Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1996 Feb;70(2):733–742. doi: 10.1016/S0006-3495(96)79613-3

Noise analysis of the glutamate-activated current in photoreceptors.

H P Larsson 1, S A Picaud 1, F S Werblin 1, H Lecar 1
PMCID: PMC1224973  PMID: 8789090

Abstract

The glutamate-activated current in photoreceptors has been attributed both to a sodium/glutamate transporter and to a glutamate-activated chloride channel. We have further studied the glutamate-activated current in single, isolated photoreceptors from the tiger salamander using noise analysis on whole-cell patch-clamp recordings. In cones, the current is generated by chloride channels with a single-channel conductance of 0.7 pS and an open lifetime of 2.4 ms. The number of channels per cell is in the range of 10,000-20,000. Activation of the channels requires the presence of both glutamate and sodium. The single-channel conductance and the open lifetime of the channel are independent of the external concentration of glutamate and sodium. External glutamate and sodium affect only the opening rate of the channels. D,L-Threo-3-hydroxyaspartate (THA), a glutamate-transport blocker, is shown to be a partial agonist for the channel. The single-channel conductance is the same regardless of whether glutamate or THA is the ligand, but the open lifetime of the channel is only 0.8 ms with THA as ligand. The glutamate-activated current in rods has a similar single-channel conductance (0.74 pS) and open lifetime (3 ms). We propose a kinetic model, consistent with these results, to explain how a transporter can simultaneously act both as a sodium/glutamate-gated chloride channel and a glutamate/sodium cotransporter.

Full text

PDF
733

Selected References

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

  1. Balcar V. J., Johnston G. A. The structural specificity of the high affinity uptake of L-glutamate and L-aspartate by rat brain slices. J Neurochem. 1972 Nov;19(11):2657–2666. doi: 10.1111/j.1471-4159.1972.tb01325.x. [DOI] [PubMed] [Google Scholar]
  2. Barbour B., Brew H., Attwell D. Electrogenic uptake of glutamate and aspartate into glial cells isolated from the salamander (Ambystoma) retina. J Physiol. 1991 May;436:169–193. doi: 10.1113/jphysiol.1991.sp018545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bridges R. J., Stanley M. S., Anderson M. W., Cotman C. W., Chamberlin A. R. Conformationally defined neurotransmitter analogues. Selective inhibition of glutamate uptake by one pyrrolidine-2,4-dicarboxylate diastereomer. J Med Chem. 1991 Feb;34(2):717–725. doi: 10.1021/jm00106a037. [DOI] [PubMed] [Google Scholar]
  4. Colquhoun D., Hawkes A. G. Relaxation and fluctuations of membrane currents that flow through drug-operated channels. Proc R Soc Lond B Biol Sci. 1977 Nov 14;199(1135):231–262. doi: 10.1098/rspb.1977.0137. [DOI] [PubMed] [Google Scholar]
  5. Eliasof S., Werblin F. Characterization of the glutamate transporter in retinal cones of the tiger salamander. J Neurosci. 1993 Jan;13(1):402–411. doi: 10.1523/JNEUROSCI.13-01-00402.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fairman W. A., Vandenberg R. J., Arriza J. L., Kavanaugh M. P., Amara S. G. An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature. 1995 Jun 15;375(6532):599–603. doi: 10.1038/375599a0. [DOI] [PubMed] [Google Scholar]
  7. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  8. Jackson M. B., Lecar H., Mathers D. A., Barker J. L. Single channel currents activated by gamma-aminobutyric acid, muscimol, and (-)-pentobarbital in cultured mouse spinal neurons. J Neurosci. 1982 Jul;2(7):889–894. doi: 10.1523/JNEUROSCI.02-07-00889.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Klöckner U., Storck T., Conradt M., Stoffel W. Functional properties and substrate specificity of the cloned L-glutamate/L-aspartate transporter GLAST-1 from rat brain expressed in Xenopus oocytes. J Neurosci. 1994 Oct;14(10):5759–5765. doi: 10.1523/JNEUROSCI.14-10-05759.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Marc R. E., Lam D. M. Uptake of aspartic and glutamic acid by photoreceptors in goldfish retina. Proc Natl Acad Sci U S A. 1981 Nov;78(11):7185–7189. doi: 10.1073/pnas.78.11.7185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Picaud S. A., Larsson H. P., Grant G. B., Lecar H., Werblin F. S. Glutamate-gated chloride channel with glutamate-transporter-like properties in cone photoreceptors of the tiger salamander. J Neurophysiol. 1995 Oct;74(4):1760–1771. doi: 10.1152/jn.1995.74.4.1760. [DOI] [PubMed] [Google Scholar]
  12. Picaud S., Larsson H. P., Wellis D. P., Lecar H., Werblin F. Cone photoreceptors respond to their own glutamate release in the tiger salamander. Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9417–9421. doi: 10.1073/pnas.92.20.9417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Sarantis M., Everett K., Attwell D. A presynaptic action of glutamate at the cone output synapse. Nature. 1988 Mar 31;332(6163):451–453. doi: 10.1038/332451a0. [DOI] [PubMed] [Google Scholar]
  14. Tachibana M., Kaneko A. L-glutamate-induced depolarization in solitary photoreceptors: a process that may contribute to the interaction between photoreceptors in situ. Proc Natl Acad Sci U S A. 1988 Jul;85(14):5315–5319. doi: 10.1073/pnas.85.14.5315. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES