Журнал высшей нервной деятельности им. И.П. Павлова, 2022, T. 72, № 3, стр. 343-359

Роль зубчатой извилины в осуществлении функций гиппокампа: эпилептический мозг

В. Ф. Кичигина 1*, Л. В. Шубина 1, И. Ю. Попова 1

1 ФГБУН Институт теоретической и экспериментальной биофизики РАН
Пущино, Россия

* E-mail: vkitchigina@gmail.com

Поступила в редакцию 28.10.2021
После доработки 03.12.2021
Принята к публикации 20.12.2021

Аннотация

Височная эпилепсия (ВЭ) характеризуется потерей клеток гиппокампа, часто приводящей к его склерозу, последующей реорганизацией гиппокампальной сети и дефицитом декларативной памяти. Несмотря на огромное количество экспериментальных, доклинических и клинических исследований, существует все еще ограниченное понимание основных механизмов, лежащих в основе развития ВЭ. Существует предположение, что именно ЗИ играет решающую роль в механизмах развития этого заболевания. Считают, что при ВЭ нарушается защитная функция ЗИ, основанная на низкой возбудимости гранулярных нейронов и предохраняющая пирамидные клетки гиппокампа от гиперактивации при сильных возбуждающих воздействиях. У пациентов с височной эпилепсией в хилусе ЗИ обнаружена потеря мшистых клеток. Уязвимость мшистых клеток рассматривается некоторыми авторами как критический фактор в развитии ВЭ: эти нейроны в норме ведут себя как предохранители, а их гибель разрывает естественную нейронную сеть, приводя к возникновению патологической активности. В предлагаемой работе рассматриваются изменения морфологических и функциональных свойств ЗИ в эпилептическом мозге, роль спрутинга мшистых волокон и нейрогенеза в развитии ВЭ, а также нарушения когнитивных функций гиппокампа при потере зубчатой извилиной ее защитной роли в условиях гиперактивации.

Ключевые слова: зубчатая извилина, височная эпилепсия, судорожная активность, эпилептический статус, гиперактивация, мшистые клетки, защитная функция, спрутинг мшистых волокон, нейрогенез, риппл-осцилляции

Список литературы

  1. Карлов В.А. Эпилепсия как клиническая и нейрофизиологическая проблема. Журнал неврологии и психиатрии. 2000. 100 (9): 7–15.

  2. Adams B., Lee M., Fahnestock M., Racine R. Long-term potentiation trains induce mossy fiber sprouting. Brain Res. 1997. 775: 193–7.

  3. Axmacher N., Elger C.E., Fell J. Ripples in the medial temporal lobe are relevant for human memory consolidation. Brain J Neurol. 2008. 131: 1806–17.

  4. Avanzi R.D., Cavarsan C.F., Santos J.G. Jr., Hamani C., Mello L.E., Covolan L. Basal dendrites are present in newly born dentate granule cells of young but not aged pilocarpine-treated chronic epileptic rats. Neuroscience. 2010. 170: 687–91.

  5. Babb T.L., Brown W.J. Pathological findings in epilepsy. Surgical treatment of the epilepsies. Ed. Engel. J.Jr. New York: Raven Press, 1987. 511–540 pp.

  6. Babb T.L., Kupfer W.R., Pretorius J.K., Crandall P.H., Levesque M.F. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience. 1991. 42: 351–363.

  7. Beck H., Blümcke I., Kral T., Clusmann H., Schramm J., Wiestler O.D., Heinemann U., Elger C.E. Properties of a delayed rectifier potassium current in dentate granule cells isolated from the hippocampus of patients with chronic temporal lobe epilepsy. Epilepsia. 1996. 37: 892–901.

  8. Bekirov I.H., Nagy V., Svoronos A., Huntley G.W., Benson D.L. Cadherin-8 and N-cadherin differentially regulate pre- and postsynaptic development of the hippocampal mossy fiber pathway. Hippocampus. 2008. 18: 349–63.

  9. Bengzon J., Kokaia Z., Elmer E., Nanobashvili A., Kokaia M., Lindvall O. Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc. Natl. Acad. Sci. U S A 1997. 94: 10432–10437.

  10. Bielefeld P., van Vliet E.A., Gorter J.A., Lucassen P.J., Fitzsimons C.P. Different subsets of newborn granule cells: a possible role in epileptogenesis? Eur. J. Neurosci. 2014. 39(1): 1–11.

  11. Binder D.K., Croll S.D., Gall C.M., Scharfman H.E. BDNF and epilepsy: too much of a good thing? Trends Neurosci. 2001. 24: 47–53.

  12. Bittencourt S., Covolan L. C.H., Hamani C., Longo B., Faria F., Freymuller E., Freymuller E., Ottersen O.P., Mello L.E. Replacement of asymmetric synaptic profiles in the molecular layer of dentate gyrus following cycloheximide in the pilocarpine model in rats. Front Psychiatry. 2015. 6: 157.

  13. Blümcke I., Zuschratter W., Schewe J.C., Suter B., Lie A.A., Riederer B.M., Meyer B., Schramm J., Elger C.E., Wiestler O.D. Cellular pathology of hilar neurons in Ammon’s horn sclerosis. The Journal of Comparative Neurology. 1999. 414: 437–453.

  14. Bragin A., Benassi S.K., Kheiri F., Engel J. Jr. Further evidence that pathological high frequency oscillations are bursts of population spikes derived from recordings of identified cells in dentate gyrus. Epilepsia. 2011. 52(1): 45–52.

  15. Bragin A., Engel J.Jr., Wilson C.L., Fried I., Buzsaki G. High-frequency oscillations in human brain. Hippocampus. 1999a. 9: 137–142.

  16. Bragin A., Engel Jr.J., Wilson C.L., Fried I., Mathern G.W. Hippocampal and entorhinal cortex high-frequency oscillations (100–500 Hz) in human epileptic brain and in kainic acid-treated rats with chronic seizures. Epilepsia. 1999b. 40: 127–137.

  17. Bragin A., Jandó G., Nádasdy Z., van Landeghem M., Buzsáki G. Dentate EEG spikes and associated interneuronal population bursts in the hippocampal hilar region of the rat. J. Neurophysiol. 1995. 73: 1691–1705.

  18. Buckmaster P.S. Mossy cell dendritic structure quantified and compared with other hippocampal neurons labeled in rats in vivo: Epilepsia. 2012. 53 (Suppl 1): 9–17.

  19. Buckmaster P. Does mossy fiber sprouting give rise to the epileptic state? Issues in Clinical Epileptology: A View From the Bench. Advances in Experimental Medicine and Biology. Ed. Scharfman H., Buckmaster P. Dordrecht: Springer, 2014. 161–168 pp.

  20. Buckmaster P.S., Abrams E., Wen X. Seizure frequency correlates with loss of dentate gyrus GABAergic neurons in a mouse model of temporal lobe epilepsy. J Comp Neurol. 2017. 525 (11): 2592–2610.

  21. Buckmaster P.S., Dudek F.E. Network properties of the dentate gyrus in epileptic rats with hilar neuron loss and granule cell axon reorganization. J. Neurophysiol. 1997. 77: 2685–2696.

  22. Buckmaster P.S., Lew F.H. Rapamycin suppresses mossy fiber sprouting but not seizure frequency in a mouse model of temporal lobe epilepsy. J. Neurosci. 2011. 31: 2337–2347.

  23. Buckmaster P.S., Jongen-Rêlo A.L. Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainate-induced epileptic rats. J. Neurosci. 1999. 19(21): 9519–9529.

  24. Buckmaster P.S., Strowbridge B.W., Kunkel D.D., Schmiege D.L., Schwartzkroin P.A. Mossy cell axonal projections to the dentate gyrus molecular layer in the rat hippocampal slice. Hippocampus. 1992. 2: 349–362.

  25. Buckmaster P.S., Schwartzkroin P.A. Hippocampal mossy cell function: a speculative view. Hippocampus. 1994. 4: 393–402.

  26. Burgess N., Maguire E., O’Keefe J. The human hippocampus and spatial and episodic memory. Neuron 2002. 35: 625–641.

  27. Cameron H.A., Woolley C.S., McEwen B.S., Gould E. Differentiationof newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience. 1993. 56: 337–344.

  28. Cameron M.C., Zhan R., Nadler J.V. Morphologic integration of hilar ectopic granule cells into dentate gyrus circuitry in the pilocarpine model of temporal lobe epilepsy. The Journal of Comparative Neurology. 2011. 519: 2175–2192.

  29. Cavarsan C.F., Malheiros J., Hamani C., Najm I., Covolan L. Is Mossy Fiber Sprouting a Potential Therapeutic Target for Epilepsy? Front. Neurol. 2018. 9: 1023.

  30. Cavazos J.E., Golarai G., Sutula T.P. Mossy fiber synaptic reorganization induced by kindling: time course of development, progression, and permanence. J Neurosci. 1991. 11(9): 2795–2803.

  31. Cho K.-O., Lybrand Z.R., Ito N., Kelly R., Tafacory F., Zhang L., Good L., Ure K., Kernie S.G., Birnbaum S.G., Scharfman H.E., Eisch A.J., Hsieh J. Aberrant hippocampal neurogenesis contributes to epilepsy and associated cognitive decline. Nat. Commun. 2015. 6: 6606.

  32. Colling S., Khana M., Collinge J., Jefferys J. Mossy fibre reorganization in the hippocampus of prion protein null mice. Brain Res. 1997. 755: 28–35.

  33. Cossart R., Dinocourt C., Hirsch J.C., Merchan-Perez A., De F.J., Ben-Ari Y., Esclapez M., Bernard C. Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat Neurosci. 2001. 4: 52–62.

  34. Coulter D.A., Carlson G.C. Functional regulation of the dentate gyrus by GABA-mediated inhibition. Prog Brain Res. 2007. 163: 235–243.

  35. Covolan L., Ribeiro L.T., Longo B.M., Mello L.E. Cell damage and neurogenesis in the dentate granule cell layer of adult rats after pilocarpine- or kainate-induced status epilepticus. Hippocampus. 2000. 10(2): 169–180.

  36. Cronin J., Obenaus A., Houser C.R., Dudek F.E. Electrophysiology of dentate granule cells after kainate-induced synaptic reorganization of the mossy fibers. Brain Res. 1992. 573(2): 305–310.

  37. Das A., Wallace G.C., Holmes C., McDowell M.L., Smith J.A., Marshall J.D., Bonilha L., Edwards J.C., Glazier S.S., Ray S.K., Banik N.L. Hippocampal tissue of patients with refractory temporal lobe epilepsy is associated with astrocyte activation, inflammation, and altered expression of channels and receptors. Neuroscience. 2012. 220: 237–246.

  38. Dashtipour K., Tran P.H., Okazaki M.M., Nadler J.V., Ribak C.E. Ultrastructural features and synaptic connections of hilar ectopic granule cells in the rat dentate gyrus are different from those of granule cells in the granule cell layer. Brain Res. 2001. 890: 261–271.

  39. de Lanerolle N.C., Brines M.L., Kim J.H., Williamson A., Philips M.F., Spencer D.D. Neurochemical remodeling of the hippocampus in human temporal lobe epilepsy. Ed. Engel J.Jr., Wasterlain C., Cavalheiro E.A., Heinemann U., Avanzini G. Epilepsy Res. (Suppl. 9). Amsterdam: Elsevier Science, 1992. 205–220 pp.

  40. Dengler C.G., Coulter D.A. Normal and epilepsy-associated pathologic function of the dentate gyrus. Prog Brain Res. 2016. 226: 155–78.

  41. Dudek F. Seizure-induced neurogenesis and epilepsy: involvement of ectopic granule cells? Epilepsy Curr. 2004. 4: 103–104.

  42. El Bahh B., Lespinet V., Lurton D., Coussemacq M., Le Gal La Salle G., RougierA. Correlations between granule cell dispersion, mossy fiber sprouting, and hippocampal cell loss in temporal lobe epilepsy. Epilepsia. 1999. 40: 1393–1401.

  43. Elmer E., Kokaia Z., Kokaia M., Lindvall O., McIntyre D. Mossy fibre sprouting: evidence against a facilitatory role in epileptogenesis. Neuroreport. 1997. 8: 1193–1196.

  44. Engel Jr.J. A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia. 2001. 42: 796–803.

  45. Gabriel S., Njunting M., Pomper J.K., Merschhemke M., Sanabria E.R.G., Eilers A., Kivi A., Zeller M., Meencke H.-J., Cavalheiro E.A., Heinemann U., Lehmann T.-N. Stimulus and potassium-induced epileptiform activity in the human dentate gyrus from patients with and without hippocampal sclerosis. J. Neurosci. 2004. 24: 10416–10430.

  46. Gilbert P.E., Kesner R.P., Lee I. Dissociating hippocampal subregions: double dissociation between dentate gyrus and CA1. Hippocampus. 2001. 11: 626–636.

  47. Gorter J., van Vliet E., Aronica E., Lopes da Silva F. Progression of spontaneous seizures after status epilepticus is associated with mossy fibre sprouting and extensive bilateral loss of hilar parvalbumin and somatostatinimmunoreactive neurons. Eur. J. Neurosci. Biobehav. Rev. 2001. 13: 657–669.

  48. Haglid K.G., Wang S., Qiner Y., Hamberger A. Excitotoxicity. Experimental correlates to human epilepsy. Mol. Neurobiol. 1994. 9: 259–263.

  49. Harvey B.D., Sloviter R.S. Hippocampal granule cell activity and c-Fos expression during spontaneous seizures in awake, chronically epileptic, pilocarpine-treated rats: implications for hippocampal epileptogenesis. J Comp Neurol. 2005. 488: 442–463.

  50. Heinemann U., Beck H., Dreier J.P., Ficker E., Stabel J., Zhang C.L. The dentate gyrus as a regulatedgate for the propagation of epileptiform activity. Epilepsy Res. 1992. Suppl 7: 273–280.

  51. Hendricks L., Chen Y., Bensen A., Westbrook G., Schnell E. Short-term depression of sprouted mossy fiber synapses from adult-born granule cells. J Neurosci. 2017. 37: 5722–5735.

  52. Heng K., Haney M., Buckmaster P. High-dose rapamycin blocks mossy fiber sprouting but not seizures in a mouse model of temporal lobe epilepsy. Epilepsia. 2013. 54: 1535–1541.

  53. Hester M.S., Danzer S.C. Accumulation of abnormal adult-generated hippocampal granule cells predicts seizure frequency and severity. J Neurosci. 2013. 33: 8926–8936.

  54. Houser C.R. Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Research. 1990. 535: 195–204.

  55. Houser C.R. Morphological changes in the dentate gyrus in human temporal lobe epilepsy. Epilepsy Res. 1992. Suppl 7: 223–234.

  56. Holtmaat A., Gorter J., De Wit J., Tolner E., Spijker S., Giger R., Lopes da Silva F.H., Verhaagen J. Transient downregulation of Sema3A mRNA in a rat model for temporal lobe epilepsy. A novel molecular event potentially contributing to mossy fiber sprouting. Exp Neurol. 2003. 182: 142–150.

  57. Hosford B.E., Liska J.P., Danzer S.C. Ablation of newly generated hippocampal granule cells has disease-modifying effects in epilepsy. J. Neurosci. 2016. 36 (43): 11013–11023.

  58. Hsu D. The dentate gyrus as a filter or gate: a look back and a look ahead. Prog Brain Res. 2007. 163: 601–613.

  59. Ikegaya Y. Abnormal targeting of developing hippocampal mossy fibers after epileptiform activities via L-type Ca2+ channel activation in vitro. J. Neurosci. 1999. 19: 802–812.

  60. Inostroza M., Brotons-Mas J.R., Laurent F., Cid E., de la Prida L.M. Specific impairment of ‘‘what-where-when’’ episodic-like memory in experimental models of temporal lobe epilepsy. J. Neurosci. 2013. 33: 17749–17762.

  61. Isokawa M., Levesque M.F., Babb T.L., Engel J.Jr. Single mossy fiber axonal systems of human dentate granule cells studied in hippocampal slices from patients with temporal lobe epilepsy. J. Neurosci. 1993. 13(4): 1511–1522.

  62. Jacobs J., LeVan P., Chander R., Hall J., Dubeau F., Gotman J. Interictal highfrequency oscillations (80–500Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain. Epilepsia. 2008. 49: 1893–1907.

  63. Jacobs J., Banks S., Zelmann R., Zijlmans M., Jones-Gotman M., Gotman J. Spontaneous ripples in the hippocampus correlate with epileptogenicity and not memory function in patients with refractory epilepsy. Epilepsy Behav. 2016. 62: 258–266.

  64. Jakubs K., Nanobashvili A., Bonde S., Ekdahl C.T., Kokaia Z., Kokaia M., Lindvall O. Environment matters: synaptic properties of neurons born in the epileptic adult brain develop to reduce excitability. Neuron. 2006. 52: 1047–1059.

  65. Jessberger S., Parent J.M. Epilepsy and adult neurogenesis. Cold Spring Harb Perspect. Biol. 2015. 7: a020677.

  66. Jessberger S., Römer B., Babu H., Kempermann G. Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells. Exp Neurol 2005. 196: 342–351.

  67. Johnson A.M., Sugo E., Barreto D., Hiew C., Lawson J.A., Connolly A.M., Somerville E., Hasic E., Bye A.M., Cunningham A.M. The severity of gliosis in hippocampal sclerosis correlates with pre-operative seizure burden and outcome after temporal lobectomy. Molecular Neurobiology. 2016. 53: 5446–5456.

  68. Jung K.H., Chu K., Kim M., Jeong S.-W., Song Y.-M., Lee S.-T., Kim J.-Y., Lee S.K., Roh J.-K. Continuous cytosine-b-Darabinofuranoside infusion reduces ectopic granule cells in adult rat hippocampus with attenuation of spontaneous recurrent seizures following pilocarpine-induced status epilepticus. Eur J Neurosci. 2004. 19: 3219–3226.

  69. Jung K.H., Chu K., Lee S.T., Kim J., Sinn D.I., Kim J.M., Park D.K., Lee J.J., Kim S.U., Kim M., Lee S.K., Roh J.K. Cyclooxygenase-2 inhibitor, celecoxib, inhibits the altered hippocampal neurogenesis with attenuation of spontaneous recurrent seizures following pilocarpine-induced status epilepticus. Neurobiol. Dis. 2006. 23: 237–246.

  70. Frauscher B., von Ellenrieder N., Ferrari-Marinho T., Avoli M., Dubeau F., Gotman J. Facilitation of epileptic activity during sleep is mediated by high amplitude slow waves. Brain J. Neurol. 2015. 138: 1629–1641.

  71. Freund T.F., Buzsaki G. Interneurons of the hippocampus. Hippocampus. 1996. 4: 347–470.

  72. Kahn J.B., Port R.G., Yue C., Takano H., Coulter D.A. Circuit-based interventions in the dentate gyrus rescue epilepsy-associated cognitive dysfunction. Brain. 2019. 142 (9): 2705–2721.

  73. Kelly T., Beck H. Functional properties of granule cells with hilar basal dendrites in the epileptic dentate gyrus. Epilepsia. 2017. 58: 160–171.

  74. Kheirbek M.A., Drew L.J., Burghardt N.S., Costantini D.O., Tannenholz L., Ahmari S.E., Fenton A.A., Hen R. Differential control of learning and anxiety along the dorsoventral axis of the dentate gyrus. Neuron. 2013. 77: 955–968.

  75. Kienzler F., Norwood B.A., Sloviter R.S. Hippocampal injury, atrophy, synaptic reorganization, and epileptogenesis after perforant pathway stimulation-induced status epilepticus in the mouse. J Comp Neurol. 2009. 515(2): 181–196.

  76. Koyama R., Yamada M.K., Fujisawa S., Katoh-Semba R., Matsuki N., Ikegaya Y. Brain-derived neurotrophic factor induces hyperexcitable reentrant circuits in the dentate gyrus. J Neurosci. 2004. 24: 7215–7224.

  77. Kron M.M., Zhang H., Parent J.M. The developmental stage of dentate granule cells dictates their contribution to seizure-induced plasticity. J. Neurosci. 2010. 30: 2051–2059.

  78. Krook-Magnuson E., Armstrong C., Bui A., Lew S., Oijala M., Soltesz I. In vivo evaluation of the dentate gate theory in epilepsy. J Physiol. 2015. 593(10): 2379–2388.

  79. Liu R., Lemieux L., Bell G., Sisodiya S., Bartlett P., Shorvon S., Sander J.W.A.S., Duncan J.S. Cerebral damage in epilepsy: a population-based longitudinal quantitative MRI study. Epilepsia. 2005. 46: 1482–1494.

  80. Longo B., Covolan L., Chadi G., Mello L. Sprouting of mossy fibers and the vacating of postsynaptic targets in the inner molecular layer of the dentate gyrus. Exp Neurol. 2003. 181: 57–67.

  81. Loscher W., Schmidt D. New horizons in the development of antiepileptic drugs: the search for new targets. Epilepsy Res. 2004. 60: 77–159.

  82. Lothman E., Bertram E. Epileptogenic effects of status epilepticus. Epilepsia. 1993. 34: 59–70.

  83. Lowenstein D.H. Structural reorganization of hippocampal networks caused by seizure activity. International Review of Neurobiology. 2001. 45: 209–236.

  84. Malheiros J., Paiva F., Longo B., Hamani C., Covolan L. Manganese-enhanced MRI: biological applications in neuroscience. Front Neurol. 2015. 6: 161.

  85. Mathern G.W., Babb T.L., Armstrong D.L. Hippocampal sclerosis. Epilepsy: a comprehensive textbook. Ed. Engel J.Jr., Pedley T.A. Philadelphia: Lippincott-Raven Publishers, 1997. 133–155 pp.

  86. Mathern G., Cifuentes F., Leite J., Pretorius J., Babb T. Hippocampal EEG excitability and chronic spontaneous seizures are associated with aberrant synaptic reorganization in the rat intrahippocampal kainate model. Electroencephalogr Clin Neurophysiol. 1993. 87: 326–339.

  87. Mathern G.W., Pretorius J.K., Leite J.P., Kornblum H.I., Mendoz D., Lozada A., Bertram E.H. Hippocampal AMPA and NMDA mRNA Levels and Subunit Immunoreactivity in Human Temporal Lobe Epilepsy Patients and a Rodent Model of Chronic Mesial Limbic Epilepsy. Epilepsy Res. 1998. 32: 154–171.

  88. McNamara J. Cellular and molecular basis of epilepsy. J Neurosci. 1994. 14: 3413–3425.

  89. Mello L., Covolan L. Neuronal injury and progressive cell damage. Encyclopedia of Basic Epilepsy Research. Ed. Schwartzkroin P.A. London: Academic Press, 2009. 125–128 pp.

  90. Mello L., Cavalheiro E., Tan A., Pretorius J., Babb T., Finch D. Granule cell dispersion in relation to mossy fiber sprouting, hippocampal cell loss, silent period and seizure frequency in the pilocarpine model of epilepsy. Epilepsy Res. 1992. 9: 51–59.

  91. Mitsueda-Ono T., Ikeda A., Sawamoto N., Aso T., Hanakawa T., Kinoshita M., Matsumoto R., Mikuni N., Amano S., Fukuyama H., Takahashi R. Internal structural changes in the hippocampus observed on 3-tesla MRI in patients with mesial temporal lobe epilepsy. Intern Med. 2013. 52: 877–885.

  92. Morimoto K., Fahnestock M., Racine R.J. Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog. Neurobiol. 2004. 73: 1–60.

  93. Myers C.E., Bermudez-Hernandez K., Scharfman H.E. The influence of ectopic migration of granule cells into the hilus on dentate gyrus-CA3 function. PLoS ONE. 2013. 8: e68208.

  94. Nadler J.V., Perry B.W., Cotman C.W. Selective reinnervation of hippocampal area CA1 and the fascia dentata after destruction of CA3-CA4 afferents with kainic acid. Brain Res. 1980. 182: 1–9.

  95. Nadler J.V. The recurrent mossy fiber pathway of the epileptic brain. Neurochem Res. 2003. 28: 1649–1658.

  96. Nairismägi J., Pitkänen A., Narkilahti S., Huttunen J., Kauppinen R., Gröhn O. Manganese-enhanced magnetic resonance imaging of mossy fiber plasticity in vivo. Neuroimage. 2006. 30: 130–5.

  97. Nakashiba T., Cushman J.D., Pelkey K.A., Renaudineau S., Buhl D.L., McHugh T.J., Rodriguez Barrera V., Chittajallu R., Iwamoto K.S., McBain C.J., Fanselow M.S., Tonegawa S. Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell. 2012.149: 188–201.

  98. Nissinen J., Lukasiuk K., Pitkänen A. Is mossy fiber sprouting present at the time of the first spontaneous seizures in rat experimental temporal lobe epilepsy? Hippocampus. 2001. 11: 299–310.

  99. Obenaus A., Esclapez M., Houser C.R. Loss of glutamate decarboxylase mRNA-containing neurons in the rat dentate gyrus following pilocarpine-induced seizures. J. Neurosci. 1993. 13(10): 4470–4485.

  100. Olney J.W. Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate. Science. 1969. 164: 719–721.

  101. Parent J.M., Elliott R.C., Pleasure S.J., Barbaro N.M., Lowenstein D.H. Aberrant seizure-induced neurogenesis in experimental temporal lobe epilepsy. Annals of Neurology. 2006. 59: 81–91.

  102. Parent J.M., Tada E., Fike J.R., Lowenstein DH. Inhibition of dentate granule cell neurogenesis with brain irradiation does not prevent seizure-induced mossy fiber synaptic reorganization in the rat. J. Neurosci. 1999. 19: 4508–4519.

  103. Parent J., Yu T., Leibowitz R., Geschwind D., Sloviter R., Lowenstein D. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci. 1997. 17: 3727–3738.

  104. Pekcec A., Lupke M., Baumann R., Seifert H., Potschka H. Modulation of neurogenesis by targeted hippocampal irradiation fails to affect kindling progression. Hippocampus. 2011. 21: 866–876.

  105. Pierce J., Melton J., Punsoni M., McCloskey D., Scharfman H. Mossy fibers are the primary source of afferent input to ectopic granule cells that are born after pilocarpine-induced seizures. Exp Neurol. 2005. 196: 316–331.

  106. Pierce J., Punsoni M., McCloskey D., Scharfman H. Mossy cell axon synaptic contacts on ectopic granule cells that are born following pilocarpine-induced seizures. Neurosci Lett. 2007. 422: 136–140.

  107. Polli R., Malheiros J., Dos Santos R., Hamani C., Longo B., Tannús A., Mello L.E., Covolan L. Changes in hippocampal volume are correlated with cell loss but not with seizure frequency in two chronic models of temporal lobe epilepsy. Front Neurol. 2014. 5: 111.

  108. Pun R.Y., Rolle I.J., Lasarge C.L., Hosford B.E., Rosen J.M., Uhl J.D., Schmeltzer S.N., Faulkner C., Bronson S.L., Murphy B.L., Richards D.A., Holland K.D., Danzer S.C. Excessive activation of mTOR in postnatally generated granule cells is sufficient to cause epilepsy. Neuron. 2012. 75: 1022–1034.

  109. Raedt R., Boon P., Persson A., Alborn A.-M., Boterberg T., Van Dycke A., Linder B., Smedt T.D., Wadman W.J., Ben-Menachem E., Eriksson P.S. Radiation of the rat brain suppresses seizure-induced neurogenesis and transiently enhances excitability during kindling acquisition. Epilepsia. 2007. 48: 1952–1963.

  110. Ratzliff A.H., Howard A.L., Santhakumar V., Osapay I., Soltesz I. Rapid Deletion of Mossy Cells Does Not Result in a Hyperexcitable Dentate Gyrus: Implications for Epileptogenesis. J. Neurosci. 2004. 24(9): 2259–2269.

  111. Ratzliff A.H., Santhakumar V., Howard A., Soltesz I. Mossy cells in epilepsy: Rigor mortis or vigor mortis? Trends. Neurosci. 2002. 25: 140–144.

  112. Ren E., Curia G. Synaptic Reshaping and Neuronal Outcomes in the Temporal Lobe Epilepsy. Int J. Mol. Sci. 2021. 22(8): 3860.

  113. Represa A., Jorquera I., Le Gal La Salle G., Ben-Ari Y. Epilepsy induced collateral sprouting of hippocampal mossy fibers: does it induce the development of ectopic synapses with granule cell dendrites? Hippocampus. 1993. 3(3): 257–268.

  114. Reyes-Garcia S.Z., Scorza C.A, Araújo N.S., Ortiz-Villatoro N.N., Jardim A., Centeno R., Targas Y.E.M., Faber J., Cavalheiro E.A. Different patterns of epileptiform-like activity are generated in the sclerotic hippocampus from patients with drug-resistant temporal lobe epilepsy. Sci Rep. 2018. 8: 7116.

  115. Ribak C.E., Shapiro L.A., Yan X.-X., Dashtipour K., Nadler J.V., Obenaus A., Spigelman I., Buckmaster P.S. Seizure-induced formation of basal dendrites on granule cells of the rodent dentate gyrus. Jasper’s Basic Mechanisms of the Epilepsies. Eds.: Noebels J.L., Avoli M., Rogawski M.A., Olsen R.W., Delgado-Escueta A.V. Bethesda (MD): National Center for Biotechnology Information (US), 2012.

  116. Roth B.L. DREADDs for neuroscientists. Neuron. 2016. 89(4): 683–694.

  117. Viscomi M.T., Oddi S., Latini L. et al. The endocannabinoid system: A new entry in remote cell death mechanisms. Exp. Neurol. 2010. 224: 56–65.

  118. Sanchez R., Ribak C., Shapiro L. Synaptic connections of hilar basal dendrites of dentate granule cells in a neonatal hypoxia model of epilepsy. Epilepsia. 2012. 53: 98–108.

  119. Santhakumar V., Bender R., Frotscher M., Ross S.T., Hollrigel G.S., Toth Z., Soltesz I. Granule cell hyperexcitability in the early post-traumatic rat dentate gyrus: the ‘irritable mossy cell’ hypothesis. J. Physiol. 2000. 524(1): 117–134.

  120. Scharfman H.E. The role of nonprincipal cells in dentate gyrus excitability and its relevance to animal models of epilepsy and temporal lobe epilepsy. Adv. Neurol. 1999. 79: 805–820.

  121. Scharfman H.E. Epilepsy as an example of neural plasticity. Neuroscientist. 2002. 8: 154–173.

  122. Scharfman H.E. Synaptic Plasticity and Transsynaptic Signalling. Stanton P.K., Bramham C.R., Scharfman H.E., editors. Springer. 2005. pp. 201–220.

  123. Scharfman H., Goodman J., McCloskey D. Ectopic granule cells of the rat dentate gyrus. Dev Neurosci. 2007. 29: 14–27.

  124. Scharfman H.E., Goodman J.H., Sollas A.L. Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. J. Neurosci. 2000. 20: 6144–6158.

  125. Scharfman H.E., Myers C.E. Hilar mossy cells of the dentate gyrus: a historical perspective. Front Neural Circuits. 2012. 6: 106.

  126. Scharfman H.E., Pierce J.P. New insights into the role of hilar ectopic granule cells in the dentate gyrus based on quantitative anatomic analysis and three-dimensional reconstruction. Epilepsia. 2012. 53(Suppl 1): 98–108.

  127. Schmeiser B., Li J., Brandt A., Zentner J., Doostkam S., Freiman T. Different mossy fiber sprouting patterns in ILAE hippocampal sclerosis types. Epilepsy Res. 2017. 136: 115–122.

  128. Shibata K., Nakahara S., Shimizu E., Yamashita T., Matsuki N., Koyama R. Repulsive guidance molecule a regulates hippocampal mossy fiber branching in vitro. Neuroreport. 2013. 24: 609–615.

  129. Scott B., Wojtowicz J., Burnham W. Neurogenesis in the dentate gyrus of the rat following electroconvulsive shock seizures. Exp Neurol. 2000. 165: 231–236.

  130. Shapiro L.A., Figueroa-Aragon S., Ribak C.E. Newly generated granule cells show rapid neuroplastic changes in the adult rat dentate gyrus during the first five days following pilocarpine-induced seizures. Eur J Neurosci. 2007. 26(3): 583–592.

  131. Sloviter R. Decreased hippocampal inhibition and selective loss of interneurons in experimental epilepsy. Science. 1987. 235: 73–76.

  132. Sloviter R.S. Feedforward and feedback inhibition of hippocampal principal cell activity evoked by perforant path stimulation: GABA-mediated mechanisms that regulate excitability in vivo. Hippocampus. 1991a. 1: 31–40.

  133. Sloviter R.S. Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the “dormant basket cell” hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus. 1991b. 1: 41–66.

  134. Sloviter R.S. The functional organization of the hippocampal dentate gyrus and its relevance to the pathogenesis of temporal lobe epilepsy. Ann Neurol. 1994. 35: 640–654.

  135. Sloviter R.S. Status epilepticus-induced neuronal injury and network reorganization. Epilepsia. 1999. 40. Suppl 1: S34-9, discussion S40-1.

  136. Sloviter R., Bumanglag A., Schwarcz R., Frotscher M. Abnormal dentate gyrus network circuitry in temporal lobe epilepsy. Jasper’s Basic Mechanisms of the Epilepsies. Eds.: Noebels J.L., Avoli M., Rogawski M.A., Olsen R.W., Delgado-Escueta A.V. Bethesda (MD): National Center for Biotechnology Information (US), 2012.

  137. Song M.Y., Tian F.F., Wang Y.Z., Huang X., Guo J.L., Ding D.X. Potential roles of the RGMa-FAK-Ras pathway in hippocampal mossy fiber sprouting in the pentylenetetrazole kindling model. Mol Med Rep. 2015. 11: 1738–1744.

  138. Song I., Orosz I., Chervoneva I., Waldman Z.J., Fried I., Wu C., Sharan A., Salamon N., Gorniak R., Dewar S., Bragin A., Engel J., Sperling M.R., Staba R., Weiss S.A. Bimodal coupling of ripples and slower oscillations during sleep in patients with focal epilepsy. Epilepsia. 2017. 58: 1972–1984.

  139. Staba R.J., Wilson C.L., Bragin A., Fried I., Engel Jr.J. Quantitative analysis of high-frequency oscillations (80–500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. J Neurophysiol. 2002. 88: 1743–1752.

  140. Spigelman I., Yan X., Obenaus A., Lee E., Wasterlain C., Ribak C. Dentate granule cells form novel basal dendrites in a rat model of temporal lobe epilepsy. Neuroscience. 1998. 86: 109–120.

  141. Sun C., Mtchedlishvili Z., Bertram E.H., Erisir A., Kapur J. Selective loss of dentate hilar interneurons contributes to reduced synaptic inhibition of granule cells in an electrical stimulation-based animal model of temporal lobe epilepsy. J. Comp Neurol. 2007. 500: 876–893.

  142. Sutula T.P., Dudek F.E. Unmasking recurrent excitation generated by mossy fiber sprouting in the epileptic dentate gyrus: an emergent property of a complex system. Prog. Brain Res. 2007. 163: 541–563.

  143. Sutula T., Cascino G., Cavazos J., Parada I., Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Annals of Neurology. 1989. 26: 321–330.

  144. Tamagnone L., Comoglio P. Signalling by semaphorin receptors: cell guidance and beyond. Trends Cell Biol. 2000. 10: 377–383.

  145. Tauck D, Nadler J. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci. (1985) 5: 1016– 22.

  146. Thind K.K., Ribak C.E, Buckmaster P.S. Synaptic input to dentate granule cell basal dendrites in a rat model of temporal lobe epilepsy. J. Comp. Neurol. 2008. 509: 190–202.

  147. Tong X., Tong X., Peng Z., Zhang N., CetinaY., Huang C.S., Wallner M., Otis, T. S., Houser C.R. Ectopic expression of α6 and δ GABAA receptor subunits in hilar somatostatin neurons increases tonic inhibition and alters network activity in the dentate gyrus. J. Neurosci. 2015. 35: 16142–16158.

  148. Tulving E. Episodic memory: from mind to brain. Annu. Rev. Psychol. 2002. 53: 1–25.

  149. Van Paesschen W., Revesz T., Duncan J.S., King M.D., Connelly A. Quantitative neuropathology and quantitative magnetic resonance imaging of the hippocampus in temporal lobe epilepsy. Annals of Neurology. 1997. 42: 756–766.

  150. von Ellenrieder N., Frauscher B., Dubeau F., Gotman J. Interaction with slow waves during sleep improves discrimination of physiologic and pathologic high-frequency oscillations (80–500Hz). Epilepsia. 2016. 57: 869–878.

  151. Walter C., Murphy B.L., Pun R.Y., Spieles-Engemann A.L., Danzer S.C. Pilocarpine-induced seizures cause selective time-dependent changes to adult-generated hippocampal dentate granule cells. J. Neurosci. 2007. 27: 7541–7552.

  152. Weiss S.A., Song I., Leng M., Pastore T., Slezak D., Waldman Z., Orosz I., Gorniak R., Donmez M., Sharan A., Wu C., Fried I., Sperling M.R., Bragin A., Engel, Jr. J., Nir Y., Staba R. Ripples Have Distinct Spectral Properties and Phase-Amplitude Coupling With Slow Waves, but Indistinct Unit Firing, in Human Epileptogenic Hippocampus. Front Neurol. 2020. 11: 174.

  153. Wittner L., Maglóczky Z., Borhegyi Z., Halász P., Tóth S., Eross L., Szabó Z., Freund T.F. Preservation of perisomatic inhibitory input of granule cells in the epileptic human dentate gyrus. Neuroscience. 2001. 108: 587–600.

  154. Wuarin J.P., Dudek F.E. Excitatory synaptic input to granule cells increases with time after kainate treatment. J. Neurophysiol. 2001. 85(3): 1067–1077.

  155. Ueda Y., Doi T., Tsuru N., Tokumaru J., Mitsuyama Y. Expression of glutamate transporters and ionotropic glutamate receptors in GLAST knockout mice. Brain Res. Mol. Brain Res. 2002. 104(2): 120–126.

  156. Zhan R.Z., Timofeeva O., Nadler J.V. High ratio of synaptic excitation to synaptic inhibition in hilar ectopic granule cells of pilocarpine-treated rats. J. Neurophysiol. 2010. 104: 3293–3304.

  157. Zhang Y., Xiong T., Tan B., Song Y., Li S., Yang L., Li Y.-C. Pilocarpineinduced epilepsy is associated with actin cytoskeleton reorganization in the mossy fiber-CA3 synapses. Epilepsy Res. 2014. 108: 379–389.

  158. Zeng L.H., Rensing N.R., Wong M. The mammalian target of rapamycin signaling pathway mediates epileptogenesis in a model of temporal lobe epilepsy. J. Neurosci. 2009. 29: 6964–6972.

  159. Zimmer J. Changes in the Timm sulfide silver staining patter of the rat hippocampus and fascia dentata following early postnatal deaferentiation. Brain Res. 1973. 64: 313–326.

  160. Zimmer J. Long-term synaptic reorganization in rat fascia dentate deafferented at adolescent and adult stages: observations with the Timm method. Brain Res. 1974. 76: 336–342.

  161. Yamawaki R., Thind K., Buckmaster P.S. Blockade of excitatory synaptogenesis with proximal dendrites of dentate granule cells following rapamycin treatment in a mouse model of temporal lobe epilepsy. J. Comp Neurol. 2015. 523: 281–297.

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