IN VITRO МОДЕЛИ ЭПИЛЕПТИФОРМНОЙ АКТИВНОСТИ
PDF

Ключевые слова

острые судорожные состояния
эпилептоподобная активность
in vitro модели эпилепсии
переживающие срезы
энторинальная кора
гиппокамп

Как цитировать

Ергина, Ю. Л., & Смирнова, Е. Ю. (2019). IN VITRO МОДЕЛИ ЭПИЛЕПТИФОРМНОЙ АКТИВНОСТИ. Российский физиологический журнал им. И. М. Сеченова, 105(8), 954–965. https://doi.org/10.1134/S0869813919080041

Аннотация

На сегодняшний день моделирование острых судорожных состояний in vitro является одним из ключевых методов получения информации о механизмах генерации, распространения и прекращения эпилептоподобной активности. С помощью in vitro моделей изучают последствия острого фармакологического и электрического воздействия на ткани мозга, изменения синаптической передачи в ходе эпилептоподобных разрядов. Применение in vitro моделей позволяет обойти часть ограничений, традиционно ассоциируемых с in vivo исследованиями; в частности, их использование значительно упрощает процесс доставки химических агентов, а также обеспечивает механическую стабильность электрофизиологической регистрации за счет отсутствия артефактов, связанных с судорогами, а также сердцебиением и дыханием. В in vitro исследованиях становятся доступными структуры вентральной поверхности мозга, лежащие у основания черепа. В обзоре описаны современные in vitro модели эпилептической активности, обсуждаются преимущества и недостатки, а также область их применения.

https://doi.org/10.1134/S0869813919080041
PDF

Литература

Yamamoto C. Intracellular study of seizure-like afterdischarges elicited in thin hippocampal sections in vitro. Exp. Neurol. 35(1):154-164. 1972.

. de Curtis M., Biella G., Buccellati C., Folco G. Simultaneous investigation of the neuronal and vascular compartments in the guinea pig brain isolated in vitro, Brain Res. Protoc. 3(2): 221–228. 1998.

. Muhlethaler M., de Curtis M., Walton K., Llinas R. The isolated and perfused brain of the guinea-pig in vitro. Eur. J. Neurosci. 5(7): 915–926. 1993.

. Chaigneau E., Oheim M., Audinat E., Charpak S. Two-photon imaging of capillary blood flow in olfactory bulb glomeruli. Proc. Natl. Acad. Sci. USA. 100(22): 13081–13086. 2003.

. Spyker D., Lynch C., Shabanowitz J., Sinn J. Poisoning with 4-aminopyridine: Report ofthree cases. Clin. Toxicol. 16: 487–497. 1980.

. Ben-Ari Y., Tremblay E., Riche D., Ghilini G., Naquet R. Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: Metabolic mapping using the deoxyglucose method with special reference to thepathology of epilepsy. Neuroscience. 6: 1361–1391. 1981.

. Baram T., Snead 3rd O. Bicuculline induced seizures in infant rats: ontogeny of behavioral and electrocortical phenomena. Brain Res. Dev. Brain Res. 57(2): 291–295. 1990.

. Pfeiffer M., Draguhn A., Meierkord H., Heinemann U. Effects of gamma-aminobutyric acid (GABA) agonists and GABA uptake inhibitors on pharmacosensitive and pharmacoresistant epileptiform activity in vitro. Br. J. Pharmacol. 119: 569–577. 1996.

. Dreier J., Zhang C., Heinemann U. Phenytoin, phenobarbital, and midazolam fail to stop status epilepticus-like activity induced by low magnesium in rat entorhinal slices, but can prevent its development. Acta Neurol. Scand. 98: 154–160. 1998.

. Balestrino M., Aitken P., Somjen G. The effects of moderate changes of extracellular K+ and Ca2+ on synaptic and neural function in the CA1 region of the hippocampal slice. Brain Res. 377: 229–239. 1986.

. Poolos N., Mauk M., Kocsis J. Activity-evoked increases in extracellular potassium modulate presynaptic excitability in the CA1 region of the hippocampus. Neurophysiology. 58: 404–416. 1987.

. Jefferys, J. G., Haas, H. L. Synchronized bursting of CA1 hippocampal pyramidal cells in the absence of synaptic transmission. Nature. 300(5891): 448–450. 1982.

. Sloviter R. 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: 675–697. 1983.

. Moshe S., Albala B. Perinatal hypoxia and subsequent development of seizures. Physiol. Behav. 35: 819-823. 1985.

. Ting J.T., Daigle T.L., Chen Q. Patch-Clamp Methods and Protocols. 1183: 221–242. 2014.

. Geiger J., Bischofberger J., Vida I., Frobe U., Pfitzinger S., Weber H. J., Haverkampf K., Jonas P. Patch-clamp recording in brain slices with improved slicer technology. Pflugers Arch. 443(3): 491–501. 2002.

. Dreier J., Heinemann U. Regional and time dependent variations of low Mg2+ induced epileptiform activity in rat temporal cortex slices. Exp. Brain Res. 87(3): 581–596. 1991.

. von Bohlen und Halbach O., Albrecht D. Tracing of axonal connectivities in a combined slice preparation of rat brains – a study by rhodamine-dextran-amine-application in the lateral nucleus of the amygdala. J. Neurosci. Methods 81(1–2): 169–175. 1998.

. Coulter D. and Lee C. Thalamocortical rhythm generation in vitro: extra- and intracellular recordings in mouse thalamocortical slices perfused with low Mg2+ medium. Brain Res. 631(1): 137–142. 1993.

. Chang W., Lu H., Shyu B. Treatment with direct-current stimulation against cingulate seizure-like activity induced by 4-aminopyridine and bicuculline in an in vitro mouse model. Exp. Neurol. 265: 180–192. 2015.

. Toprani S., Durand D. Fiber tract stimulation can reduce epileptiform activity in an in-vitro bilateral hippocampal slice preparation. Exp. Neurol. 240: 28–43. 2013.

. Buzsáki G. Large-scale recording of neuronal ensembles. Nat. Neurosci. 7(5): 446-451. 2004.

. Martina M. Patch-Clamp Methods and Protocols. Totowa, NJ. Humana Press. 2014.

. Amakhin D.V., Soboleva E.B., Ergina J.L., Malkin S.L., Chizhov A.V., Zaitsev A.V. Seizure-Induced Potentiation of AMPA Receptor-Mediated Synaptic Transmission in the Entorhinal Cortex. Front. Cell. Neurosci. 12 (486). 2018.

. Smirnova E.Y., Amakhin D.V., Malkin S.L., Chizhov A.V., Zaitsev A.V. Acute Changes in Electrophysiological Properties of Cortical Regular-Spiking Cells Following Seizures in a Rat Lithium-Pilocarpine Model. Neuroscience. 379: 202-215. 2018.

. Schurr A., Payne R.S., Heine M.F., Rigor B.M. Hypoxia, excitotoxicity, and neuroprotection in the hippocampal slice preparation. J. Neurosci. Methods. 59(1): 129-138. 1995.

. Whittington M., Traub R. Interneuron Diversity series: Inhibitory interneurons and network oscillations in vitro. Trends Neurosci. 26(12): 676–682. 2003.

. Freund T., Buzsáki G. Interneurons of the hippocampus. Hippocampus. 6(4): 347–470. 1996.

. Fukuda A., Czurkó A., Hida H., Muramatsu K., Lénárd L., Nishino H. Appearance ofdeteriorated neurons on regionally different time tables in rat brain thin slices maintained in physiological condition. Neurosci. Lett. 184(1): 13-16. 1995.

. Zhang M., Ladas T.P., Qiu C., Shivacharan R.S., Gonzalez-Reyes L.E., Durand D.M. Propagation of Epileptiform Activity Can Be Independent of Synaptic Transmission, Gap Junctions, or Diffusion and Is Consistent with Electrical Field Transmission. J. Neurosci. 34. 2014.

. Jackson J., Amilhon B., Goutagny R., Bott J-B., Manseau F., Kortleven C., Bressler S., Williams S. Reversal of theta rhythm flow through intact hippocampal circuits. Nat. Neurosci. 17: 1362–1370. 2014.

. de Curtis M., Paré D., Llinás R.R. The electrophysiology of the olfactory-hippocampal circuit in the isolated and perfused adult mammalian brain in vitro. Hippocampus. 1: 341–354. 1991.

. de Curtis M., Biella G., Forti M., Panzica F. Multifocal spontaneous epileptic activity induced by restricted bicuculline ejection in the piriform cortex of the isolated guinea pig brain. J. Neurophysiol. 71(6): 2463–2476. 1994.

. Librizzi L., Janigro D., de Biasi S., de Curtis M. Blood-brain barrier preservation in the in vitro isolated guinea pig brain preparation. J. Neurosci. Res. 66(2): 289–297. 2001.

. Librizzi L., Noe F., Vezzani A., de Curtis M., Ravizza T. Seizure-induced brain-borne inflammation sustains seizure recurrence and blood-brain barrier damage. Ann. Neurol. 72(1): 82–90. 2012.

. Raimondo J., Heinemann U., de Curtis M., Goodkin H., Dulla C., Janigro D., Ikeda A., Lin C., Jiruska P., Galanopoulou A., Bernard C. Methodological standards for in vitro models of epilepsy and epileptic seizures. A TASK1-WG4 report of theAES/ILAE Translational Task Force of the ILAE. Epilepsia. 58: 40-52. 2017.

. Dyhrfjeld-Johnsen J., Berdichevsky Y., Swiercz W., Sabolek H., Staley K.J. Interictal spikes precede ictal discharges in an organotypic hippocampal slice culture model of epileptogenesis. J. Clin. Neurophysiol. 27: 418–24. 2010.

. de Simoni A., Yu L. Preparation of organotypic hippocampal slice cultures: interface method. Nat. Protoc. 1: 1439–1445. 2006.

. Wong M., Yamada K. Developmental characteristics of epileptiform activity in immature rat neocortex: a comparison of four in vitro seizure models. Brain Res. Dev. Brain Res. 128(2): 113–120. 2001.

. Schwartzkroin P.A., Baraban S.C., Hochman D.W. Osmolarity, ionic flux, and changes in brain excitability. Epilepsy Res. 32(1-2): 275-285. 1998.

. Dudek F.E., Obenaus A., Tasker J.G. Osmolality-induced changes in extracellular volume alter epileptiform bursts independent of chemical synapses in the rat: importance of non-synaptic mechanisms in hippocampal epileptogenesis. Neurosci. Lett. 120: 267–270. 1990.

. Chesler M. Regulation and modulation of pH in the brain. Physiol. Rev. 83: 1183–1221. 2003.

. Taira T., Smirnov S., Voipio J., Kaila K. Intrinsic proton modulation of excitatory transmission in rat hippocampal slices. Neuroreport. 4 (93): 93-96. 1993.

. Pasternack M., Smirnov S., Kaila K. Proton Modulation of Functionally Distinct GABAA Receptors in Acutely Isolated Pyramidal Neurons of Rat Hippocampus. Neuropharmacology. 35: 1279–1288. 1996.

. Hodgkin A.L., Katz B. The effect of temperature on the electrical activity of the giant axon of the squid. J. Physiol. 109: 240–249. 1949.

. Hill M.W., Wong M., Amarakone A., Rothman S.M. Rapid Cooling Aborts Seizure-Like Activity in Rodent Hippocampal-Entorhinal Slices. Epilepsia. 41: 1241–1248. 2000.

. Schuchmann S., Meierkord H., Stenkamp K., Breustedt J., Windmüller O., Heinemann U., Buchheim K. Synaptic and nonsynaptic ictogenesis occurs at different temperatures in submerged and interface rat brain slices. J. Neurophysiol. 87: 2929–2935. 2002.

. Fisher R.S., Scharfman H.E., de Curtis M. How can we identify ictal and interictal abnormal activity? Adv. Exp. Med. Biol. 813: 3-23. 2014.

. Borgstrom L., Chapman A.G., Siesjo B.K. Glucose consumption in the cerebral cortex of the rat during bicuculline-induced status epilepticus. J. Neurochem. 27: 971–973. 1976.

. Schwartzkroin P., Prince D. Cellular and field potential properties of epileptogenic hippocampal slices. Brain Res. 147(1): 117–130. 1978.

. Wong R., Traub R., Miles R. Cellular basis of neuronal synchrony in epilepsy. Adv. Neurol. 44: 583–592. 1986.

. Williamson R., Wheal H. The contribution of AMPA and NMDA receptors to graded bursting activity in the hippocampal CA1 region in an acute in vitro model of epilepsy. Epilepsy Res. 12(2): 179–188. 1992.

. Traub R., Borck C., Colling S., Jefferys J. On the structure of ictal events in vitro. Epilepsia. 37(9): 879–891. 1996.

. Khalilov I., Esclapez M., Medina I., Aggoun D., Lamsa K., Leinekugel X., Khazipov R., Ben-Ari Y. A novel in vitro preparation: the intact hippocampal formation. Neuron. 19: 743–749. 1997.

. Karnup S., Stelzer A. Seizure-like activity in the disinhibited CA1 minislice of adult guinea-pigs. J. Physiol. 532(3): 713–730. 2001.

. Meier C., Dudek F. Spontaneous and stimulation-induced synchronized burst afterdischarges in the isolated CA1 of kainate-treated rats. J. Neurophysiol. 76(4): 2231–2239. 1996.

. Yao J.A., Tseng G.N. Modulation of 4-AP block of a mammalian A-type K channel clone by channel gating and membrane voltage. Biophys. J. 67(1): 130-142. 1994.

. Choquet D., Korn H. Mechanism of 4-aminopyridine action on voltage-gated potassium channels in lymphocytes. J. Gen. Physiol. 99(2): 217-240. 1992.

. Buckle P.J., Haas H.L. Enhancement of synaptic transmission by 4-aminopyridine in hippocampal slices of the rat. J. Physiol. 326: 109–122. 1982.

. Galvan M., Grafe P., ten Bruggencate G. Convulsant actions of 4-aminopyridine onthe guinea-pig olfactory cortex slice. Brain Res. 241(1): 75-86. 1982.

. Amakhin D.V., Ergina J.L., Chizhov A.V., Zaitsev A.V. Synaptic conductances during interictal discharges in pyramidal neurons of rat entorhinal cortex. Front. Cell. Neurosci. 10(233). 2016.

. Gonzalez-Sulser A., Wang J., Motamedi G.K., Avoli M., Vicini S., Dzakpasu R. The 4-aminopyridine in vitro epilepsy model analyzed with a perforated multi-electrode array. Neuropharmacology. 60(7-8): 1142–1153. 2011.

. Avoli M., D'Antuono M., Louvel J., Kohling R., Biagini G., Pumain R., D'Arcangelo G., Tancredi V. Network and pharmacological mechanisms leading to epileptiform synchronization in the limbic system in vitro. Prog. Neurobiol. 68(3): 167–207. 2002.

. Ben-Ari Y., Cossart R. Kainate, a double agent that generates seizures: Two decades of progress. Trends Neurosci. 23(11): 580–587. 2000.

. Huettner J. Kainate receptors and synaptic transmission. Prog. Neurobiol. 70(5): 387–407. 2003.

. Шубина Л.В., Мальков А.Е., Кичигина В.Ф. Каиновая модель височной эпилепсии и ее применение для изучения роли эндоканнабиноидной системы в нейропротекции. Рос. физиол. журн. им. И. М. Сеченова. 105(6): 680–693. 2019. [Shubina L.V., Malkov A.E., Kitchigina V.F. The Kainic Acid Model of Temporal Lobe Epilepsy and its Application for Studying the Role of the Endocannabinoid System in Neuroprotection. Russ. J. Physiol. 105(6): 680–693. 2019. (In Russ.)].

. Westbrook G., Lothman E. Cellular and synaptic basis of kainic acid-induced hippocampal epileptiform activity. Brain Res. 273(1): 97–109. 1983.

. Cossart R., Esclapez M., Hirsch J., Bernard C., Ben-Ari Y. GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat. Neurosci. 1(6): 470–478. 1998.

. Melyan Z., Wheal H., Lancaster B. Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron. 34(1): 107–114. 2002.

. Khalilov I., Holmes G., Ben-Ari Y. In vitro formation of a secondary epileptogenic mirror focus by interhippocampal propagation of seizures. Nat. Neurosci. 6(10): 1079–1085. 2003.

. Khalilov I., Dzhala V., Medina I., Leinekugel X., Melyan Z., Lamsa K., Khazipov R., Ben-Ari Y. Maturation of kainate-induced epileptiform activities in interconnected intact neonatal limbic structures in vitro. Eur. J. Neurosci. 11(10): 3468–3480. 1999.

. Mody I., Lambert J., Heinemann U. Low extracellular magnesium induces epileptiform activity and spreading depression in rat hippocampal slices. J. Neurophysiol. 57(3): 869–888. 1987.

. Stanton P., Jones R., Mody I., Heinemann U. Epileptiform activity induced by lowering extracellular [Mg2+] in combined hippocampal-entorhinal cortex slices: Modulation by receptors for norepinephrine and N-methyl-d-aspartate. Epilepsy Res. 1(1): 53–62. 1987.

. Moser J., Kilb W., Werhahn K.J., Luhmann H.J. Early developmental alterations of low-Mg2+ -induced epileptiform activity in the intact corticohippocampal formation of the newborn mouse in vitro. Brain Res. 1077(1): 170–177. 2006.

. Jiang Q., Wang J., Wu X., Jiang Y. Alterations of NR2B and PSD-95 expression after early-life epileptiform discharges in developing neurons. Int. J. Dev. Neurosci. 25(3): 165–170. 2007.

. Jensen M., Yaari Y. The relationshp between interictal and ictal paroxysms in an in vitro model of focal hippocampal epilepsy. Ann. Neurol. 591–598. 1988.

. Poolos N.P., Mauk M.D., Kocsis J.D. Activity-evoked increases in extracellular potassium modulate presynaptic excitability in the CA1 region of the hippocampus. Neurophysiology. 58: 404–416. 1987.

. Huberfeld G., Blauwblomme T., Miles R. Hippocampus and epilepsy: Findings from human tissues. Rev. Neurol. 171(3): 236–251. 2015.

. Смирнова Е.Ю., Ерофеев А.И., Власова О.Л., Чижов А.В., Зайцев А.В. Система биологической обратной связи для подавления эпилептической активности в оптогенетическом эксперименте. Рос. физиол. журн. им. И. М. Сеченова. 104 (6): 731-737. 2018. [Smirnova E.Y., Erofeev A.I., Vlasova O.L., Chizhov A.V., Zaitsev A.V. A biological closed-loop system in optogenetic experiments for suppression of epileptic activity. Russ. J. Physiol. 104 (6): 731-737. 2018. (In Russ.)].

. Yekhlef L., Breschi G., Lagostena L., Russo G., Taverna S. Selective activation of parvalbumin- or somatostatin-expressing interneurons triggers epileptic seizure like activity in mouse medial entorhinal cortex. J. Neurophysiol. 113(5): 1616-1630. 2015.

. Avoli M., de Curtis M. GABAergic synchronization in the limbic system andits role in the generation of epileptiform activity. Prog. Neurobiol. 95: 104–132. 2011.

. Dreier J., Heinemann U. Late low magnesium-induced epileptiform activity inrat entorhinal cortex slices becomes insensitive to the anticonvulsant valproicacid. Neurosci. Lett. 119 (1): 68-70. 1990.

. Jensen M., Yaari Y. Role of intrinsic burst firing, potassium accumulation,and electrical coupling in the elevated potassium model of hippocampal epilepsy. J. Neurophysiol. 77(3): 1224-1233. 1997.

. Bear J., Lothman E. An in vitro study of focal epileptogenesis in combined hippocampal-parahippocampal slices. Epilepsy Res. 14(3): 183–193. 1993.

. Barbarosie M., Avoli M. CA3-driven hippocampal-entorhinal loop controls rather than sustains in vitro limbic seizures. J. Neurosci. 17(23): 9308–9314. 1997.

. Uva L., Librizzi L., Wendling F., de Curtis M. Propagation dynamics of epileptiform activity acutely induced by bicuculline in the hippocampal-parahippocampal region of the isolated guinea pig brain. Epilepsia. 46(12): 1914–1925. 2005.