGoogle Scholar
  116. 116.
    Sandmann S, Spormann J, Prenzel F, Shaw L, Unger T (2002) Calcium channel blockade limits transcriptional, translational and functional up-regulation of the cardiac calpain system after myocardial infarction. Eur J Pharmacol 453(1):99–109PubMedGoogle Scholar
  117. 117.
    Schramm J (2008) Temporal lobe epilepsy surgery and the quest for optimal extent of resection: a review. Epilepsia 49(8):1296–1307PubMedGoogle Scholar
  118. 118.
    Schulz R, Luders HO, Hoppe M, Tuxhorn I, May T, Ebner A (2000) Interictal EEG and ictal scalp EEG propagation are highly predictive of surgical outcome in mesial temporal lobe epilepsy. Epilepsia 41(5):564–570PubMedGoogle Scholar
  119. 119.
    Schwartzkroin PA (1993) Epilepsy: models, mechanisms, and concepts. Cambridge University Press, CambridgeGoogle Scholar
  120. 120.
    Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119(1):7–35PubMedCentralPubMedGoogle Scholar
  121. 121.
    Stefan H, Hildebrandt M, Kerling F, Kasper BS, Hammen T, Dorfler A, Weigel D, Buchfelder M, Blumcke I, Pauli E (2009) Clinical prediction of postoperative seizure control: structural, functional findings and disease histories. J Neurol Neurosurg Psychiatry 80(2):196–200PubMedGoogle Scholar
  122. 122.
    Tassi L, Garbelli R, Colombo N, Bramerio M, Lo Russo G, Deleo F, Milesi G, Spreafico R (2010) Type I focal cortical dysplasia: surgical outcome is related to histopathology. Epileptic Disord 12(3):181–191PubMedGoogle Scholar
  123. 123.
    Teitelbaum JS, Zatorre RJ, Carpenter S, Gendron D, Evans AC, Gjedde A, Cashman NR (1990) Neurologic sequelae of domoic acid intoxication due to the ingestion of contaminated mussels [see comments]. N Engl J Med 322(25):1781–1787PubMedGoogle Scholar
  124. 124.
    Thom M, Eriksson S, Martinian L, Caboclo LO, McEvoy AW, Duncan JS, Sisodiya SM (2009) Temporal lobe sclerosis associated with hippocampal sclerosis in temporal lobe epilepsy: neuropathological features. J Neuropathol Exp Neurol 68(8):928–938PubMedCentralPubMedGoogle Scholar
  125. 125.
    Thom M, Liagkouras I, Elliot KJ, Martinian L, Harkness W, McEvoy A, Caboclo LO, Sisodiya SM (2010) Reliability of patterns of hippocampal sclerosis as predictors of postsurgical outcome. Epilepsia 51(9):1801–1808PubMedGoogle Scholar
  126. 126.
    Thom M, Zhou J, Martinian L, Sisodiya S (2005) Quantitative post-mortem study of the hippocampus in chronic epilepsy: seizures do not inevitably cause neuronal loss. Brain 128(Pt 6):1344–1357PubMedGoogle Scholar
  127. 127.
    Trevathan E, Gilliam F (2003) Lost years: delayed referral for surgically treatable epilepsy. Neurology 61(4):432–433PubMedGoogle Scholar
  128. 128.
    Turski WA, Cavalheiro EA, Schwarz M, Czuczwar SJ, Kleinrok Z, Turski L (1983) Limbic seizures produced by pilocarpine in rats: behavioural, electroencephalographic and neuropathological study. Behav Brain Res 9(3):315–335PubMedGoogle Scholar
  129. 129.
    Tuunanen J, Pitkanen A (2000) Do seizures cause neuronal damage in rat amygdala kindling? Epilepsy Res 39(2):171–176PubMedGoogle Scholar
  130. 130.
    Vaugier L, Aubert S, McGonigal A, Trebuchon A, Guye M, Gavaret M, Regis J, Chauvel P, Wendling F, Bartolomei F (2009) Neural networks underlying hyperkinetic seizures of “temporal lobe” origin. Epilepsy Res 86(2–3):200–208PubMedGoogle Scholar
  131. 131.
    Velasco TR, Wichert-Ana L, Leite JP, Araujo D, Terra-Bustamante VC, Alexandre V Jr, Kato M, Assirati JA Jr, Machado HR, Carlotti CG Jr, Sakamoto AC (2002) Accuracy of ictal SPECT in mesial temporal lobe epilepsy with bilateral interictal spikes. Neurology 59(2):266–271PubMedGoogle Scholar
  132. 132.
    Vezzani A, Friedman A, Dingledine RJ (2013) The role of inflammation in epileptogenesis. Neuropharmacology 69:16–24PubMedCentralPubMedGoogle Scholar
  133. 133.
    Vincent A, Bien CG, Irani SR, Waters P (2011) Autoantibodies associated with diseases of the CNS: new developments and future challenges. Lancet Neurol 10(8):759–772PubMedGoogle Scholar
  134. 134.
    Vinton AB, Carne R, Hicks RJ, Desmond PM, Kilpatrick C, Kaye AH, O’Brien TJ (2007) The extent of resection of FDG-PET hypometabolism relates to outcome of temporal lobectomy. Brain 130(Pt 2):548–560PubMedGoogle Scholar
  135. 135.
    Wiebe S, Blume WT, Girvin JP, Eliasziw M (2001) A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med 345(5):311–318PubMedGoogle Scholar
  136. 136.
    Wieser HG (2004) ILAE Commission Report. Mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia 45(6):695–714PubMedGoogle Scholar
  137. 137.
    Wong CH, Bleasel A, Wen L, Eberl S, Byth K, Fulham M, Somerville E, Mohamed A (2010) The topography and significance of extratemporal hypometabolism in refractory mesial temporal lobe epilepsy examined by FDG-PET. Epilepsia 51(8):1365–1373PubMedGoogle Scholar
  138. 138.
    Wyler AR, Dohan FC, Schweitzer JB, Berry AD (1992) A grading system for mesial temporal pathology (hippocampal sclerosis) from anterior temporal lobectomy. J Epilepsy 5:220–225Google Scholar
  139. 139.
    Yasuda CL, Valise C, Saude AV, Pereira AR, Pereira FR, Ferreira Costa AL, Morita ME, Betting LE, Castellano G, Guerreiro CAM, Tedeschi H, de Oliveira E, Cendes F (2010) Dynamic changes in white and gray matter volume are associated with outcome of surgical treatment in temporal lobe epilepsy. Neuroimage 49(1):71–79PubMedGoogle Scholar
  140. 140.
    Yoon HH, Kwon HL, Mattson RH, Spencer DD, Spencer SS (2003) Long-term seizure outcome in patients initially seizure-free after resective epilepsy surgery. Neurology 61(4):445–450PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Fernando Cendes
    • 1
  • Americo C. Sakamoto
    • 2
  • Roberto Spreafico
    • 3
  • William Bingaman
    • 4
  • Albert J. Becker
    • 5
  1. 1.Department of Neurology, FCMUniversity of Campinas-UNICAMPCampinasBrazil
  2. 2.Center for Epilepsy Surgery (CIREP), Hospital das Clínicas de Ribeirão PretoUniversity of São PauloSão PauloBrazil
  3. 3.Epilepsy Clinic and Experimental Neurophysiology UnitFondazione IRCCS, Istituto Neurologico “C. Besta”MilanItaly
  4. 4.Neurologic Institute Cleveland ClinicClevelandUSA
  5. 5.Department of NeuropathologyUniversity of Bonn Medical CenterBonnGermany

Personalised recommendations