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Kainate receptors mediate synaptic transmission between cones and ‘Off’ bipolar cells in a mammalian retina

Nature volume 397, pages 157–160 (1999)Cite this article

Abstract

Light produces a graded hyperpolarization in retinal photoreceptors1,2 that decreases their release of synaptic neurotransmitter3,4. Cone photoreceptors use glutamate5,6 as a neurotransmitter with which to communicate with two types of bipolar cell. Activation of metabotropic glutamate receptors in ‘On’ bipolar cells7,8 initiates a second-messenger cascade that can amplify small synaptic inputs from cones. In contrast, it is not known how the ionotropic glutamate receptors that are activated in ‘Off’ bipolar cells9,10 are optimized for transmitting small, graded signals. Here we show, by recording from a cone and a synaptically connected ‘Off’ bipolar cell in slices of retina from the ground squirrel, that transmission is mediated by glutamate receptors of the kainate-preferring subtype. In the dark, a cone releases sufficient neurotransmitter to desensitize most postsynaptic kainate receptors. The small postsynaptic current that persists (<5% of maximum) is quickly modulated by changes in presynaptic voltage. Since recovery from desensitization is slow (the decay time constant is roughly 500 milliseconds), little recovery can occur during the brief (roughly 100-millisecond) hyperpolarization that is produced in cones by a flash of light. By limiting the postsynaptic current, receptor desensitization prevents saturation of the ‘Off’ bipolar cell's voltage response and allows the synapse to operate over the cone's entire physiological voltage range.

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Figure 1: Synaptic transmission from cone photoreceptors to ‘Off’ bipolar cells.
Figure 2: Ca2+ and voltage dependence of synaptic transmission.
Figure 3: Rate of recovery of synaptic and kainate-receptor sensitivity.
Figure 4: Pharmacological characterization of synaptic receptors.
Figure 5: The postsynaptic current is reduced by receptor desensitization at physiological voltages.

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References

  1. Penn, R. D. & Hagins, W. A. Signal transmission along retinal rods and the origin of the electroretinographic a-wave. Nature 223, 201–205 (1969).

    Article  ADS  CAS  Google Scholar 

  2. Baylor, D. A. & Fuortes, M. G. F. Electrical responses of single cones in the retina of the turtle. J. Physiol. (Lond.) 207, 77–92 (1970).

    Article  CAS  Google Scholar 

  3. Trifonov, Y. A. Study of synaptic transmission between the photoreceptor and the horizontal cell using electrical stimulation of the retina. Biofizika 13, 809–817 (1968).

    CAS  PubMed  Google Scholar 

  4. Dowling, J. E. & Ripps, H. Effect of magnesium on horizontal cell activity in the skate retina. Nature 242, 101–103 (1973).

    Article  ADS  CAS  Google Scholar 

  5. Miller, A. M. & Schwartz, E. A. Evidence for the identification of synaptic transmitters released by photoreceptors of the toad retina. J. Physiol. (Lond.) 334, 325–349 (1983).

    Article  CAS  Google Scholar 

  6. Copenhagen, D. R. & Jahr, C. E. Release of endogenous excitatory amino acids from turtle photoreceptors. Nature 341, 536–539 (1989).

    Article  ADS  CAS  Google Scholar 

  7. Nawy, S. & Jahr, C. E. cGMP-gated conductance in retinal bipolar cells is suppressed by the photoreceptor transmitter. Neuron 7, 677–683 (1991).

    Article  CAS  Google Scholar 

  8. Masu, M. et al. Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell 80, 757–765 (1995).

    Article  CAS  Google Scholar 

  9. Saito, T. & Kaneko, A. Ionic mechanisms underlying the responses of off-center bipolar cells in the carp retina. J. Gen. Physiol. 81, 589–601 (1983).

    Article  CAS  Google Scholar 

  10. Attwell, D., Mobbs, P., Tessier-Lavigne, M. & Wilson, M. Neurotransmitter-induced currents in retinal bipolar cells of the axolotl, Ambystoma mexicanum. J. Physiol. (Lond.) 387, 125–161 (1987).

    Article  CAS  Google Scholar 

  11. Famiglietti, E. V. & Kolb, H. Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194, 193–195 (1976).

    Article  ADS  Google Scholar 

  12. West, R. W. Light and electron microscopy of the ground squirrel retina: functional considerations. J. Comp. Neurol. 168, 355–378 (1976).

    Article  CAS  Google Scholar 

  13. von Gersdorff, H. & Matthews, G. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature 367, 735–739 (1994).

    Article  ADS  CAS  Google Scholar 

  14. Ozawa, S., Kamiya, H. & Tsuzuki, K. Glutamate receptors in the mammalian central nervous system. Prog. Neurobiol. 54, 581–618 (1998).

    Article  CAS  Google Scholar 

  15. Mayer, M. L., Westbrook, G. L. & Guthrie, P. B. Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature 309, 261–263 (1984).

    Article  ADS  CAS  Google Scholar 

  16. Paternain, A. V., Morales, M. & Lerma, J. Selective antagonism of AMPA receptors unmasks kainate receptor-mediated responses in hippocampal neurons. Neuron 14, 185–189 (1995).

    Article  CAS  Google Scholar 

  17. Partin, K. M. et al. Selective modulation of desensitization at AMPA versus kainate receptors by cyclothiazide and Concanavalin A. Neuron 11, 1069–1082 (1993).

    Article  CAS  Google Scholar 

  18. Patneau, D. K. et al. Glial cells of the oligodendrocyte lineage express both kainate- and AMPA-preferring subtypes of glutamate receptor. Neuron 12, 357–371 (1994).

    Article  CAS  Google Scholar 

  19. Rice, S. O. Mathematical analysis of random noise. Bell Syst. Tech. J. 23, 282–332 (1944).

    Article  MathSciNet  Google Scholar 

  20. Katz, B. & Miledi, R. The statistical nature of the acetylcholine potential and its molecular components. J. Physiol. (Lond.) 224, 665–699 (1972).

    Article  CAS  Google Scholar 

  21. Mennerick, S. & Matthews, G. Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron 17, 1241–1249 (1996).

    Article  CAS  Google Scholar 

  22. Leeper, H. F. & Charlton, J. S. Response properties of horizontal cells and photoreceptor cells in the retina of the tree squirrel, Sciurus carolinensis. J. Neurophysiol. 54, 1157–1166 (1985).

    Article  CAS  Google Scholar 

  23. Kraft, T. Photocurrents of cone photoreceptors of the golden-mantled ground squirrel. J. Physiol. (Lond.) 404, 199–213 (1988).

    Article  CAS  Google Scholar 

  24. Lindberg, K. A., Suemune, S. & Fisher, S. K. Retinal neurons of the California ground squirrel, Spermophilus beecheyi: a Golgi study. J. Comp. Neurol. 365, 173–216 (1996).

    Article  Google Scholar 

  25. Falk, G. Signal transmission from rods to bipolar and horizontal cells: a synthesis. Prog. Retinal Res. 8, 255–279 (1989).

    Article  Google Scholar 

  26. Lukasiewicz, P. & Werblin, F. Aslowly inactivating potassium current truncates spike activity in ganglion cells of the tiger salamander retina. J. Neurosci. 8, 4470–4481 (1988).

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by an NIH grant (to E.A.S.) and a Research to Prevent Blindness Junior Investigator Award (to S.H.D.).

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Authors and Affiliations

  1. Department of Ophthalmology and Visual Science, University of Texas Houston Health Science Center, Houston, 77030, Texas, USA

    Steven H. DeVries

  2. Department of Pharmacological and Physiological Sciences, University of Chicago, Chicago, Illinois, 60637, USA

    Eric A. Schwartz

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  1. Steven H. DeVries
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  2. Eric A. Schwartz
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Correspondence to Steven H. DeVries.

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DeVries, S., Schwartz, E. Kainate receptors mediate synaptic transmission between cones and ‘Off’ bipolar cells in a mammalian retina. Nature 397, 157–160 (1999). https://doi.org/10.1038/16462

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