Современные проблемы синаптической пластичности

Vladimir G. Skrebitsky1, Irina N. Sharonova1
1ФГБНУ «Научный центр неврологии», Москва, Россия

Аннотация


В настоящем обзоре рассмотрены результаты современных исследований, которые с новых позиций подтверждают идеи, высказанные в середине прошлого века о влиянии разряда нейрона на эффективность его синаптических входов. Эта концепция развиваются сегодня на рецепторном, канальном и внутриклеточном уровнях, что позволяет раскрыть особую роль ионов кальция в запуске целого ряда каскадов, приводящих к временным или стойким изменениям синаптической передачи. Подчеркивается важная роль различных физиологически активных соединений, влияющих на синаптическую пластичность, а через нее и на когнитивные процессы у человека, что имеет не только фундаментальное, но и прикладное значение. Подробно рас-cматриваются клеточные и рецепторные мишени современных ноотропных препаратов, направленных на коррекцию различных по своему характеру когнитивных нарушений.

Литература

1. Hebb O.D. The Organization of Behavior. NY: Wiley, 1949. 335 p.

2. Brindley G.S. The classification of modifiable synapses and their use in models for conditioning. Proc. Royal Soc Lond B Biol Sci 1967; 168: 361-367. DOI: 10.1098/rspb.1967.0070.

3. Gerbrandt L.K., Skrebitsky V.G., Burešová O., Bureš J.Plastic changes of unit activity induced by tactile stimuli followed by electrical stimulation of single hippocampal and reticular neurons. Neuropsychologia 1968; 6: 3-10. DOI. org/10.1016/0028-3932(68)90034-1. DOI: 10.1016/0028-3932(68)90034-1.

4. Русинова Е.В., Скребицкий В.Г. Влияние разряда нейрона на эффективность его синаптических входов. Журнал высшей нервной деятельности. им. И.П. Павлова 1975; 25(6): 1312-1315. PMID: 1210783.

5. Baranyi A., Szente M.B. Long-lasting potentiation of synaptic transmission requires postsynaptic modifications in the neocortex. Brain Res 1987; 423(1-2): 378-384. DOI: 10.1016/0006-8993(87)90867-5. PMID: 2823992.

6. Skrebitsky V.G., Chepkova A.N. Hebbian synapses in cortical and hippocampal pathways. Rev Neurosci 1998; 9(4): 243-264. DOI: 10.1515/REVNEURO. 1998.9.4.243. PMID: 9886140.

7. Bliss T.V., Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 1973; 232(2): 331-356. DOI: 10.1113/jphysiol.1973.sp010273. PMID: 4727084.

8. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993; 361(6407): 31-39. DOI: 10.1038/361031a0. PMID: 8421494.

9. Bliss T.V., Collingridge G.L., Morris R.G. Synaptic plasticity in health and disease: introduction and overview. Philos Trans R Soc Lond B Biol Sci 2013; 369(1633): 20130129. DOI: 10.1098/rstb.2013.0129. PMID: 24298133.

10. Voronin L.L. Long-term potentiation in the hippocampus. Neuroscience 1983; 10(4): 1051-1069. DOI: 10.1016/0306-4522(83)90099-4. PMID: 6141538.

11. Sastry B.R., Goh J.W., Auyeung A. Associative induction of posttetanic and long-term potentiation in CA1 neurons of rat hippocampus. Science 1986; 232(4753): 988-990. DOI: 10.1126/science.3010459. PMID: 3010459.

12. Kelso S.R., Ganong A.H., Brown T.H. Hebbian synapses in hippocampus. Proc Natl Acad Sci USA 1986; 83(14): 5326-5330. DOI: 10.1073/pnas.83.14.5326. PMID: 3460096.

13. Lodge D., Watkins J.C., Bortolotto Z.A., Jane D.E, Volianskis A. The 1980s: D-AP5,LTP and a decade of NMDA receptor discoveries. Neurochem Res 2018. DOI: 10.1007/s11064-018-2640-6. PMID: 30284673.

14. Morris R.G. NMDA receptors and memory encoding. Neuropharmacology 2013; 74: 32-40. DOI: 10.1016/j.neuropharm.2013.04.014. PMID: 23628345.

15. Magee J.C., Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 1997; 275(5297):209-213. DOI: 10.1126/science.275.5297.209. PMID: 8985013.

16. Markram H., Lübke J., Frotscher M., Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 1997; 275(5297): 213-215. DOI: 10.1126/science.275.5297.213. PMID: 8985014.

17. Bliss T.V., Douglas R.M., Errington M.L., Lynch M.A. Correlation between long-term potentiation and release of endogenous amino acids from dentate gyrus of anaesthetized rats. J Physiol 1986; 377: 391-408. DOI: 10.1113/jphysiol. 1986.sp016193. PMID: 2879038.

18. Maren S., Tocco G., Standley S., Baudry M., Thompson R.F. Postsynaptic factors in the expression of long-term potentiation (LTP): increased glutamate receptor binding following LTP induction in vivo. Proc Natl Acad Sci USA 1993; 90(20): 9654-9658. DOI: 10.1073/pnas.90.20.9654. PMID: 8415757.

19. Frey U., Krug M., Reymann K.G., Matthies H. Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 1988; 452 (1-2): 57-65. DOI: 10.1016/0006- 8993(88)90008-X. PMID: 3401749.

20. Frey U., Huang Y.Y., Kandel E.R. Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 1993; 260 (5114): 1661-1664. DOI:10.1126/science.8389057. PMID: 8389057.

21. Mayford M., Siegelbaum S.A., Kandel E.R. Synapses and memory storage. Cold Spring Harb Perspect Biol 2012; 4(6). DOI: 10.1101/cshperspect.a005751. PMID: 2249638.

22. Danysz W., Zajaczkowski W., Parsons C.G. Modulation of learning processes by ionotropic glutamate receptor ligands. Behav Pharmacol 1995; 6 (5–6): 455- 474. PMID: 11224354.

23. Barnes C.A. Involvement of LTP in memory: are we “searching under the street light”? Neuron 1995; 15 (4): 751-754. DOI: 10.1016/0896-6273(95)90166- 3. PMID: 7576624.

24. Mayford M., Abel T., Kandel E.R. Transgenic approaches to cognition. Curr Opin Neurobiol 1995; 5(2): 141-148. DOI: 10.1016/0959-4388(95)80019-0. PMID: 7620300.

25. Wigström H., Gustafsson B. Large long-lasting potentiation in the dentate gyrus in vitro during blockade of inhibition. Brain Res 1983; 275(1): 153-158. DOI: 10.1016/0006-8993(83)90428-6. PMID: 6313124.

26. Ormond J., Woodin M.A. Disinhibition mediates a form of hippocampal long-term potentiation in area CA1. PLoS One 2009; 4(9): e7224. DOI: 10.1371/ journal.pone.0007224. PMID: 19787049.

27. Davies C.H., Collingridge G.L. The physiological regulation of synaptic inhibition by GABAB autoreceptors in rat hippocampus. J Physiol 1993; 472: 245- 265. DOI: 10.1113/jphysiol.1993.sp019945. PMID: 8145143.

28. Fedorov N.B., Sergeeva O.A., Skrebitsky V.G. Priming stimulation facilitates Hebb-type plasticity in the Schaffer collateral-commissural pathways of the mouse hippocampus. Exp Brain Res 1993; 94(2): 270-272. DOI: 10.1007/ BF00230295. PMID: 8359243.

29. Виноградова О.С. Гиппокамп и память. М.: Наука, 1975. 333 с.

30. Larson J., Munkácsy E. Theta-burst LTP. Brain Res 2015; 1621: 38-50. DOI: 10.1016/j.brainres.2014.10.034. PMID: 25452022.

31. Skrebitsky V.G. Nonspecific influences on neuronal firing in the central visual pathway. Exp Brain Res 1969; 9(4): 269-283. DOI: 10.1007/BF00235239. PMID: 5364413.

32. Skrebitsky V.G., Sharonova I.N. Reticular suppression of flash-evoked IPSPs in visual cortex neurons. Brain Res 1976; 111(1): 67-78. DOI: 10.1016/0006-8993(76)91049-0. PMID: 953705.

33. Klausberger T., Magill P.J., Márton L.F., Roberts J.D., Cobden P.M., Buzsáki G., Somogyi P. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 2003; 421(6925): 844-848. DOI: 10.1038/nature01374. PMID: 12594513.

34. Dykes R.W. Mechanisms controlling neuronal plasticity in somatosensory cortex. Can J Physiol Pharmacol 1997; 75(5): 535-545. DOI: 10.1139/y97-089. PMID: 9250389.

35. Павлов И.П. Лекции о работе больших полушарий головного мозга. Полное собр. соч. Т.4, М.: АН СССР, 1951. 452 с.

36. Sara S.J. Noradrenergic modulation of selective attention: its role in memory retrieval. Ann N Y Acad Sci 1985; 444: 178-193. DOI: 10.1111/j.1749-6632.1985. tb37588.x. PMID: 2990290.

37. Skrebitsky V.G., Chepkova A.N., Sharonova I.N. Reticular suppression of cortical inhibitory postsynaptic potentials. In: Hobson J.A., Brzier M.A. (Eds) Reticular Formation Revisited. NY: Raven Press, 1980: 67-78.

38. Doze V.A., Cohen G.A., Madison D.V. Synaptic localization of adrenergic disinhibition in the rat hippocampus. Neuron 1991; 6(6): 889-900. DOI: 10.1016/0896-6273(91)90229-S. PMID: 1675862.

39. Griffith J.S. A theory of the nature of memory. Nature 1966; 211(5054): 1160-1163. DOI: 10.1038/2111160a0. PMID: 5970018.

40. Brown T.H., Chapman P.F., Kairiss E.W., Keenan C.L. Long-term synaptic potentiation. Science 1988; 242 (4879): 724-728. DOI: 10.1126/science.2903551. PMID: 2903551.

41. Solari N., Hangya B. Cholinergic modulation of spatial learning, memory and navigation. Eur J Neurosci 2018; 48(5): 2199-2230. DOI: 10.1111/ejn.14089. PMID: 30055067.

42. Lin Y.W., Min M.Y., Chiu T.H., Yang H.W. Enhancement of associative longterm potentiation by activation of beta-adrenergic receptors at CA1 synapses in rat hippocampal slices. J Neurosci. 2003, 23(10): 4173-4181. DOI: 10.1523/ JNEUROSCI.23-10-04173.2003. PMID: 12764105.

43. O’Dell T.J., Connor S.A., Guglietta R., Nguyen P.V. β-Adrenergic receptor signaling and modulation of long-term potentiation in the mammalian hippocampus. Learn Mem 2015; 22(9): 461-471. DOI: 10.1101/lm.031088.113. PMID: 26286656.

44. Hansen N., Manahan-Vaughan D. Hippocampal long-term potentiation that is elicited by perforant path stimulation or that occurs in conjunction with spatial learning is tightly controlled by beta-adrenoreceptors and the locus coeruleus. Hippocampus 2015: 25(11): 1285-1298. DOI: 10.1002/hipo.22436. PMID: 25727388.

45. Takeuchi T., Duszkiewicz A.J., Sonneborn A. et al. Locus coeruleus and dopaminergic consolidation of everyday memory. Nature 2016; 537: 357-362. DOI: 10.1038/nature19325. PMID: 27602521.

46. Wei X., Ma T., Cheng Y. et al. Dopamine D1 or D2 receptor-expressing neurons in the central nervous system. Addict Biol 2018; 23(2): 569-584. DOI: 10.1111/adb.12512. PMID: 28436559.

47. Hammad H., Wagner J.J. Dopamine-mediated disinhibition in the CA1 region of rat hippocampus via D3 receptor activation. J Pharmacol Exp Ther 2006; 316(1):113-120. DOI: 10.1124/jpet.105.091579. PMID: 16162819.

48. Lemon N., Manahan-Vaughan D. Dopamine D1/D5 receptors gate the acquisition of novel information through hippocampal long-term potentiation and long-term depression. J Neurosci 2006; 26(29): 7723-7729. DOI: 10.1523/ JNEUROSCI.1454-06.2006. PMID: 16855100.

49. Lin J.S., Anaclet C., Sergeeva O.A., Haas H.L. The waking brain: an update. Cell Mol Life Sci 2011; 68(15): 2499-2512. DOI: 10.1007/s00018-011-0631-8. Review. PMID: 21318261.

50. Vorobjev V.S, Sharonova I.N., Walsh I.B., Haas H.L. Histamine potentiates N-methyl-D-aspartate responses in acutely isolated hippocampal neurons. Neuron 1993; 11(5): 837-844. DOI: 10.1016/0896-6273(93)90113-6. PMID: 8240807.

51. Kovacs G.L, De Wied D. Peptidergic modulation of learning and memory processes. Pharmacol Rev 1994; 46(3): 269-291. PMID: 7831381.

52. Чепкова А.Н. Влияние вазопрессина на свойства длительной посттетанической потенциации в срезах гиппокампа. Журнал высшей нервной деятельности им. И.П. Павлова 1981: 32(2): 427-429.

53. Chepkova A.N., Skrebitskii V.G. Effects of some adrenergic drugs and neuropeptides on long-term potentiation in hippocampal slices. In: Ajmone Marsan C., Matthies H.(eds). Neuronal Plasticity and Memory Formation. NY: Raven Press, 1982: 255-263.

54. Reijmers L.G., van Ree J.M., Spruijt B.M. et al. Vasopressin metabolites: a link between vasopressin and memory? Prog Brain Res 1998;119: 523-535. DOI: 10.1016/S0079-6123(08)61591-5. PMID: 10074810.

55. Rong X.W., Chen X.F., Du Y.C. Potentiation of synaptic transmission by neuropeptide AVP4-8 (ZNC(C)PR) in rat hippocampal slices. Neuroreport 1993; 4(9): 1135-1138. PMID: 8219041.

56. van den Hooff P., Urban I.J., de Wied D. Vasopressin maintains long-term potentiation in rat lateral septum slices. Brain Res 1989; 505(2): 181-186. DOI: 10.1016/0006-8993(89)91440-6. PMID: 2532055.

57. Chepkova A.N., French P., De Wied D. et al. Long-lasting enhancement of synaptic excitability of CA1/subiculum neurons of the rat ventral hippocampus by vasopressin and vasopressin(4-8). Brain Res 1995; 701(1-2): 255-566. DOI: 10.1016/0006-8993(95)01006-7. PMID: 8925289.

58. Ishihara K., Katsuki H., Kawabata A. et al. Effects of thyrotropin-releasing hormone and a related analog, CNK-602A, on long-term potentiation in the mossy fiber-CA3 pathway of guinea pig hippocampal slices. Brain Res 1991; 554(1-2): 203-208. DOI: 10.1016/0006-8993(91)90190-7. PMID: 1933301.

59. Matsuoka N., Kaneko S., Satoh M. Somatostatin augments long-term potentiation of the mossy fiber-CA3 system in guinea-pig hippocampal slices. Brain Res 1991; 553(2): 188-194. DOI: 10.1016/0006-8993(91)90823-E. PMID: 1681981.

60. Гудашева Т.А. Теоретические основы и технологии создания дипептидных лекарств Известия Академии наук. Серия химическая 2015; 9: 2012–2021.

61. Olpe H.R., Lynch G.S. The action of piracetam on the electrical activity of the hippocampal slice preparation: a field potential analysis. Eur J Pharmacol 1982; 80(4): 415-419. DOI: 10.1016/0014-2999(82)90088-7. PMID: 7106192.

62. Satoh M., Ishihara K., Katsuki H. Different susceptibilities of long-term potentiations in CA3 and CA1 regions of guinea pig hippocampal slices to nootropic drugs. Neurosci Lett 1988; 93(2-3): 236-241. DOI: 10.1016/0304- 3940(88)90088-2. PMID: 2853846.

63. Чепкова А.Н., Дореули Н.В., Островская Р.У. и др. Сохранение пластических свойств синаптической передачи в долгоживущих срезах гиппокампа под действием пептидного аналога пирацетама, L-pGlu-DAla- NH2. Бюллетень экспериментальной биологии и медицины 1990; 115: 602-604. PMID: 1964611.

64. Chepkova A.N., Doreulee N.V., Trofimov S.S. et al. Nootropic compound L-pyroglutamyl-D-alanine-amide restores hippocampal long-term potentiation impaired by exposure to ethanol in rats. Neurosci Lett 1995; 188(3): 163-166. DOI: 10.1016/0304-3940(95)11421-R. PMID: 7609900.

65. Островская Р.У., Гудашева Т.А., Воронина Т.А., Середенин С. Б. Оригинальный ноотропный и нейропротективный дипептид ноопепт (ГВС-111). Экспериментальная и клиническая фармакология 2002; 65(5): 66–72.

66. Островская Р.У., Бельник А.П., Сторожева З.И. Эффективность препарата «Ноопепт» при экспериментальной модели болезни Альцгеймера (когнитивный дефицит, вызванный введением β-амилоида 25–35 в базальные ядра Мейнерта крыс Бюллетень экспериментальной биологии и медицины 2011; 146(1): 84-88. PMID: 19145356.

67. Jia X., Gharibyan A.L., Öhman A. et al. Neuroprotective and nootropic drug noopept rescues α-synuclein amyloid cytotoxicity. J Mol Biol 2011; 414(5): 699- 712. DOI: 10.1016/j.jmb.2011.09.044. PMID: 21986202.

68. Бочкарев В.К., Телешова Е.С., Сюняков С.А. и др. Клинико-электрoэнцефалографическая характеристика действия ноопепта у больных с легкими когнитивными расстройствами посттравматического и сосудистого генеза. Журнал неврологии и психиатрии им. С.С. Корсакова 2008; 108(11): 47-55: PMID: 19008801.

69. Vakhitova Y.V., Sadovnikov S.V., Borisevich S.S. et al. Molecular mechanism underlying the action of substituted Pro-Gly Dipeptide Noopept. Acta Naturae 2016; 8(1): 82-89. PMID: 27099787.

70. Kondratenko R.V., Derevyagin V.I., Skrebitsky V.G. Novel nootropic dipeptide Noopept increases inhibitory synaptic transmission in CA1 pyramidal cells. Neurosci Lett 2010; 476(2): 70-73. DOI: 10.1016/j.neulet.2010.04.005. PMID: 20382202.

71. Колбаев С.Н., Александрова О.П., Шаронова И.Н., Скребицкий В.Г. Влияние ноопепта на динамику [Ca2+]i в нейронах культивируемых срезов гиппокампа крысы. Бюллетень экспериментальной биологии и медицины 2017; 164(9): 309-313. DOI 10.1007/s10517-018-3983-3. PMID: 29313229.


Ключевые слова

синаптическая пластичность; синапсы Хебба; длительная потенциация; растормаживание; нейропептиды; ноотропы

Полный текст:

PDF

Литература

Hebb O.D. The Organization of Behavior. NY: Wiley, 1949. 335 p.

Brindley G.S. The classification of modifiable synapses and their use in models for conditioning. Proc. Royal Soc Lond B Biol Sci 1967; 168: 361-367. DOI:

1098/rspb.1967.0070.

Gerbrandt L.K., Skrebitsky V.G., Burešová O., Bureš J.Plastic changes of unit activity induced by tactile stimuli followed by electrical stimulation of single hippocampal and reticular neurons. Neuropsychologia 1968; 6: 3-10. DOI. org/10.1016/0028-3932(68)90034-1. DOI: 10.1016/0028-3932(68)90034-1.

Rusinova E.V., Skrebitskii V.G. Vliyanie razryada nejrona na ehffektivnost’ ego sinapticheskikh vkhodov. [The influence of neuronal discharge on the effectiveness of its synaptic inputs]. Zhurnal Vysshey Nervnoy Deiatel’njsti Im I.P. Pavlova 1975; 25(6): 1312-1315. PMID: 1210783. (In Russ.)

Baranyi A., Szente M.B. Long-lasting potentiation of synaptic transmission requires postsynaptic modifications in the neocortex. Brain Res 1987; 423(1-2): 378-384. DOI: 10.1016/0006-8993(87)90867-5. PMID: 2823992.

Skrebitsky V.G., Chepkova A.N. Hebbian synapses in cortical and hippocampal pathways. Rev Neurosci 1998; 9(4): 243-264. DOI: 10.1515/REVNEURO. 1998.9.4.243. PMID: 9886140.

Bliss T.V., Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 1973; 232(2): 331-356. DOI: 10.1113/jphysiol.1973.sp010273. PMID: 4727084.

Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993; 361(6407): 31-39. DOI: 10.1038/361031a0. PMID: 8421494.

Bliss T.V., Collingridge G.L., Morris R.G. Synaptic plasticity in health and disease: introduction and overview. Philos Trans R Soc Lond B Biol Sci 2013; 369(1633): 20130129. DOI: 10.1098/rstb.2013.0129. PMID: 24298133.

Voronin L.L. Long-term potentiation in the hippocampus. Neuroscience 1983; 10(4): 1051-1069. DOI: 10.1016/0306-4522(83)90099-4. PMID: 6141538.

Sastry B.R., Goh J.W., Auyeung A. Associative induction of posttetanic and long-term potentiation in CA1 neurons of rat hippocampus. Science 1986; 232(4753): 988-990. DOI: 10.1126/science.3010459. PMID: 3010459.

Kelso S.R., Ganong A.H., Brown T.H. Hebbian synapses in hippocampus. Proc Natl Acad Sci USA 1986; 83(14): 5326-5330. DOI: 10.1073/pnas.83.14.5326. PMID: 3460096.

Lodge D., Watkins J.C., Bortolotto Z.A., Jane D.E, Volianskis A. The 1980s: D-AP5,LTP and a decade of NMDA receptor discoveries. Neurochem Res 2018. DOI: 10.1007/s11064-018-2640-6. PMID: 30284673.

Morris R.G. NMDA receptors and memory encoding. Neuropharmacology 2013; 74: 32-40. DOI: 10.1016/j.neuropharm.2013.04.014. PMID: 23628345.

Magee J.C., Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 1997; 275(5297):209-213. DOI: 10.1126/science.275.5297.209. PMID: 8985013.

Markram H., Lübke J., Frotscher M., Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 1997; 275(5297): 213-215. DOI: 10.1126/science.275.5297.213. PMID: 8985014.

Bliss T.V., Douglas R.M., Errington M.L., Lynch M.A. Correlation between long-term potentiation and release of endogenous amino acids from dentate gyrus of anaesthetized rats. J Physiol 1986; 377: 391-408. DOI: 10.1113/jphysiol. 1986.sp016193. PMID: 2879038.

Maren S., Tocco G., Standley S., Baudry M., Thompson R.F. Postsynaptic factors in the expression of long-term potentiation (LTP): increased glutamate receptor binding following LTP induction in vivo. Proc Natl Acad Sci USA 1993; 90(20): 9654-9658. DOI: 10.1073/pnas.90.20.9654. PMID: 8415757.

Frey U., Krug M., Reymann K.G., Matthies H. Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 1988; 452 (1-2): 57-65. DOI: 10.1016/0006- 8993(88)90008-X. PMID: 3401749.

Frey U., Huang Y.Y., Kandel E.R. Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 1993; 260 (5114): 1661-1664. DOI: 10.1126/science.8389057. PMID: 8389057.

Mayford M., Siegelbaum S.A., Kandel E.R. Synapses and memory storage. Cold Spring Harb Perspect Biol 2012; 4(6). DOI: 10.1101/cshperspect.a005751. PMID: 2249638.

Danysz W., Zajaczkowski W., Parsons C.G. Modulation of learning processes

by ionotropic glutamate receptor ligands. Behav Pharmacol 1995; 6 (5–6): 455- 474. PMID: 11224354.

Barnes C.A. Involvement of LTP in memory: are we “searching under the street light”? Neuron 1995; 15 (4): 751-754. DOI: 10.1016/0896-6273(95)90166-3. PMID: 7576624.

Mayford M., Abel T., Kandel E.R. Transgenic approaches to cognition. Curr Opin Neurobiol 1995; 5(2): 141-148. DOI: 10.1016/0959-4388(95)80019-0. PMID: 7620300.

Wigström H., Gustafsson B. Large long-lasting potentiation in the dentate gyrus in vitro during blockade of inhibition. Brain Res 1983; 275(1): 153-158. DOI: 10.1016/0006-8993(83)90428-6. PMID: 6313124.

Ormond J., Woodin M.A. Disinhibition mediates a form of hippocampal long-term potentiation in area CA1. PLoS One 2009; 4(9): e7224. DOI: 10.1371/ journal.pone.0007224. PMID: 19787049.

Davies C.H., Collingridge G.L. The physiological regulation of synaptic inhibition by GABAB autoreceptors in rat hippocampus. J Physiol 1993; 472: 245- 265. DOI: 10.1113/jphysiol.1993.sp019945. PMID: 8145143.

Fedorov N.B., Sergeeva O.A., Skrebitsky V.G. Priming stimulation facilitates Hebb-type plasticity in the Schaffer collateral-commissural pathways of the mouse hippocampus. Exp Brain Res 1993; 94(2): 270-272. DOI: 10.1007/ BF00230295. PMID: 8359243.

Vinogradova O.S. Gippokamp i pamyat’ [Hippocampus and memory]. М.: Nauka, 1975. 333 p. (In Russ.)

Larson J., Munkácsy E. Theta-burst LTP. Brain Res 2015; 1621: 38-50. DOI: 10.1016/j.brainres.2014.10.034. PMID: 25452022.

Skrebitsky V.G. Nonspecific influences on neuronal firing in the central visual pathway. Exp Brain Res 1969; 9(4): 269-283. DOI: 10.1007/BF00235239.

PMID: 5364413.

Skrebitsky V.G., Sharonova I.N. Reticular suppression of flash-evoked IPSPs in visual cortex neurons. Brain Res 1976; 111(1): 67-78. DOI: 10.1016/0006- 8993(76)91049-0. PMID: 953705.

Klausberger T., Magill P.J., Márton L.F., Roberts J.D., Cobden P.M., Buzsáki G., Somogyi P. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 2003; 421(6925): 844-848. DOI: 10.1038/nature01374. PMID: 12594513.

Dykes R.W. Mechanisms controlling neuronal plasticity in somatosensory cortex. Can J Physiol Pharmacol 1997; 75(5): 535-545. DOI: 10.1139/y97-089. PMID: 9250389.

Pavlov I.P. Lektsii o rabote bol’shikh polushariy mozga [Lectures on functions of cerebral hemispheres]. Complete collected works. V.4. Мoscow: AN SSSR, 1951. 452 p.

Sara S.J. Noradrenergic modulation of selective attention: its role in memory retrieval. Ann N Y Acad Sci 1985; 444: 178-193. DOI: 10.1111/j.1749-6632.1985. tb37588.x. PMID: 2990290.

Skrebitsky V.G., Chepkova A.N., Sharonova I.N. Reticular suppression of cortical inhibitory postsynaptic potentials. In: Hobson J.A., Brzier M.A. (Eds) Reticular Formation Revisited. NY: Raven Press, 1980: 67-78.

Doze V.A., Cohen G.A., Madison D.V. Synaptic localization of adrenergic disinhibition in the rat hippocampus. Neuron 1991; 6(6): 889-900. DOI: 10.1016/0896-6273(91)90229-S. PMID: 1675862.

Griffith J.S. A theory of the nature of memory. Nature 1966; 211(5054): 1160- 1163. DOI: 10.1038/2111160a0. PMID: 5970018.

Brown T.H., Chapman P.F., Kairiss E.W., Keenan C.L. Long-term synaptic potentiation. Science 1988; 242 (4879): 724-728. DOI: 10.1126/science.2903551. PMID: 2903551.

Solari N., Hangya B. Cholinergic modulation of spatial learning, memory and navigation. Eur J Neurosci 2018; 48(5): 2199-2230. DOI: 10.1111/ejn.14089. PMID: 30055067.

Lin Y.W., Min M.Y., Chiu T.H., Yang H.W. Enhancement of associative longterm

potentiation by activation of beta-adrenergic receptors at CA1 synapses in rat hippocampal slices. J Neurosci. 2003, 23(10): 4173-4181. DOI: 10.1523/ JNEUROSCI.23-10-04173.2003. PMID: 12764105.

O’Dell T.J., Connor S.A., Guglietta R., Nguyen P.V. β-Adrenergic receptor signaling and modulation of long-term potentiation in the mammalian hippocampus. Learn Mem 2015; 22(9): 461-471. DOI: 10.1101/lm.031088.113. PMID: 26286656.

Hansen N., Manahan-Vaughan D. Hippocampal long-term potentiation that is elicited by perforant path stimulation or that occurs in conjunction with spatial learning is tightly controlled by beta-adrenoreceptors and the locus coeruleus. Hippocampus 2015: 25(11): 1285-1298. DOI: 10.1002/hipo.22436. PMID: 25727388.

Takeuchi T., Duszkiewicz A.J., Sonneborn A. et al. Locus coeruleus and dopaminergic

consolidation of everyday memory. Nature 2016; 537: 357-362. DOI: 10.1038/nature19325. PMID: 27602521.

Wei X., Ma T., Cheng Y. et al. Dopamine D1 or D2 receptor-expressing neurons in the central nervous system. Addict Biol 2018; 23(2): 569-584. DOI: 10.1111/adb.12512. PMID: 28436559.

Hammad H., Wagner J.J. Dopamine-mediated disinhibition in the CA1 region of rat hippocampus via D3 receptor activation. J Pharmacol Exp Ther 2006; 316(1):113-120. DOI: 10.1124/jpet.105.091579. PMID: 16162819.

Lemon N., Manahan-Vaughan D. Dopamine D1/D5 receptors gate the acquisition of novel information through hippocampal long-term potentiation and long-term depression. J Neurosci 2006; 26(29): 7723-7729. DOI: 10.1523/ JNEUROSCI.1454-06.2006. PMID: 16855100.

Lin J.S., Anaclet C., Sergeeva O.A., Haas H.L. The waking brain: an update. Cell Mol Life Sci 2011; 68(15): 2499-2512. DOI: 10.1007/s00018-011-0631-8. Review. PMID: 21318261.

Vorobjev V.S, Sharonova I.N., Walsh I.B., Haas H.L. Histamine potentiates N-methyl-D-aspartate responses in acutely isolated hippocampal neurons. Neuron 1993; 11(5): 837-844. DOI: 10.1016/0896-6273(93)90113-6. PMID: 8240807.

Kovacs G.L, De Wied D. Peptidergic modulation of learning and memory processes. Pharmacol Rev 1994; 46(3): 269-291. PMID: 7831381.

Chepkova A.N. Vliyanie vasopressina na svoystva dlitel’noy posttetanicheskoy potentsiatsii v srezakh gippokampa [Effect of vasopressin on the characteristics of prolonged posttetanic potentiation in hippocampal slices]. Zhurnal Vysshey Nervnoy Deiatel’nosti Im I.P. Pavlova 1981; 31(2): 427-430. PMID: 7269796. (In Russ.).

Chepkova A.N., Skrebitskii V.G. Effects of some adrenergic drugs and neuropeptides on long-term potentiation in hippocampal slices. In: Ajmone Marsan C., Matthies H.(eds). Neuronal Plasticity and Memory Formation. NY: Raven Press, 1982: 255-263.

Reijmers L.G., van Ree J.M., Spruijt B.M. et al. Vasopressin metabolites: a link between vasopressin and memory? Prog Brain Res 1998;119: 523-535. DOI: 10.1016/S0079-6123(08)61591-5. PMID: 10074810.

Rong X.W., Chen X.F., Du Y.C. Potentiation of synaptic transmission by neuropeptide AVP4-8 (ZNC(C)PR) in rat hippocampal slices. Neuroreport 1993; 4(9): 1135-1138. PMID: 8219041.

van den Hooff P., Urban I.J., de Wied D. Vasopressin maintains long-term potentiation in rat lateral septum slices. Brain Res 1989; 505(2): 181-186. DOI: 10.1016/0006-8993(89)91440-6. PMID: 2532055.

Chepkova A.N., French P., De Wied D. et al. Long-lasting enhancement of synaptic excitability of CA1/subiculum neurons of the rat ventral hippocampus by vasopressin and vasopressin(4-8). Brain Res 1995; 701(1-2): 255-566. DOI: 10.1016/0006-8993(95)01006-7. PMID: 8925289.

Ishihara K., Katsuki H., Kawabata A. et al. Effects of thyrotropin-releasing hormone and a related analog, CNK-602A, on long-term potentiation in the mossy fiber-CA3 pathway of guinea pig hippocampal slices. Brain Res 1991; 554(1-2): 203-208. DOI: 10.1016/0006-8993(91)90190-7. PMID: 1933301.

Matsuoka N., Kaneko S., Satoh M. Somatostatin augments long-term potentiation of the mossy fiber-CA3 system in guinea-pig hippocampal slices. Brain Res 1991; 553(2): 188-194. DOI: 10.1016/0006-8993(91)90823-E. PMID: 1681981.

Gudasheva Т.А. Teoreticheskiye osnovy i tekhnologii sozdaniya dipeptidnykh lekarstv [Theoretic basis and technologies of creating dipeptide drugs]. Izvestiya akademii nauk. Seriya khimicheskaya 2015; 9: 2012-2021. (In Russ.)

Olpe H.R., Lynch G.S. The action of piracetam on the electrical activity of the hippocampal slice preparation: a field potential analysis. Eur J Pharmacol 1982; 80(4): 415-419. DOI: 10.1016/0014-2999(82)90088-7. PMID: 7106192.

Satoh M., Ishihara K., Katsuki H. Different susceptibilities of long-term potentiations in CA3 and CA1 regions of guinea pig hippocampal slices to nootropic drugs. Neurosci Lett 1988; 93(2-3): 236-241. DOI: 10.1016/0304- 3940(88)90088-2. PMID: 2853846.

Chepkova A.N., Doreuli N.V., Ostrovskaia R.U. et al. Sokhraneniye plasticheskikh svoystv sinapticheskoy peredachi v dolgozhivyshchikh srezakh gipppokampa pod deystviyem peptidnogo analoga piratsetama [Preservation of plastic properties of synaptic transmission in long-lasting hippocampal slices under the effects of a peptide analog of piracetam, L-pGlu-D-Ala-NH2]. Biull Eksp Biol Med 1990; 110(12): 602-604. PMID: 1964611. (In Russ.).

Chepkova A.N., Doreulee N.V., Trofimov S.S. et al. Nootropic compound L-pyroglutamyl-D-alanine-amide restores hippocampal long-term potentiation impaired by exposure to ethanol in rats. Neurosci Lett 1995; 188(3): 163-166. DOI: 10.1016/0304-3940(95)11421-R. PMID: 7609900.

Ostrovskaia R.U., Gudasheva T.A., Voronina T.A., Seredenin S.B. Original’niy nootropniy I neyroprotektivniy dipeptide noopept (GVS-111) [The original novel nootropic and neuroprotective agent noopept]. Eksp Klin Farmakol 2002; 65(5): 66-72. PMID: 12596521. (In Russ.).

Ostrovskaya R.U., Belnik A.P., Storozheva Z.I. [Noopept efficiency in experimental Alzheimer disease (cognitive deficiency caused by beta-amyloid25-35 injection into Meynert basal nuclei of rats)]. Bull Exp Biol Med 2008; 146(1): 77- 80. PMID: 19145356. (In Russ.).

Jia X., Gharibyan A.L., Öhman A. et al. Neuroprotective and nootropic drug noopept rescues α-synuclein amyloid cytotoxicity. J Mol Biol 2011; 414(5): 699- 712. DOI: 10.1016/j.jmb.2011.09.044. PMID: 21986202.

Bochkarev V.К., Teleshova Е.S., Sinyukov S.А. et al. Kliniko-elektroentsefalograficheskaya

kharakteristika deystviya noopepta u bol’nykh s legkimi kognitivnymi rassroystvami posttravmaticheskogo I sosudistogo geneza [Clinical and electroencephalographic characteristic of noopept in patients with mild cognitive impairment of posttraumatic and vascular origin]. Zh Nevrol Psikhiatr Im S S Korsakova 2008; 108(11): 47-54. PMID: 19008801. (In Russ.)

Vakhitova Y.V., Sadovnikov S.V., Borisevich S.S. et al. Molecular mechanism underlying the action of substituted Pro-Gly Dipeptide Noopept. Acta Naturae 2016; 8(1): 82-89. PMID: 27099787.

Kondratenko R.V., Derevyagin V.I., Skrebitsky V.G. Novel nootropic dipeptide Noopept increases inhibitory synaptic transmission in CA1 pyramidal cells. Neurosci Lett 2010; 476(2): 70-73. DOI: 10.1016/j.neulet.2010.04.005. PMID: 20382202.

Колбаев С.Н., Александрова О.П., Шаронова И.Н., Скребицкий В.Г. Vliyanie noopepta na dinamiku [Ca2+]i v neyronakh kul’tiviruemukh srezov gippokampa krysy [Effect of Noopept on dynamics of intracellular calcium in neurons of cultured rat hippocampal slices]. Bull Exp Biol Med 2018; 164(3): 330- 333. DOI: 10.1007/s10517-018-3983-3. PMID: 29313229.




DOI: http://dx.doi.org/10.25692/ACEN.2018.5.8