Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-13T02:33:41.523Z Has data issue: false hasContentIssue false
  • English
  • Français

Rapid AMPA receptor desensitization in catfish cone horizontal cells

Published online by Cambridge University Press:  02 June 2009

Scott Eliasof  and
Craig E. Jahr
Scott Eliasof
Affiliation:
Vollum Institute, Oregon Health Sciences University, Portland, OR
Craig E. Jahr
Affiliation:
Vollum Institute, Oregon Health Sciences University, Portland, OR
Get access Rights & Permissions [Opens in a new window]

Abstract

AMPA and NMDA type glutamate receptors were studied in isolated catfish cone horizontal cells using the whole-cell and outside-out patch-recording techniques. In whole-cell recordings, cyclothiazide (CTZ) enhanced the peak current in response to glutamate (in the presence of NMDA receptor antagonists). In patch recordings, currents evoked by rapid and maintained applications of glutamate desensitized with a time constant of one millisecond. CTZ blocked this rapid desensitization. Recovery from desensitization of the AMPA receptors was rapid, having a time constant of 8.65 ms. In contrast, the whole-cell and patch responses to applications of NMDA were much smaller than the AMPA receptor responses and did not desensitize. The relative contribution of these two receptor subtypes depends critically on the condition of the synapse: if glutamate levels are tonically present, the NMDA receptors contribute significantly to the postsynaptic response. If glutamate levels fall rapidly following the release of a single quantum of glutamate, then AMPA receptor currents will dominate the postsynaptic response.

Keywords

RetinaHorizontal cellGlutamate receptorDesensitizationSynaptic transmission
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 1 , January 1997 , pp. 13 - 18
Copyright
Copyright © Cambridge University Press 1997

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Attwell, D. (1990). The photoreceptor output synapse. Progress in Retinal Research 9, 337–362.CrossRefGoogle Scholar
Ayoub, G.S., Korenbrot, J.I. & Copenhagen, D.R. (1989). Release of endogenous glutamate from isolated cone photoreceptors of the lizard. Neuroscience Research (Suppl.) 10, S47–56.Google Scholar
Barnes, S., Merchant, V. & Mahmud, F. (1993). Modulation of transmission gain by protons at the photoreceptor output synapse. Proceedings of the National Academy of Sciences of the U.S.A. 90, 10081–10085.CrossRefGoogle ScholarPubMed
Brew, H. & Attwell, D. (1987). Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells. Nature 327, 707–709.CrossRefGoogle Scholar
Copenhagen, D.R. & Jahr, C.E. (1989). Release of endogenous excitatory amino acids from turtle photoreceptors. Nature 341, 536–539.CrossRefGoogle ScholarPubMed
Cull-Candy, S.G. & Usowicz, M.M. (1987). Multiple-conductance channels activated by excitatory amino acids in cerebellar neurones. Nature 325, 525–528.Google Scholar
DeVries, S.H. & Schwartz, E.A. (1989). Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. Journal of Physiology 414, 351–375.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge: Belknapp Press of Harvard University Press.Google Scholar
Eliasof, S. & Werblin, F. (1993). Characterization of the glutamate transporter in retinal cones of the tiger salamander. Journal of Neuroscience 13, 402–411.CrossRefGoogle ScholarPubMed
Hals, G., Christensen, B.N., O'Dell, T., Christensen, M. & Shingai, R. (1986). Voltage clamp analysis of currents produced by glutamate and some glutamate analogues in horizontal cells isolated from the catfish retina. Journal of Neurophysiology 56, 19–31.CrossRefGoogle ScholarPubMed
Hollmann, M. & Heinemann, S. (1994). Cloned glutamate receptors. Annual Review of Neuroscience 17, 31–108.CrossRefGoogle ScholarPubMed
Jahr, C.E. & Stevens, C.F. (1987). Glutamate activates multiple single channel conductances in hippocampal neurones. Nature 325, 522–525.CrossRefGoogle Scholar
Knapp, A.G. & Dowling, J.E. (1987). Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. Nature 325, 437–439.CrossRefGoogle ScholarPubMed
Lester, R.A.J. & Jahr, C.E. (1992). NMDA channel behavior depends on agonist affinity. Journal of Neuroscience 12, 635–643.Google Scholar
MacDonald, J.F. & Nowak, L.M. (1990). Mechanisms of blockade of excitatory amino acid receptor channels. Trends in Pharmacological Sciences 11, 167–172.CrossRefGoogle ScholarPubMed
O'Dell, T.J. & Christensen, B.N. (1986). N-Methyl-D-Aspartate receptors coexist with kainate and quisqualate receptors on single isolated catfish horizontal cells. Brain Research 381, 359–362.Google Scholar
O'Dell, T.J. & Christensen, B.N. (1989 a). A voltage-clamp study of isolated stingray horizontal cell non-NMDA amino acid receptors. Journal of Neurophysiology 59, 162–172.CrossRefGoogle Scholar
O'Dell, T.J. & Christensen, B.N. (1989 b). Horizontal cells isolated from catfish retina contain two types of excitatory amino acid receptors. Journal of Neurophysiology 61, 1097–1109.CrossRefGoogle ScholarPubMed
Partin, K.M., Patneau, D.K. & Mayer, M.L. (1994). Cyclothiazide differentially modulates desensitization of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor splice variants. Molecular Pharmacology 46, 129–138.Google Scholar
Partin, K.M., Patneau, D.K., Winters, C.A., Mayer, M.L. & Buonanno, A. (1993). Selective modulation of desensitization at AMPA versus kainate receptors by cyclothiazide and concanavalin A. Neuron 11, 1069–1082.Google Scholar
Patneau, D.K., Vyklicky, L. & Mayer, M.L. (1993). Hippocampal neurons exhibit cyclothiazide-sensitive rapidly desensitizing responses to kainate. Journal of Neuroscience 13, 3496–3509.Google Scholar
Raman, I.M. & Trussell, L.O. (1992). The kinetics of the response to glutamate and kainate in neurons of the avian cochlear nucleus. Neuron 9, 173–186.CrossRefGoogle ScholarPubMed
Schmidt, K.F., Kruse, M. & Hatt, H. (1994). Dopamine alters glutamate receptor desensitization in retinal horizontal cells of the perch (perca fluviatilis). Proceedings of the National Academy of Sciences of the U.S.A. 91, 8288–8291.CrossRefGoogle ScholarPubMed
Tachibana, M. & Kaneko, A. (1988). L-Glutamate-induced depolarization in solitary photoreceptors: A process that may contribute to the interaction between photoreceptors in situ. Proceedings of the National Academy of Sciences of the U.S.A. 85, 5315–5319.Google Scholar
Witkovsky, P. & Dearry, A. (1992). Functional roles of dopamine in the vertebrate retina. Progress in Retinal Research 12, 247–292.Google Scholar
Yamada, K.A. & Tang, C.M. (1993). Benzothiadiazides inhibit rapid glutamate receptor desensitization and enhance glutamatergic synaptic currents. Journal of Neuroscience 13, 3904–3915.CrossRefGoogle ScholarPubMed