Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1985 May;362:51–67. doi: 10.1113/jphysiol.1985.sp015662

Effect of excitatory amino acids on gamma-aminobutyric acid release from frog horizontal cells.

J R Cunningham, M J Neal
PMCID: PMC1192881  PMID: 3874955

Abstract

The effects of excitatory amino acids, analogues and K on [3H]gamma-aminobutyric acid [3H]GABA) release from horizontal cells of the isolated superfused frog retina were studied. Exposure of the retina to medium containing high concentrations (25-100 mM) of KCl increased the release of [3H]GABA to a maximum which was 40 times the spontaneous resting release. The K-evoked release of [3H]GABA was almost abolished in high-Mg/low-Ca medium. Glutamate, aspartate, kainate and quisqualate also stimulated the release of [3H]GABA from horizontal cells, the maximum evoked release being similar to that produced by KCl. The release of [3H]GABA evoked by glutamate, aspartate, kainate and quisqualate was abolished in high-Mg/low-Ca medium and by Na-free medium. The evoked releases of [3H]GABA were not reduced by tetrodotoxin. N-Methyl-D-aspartate (NMDA) at concentrations up to 10 mM had virtually no effect on [3H]GABA release from horizontal cells. In Mg-free medium, NMDA stimulated [3H]GABA release, but the maximum release was only 10% of that produced by other agonists. Mg-free medium did not significantly affect the evoked release of [3H]GABA by other agonists. NMDA apparently possessed affinity for the kainate receptor, because in normal medium it antagonized the effects of kainate but not glutamate, aspartate or quisqualate. The non-selective antagonist of excitatory amino acids, (+/-)-cis-2,3-piperidine dicarboxylic acid (PDA) antagonized the action of glutamate, aspartate, kainate and quisqualate on horizontal cell [3H]GABA release. D(-)-2-Amino-4-phosphonobutyrate (APB) and D-gamma-glutamylglycine (D-gamma-GG) antagonized the actions of kainate on horizontal cell [3H]GABA release at concentrations which had little affect on quisqualate-evoked responses. Approximate estimates of pA2 values (Schild, 1947) showed that the specificity and potency of the antagonists was low. Nevertheless, the retinal 'non-NMDA' receptors can probably be subdivided into kainate and quisqualate types. Glutamate diethylester (GDEE) did not affect the action of any agonist. We conclude that glutamate (and aspartate) probably stimulate the release of [3H]GABA from frog horizontal cells by activating receptors of the non-NMDA type. This activation may trigger the opening of tetrodotoxin-insensitive Na channels, resulting in the depolarization of the cell membrane and an increase in the conductance of voltage-sensitive Ca-channels. An influx of Ca ions would then trigger the release of [3H]GABA. Our results are not consistent with previous suggestions that GABA release from horizontal cells involves an outwardly directed transport process.

Full text

PDF
51

Selected References

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

  1. Ames A., 3rd, Tsukada Y., Nesbett F. B. Intracellular Cl-, Na+, K+, Ca2+, Mg2+, and P in nervous tissue; response to glutamate and to changes in extracellular calcium. J Neurochem. 1967 Feb;14(2):145–159. doi: 10.1111/j.1471-4159.1967.tb05887.x. [DOI] [PubMed] [Google Scholar]
  2. Ault B., Evans R. H., Francis A. A., Oakes D. J., Watkins J. C. Selective depression of excitatory amino acid induced depolarizations by magnesium ions in isolated spinal cord preparations. J Physiol. 1980 Oct;307:413–428. doi: 10.1113/jphysiol.1980.sp013443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cervetto L., MacNichol E. F., Jr Inactivation of horizontal cells in turtle retina by glutamate and aspartate. Science. 1972 Nov 17;178(4062):767–768. doi: 10.1126/science.178.4062.767. [DOI] [PubMed] [Google Scholar]
  4. Cunningham J., Neal M. J. On the mechanism by which veratridine causes a calcium-independent release of gamma-aminobutyric acid from brain slices. Br J Pharmacol. 1981 Jul;73(3):655–667. doi: 10.1111/j.1476-5381.1981.tb16801.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Davies J., Evans R. H., Jones A. W., Smith D. A., Watkins J. C. Differential activation and blockade of excitatory amino acid receptors in the mammalian and amphibian central nervous systems. Comp Biochem Physiol C. 1982;72(2):211–224. doi: 10.1016/0306-4492(82)90086-7. [DOI] [PubMed] [Google Scholar]
  6. Dowling J. E., Ripps H. Adaptation in skate photoreceptors. J Gen Physiol. 1972 Dec;60(6):698–719. doi: 10.1085/jgp.60.6.698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Goodchild M., Neal M. J. The uptake of 3Hp -aminobutyric acid by the retina. Br J Pharmacol. 1973 Mar;47(3):529–542. doi: 10.1111/j.1476-5381.1973.tb08184.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ishida A. T., Fain G. L. D-aspartate potentiates the effects of L-glutamate on horizontal cells in goldfish retina. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5890–5894. doi: 10.1073/pnas.78.9.5890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ishida A. T., Kaneko A., Tachibana M. Responses of solitary retinal horizontal cells from Carassius auratus to L-glutamate and related amino acids. J Physiol. 1984 Mar;348:255–270. doi: 10.1113/jphysiol.1984.sp015108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ishida A. T., Kaneko A., Tachibana M. Solitary horizontal cells in culture--II. A new tool for examining effects of photoreceptor neurotransmitter candidates. Vision Res. 1983;23(11):1217–1220. doi: 10.1016/0042-6989(83)90096-2. [DOI] [PubMed] [Google Scholar]
  11. Lam D. M., Ayoub G. S. Biochemical and biophysical studies of isolated horizontal cells from the teleost retina. Vision Res. 1983;23(4):433–444. doi: 10.1016/0042-6989(83)90090-1. [DOI] [PubMed] [Google Scholar]
  12. Lam D. M. Biosynthesis of gamma-aminobutyric acid by isolated axons of cone horizontal cells in the goldfish retina. Nature. 1975 Mar 27;254(5498):345–347. doi: 10.1038/254345a0. [DOI] [PubMed] [Google Scholar]
  13. Lam D. M., Lasater E. M., Naka K. I. gamma-Aminobutyric acid: a neurotransmitter candidate for cone horizontal cells of the catfish retina. Proc Natl Acad Sci U S A. 1978 Dec;75(12):6310–6313. doi: 10.1073/pnas.75.12.6310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lasater E. M., Dowling J. E. Carp horizontal cells in culture respond selectively to L-glutamate and its agonists. Proc Natl Acad Sci U S A. 1982 Feb;79(3):936–940. doi: 10.1073/pnas.79.3.936. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Marc R. E., Stell W. K., Bok D., Lam D. M. GABA-ergic pathways in the goldfish retina. J Comp Neurol. 1978 Nov 15;182(2):221–244. doi: 10.1002/cne.901820204. [DOI] [PubMed] [Google Scholar]
  16. Marshall J., Voaden M. An autoradiographic study of the cells accumulating 3H gamma-aminobutyric acid in the isolated retinas of pigeons and chickens. Invest Ophthalmol. 1974 Aug;13(8):602–607. [PubMed] [Google Scholar]
  17. Marshall J., Voaden M. Autoradiographic identification of the cells accumulating 3H gamma-aminobutyric acid in mammalian retinae: a species comparison. Vision Res. 1975 Mar;15(3):459–461. doi: 10.1016/0042-6989(75)90102-9. [DOI] [PubMed] [Google Scholar]
  18. McIlwain H., Harvery J. A., Rodriguez G. Tetrodotoxin on the sodium and other ions of cerebral tissues, excited electrically and with glutamate. J Neurochem. 1969 Mar;16(3):363–370. doi: 10.1111/j.1471-4159.1969.tb10375.x. [DOI] [PubMed] [Google Scholar]
  19. Murakami M., Otsu K., Otsuka T. Effects of chemicals on receptors and horizontal cells in the retina. J Physiol. 1972 Dec;227(3):899–913. doi: 10.1113/jphysiol.1972.sp010065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Neal M. J. Amino acid transmitter substances in the vertebrate retina. Gen Pharmacol. 1976 Oct;7(5):321–332. doi: 10.1016/0306-3623(76)90014-8. [DOI] [PubMed] [Google Scholar]
  21. Neal M. J., Bowery N. G. Differential effects of veratridine and potassium depolarization on neuronal and glial GABA release. Brain Res. 1979 May 11;167(2):337–343. doi: 10.1016/0006-8993(79)90827-8. [DOI] [PubMed] [Google Scholar]
  22. Neal M. J., Cunningham J. R., Marshall J. The uptake and radioautographical localization in the frog retina of [3H](+/-)-aminocyclohexane carboxylic acid, a selective inhibitor of neuronal GABA transport. Brain Res. 1979 Nov 2;176(2):285–296. doi: 10.1016/0006-8993(79)90984-3. [DOI] [PubMed] [Google Scholar]
  23. Neal M. J., Iversen L. L. Autoradiographic localization of 3 H-GABA in rat retina. Nat New Biol. 1972 Feb 16;235(59):217–218. doi: 10.1038/newbio235217a0. [DOI] [PubMed] [Google Scholar]
  24. Okamoto K., Quastel J. H. Water uptake and energy metabolism in brain slices from the rat. Biochem J. 1970 Nov;120(1):25–36. doi: 10.1042/bj1200025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rowe J. S., Ruddock K. H. Depolarization of retinal horizontal cells by excitatory amino acid neurotransmitter agonists. Neurosci Lett. 1982 Jun 30;30(3):257–262. doi: 10.1016/0304-3940(82)90409-8. [DOI] [PubMed] [Google Scholar]
  26. Schwartz E. A. Calcium-independent release of GABA from isolated horizontal cells of the toad retina. J Physiol. 1982 Feb;323:211–227. doi: 10.1113/jphysiol.1982.sp014069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Shiells R. A., Falk G., Naghshineh S. Action of glutamate and aspartate analogues on rod horizontal and bipolar cells. Nature. 1981 Dec 10;294(5841):592–594. doi: 10.1038/294592a0. [DOI] [PubMed] [Google Scholar]
  28. Shingai R., Christensen B. N. Sodium and calcium currents measured in isolated catfish horizontal cells under voltage clamp. Neuroscience. 1983 Nov;10(3):893–897. doi: 10.1016/0306-4522(83)90227-0. [DOI] [PubMed] [Google Scholar]
  29. Slaughter M. M., Miller R. F. An excitatory amino acid antagonist blocks cone input to sign-conserving second-order retinal neurons. Science. 1983 Mar 11;219(4589):1230–1232. doi: 10.1126/science.6131536. [DOI] [PubMed] [Google Scholar]
  30. Slaughter M. M., Miller R. F. The role of excitatory amino acid transmitters in the mudpuppy retina: an analysis with kainic acid and N-methyl aspartate. J Neurosci. 1983 Aug;3(8):1701–1711. doi: 10.1523/JNEUROSCI.03-08-01701.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sugawara K., Negishi K. Effects of some amino acids on the horizontal cell membrane potential in the isolated carp retina. Vision Res. 1973 May;13(5):977–981. doi: 10.1016/0042-6989(73)90076-x. [DOI] [PubMed] [Google Scholar]
  32. Voaden M. J., Marshall J., Murani N. The uptake of [3H]gamma-amino butyric acid and [3H]glycine by the isolated retina of the frog. Brain Res. 1974 Feb 15;67(1):115–132. doi: 10.1016/0006-8993(74)90302-3. [DOI] [PubMed] [Google Scholar]
  33. Wu S. M., Dowling J. E. L-aspartate: evidence for a role in cone photoreceptor synaptic transmission in the carp retina. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5205–5209. doi: 10.1073/pnas.75.10.5205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Yazulla S., Kleinschmidt J. Carrier-mediated release of GABA from retinal horizontal cells. Brain Res. 1983 Mar 14;263(1):63–75. doi: 10.1016/0006-8993(83)91201-5. [DOI] [PubMed] [Google Scholar]
  35. Yazulla S. Stimulation of GABA release from retinal horizontal cells by potassium and acidic amino acid agonists. Brain Res. 1983 Sep 19;275(1):61–74. doi: 10.1016/0006-8993(83)90417-1. [DOI] [PubMed] [Google Scholar]
  36. Zieglgänsberger W., Puil E. A. Tetrodotoxin interference of CNS excitation by glutamic acid. Nat New Biol. 1972 Oct 18;239(94):204–205. doi: 10.1038/newbio239204a0. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES