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. 1993 Feb;108(2):422–430. doi: 10.1111/j.1476-5381.1993.tb12820.x

Actions of agonists of metabotropic glutamate receptors on synaptic transmission and transmitter release in the olfactory cortex.

G G Collins 1
PMCID: PMC1907988  PMID: 7680593

Abstract

1. The effects of agonists of metabotropic glutamate receptors on the evoked N-wave complex in slices of mouse olfactory cortex have been studied: most experiments were carried out using slices perfused with Mg(2+)-free solution to which 10 microM of either 6,7-dinitroquinoxaline-2,3-dione or 6-cyano-7-nitroquinoxaline-2,3-dione was applied. 2. Following agonist washout, a slowly developing, long lasting potentiation of the complex occurred which was confined to the N-methyl-D-aspartate (NMDA) receptor-mediated component of the potential. The relative agonist potencies were 1S,3R-1-aminocyclopentane-1,3-dicarboxylic acid (1S,3R-ACPD, 5-250 microM) = quisqualate (5-50 microM) > 1RS,3RS-cis-1-aminocyclopentane-1,3-dicarboxylic acid (ACPD, 25-1000 microM) > L-glutamate (0.25-2.5 mM); NMDA, alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionate (AMPA) and L-aspartate were inactive. 3. Potentiation of the NMDA receptor-mediated component by 1S,3R-ACPD (0.1 mM) was non-competitively antagonised by S-(+)- but not R-(-)-2-amino-3-phosphonopropionate (AP3, 0.125 mM), equally by D-(-) and L-(+)-2-amino-4-phosphonobutyrate (0.25 mM) and also by the protein kinase C inhibitors sphingosine, (25 microM), sangivamycin (25 microM) and 5-(isoquinolinylsulphonyl)-3-methylpiperazine (50 microM). 4. In a series of input-output experiments, 1S,3R-ACPD (0.1 mM) reversibly reduced the latency to peak of the NMDA receptor-mediated component at submaximal stimulus intensities, an effect blocked by S-(+)-AP3 (0.125 mM).(ABSTRACT TRUNCATED AT 250 WORDS)

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Selected References

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

  1. Aniksztejn L., Bregestovski P., Ben-Ari Y. Selective activation of quisqualate metabotropic receptor potentiates NMDA but not AMPA responses. Eur J Pharmacol. 1991 Dec 3;205(3):327–328. doi: 10.1016/0014-2999(91)90921-c. [DOI] [PubMed] [Google Scholar]
  2. Anson J., Collins G. G. Possible presynaptic actions of 2-amino-4-phosphonobutyrate in rat olfactory cortex. Br J Pharmacol. 1987 Aug;91(4):753–761. doi: 10.1111/j.1476-5381.1987.tb11273.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aramori I., Nakanishi S. Signal transduction and pharmacological characteristics of a metabotropic glutamate receptor, mGluR1, in transfected CHO cells. Neuron. 1992 Apr;8(4):757–765. doi: 10.1016/0896-6273(92)90096-v. [DOI] [PubMed] [Google Scholar]
  4. Baird J. G., Challiss R. A., Nahorski S. R. Role for ionotropic and metabotropic receptors in quisqualate-stimulated inositol polyphosphate accumulation in rat cerebral cortex. Mol Pharmacol. 1991 Jun;39(6):745–753. [PubMed] [Google Scholar]
  5. Baskys A., Malenka R. C. Agonists at metabotropic glutamate receptors presynaptically inhibit EPSCs in neonatal rat hippocampus. J Physiol. 1991 Dec;444:687–701. doi: 10.1113/jphysiol.1991.sp018901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Birch P. J., Grossman C. J., Hayes A. G. 6,7-Dinitro-quinoxaline-2,3-dion and 6-nitro,7-cyano-quinoxaline-2,3-dion antagonise responses to NMDA in the rat spinal cord via an action at the strychnine-insensitive glycine receptor. Eur J Pharmacol. 1988 Oct 26;156(1):177–180. doi: 10.1016/0014-2999(88)90163-x. [DOI] [PubMed] [Google Scholar]
  7. Brown D. A., Galvan M. Responses of the guinea-pig isolated olfactory cortex slice to gamma-aminobutyric acid recorded with extracellular electrodes. Br J Pharmacol. 1979 Feb;65(2):347–353. doi: 10.1111/j.1476-5381.1979.tb07836.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Castagna M., Takai Y., Kaibuchi K., Sano K., Kikkawa U., Nishizuka Y. Direct activation of calcium-activated, phospholipid-dependent protein kinase by tumor-promoting phorbol esters. J Biol Chem. 1982 Jul 10;257(13):7847–7851. [PubMed] [Google Scholar]
  9. Challiss R. A., Batty I. H., Nahorski S. R. Mass measurements of inositol(1,4,5)trisphosphate in rat cerebral cortex slices using a radioreceptor assay: effects of neurotransmitters and depolarization. Biochem Biophys Res Commun. 1988 Dec 15;157(2):684–691. doi: 10.1016/s0006-291x(88)80304-8. [DOI] [PubMed] [Google Scholar]
  10. Charpak S., Gähwiler B. H., Do K. Q., Knöpfel T. Potassium conductances in hippocampal neurons blocked by excitatory amino-acid transmitters. Nature. 1990 Oct 25;347(6295):765–767. doi: 10.1038/347765a0. [DOI] [PubMed] [Google Scholar]
  11. Clark R. M., Collins G. G. The release of endogenous amino acids from the rat visual cortex. J Physiol. 1976 Nov;262(2):383–400. doi: 10.1113/jphysiol.1976.sp011600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Collingridge G. L., Lester R. A. Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacol Rev. 1989 Jun;41(2):143–210. [PubMed] [Google Scholar]
  13. Collins G. G. Pharmacological evidence that NMDA receptors contribute to mono- and di-synaptic potentials in slices of mouse olfactory cortex. Neuropharmacology. 1991 Jun;30(6):547–555. doi: 10.1016/0028-3908(91)90072-j. [DOI] [PubMed] [Google Scholar]
  14. Collins G. G., Richards W. J. Pharmacological evidence that protein kinase C modulates monosynaptic excitations in the olfactory cortex. Naunyn Schmiedebergs Arch Pharmacol. 1990 Jan-Feb;341(1-2):114–122. doi: 10.1007/BF00195067. [DOI] [PubMed] [Google Scholar]
  15. Collins G. G., Surtees L. "Desensitization" of excitatory amino acid responses in the rat olfactory cortex. Neuropharmacology. 1986 Mar;25(3):231–240. doi: 10.1016/0028-3908(86)90245-5. [DOI] [PubMed] [Google Scholar]
  16. Crepel F., Daniel H., Hemart N., Jaillard D. Effects of ACPD and AP3 on parallel-fibre-mediated EPSPs of Purkinje cells in cerebellar slices in vitro. Exp Brain Res. 1991;86(2):402–406. doi: 10.1007/BF00228964. [DOI] [PubMed] [Google Scholar]
  17. Desai M. A., Conn P. J. Excitatory effects of ACPD receptor activation in the hippocampus are mediated by direct effects on pyramidal cells and blockade of synaptic inhibition. J Neurophysiol. 1991 Jul;66(1):40–52. doi: 10.1152/jn.1991.66.1.40. [DOI] [PubMed] [Google Scholar]
  18. Gilbey M. P., Wooster M. J. Mono-and multi-synaptic origin of the early surface-negative wave recorded from guinea-pig olfactory cortex in vitro. J Physiol. 1979 Aug;293:153–172. doi: 10.1113/jphysiol.1979.sp012883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Haberly L. B., Bower J. M. Olfactory cortex: model circuit for study of associative memory? Trends Neurosci. 1989 Jul;12(7):258–264. doi: 10.1016/0166-2236(89)90025-8. [DOI] [PubMed] [Google Scholar]
  20. Hidaka H., Inagaki M., Kawamoto S., Sasaki Y. Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry. 1984 Oct 9;23(21):5036–5041. doi: 10.1021/bi00316a032. [DOI] [PubMed] [Google Scholar]
  21. Hu G. Y., Storm J. F. Excitatory amino acids acting on metabotropic glutamate receptors broaden the action potential in hippocampal neurons. Brain Res. 1991 Dec 24;568(1-2):339–344. doi: 10.1016/0006-8993(91)91423-x. [DOI] [PubMed] [Google Scholar]
  22. Irving A. J., Schofield J. G., Watkins J. C., Sunter D. C., Collingridge G. L. 1S,3R-ACPD stimulates and L-AP3 blocks Ca2+ mobilization in rat cerebellar neurons. Eur J Pharmacol. 1990 Sep 21;186(2-3):363–365. doi: 10.1016/0014-2999(90)90462-f. [DOI] [PubMed] [Google Scholar]
  23. Johnson J. W., Ascher P. Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature. 1987 Feb 5;325(6104):529–531. doi: 10.1038/325529a0. [DOI] [PubMed] [Google Scholar]
  24. Kanter E. D., Haberly L. B. NMDA-dependent induction of long-term potentiation in afferent and association fiber systems of piriform cortex in vitro. Brain Res. 1990 Aug 13;525(1):175–179. doi: 10.1016/0006-8993(90)91337-g. [DOI] [PubMed] [Google Scholar]
  25. Kemp J. A., Foster A. C., Leeson P. D., Priestley T., Tridgett R., Iversen L. L., Woodruff G. N. 7-Chlorokynurenic acid is a selective antagonist at the glycine modulatory site of the N-methyl-D-aspartate receptor complex. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6547–6550. doi: 10.1073/pnas.85.17.6547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kinney G. A., Slater N. T. Potentiation of mossy fiber-evoked EPSPs in turtle cerebellar Purkinje cells by the metabotropic glutamate receptor agonist 1S,3R-ACPD. J Neurophysiol. 1992 Apr;67(4):1006–1008. doi: 10.1152/jn.1992.67.4.1006. [DOI] [PubMed] [Google Scholar]
  27. Loomis C. R., Bell R. M. Sangivamycin, a nucleoside analogue, is a potent inhibitor of protein kinase C. J Biol Chem. 1988 Feb 5;263(4):1682–1692. [PubMed] [Google Scholar]
  28. Lovinger D. M. Trans-1-aminocyclopentane-1,3-dicarboxylic acid (t-ACPD) decreases synaptic excitation in rat striatal slices through a presynaptic action. Neurosci Lett. 1991 Aug 5;129(1):17–21. doi: 10.1016/0304-3940(91)90710-b. [DOI] [PubMed] [Google Scholar]
  29. Manzoni O. J., Finiels-Marlier F., Sassetti I., Blockaert J., le Peuch C., Sladeczek F. A. The glutamate receptor of the Qp-type activates protein kinase C and is regulated by protein kinase C. Neurosci Lett. 1990 Feb 5;109(1-2):146–151. doi: 10.1016/0304-3940(90)90553-l. [DOI] [PubMed] [Google Scholar]
  30. Mayer M. L., Westbrook G. L. The physiology of excitatory amino acids in the vertebrate central nervous system. Prog Neurobiol. 1987;28(3):197–276. doi: 10.1016/0301-0082(87)90011-6. [DOI] [PubMed] [Google Scholar]
  31. McBain C. J., Kleckner N. W., Wyrick S., Dingledine R. Structural requirements for activation of the glycine coagonist site of N-methyl-D-aspartate receptors expressed in Xenopus oocytes. Mol Pharmacol. 1989 Oct;36(4):556–565. [PubMed] [Google Scholar]
  32. McGuinness N., Anwyl R., Rowan M. The effects of trans-ACPD on long-term potentiation in the rat hippocampal slice. Neuroreport. 1991 Nov;2(11):688–690. doi: 10.1097/00001756-199111000-00014. [DOI] [PubMed] [Google Scholar]
  33. McGuinness N., Anwyl R., Rowan M. Trans-ACPD enhances long-term potentiation in the hippocampus. Eur J Pharmacol. 1991 May 17;197(2-3):231–232. doi: 10.1016/0014-2999(91)90529-y. [DOI] [PubMed] [Google Scholar]
  34. Monaghan D. T., Bridges R. J., Cotman C. W. The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. Annu Rev Pharmacol Toxicol. 1989;29:365–402. doi: 10.1146/annurev.pa.29.040189.002053. [DOI] [PubMed] [Google Scholar]
  35. Murphy S. N., Miller R. J. A glutamate receptor regulates Ca2+ mobilization in hippocampal neurons. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8737–8741. doi: 10.1073/pnas.85.22.8737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Murphy S. N., Miller R. J. Two distinct quisqualate receptors regulate Ca2+ homeostasis in hippocampal neurons in vitro. Mol Pharmacol. 1989 May;35(5):671–680. [PubMed] [Google Scholar]
  37. 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]
  38. Otani S., Ben-Ari Y. Metabotropic receptor-mediated long-term potentiation in rat hippocampal slices. Eur J Pharmacol. 1991 Dec 3;205(3):325–326. doi: 10.1016/0014-2999(91)90920-l. [DOI] [PubMed] [Google Scholar]
  39. Pickles H. G., Simmonds M. A. Field potentials, inhibition and the effect of pentobarbitone in the rat olfactory cortex slice. J Physiol. 1978 Feb;275:135–148. doi: 10.1113/jphysiol.1978.sp012181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Pickles H. G., Simmonds M. A. Possible presynaptic inhibition in rat olfactory cortex. J Physiol. 1976 Sep;260(2):475–486. doi: 10.1113/jphysiol.1976.sp011526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Poncet M. F., Damase-Michel C., Tavernier G., Tran M. A., Berlan M., Montastruc J. L., Montastruc P. Changes in plasma catecholamine and neuropeptide Y levels after sympathetic activation in dogs. Br J Pharmacol. 1992 Jan;105(1):181–183. doi: 10.1111/j.1476-5381.1992.tb14232.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Schoepp D. D., Johnson B. G., Smith E. C., McQuaid L. A. Stereoselectivity and mode of inhibition of phosphoinositide-coupled excitatory amino acid receptors by 2-amino-3-phosphonopropionic acid. Mol Pharmacol. 1990 Aug;38(2):222–228. [PubMed] [Google Scholar]
  43. Schoepp D. D., Johnson B. G., True R. A., Monn J. A. Comparison of (1S,3R)-1-aminocyclopentane-1,3-dicarboxylic acid (1S,3R-ACPD)- and 1R,3S-ACPD-stimulated brain phosphoinositide hydrolysis. Eur J Pharmacol. 1991 Aug 14;207(4):351–353. doi: 10.1016/0922-4106(91)90010-f. [DOI] [PubMed] [Google Scholar]
  44. Schoepp D., Bockaert J., Sladeczek F. Pharmacological and functional characteristics of metabotropic excitatory amino acid receptors. Trends Pharmacol Sci. 1990 Dec;11(12):508–515. doi: 10.1016/0165-6147(90)90052-a. [DOI] [PubMed] [Google Scholar]
  45. Sladeczek F., Pin J. P., Récasens M., Bockaert J., Weiss S. Glutamate stimulates inositol phosphate formation in striatal neurones. Nature. 1985 Oct 24;317(6039):717–719. doi: 10.1038/317717a0. [DOI] [PubMed] [Google Scholar]
  46. Sladeczek F., Récasens M., Bockaert J. A new mechanism for glutamate receptor action: phosphoinositide hydrolysis. Trends Neurosci. 1988 Dec;11(12):545–549. doi: 10.1016/0166-2236(88)90183-x. [DOI] [PubMed] [Google Scholar]
  47. Stratton K. R., Worley P. F., Baraban J. M. Excitation of hippocampal neurons by stimulation of glutamate Qp receptors. Eur J Pharmacol. 1989 Dec 7;173(2-3):235–237. doi: 10.1016/0014-2999(89)90529-3. [DOI] [PubMed] [Google Scholar]
  48. Stratton K. R., Worley P. F., Baraban J. M. Pharmacological characterization of phosphoinositide-linked glutamate receptor excitation of hippocampal neurons. Eur J Pharmacol. 1990 Sep 21;186(2-3):357–361. doi: 10.1016/0014-2999(90)90461-e. [DOI] [PubMed] [Google Scholar]
  49. Sugiyama H., Ito I., Hirono C. A new type of glutamate receptor linked to inositol phospholipid metabolism. Nature. 1987 Feb 5;325(6104):531–533. doi: 10.1038/325531a0. [DOI] [PubMed] [Google Scholar]
  50. Zheng F., Gallagher J. P. Metabotropic glutamate receptors are required for the induction of long-term potentiation. Neuron. 1992 Jul;9(1):163–172. doi: 10.1016/0896-6273(92)90231-2. [DOI] [PubMed] [Google Scholar]

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