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Transient Morphological Alterations in the Hippocampus After Pentylenetetrazole-Induced Seizures in Rats

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Abstract

The relationships between seizures, neuronal death, and epilepsy remain one of the most disputed questions in translational neuroscience. Although it is broadly accepted that prolonged and repeated seizures cause neuronal death and epileptogenesis, whether brief seizures can produce a mild but similar effect is controversial. In the present work, using a rat pentylenetetrazole (PTZ) model of seizures, we evaluated how a single episode of clonic–tonic seizures affected the viability of neurons in the hippocampus, the area of the brain most vulnerable to seizures, and morphological changes in the hippocampus up to 1 week after PTZ treatment (recovery period). The main findings of the study were: (1) PTZ-induced seizures caused the transient appearance of massively shrunken, hyperbasophilic, and hyperelectrondense (dark) cells but did not lead to detectable neuronal cell loss. These dark neurons were alive, suggesting that they could cope with seizure-related dysfunction. (2) Neuronal and biochemical alterations following seizures were observed for at least 1 week. The temporal dynamics of the appearance and disappearance of dark neurons differed in different zones of the hippocampus. (3) The numbers of cells with structural and functional abnormalities in the hippocampus after PTZ-induced seizures decreased in the following order: CA1 > CA3b,c > hilus > dentate gyrus. Neurons in the CA3a subarea were most resistant to PTZ-induced seizures. These results suggest that even a single seizure episode is a potent stressor of hippocampal neurons and that it can trigger complex neuroplastic changes in the hippocampus.

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References

  1. 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. https://doi.org/10.1007/978-94-017-8914-1_9

    Article  PubMed  PubMed Central  Google Scholar 

  2. Henshall DC, Meldrum BS (2012) Cell death and survival mechanisms after single and repeated brief seizures. In: Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV (eds) Jasper’s basic mechanisms of the epilepsies, 4th edn. Oxford, Bethesda (MD)

    Google Scholar 

  3. Pitkanen A, Lukasiuk K (2009) Molecular and cellular basis of epileptogenesis in symptomatic epilepsy. Epilepsy Behav 14 (Suppl 1):16–25. https://doi.org/10.1016/j.yebeh.2008.09.023

    Article  PubMed  Google Scholar 

  4. Dinocourt C, Petanjek Z, Freund TF, Ben-Ari Y, Esclapez M (2003) Loss of interneurons innervating pyramidal cell dendrites and axon initial segments in the CA1 region of the hippocampus following pilocarpine-induced seizures. J Comp Neurol 459(4):407–425. https://doi.org/10.1002/cne.10622

    Article  PubMed  Google Scholar 

  5. Magloczky Z, Freund TF (1993) Selective neuronal death in the contralateral hippocampus following unilateral kainate injections into the CA3 subfield. Neuroscience 56(2):317–335

    Article  PubMed  CAS  Google Scholar 

  6. Aniol VA, Stepanichev MY, Lazareva NA, Gulyaeva NV (2011) An early decrease in cell proliferation after pentylenetetrazole-induced seizures. Epilepsy Behav 22(3):433–441. https://doi.org/10.1016/j.yebeh.2011.08.002

    Article  PubMed  CAS  Google Scholar 

  7. Gallyas F, Kiglics V, Baracskay P, Juhasz G, Czurko A (2008) The mode of death of epilepsy-induced “dark” neurons is neither necrosis nor apoptosis: an electron-microscopic study. Brain Res 1239:207–215. https://doi.org/10.1016/j.brainres.2008.08.069

    Article  PubMed  CAS  Google Scholar 

  8. Zaitsev AV, Kim KK, Vasilev DS, Lukomskaya NY, Lavrentyeva VV, Tumanova NL, Zhuravin IA, Magazanik LG (2015) N-methyl-D-aspartate receptor channel blockers prevent pentylenetetrazole-induced convulsions and morphological changes in rat brain neurons. J Neurosci Res 93(3):454–465. https://doi.org/10.1002/jnr.23500

    Article  PubMed  CAS  Google Scholar 

  9. Zhvania MG, Ksovreli M, Japaridze NJ, Lordkipanidze TG (2015) Ultrastructural changes to rat hippocampus in pentylenetetrazol- and kainic acid-induced status epilepticus: a study using electron microscopy. Micron 74:22–29. https://doi.org/10.1016/j.micron.2015.03.015

    Article  PubMed  CAS  Google Scholar 

  10. Ooigawa H, Nawashiro H, Fukui S, Otani N, Osumi A, Toyooka T, Shima K (2006) The fate of Nissl-stained dark neurons following traumatic brain injury in rats: difference between neocortex and hippocampus regarding survival rate. Acta Neuropathol 112(4):471–481. https://doi.org/10.1007/s00401-006-0108-2

    Article  PubMed  CAS  Google Scholar 

  11. Kovesdi E, Pal J, Gallyas F (2007) The fate of “dark” neurons produced by transient focal cerebral ischemia in a non-necrotic and non-excitotoxic environment: neurobiological aspects. Brain Res 1147:272–283. https://doi.org/10.1016/j.brainres.2007.02.011

    Article  PubMed  CAS  Google Scholar 

  12. Jortner BS (2006) The return of the dark neuron. A histological artifact complicating contemporary neurotoxicologic evaluation. Neurotoxicology 27(4):628–634. https://doi.org/10.1016/j.neuro.2006.03.002

    Article  PubMed  CAS  Google Scholar 

  13. Csordas A, Mazlo M, Gallyas F (2003) Recovery versus death of “dark” (compacted) neurons in non-impaired parenchymal environment: light and electron microscopic observations. Acta Neuropathol 106(1):37–49. https://doi.org/10.1007/s00401-003-0694-1

    Article  PubMed  CAS  Google Scholar 

  14. Auer RN, Kalimo H, Olsson Y, Siesjo BK (1985) The temporal evolution of hypoglycemic brain damage. I. Light- and electron-microscopic findings in the rat cerebral cortex. Acta Neuropathol 67(1–2):13–24

    Article  PubMed  CAS  Google Scholar 

  15. Dietrich WD, Halley M, Alonso O, Globus MY, Busto R (1992) Intraventricular infusion of N-methyl-D-aspartate. 2. Acute neuronal consequences. Acta Neuropathol 84(6):630–637

    Article  PubMed  CAS  Google Scholar 

  16. Luttjohann A, Fabene PF, van Luijtelaar G (2009) A revised Racine’s scale for PTZ-induced seizures in rats. Physiol Behav 98(5):579–586. https://doi.org/10.1016/j.physbeh.2009.09.005

    Article  PubMed  CAS  Google Scholar 

  17. Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32(3):281–294

    Article  PubMed  CAS  Google Scholar 

  18. Zhuravin I, Tumanova N, Ozirskaya E, Vasil’ev D, Dubrovskaya N (2006) Formation of the structural and ultrastructural organization of the striatum in early postnatal ontogenesis of rats in altered conditions of embryonic development. Neurosci Behav Physiol 36(5):473–478

    Article  PubMed  CAS  Google Scholar 

  19. D’Amelio M, Sheng M, Cecconi F (2012) Caspase-3 in the central nervous system: beyond apoptosis. Trends Neurosci 35(11):700–709. https://doi.org/10.1016/j.tins.2012.06.004

    Article  PubMed  CAS  Google Scholar 

  20. Kim KK, Adelstein RS, Kawamoto S (2009) Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J Biol Chem 284(45):31052–31061. https://doi.org/10.1074/jbc.M109.052969

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116(1):201–211

    PubMed  CAS  Google Scholar 

  22. Kherani ZS, Auer RN (2008) Pharmacologic analysis of the mechanism of dark neuron production in cerebral cortex. Acta Neuropathol 116(4):447–452. https://doi.org/10.1007/s00401-008-0386-y

    Article  PubMed  Google Scholar 

  23. Huang RQ, Bell-Horner CL, Dibas MI, Covey DF, Drewe JA, Dillon GH (2001) Pentylenetetrazole-induced inhibition of recombinant gamma-aminobutyric acid type A (GABA(A)) receptors: mechanism and site of action. J Pharmacol Exp Ther 298(3):986–995

    PubMed  CAS  Google Scholar 

  24. Ramanjaneyulu R, Ticku MK (1984) Interactions of pentamethylenetetrazole and tetrazole analogues with the picrotoxinin site of the benzodiazepine-GABA receptor-ionophore complex. Eur J Pharmacol 98(3–4):337–345

    Article  PubMed  CAS  Google Scholar 

  25. Kanamori K, Ross BD (2011) Chronic electrographic seizure reduces glutamine and elevates glutamate in the extracellular fluid of rat brain. Brain Res 1371:180–191. https://doi.org/10.1016/j.brainres.2010.11.064

    Article  PubMed  CAS  Google Scholar 

  26. Meurs A, Clinckers R, Ebinger G, Michotte Y, Smolders I (2008) Seizure activity and changes in hippocampal extracellular glutamate, GABA, dopamine and serotonin. Epilepsy Res 78(1):50–59. https://doi.org/10.1016/j.eplepsyres.2007.10.007

    Article  PubMed  CAS  Google Scholar 

  27. Millan MH, Obrenovitch TP, Sarna GS, Lok SY, Symon L, Meldrum BS (1991) Changes in rat brain extracellular glutamate concentration during seizures induced by systemic picrotoxin or focal bicuculline injection: an in vivo dialysis study with on-line enzymatic detection. Epilepsy Res 9(2):86–91

    Article  PubMed  CAS  Google Scholar 

  28. Minamoto Y, Itano T, Tokuda M, Matsui H, Janjua NA, Hosokawa K, Okada Y, Murakami TH, Negi T, Hatase O (1992) In vivo microdialysis of amino acid neurotransmitters in the hippocampus in amygdaloid kindled rat. Brain Res 573(2):345–348

    Article  PubMed  CAS  Google Scholar 

  29. Pena F, Tapia R (2000) Seizures and neurodegeneration induced by 4-aminopyridine in rat hippocampus in vivo: role of glutamate- and GABA-mediated neurotransmission and of ion channels. Neuroscience 101(3):547–561

    Article  PubMed  CAS  Google Scholar 

  30. Szyndler J, Maciejak P, Turzynska D, Sobolewska A, Lehner M, Taracha E, Walkowiak J, Skorzewska A, Wislowska-Stanek A, Hamed A, Bidzinski A, Plaznik A (2008) Changes in the concentration of amino acids in the hippocampus of pentylenetetrazole-kindled rats. Neurosci Lett 439(3):245–249. https://doi.org/10.1016/j.neulet.2008.05.002

    Article  PubMed  CAS  Google Scholar 

  31. Doi T, Ueda Y, Nagatomo K, Willmore LJ (2009) Role of glutamate and GABA transporters in development of pentylenetetrazol-kindling. Neurochem Res 34(7):1324–1331. https://doi.org/10.1007/s11064-009-9912-0

    Article  PubMed  CAS  Google Scholar 

  32. Duan S, Anderson CM, Stein BA, Swanson RA (1999) Glutamate induces rapid upregulation of astrocyte glutamate transport and cell-surface expression of GLAST. J Neurosci 19(23):10193–10200

    Article  PubMed  CAS  Google Scholar 

  33. Sheldon AL, Robinson MB (2007) The role of glutamate transporters in neurodegenerative diseases and potential opportunities for intervention. Neurochem Int 51(6–7):333–355. https://doi.org/10.1016/j.neuint.2007.03.012

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Mathern GW, Adelson PD, Cahan LD, Leite JP (2002) Hippocampal neuron damage in human epilepsy: Meyer’s hypothesis revisited. Prog Brain Res 135:237–251

    Article  PubMed  Google Scholar 

  35. Jarero-Basulto JJ, Gasca-Martinez Y, Rivera-Cervantes MC, Urena-Guerrero ME, Feria-Velasco AI, Beas-Zarate C (2018) Interactions between epilepsy and plasticity. Pharmaceuticals. https://doi.org/10.3390/ph11010017

    Article  PubMed  PubMed Central  Google Scholar 

  36. Fujikawa DG (1996) The temporal evolution of neuronal damage from pilocarpine-induced status epilepticus. Brain Res 725(1):11–22

    Article  PubMed  CAS  Google Scholar 

  37. Covolan L, Mello LE (2000) Temporal profile of neuronal injury following pilocarpine or kainic acid-induced status epilepticus. Epilepsy Res 39(2):133–152

    Article  PubMed  CAS  Google Scholar 

  38. Poirier JL, Capek R, De Koninck Y (2000) Differential progression of dark neuron and Fluoro-Jade labelling in the rat hippocampus following pilocarpine-induced status epilepticus. Neuroscience 97(1):59–68

    Article  PubMed  CAS  Google Scholar 

  39. Weise J, Engelhorn T, Dorfler A, Aker S, Bahr M, Hufnagel A (2005) Expression time course and spatial distribution of activated caspase-3 after experimental status epilepticus: contribution of delayed neuronal cell death to seizure-induced neuronal injury. Neurobiol Dis 18(3):582–590. https://doi.org/10.1016/j.nbd.2004.10.025

    Article  PubMed  CAS  Google Scholar 

  40. Wang L, Liu YH, Huang YG, Chen LW (2008) Time-course of neuronal death in the mouse pilocarpine model of chronic epilepsy using Fluoro-Jade C staining. Brain Res 1241:157–167. https://doi.org/10.1016/j.brainres.2008.07.097

    Article  PubMed  CAS  Google Scholar 

  41. do Nascimento AL, Dos Santos NF, Campos Pelagio F, Aparecida Teixeira S, de Moraes Ferrari EA, Langone F (2012) Neuronal degeneration and gliosis time-course in the mouse hippocampal formation after pilocarpine-induced status epilepticus. Brain Res 1470:98–110. https://doi.org/10.1016/j.brainres.2012.06.008

    Article  PubMed  CAS  Google Scholar 

  42. Cavazos JE, Das I, Sutula TP (1994) Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J Neurosci 14(5 Pt 2):3106–3121

    Article  PubMed  CAS  Google Scholar 

  43. Sloviter RS (1983) “Epileptic” brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies. Brain Res Bull 10(5):675–697. https://doi.org/10.1016/0361-9230(83)90037-0

    Article  PubMed  CAS  Google Scholar 

  44. Franke H, Kittner H (2001) Morphological alterations of neurons and astrocytes and changes in emotional behavior in pentylenetetrazol-kindled rats. Pharmacol Biochem Behav 70(2–3):291–303

    Article  PubMed  CAS  Google Scholar 

  45. Tian FF, Zeng C, Guo TH, Chen Y, Chen JM, Ma YF, Fang J, Cai XF, Li FR, Wang XH, Huang WJ, Fu JJ, Dang J (2009) Mossy fiber sprouting, hippocampal damage and spontaneous recurrent seizures in pentylenetetrazole kindling rat model. Acta Neurol Belg 109(4):298–304

    PubMed  Google Scholar 

  46. Zhu X, Dong J, Shen K, Bai Y, Zhang Y, Lv X, Chao J, Yao H (2015) NMDA receptor NR2B subunits contribute to PTZ-kindling-induced hippocampal astrocytosis and oxidative stress. Brain Res Bull 114:70–78. https://doi.org/10.1016/j.brainresbull.2015.04.002

    Article  PubMed  CAS  Google Scholar 

  47. Fröhlich F (2016) Chap. 8—Microcircuits of the hippocampus. In: F. Fröhlich (Ed.), Network neuroscience. Academic Press, San Diego, p 97–109. https://doi.org/10.1016/B978-0-12-801560-5.00008-2

    Chapter  Google Scholar 

  48. Cappaert NLM, Van Strien NM, Witter MP (2015) Chap. 20—Hippocampal formation A2—Paxinos, George. In: Cappaert N.L.M., Van Strien N.M., & M.P. Witter (Eds.), The rat nervous system, 4th edn. Academic Press, San Diego, p 511–573. https://doi.org/10.1016/B978-0-12-374245-2.00020-6

    Chapter  Google Scholar 

  49. Gallyas F, Guldner FH, Zoltay G, Wolff JR (1990) Golgi-like demonstration of “dark” neurons with an argyrophil III method for experimental neuropathology. Acta Neuropathol 79(6):620–628

    Article  PubMed  CAS  Google Scholar 

  50. Rajasekaran K, Todorovic M, Kapur J (2012) Calcium-permeable AMPA receptors are expressed in a rodent model of status epilepticus. Ann Neurol 72(1):91–102. https://doi.org/10.1002/ana.23570

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Prince HC, Tzingounis AV, Levey AI, Conn PJ (2000) Functional downregulation of GluR2 in piriform cortex of kindled animals. Synapse 38 (4):489–498

    Article  PubMed  CAS  Google Scholar 

  52. Sanchez RM, Koh S, Rio C, Wang C, Lamperti ED, Sharma D, Corfas G, Jensen FE (2001) Decreased glutamate receptor 2 expression and enhanced epileptogenesis in immature rat hippocampus after perinatal hypoxia-induced seizures. J Neurosci 21(20):8154–8163

    Article  PubMed  CAS  Google Scholar 

  53. Malkin SL, Amakhin DV, Veniaminova EA, Kim K, Zubareva OE, Magazanik LG, Zaitsev AV (2016) Changes of AMPA receptor properties in the neocortex and hippocampus following pilocarpine-induced status epilepticus in rats. Neuroscience 327:146–155. https://doi.org/10.1016/j.neuroscience.2016.04.024

    Article  PubMed  CAS  Google Scholar 

  54. Gorter JA, Petrozzino JJ, Aronica EM, Rosenbaum DM, Opitz T, Bennett MVL, Connor JA, Zukin RS (1997) Global ischemia induces downregulation of Glur2 mRNA and increases AMPA receptor-mediated Ca2+ influx in hippocampal CA1 neurons of gerbil. J Neurosci 17(16):6179–6188

    Article  PubMed  CAS  Google Scholar 

  55. Sloviter RS, Dempster DW (1985) “Epileptic” brain damage is replicated qualitatively in the rat hippocampus by central injection of glutamate or aspartate but not by GABA or acetylcholine. Brain Res Bull 15(1):39–60

    Article  PubMed  CAS  Google Scholar 

  56. Kalimo H, Auer RN, Siesjo BK (1985) The temporal evolution of hypoglycemic brain damage: III. Light and electron microscopic findings in the rat caudoputamen. Acta Neuropathol 67(1–2):37–50

    Article  PubMed  CAS  Google Scholar 

  57. Duan W, Zhang YP, Hou Z, Huang C, Zhu H, Zhang CQ, Yin Q (2015) Novel insights into NeuN: from neuronal marker to splicing regulator. Mol Neurobiol. https://doi.org/10.1007/s12035-015-9122-5

    Article  PubMed  Google Scholar 

  58. Lavezzi AM, Corna MF, Matturri L (2013) Neuronal nuclear antigen (NeuN): a useful marker of neuronal immaturity in sudden unexplained perinatal death. J Neurol Sci 329(1–2):45–50. https://doi.org/10.1016/j.jns.2013.03.012

    Article  PubMed  CAS  Google Scholar 

  59. Muller GJ, Stadelmann C, Bastholm L, Elling F, Lassmann H, Johansen FF (2004) Ischemia leads to apoptosis- and necrosis-like neuron death in the ischemic rat hippocampus. Brain Pathol 14(4):415–424

    Article  PubMed  Google Scholar 

  60. Andre V, Marescaux C, Nehlig A, Fritschy JM (2001) Alterations of hippocampal GABAergic system contribute to development of spontaneous recurrent seizures in the rat lithium-pilocarpine model of temporal lobe epilepsy. Hippocampus 11(4):452–468. https://doi.org/10.1002/hipo.1060

    Article  PubMed  CAS  Google Scholar 

  61. Radian R, Ottersen OP, Storm-Mathisen J, Castel M, Kanner BI (1990) Immunocytochemical localization of the GABA transporter in rat brain. J Neurosci 10(4):1319–1330

    Article  PubMed  CAS  Google Scholar 

  62. Conti F, Melone M, De Biasi S, Minelli A, Brecha NC, Ducati A (1998) Neuronal and glial localization of GAT-1, a high-affinity gamma-aminobutyric acid plasma membrane transporter, in human cerebral cortex: with a note on its distribution in monkey cortex. J Comp Neurol 396(1):51–63

    Article  PubMed  CAS  Google Scholar 

  63. Lie MEK, Al-Khawaja A, Damgaard M, Haugaard AS, Schousboe A, Clarkson AN, Wellendorph P (2017) Glial GABA transporters as modulators of inhibitory signalling in epilepsy and stroke. Adv Neurobiol. https://doi.org/10.1007/978-3-319-55769-4_7

    Article  PubMed  Google Scholar 

  64. Hirao T, Morimoto K, Yamamoto Y, Watanabe T, Sato H, Sato K, Sato S, Yamada N, Tanaka K, Suwaki H (1998) Time-dependent and regional expression of GABA transporter mRNAs following amygdala-kindled seizures in rats. Mol Brain Res 54(1):49–55

    Article  PubMed  CAS  Google Scholar 

  65. Medina-Ceja L, Sandoval-Garcia F, Morales-Villagran A, Lopez-Perez SJ (2012) Rapid compensatory changes in the expression of EAAT-3 and GAT-1 transporters during seizures in cells of the CA1 and dentate gyrus. J Biomed Sci 19:78. https://doi.org/10.1186/1423-0127-19-78

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Su J, Yin J, Qin W, Sha S, Xu J, Jiang C (2015) Role for pro-inflammatory cytokines in regulating expression of GABA transporter type 1 and 3 in specific brain regions of kainic acid-induced status epilepticus. Neurochem Res 40(3):621–627. https://doi.org/10.1007/s11064-014-1504-y

    Article  PubMed  CAS  Google Scholar 

  67. Postnikova TY, Trofimova AM, Zaitsev AV, Magazanik LG (2017) Status epilepticus induced by pentylenetetrazole increases short-term synaptic facilitation in the hippocampus of juvenile rats. Dokl Biol Sci 477(1):207–209. https://doi.org/10.1134/S0012496617060102

    Article  PubMed  Google Scholar 

  68. Postnikova TY, Zubareva OE, Kovalenko AA, Kim KK, Magazanik LG, Zaitsev AV (2017) Status epilepticus impairs synaptic plasticity in rat hippocampus and is followed by changes in expression of NMDA receptors. Biochemistry 82(3):282–290. https://doi.org/10.1134/s0006297917030063

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by the Russian Science Foundation (Grant Number 16-15-10202). The electron microscopy part of the study was performed in the Research Resource Center of Sechenov Institute of Evolutionary Physiology and Biochemistry and was carried out within the state assignment of FASO of Russia (АААА-А18-118012290373-7).

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  1. Sechenov Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of Sciences, pr. Toreza 44, Saint Petersburg, Russia, 194223

    Dmitry S. Vasilev, Natalia L. Tumanova, Kira Kh. Kim, Valeria V. Lavrentyeva, Nera Y. Lukomskaya, Igor A. Zhuravin, Lev G. Magazanik & Aleksey V. Zaitsev

  2. Saint Petersburg State University, Saint Petersburg, Russia, 199034

    Lev G. Magazanik

  3. Institute of Experimental Medicine, Almazov National Medical Research Centre, Saint Petersburg, Russia, 197376

    Aleksey V. Zaitsev

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  1. Dmitry S. Vasilev
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Vasilev, D.S., Tumanova, N.L., Kim, K.K. et al. Transient Morphological Alterations in the Hippocampus After Pentylenetetrazole-Induced Seizures in Rats. Neurochem Res 43, 1671–1682 (2018). https://doi.org/10.1007/s11064-018-2583-y

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