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. 1993 Aug 1;90(15):7114–7118. doi: 10.1073/pnas.90.15.7114

Reduced Mg2+ block of N-methyl-D-aspartate receptor-mediated synaptic potentials in developing visual cortex.

N Kato 1, H Yoshimura 1
PMCID: PMC47086  PMID: 8394010

Abstract

Molecular cloning has demonstrated a diversity of artificially expressed N-methyl-D-aspartate (NMDA) receptors, implying a similar diversity of naturally occurring NMDA receptors in situ. Particularly significant was the success in expression of NMDA receptor classes exhibiting various sensitivities to Mg2+ block, a voltage-dependent channel blockade by Mg2+ that is essential to NMDA receptor functioning. Release from Mg2+ block often allows or facilitates the occurrence of long-term potentiation, a form of synaptic plasticity. Here we show that in the immature visual cortex, which is more susceptible to long-term potentiation than adult visual cortex, synaptically activated NMDA receptors, unlike those in the adult, have varying but clearly reduced sensitivities to Mg2+ block. We propose that the initially expressed, later-eliminated NMDA receptors exhibiting a reduced Mg2+ block may underlie the greater susceptibility to plasticity in the immature neocortex.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Artola A., Singer W. The Involvement of N-Methyl-D-Aspartate Receptors in Induction and Maintenance of Long-Term Potentiation in Rat Visual Cortex. Eur J Neurosci. 1990;2(3):254–269. doi: 10.1111/j.1460-9568.1990.tb00417.x. [DOI] [PubMed] [Google Scholar]
  2. Ben-Ari Y., Cherubini E., Krnjevic K. Changes in voltage dependence of NMDA currents during development. Neurosci Lett. 1988 Nov 22;94(1-2):88–92. doi: 10.1016/0304-3940(88)90275-3. [DOI] [PubMed] [Google Scholar]
  3. Bowe M. A., Nadler J. V. Developmental increase in the sensitivity to magnesium of NMDA receptors on CA1 hippocampal pyramidal cells. Brain Res Dev Brain Res. 1990 Oct 1;56(1):55–61. doi: 10.1016/0165-3806(90)90164-t. [DOI] [PubMed] [Google Scholar]
  4. Burnashev N., Schoepfer R., Monyer H., Ruppersberg J. P., Günther W., Seeburg P. H., Sakmann B. Control by asparagine residues of calcium permeability and magnesium blockade in the NMDA receptor. Science. 1992 Sep 4;257(5075):1415–1419. doi: 10.1126/science.1382314. [DOI] [PubMed] [Google Scholar]
  5. Carmignoto G., Vicini S. Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science. 1992 Nov 6;258(5084):1007–1011. doi: 10.1126/science.1279803. [DOI] [PubMed] [Google Scholar]
  6. Chen L., Huang L. Y. Protein kinase C reduces Mg2+ block of NMDA-receptor channels as a mechanism of modulation. Nature. 1992 Apr 9;356(6369):521–523. doi: 10.1038/356521a0. [DOI] [PubMed] [Google Scholar]
  7. Collingridge G. L., Singer W. Excitatory amino acid receptors and synaptic plasticity. Trends Pharmacol Sci. 1990 Jul;11(7):290–296. doi: 10.1016/0165-6147(90)90011-v. [DOI] [PubMed] [Google Scholar]
  8. Connors B. W., Prince D. A. Effects of local anesthetic QX-314 on the membrane properties of hippocampal pyramidal neurons. J Pharmacol Exp Ther. 1982 Mar;220(3):476–481. [PubMed] [Google Scholar]
  9. Davies S. N., Collingridge G. L. Role of excitatory amino acid receptors in synaptic transmission in area CA1 of rat hippocampus. Proc R Soc Lond B Biol Sci. 1989 May 22;236(1285):373–384. doi: 10.1098/rspb.1989.0028. [DOI] [PubMed] [Google Scholar]
  10. Gustafsson B., Wigström H., Abraham W. C., Huang Y. Y. Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials. J Neurosci. 1987 Mar;7(3):774–780. doi: 10.1523/JNEUROSCI.07-03-00774.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hestrin S. Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature. 1992 Jun 25;357(6380):686–689. doi: 10.1038/357686a0. [DOI] [PubMed] [Google Scholar]
  12. Hestrin S., Nicoll R. A., Perkel D. J., Sah P. Analysis of excitatory synaptic action in pyramidal cells using whole-cell recording from rat hippocampal slices. J Physiol. 1990 Mar;422:203–225. doi: 10.1113/jphysiol.1990.sp017980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jones K. A., Baughman R. W. NMDA- and non-NMDA-receptor components of excitatory synaptic potentials recorded from cells in layer V of rat visual cortex. J Neurosci. 1988 Sep;8(9):3522–3534. doi: 10.1523/JNEUROSCI.08-09-03522.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kato N., Artola A., Singer W. Developmental changes in the susceptibility to long-term potentiation of neurones in rat visual cortex slices. Brain Res Dev Brain Res. 1991 May 20;60(1):43–50. doi: 10.1016/0165-3806(91)90153-a. [DOI] [PubMed] [Google Scholar]
  15. Kim Y. I., Dudek F. E. Intracellular electrophysiological study of suprachiasmatic nucleus neurons in rodents: excitatory synaptic mechanisms. J Physiol. 1991 Dec;444:269–287. doi: 10.1113/jphysiol.1991.sp018877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kutsuwada T., Kashiwabuchi N., Mori H., Sakimura K., Kushiya E., Araki K., Meguro H., Masaki H., Kumanishi T., Arakawa M. Molecular diversity of the NMDA receptor channel. Nature. 1992 Jul 2;358(6381):36–41. doi: 10.1038/358036a0. [DOI] [PubMed] [Google Scholar]
  17. LoTurco J. J., Blanton M. G., Kriegstein A. R. Initial expression and endogenous activation of NMDA channels in early neocortical development. J Neurosci. 1991 Mar;11(3):792–799. doi: 10.1523/JNEUROSCI.11-03-00792.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mayer M. L., Westbrook G. L. A voltage-clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurones. J Physiol. 1983 Jul;340:19–45. doi: 10.1113/jphysiol.1983.sp014747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mayer M. L., Westbrook G. L., Guthrie P. B. Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature. 1984 May 17;309(5965):261–263. doi: 10.1038/309261a0. [DOI] [PubMed] [Google Scholar]
  20. McCormick D. A., Prince D. A. Post-natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. J Physiol. 1987 Dec;393:743–762. doi: 10.1113/jphysiol.1987.sp016851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. McDonald J. W., Silverstein F. S., Johnston M. V. Neurotoxicity of N-methyl-D-aspartate is markedly enhanced in developing rat central nervous system. Brain Res. 1988 Aug 30;459(1):200–203. doi: 10.1016/0006-8993(88)90306-x. [DOI] [PubMed] [Google Scholar]
  22. Miller B., Sarantis M., Traynelis S. F., Attwell D. Potentiation of NMDA receptor currents by arachidonic acid. Nature. 1992 Feb 20;355(6362):722–725. doi: 10.1038/355722a0. [DOI] [PubMed] [Google Scholar]
  23. Mishina M., Takai T., Imoto K., Noda M., Takahashi T., Numa S., Methfessel C., Sakmann B. Molecular distinction between fetal and adult forms of muscle acetylcholine receptor. Nature. 1986 May 22;321(6068):406–411. doi: 10.1038/321406a0. [DOI] [PubMed] [Google Scholar]
  24. Monyer H., Sprengel R., Schoepfer R., Herb A., Higuchi M., Lomeli H., Burnashev N., Sakmann B., Seeburg P. H. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science. 1992 May 22;256(5060):1217–1221. doi: 10.1126/science.256.5060.1217. [DOI] [PubMed] [Google Scholar]
  25. Mori H., Masaki H., Yamakura T., Mishina M. Identification by mutagenesis of a Mg(2+)-block site of the NMDA receptor channel. Nature. 1992 Aug 20;358(6388):673–675. doi: 10.1038/358673a0. [DOI] [PubMed] [Google Scholar]
  26. Morrisett R. A., Mott D. D., Lewis D. V., Wilson W. A., Swartzwelder H. S. Reduced sensitivity of the N-methyl-D-aspartate component of synaptic transmission to magnesium in hippocampal slices from immature rats. Brain Res Dev Brain Res. 1990 Nov 1;56(2):257–262. doi: 10.1016/0165-3806(90)90090-l. [DOI] [PubMed] [Google Scholar]
  27. Movshon J. A., Van Sluyters R. C. Visual neural development. Annu Rev Psychol. 1981;32:477–522. doi: 10.1146/annurev.ps.32.020181.002401. [DOI] [PubMed] [Google Scholar]
  28. Nakanishi S. Molecular diversity of glutamate receptors and implications for brain function. Science. 1992 Oct 23;258(5082):597–603. doi: 10.1126/science.1329206. [DOI] [PubMed] [Google Scholar]
  29. Nowak L., Bregestovski P., Ascher P., Herbet A., Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature. 1984 Feb 2;307(5950):462–465. doi: 10.1038/307462a0. [DOI] [PubMed] [Google Scholar]
  30. Perkins A. T., 4th, Teyler T. J. A critical period for long-term potentiation in the developing rat visual cortex. Brain Res. 1988 Jan 26;439(1-2):222–229. doi: 10.1016/0006-8993(88)91478-3. [DOI] [PubMed] [Google Scholar]
  31. Peterson C., Neal J. H., Cotman C. W. Development of N-methyl-D-aspartate excitotoxicity in cultured hippocampal neurons. Brain Res Dev Brain Res. 1989 Aug 1;48(2):187–195. doi: 10.1016/0165-3806(89)90075-8. [DOI] [PubMed] [Google Scholar]
  32. Takahashi T., Momiyama A., Hirai K., Hishinuma F., Akagi H. Functional correlation of fetal and adult forms of glycine receptors with developmental changes in inhibitory synaptic receptor channels. Neuron. 1992 Dec;9(6):1155–1161. doi: 10.1016/0896-6273(92)90073-m. [DOI] [PubMed] [Google Scholar]

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