Українська Русский English

ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2010; 56(6): 3-11

Nonuniform distribution andcontribution of the P- and P/Q-typescalcium channels to short-terminhibitory synaptic plasticity incultured hippocampal neurons

O.P. Mizerna, S.A. Fedulova, N.S. Veselovsky.

    O.O.Bogomoletz Institute of Physiology, National Academyof Sciences of Ukraine, Kyiv


Abstract

In the present study, we investigated the sensitivity of GABAergic short-term plasticity to the selective P- and P/Q-type calcium channels blocker omega-agatoxin-IVA. To block the P-type channels we used 30 nM of this toxin and 200 nM of the toxin was used to block the P/Q channel types. The evoked inhibitory postsynaptic currents (eIPSC) were studied using patch-clamp technique in whole-cell configuration in postsynaptic neuron and local extracellular stimulation of single presynaptic axon by rectangular pulse. The present data show that the contribution of P- and P/Q-types channels to GABAergic synaptic transmission in cultured hippocampal neurons are 30% and 45%, respectively. It was shown that the mediate contribution of the P- and P/Q-types channels to the amplitudes of eIPSC is different to every discovered neuron. It means that distribution of these channels is non-uniform. To study the short-term plasticity of inhibitory synaptic trans­mission, axons of presynaptic neurons were paired-pulse stimu­lated with the interpulse interval of 150 ms. Neurons demon­strated both the depression and facilitation. The application of 30 nM and 200nM of the blocker decreased the depression and increased facilitation to 8% and 11%, respectively. In addition, we found that the mediate contribution of the P- and P/Q-types channels to realization of synaptic transmission after the second stimuli is 4% less compared to that after the first one. Therefore, blocking of both P- and P/Q-types calciumchannels can change the efficiency of synaptic transmission. In this instance it facilitates realization of the transmission via decreased depression or increased facilitation. These results confirm that the P- and P/Q-types calcium channels are involved in regulation of the short-term inhibitory synaptic plasticity in cultured hippocampal neurons.

Keywords: P- and P/Q-types calcium channels, omegaagatoxin-IVA, GABAergic synaptic transmission, short-term plasticity

Full text: (PDF, in Ukrainian)

References

  1. Мізерна О.П., Федулова С.А., Веселовський М.С. Вплив тапсигаргіну на гальмівну синаптичну передачу в культурі нейронів гіпокампа щура// Нейрофизиология/Neurophysiology. - 2007. - 39, №4/5. - P. 374-376.
  2. Мізерна О.П., Федулова С.А., Веселовський М.С. Участь N-типу потенціалкерованих кальцієвих каналів в регуляції пластичності гальмівної синап-тичної передачі між нейронами культури гіпокампа// Фізіол.журн. - 2009. - 55, № 4. - P. 17-23.
  3. Adams M.E., Myers R.A., Imperial J.S., Olivera B.M. Toxityping rat brain calcium channels with omega-tox­ins from spider and cone snail venoms // Biochemistry. -1993. - 32. - P. 12566-12570.
  4. Borst J.G., Sakmann B. Calcium influx and transmitter release in a fast CNS synapse// Nature. - 1996. - 383. -P. 431-434.
  5. Davies C.H., Davies S.N., Collingridge G.L. Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocam­pus// Neuron. - 1990. - 424. - P. 513-531.
  6. Dietrich D., Kirschstein T., Kukley M., von der Pereverzev ABC, Schneider T., Beck H. Functional specialization of presynaptic Cav2.3 Ca2+ channels// Neuron. - 2003. - 39. - P. 483-496.
  7. Doze V.A., Cohen G.A., Madison D.V. Calcium channel involvement in GABAB receptor-mediated inhibition of GABA release in area CA1 of the rat hippocampus// J. Neurophysiol. - 1995. - 74. - P. 43-53.
  8. Dunlap K., Luebke J.I., Turner T.J. Exocytotic Ca2+ channels in mammalian central neurons// Trends Neurisci. - 1995. - 18. - P. 89-98.
  9. 9. Fagg G.E. Foster A.C. Amino acid neurotransmitters and their pathways in the mammalian central nervous system// Neuroscience. - 1983. - 9. - P. 701-719.
  10. 10. Gasparini S, Kasyanov A.M., Pietrobon D., Voronin L.L., Cherubini E. Presynaptic R-type calcium channels contribute to fast excitatory synaptic transmission in the rat hippocampus// J. Neurosci. - 2001. - 21. -P. 8715-8721.
  11. Jensen K., Lambert J.D., Jensen M.S. Activity-depen­dent depression of GABAergic IPSCs in cultured hippocampal neurons// J. Neurophysiol. - 1999. - 82. -P. 42-49.
  12. Katz B. Miledi R. The role of calcium in neuromuscular facilitation// J. Physiol. - 1968. - 195. - P. 481-492.
  13. Liu S., Friel D.D. Impact of the leaner P/Q-type Ca2+ channel mutation on excitatory synaptic transmission in cerebellar Purkinje cells// Ibid. - 2008. - 586. -P. 4501-4515.
  14. Llinas R., Steinberg I.Z., Walton K. Relationship be­tween presynaptic calcium current and postsynaptic potential in squid giant synapse// Biohys.J. - 1981. -33. - P. 323-351.
  15. Llinas R., Sugimori M., Silver R.B. Presynaptic calcium concentration microdomains and transmitter release// J. Physiol. Paris - 1992. - 86. - P. 135-138.
  16. Luebke J.l., Dunlap K., Turner T.J. Multiple calcium channel types control glutamatergic synaptic transmission in the hippocampus// Neuron. -1993. - 11. - P.895-902.
  17. Macdonald R. L., Olsen R. W. GABA receptor channels/ / Annu. Rev. Neurosci. - 1994. - 17. A- P. 569-602.
  18. Mintz I.M. Block of Ca channels in rat central neurons by the spider toxin omega-Aga-IIIA// J. Neurosci. -1994. - 14. - P. 2844-2853.
  19. 19. Mintz I.M., Sabatini B.L., Regehr W.G. Calcium con­trol of transmitter release at a cerebellar synapse// Neuron. - 1995. - 15. - P. 675-688.
  20. 20. Miyazaki K., Ishizuka T., Yawo H. Synapse-to-syn­apse variation of calcium channel subtype contribu­tions in large mossy fiber terminals of mouse hippoc­ampus// Neuroscience. - 2005. - 136. - P. 1003-1014.
  21. Murakami N., Ishibashi H., Katsurabayashi S., Akaike N. Calcium channel subtypes on single GABAergic presynaptic terminal projecting to rat hippocampal neurons// Brain Res. - 2002. - 951. - P. 121-129.
  22. Nathan T., Lambert J.D. Depression of the fast IPSP underlies paired-pulse facilitation in area CA1 of the rat hippocampus// J. Neurophysiol. - 1991. - 66. -P. 1704-1715.
  23. Ohno-Shosaku T., Hirata K., Sawada S., Yamamoto C. Contributions of multiple calcium channel types to GABAergic transmission in rat cultured hippocampal neurons// Neurosci. Lett. - 1994. - 181. - P. 145-148.
  24. Olivera B.M., Miljanich G.P., Ramachandran J., Adams M.E. Calcium channel diversity and neurotransmitter release: the omega-conotoxins and omega-agatoxins// Ann. Rev. Biochem. - 1994. - 63. - P. 823-867.
  25. Regehr W.G., Mintz I.M. Participation of multiple calcium channel types in transmission at single climbing fiber to Purkinje cell synapses// Neuron. - 1994. - 12. -P. 605-613.
  26. Reid C.A., Clements J.D., Bekkers J.M. Nonuniform distribution of Ca2+ channel subtypes on presynaptic terminals of excitatory synapses in hippocampal cultures// J. Neurosci. - 1997. - 15. - P. 2738-2745.
  27. Reid C.A., Bekkers J.M., Clements J.D. N-and P/Q-Type Ca2+ channels mediate transmitter release with a similar cooperativety at rat hippocampal autaps// Ibid. -1998. – 18. – P. 2849–2855.
  28. Reuter H. Measurements of exocytosis from single presynaptic nerve terminals reveal heterogeneous inhibition by Ca(2+)-channel blockers//Neuron. – 1995. – 14. – P. 773–779.
  29. 29. Rosato-Siri M., Grandolfo M., Ballerini L. Activity-dependent modulation of GABAergic synapses in developing rat spinal networks in vitro//Eur. J. Neurosci. – 2002. – 16. – P. 2123–2135.
  30. 30. Schneggenburger R., Neher E. Presynaptic calcium and control of vesicle fusion// Curr. Opin. Neurobiol. – 2005. – 15. – P. 266–274.
  31. Scholz K.P., Miller R.J. Presynaptic inhibition at exci­tatory hippocampal synapses: development and role of presynaptic Ca2+ channels// J. Neurophysiol. – 1996. – 76. – P. 39–46.
  32. Shen K.Z., Zhu Z.T., Munhall A. and Johnson S.W. Synaptic plasticity in rat subthalamic nucleus induced by high-frequency stimulation// Synapse. –2003. – 50. – P. 314–319.
  33. Smith S.J., Buchanan J., Osses L.R., Charlton M.P., Augustine G.J. The spatial distribution of calcium sig­nals in squid presynaptic terminals// J. Physiol. –1993. – 472. – P. 573–593.
  34. Stanley E.F. The calcium channel and the organization of the presynaptic transmitter release face// Trends Neurosci. –1997. – 20. – P.404–409.
  35. Takahashi T., Momiyama A. Different types of calcium channels mediate central synaptic transmission// Na­ture. –1993. – 366. – P.156–158.
  36. Tanabe M., Kaneko T. Paired pulse facilitation of GABAergic IPSCs in ventral horn neurons in neonatal rat spinal cord// Brain Res. –1996. – 716. – P.101–106.
  37. Veselovsky N.S., Engert F., Lux H.D. Fast local superfusion technique// Pflug. Arch. –1996. – 432. – P. 351–354.
  38. Wheeler D.B., Randall A., Tsien R.W. Changes in ac­tion potential duration alter reliance of excitatory syn-aptic transmission on multiple types of Ca2+ channels in rat hippocampus// J. Neurosci. – 1996. – 16. – P. 2226–2237.
  39. 39. Wilcox K.S., Dichter M.A. Paired pulse depression in cultured hippocampal neurons is due to a presynaptic mechanism independent of GABA autoreceptor acti-vation// Ibid. – 1994. – 14. – P. 17B75–1788.
  40. 40. Wu L.G., Saggau P. Pharmacological identification of two types of presynaptic voltage-dependent calcium channels at CA3-CA1 synapses of the hippocampus// Ibid. – P. 5613–5622.
  41. Wu L.G., Saggau P. Block of multiple presynaptic calcium channel types by omega-conotoxin-MVIIC at hippocampal CA3 to CA1 synapses// J. Neurophysiol. – 1995. – 73. – P. 1965–1972.
  42. Wu L.G., Borst J.G., Sakmann B. R-type Ca2+ currents evoke transmitter release at a rat central synapse// Proc. Natl. Acad. Sci. USA. – 1998. – 95. – P. 4720–4727.
  43. Wu L.G., Borst J.G. The reduced release probability of releasable vesicles during recovery from short-term synaptic depression// Neuron. – 1999. – 23. – P. 821–832.
  44. Xu J., He L., Wu L.G. Role of Ca(2+) channels in short-term synaptic plasticity// Curr. Opin. Neurobiol. – 2007. – 17. – P. 352–359.
  45. Zucker R.S., Regehr W.G. Short-term synaptic plas-ticity// Annu. Rev. Physiol. – 2002. – 64. – P. 355–405.
© National Academy of Sciences of Ukraine, Bogomoletz Institute of Physiology, 2014-2019.