Efficiency of synaptic transmission of single-photon events from rod photoreceptor to rod bipolar dendrite

Biophysical Journal

Volumn 91, Issue 9, 2006, Pages 3257-3267

  Schein, Stan ^a   Ahmad, Kareem M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; NEUROTRANSMITTER; RHODOPSIN;

ARTICLE; DENDRITE; ISOMERIZATION; MATHEMATICAL MODEL; NEGATIVE FEEDBACK; NEUROTRANSMITTER RELEASE; PHOTORECEPTOR; RETINA ROD; SYNAPTIC TRANSMISSION;

EID: 33751227215     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.091744     Document Type: Article

References (57)

1. Schein, S., and K. M. Ahmad. 2005. A clockwork hypothesis: synaptic release by rod photoreceptors must be regular. Biophys. J. 89:3931-3949.
2. Sterling, P., and G. Matthews. 2005. Structure and function of ribbon synapses. Trends Neurosci. 28:20-29.
3. Rieke, F., and E. A. Schwartz. 1996. Asynchronous transmitter release: control of exocytosis and endocytosis at the salamander rod synapse. J. Physiol. (Lond.). 493:1-8.
4. Rao-Mirotznik, R., G. Buchsbaum, and P. Sterling. 1998. Transmitter concentration at a three-dimensional synapse. J. Neurophysiol. 80:3163-3172.
5. van Rossum, M. C., and R. G. Smith. 1998. Noise removal at the rod synapse of mammalian retina. Vis. Neurosci. 15:809-821.
6. Choi, S. Y., B. Borghuis, R. Rea, E. S. Levitan, P. Sterling, and R. H. Kramer. 2005. Encoding light intensity by the cone photoreceptor synapse. Neuron. 48:555-562.
7. Hood, D. C., and M. A. Finkelstein. 1986. Sensitivity to light. In Handbook of Perception and Human Performance, Vol. 1: Sensory Processes and Perception. K. R. Boff, L. Kaufman, and J. P. Thomas, editors. John Wiley & Sons, New York. 5.1-5.66.
8. Walraven, J., C. Enroth-Cugell, D. C. Hood, D. I. A. MacLeod, and J. L. Schnapf. 1990. The control of visual sensitivity: Receptoral and postreceptoral processes. In The Neurophysiological Foundations of Visual Perception. L. Spillman, and J. Werner, editors. Academic Press, San Diego, CA. 53-101.
9. Robson, J. G., and L. J. Frishman. 1999. Dissecting the dark-adapted electroretinogram. Doc. Ophthalmol. 95:187-215.
10. Field, G. D., and F. Rieke. 2002. Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron. 34:773-785.
11. Baylor, D. A., B. J. Nunn, and J. L. Schnapf. 1984. The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. J. Physiol. (Lond.). 357:575-607.
12. Schneeweis, D. M., and J. L. Schnapf. 1995. Photovoltage of rods and cones in the macaque retina. Science. 268:1053-1056.
13. Sampath, A. P., and R. Rieke. 2004. Selective transmission of single photon responses by saturation at the rod-to-rod bipolar synapse. Neuron. 41:431-443.
14. Field, G. D., A. P. Sampath, and R. Rieke. 2005. Retinal processing near absolute threshold: from behavior to mechanism. In Annual Review of Physiology, Vol. 67. J. F. Hoffman, editor. Annual Reviews, Palo Alto, CA. 491-514.
15. 2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron. 42:595-605.
16. Collins, M. O., Y. Lu, M. P. Coba, H. Husi, I. Campuzano, W. P. Blackstock, J. S. Choudhary, and S. G. N. Grant. 2005. Proteomic analysis of in vivo phosphorylated synaptic proteins. J. Biol. Chem. 280:5972-5982.
17. de Ruyter van Steveninck, R. R., G. D. Lewen, S. P. Strong, R. Koberle, and W. Bialek. 1997. Reproducibility and variability in neural spike trains. Science. 275:1805-1808.
18. Berry, M. J., and M. Meister. 1998. Refractoriness and neural precision. J. Neurosci. 18:2200-2211.
19. Migdale, K., S. Herr, K. Klug, K. Ahmad, K. Linberg, P. Sterling, and S. Schein. 2003. Two ribbon synaptic units in rod photoreceptors of macaque, human, and cat. J. Comp. Neurol. 455:100-112.
20. Townes-Anderson, E., P. R. MacLeish, and E. Raviola. 1985. Rod cells dissociated from mature salamander retina: Ultrastructure and uptake of horseradish peroxidase. J. Cell Biol. 100:175-188.
21. Barlow, H. B. 1956. Retinal noise and absolute threshold. J. Opt. Soc. Am. 8:634-639.
22. Donner, K. 1992. Noise and the absolute thresholds of cone and rod vision. Vision Res. 32:853-866.
23. Rodieck, R. W. 1998. The First Steps in Seeing. Sinauer, Sunderland, MA.
24. Bader, C. R., D. Bertrand, and E. A. Schwartz. 1982. Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. J. Physiol. (Lond.). 331:253-284.
25. Corey, D. P., J. M. Dubinsky, and E. A. Schwartz. 1984. The calcium current in inner segments of rods from the salamander (Ambystoma tigrinum) retina. J. Physiol. (Lond.). 354:557-575.
26. Taylor, W. R., and C. Morgans. 1998. Localization and properties of voltage-gated calcium channels in cone photoreceptors of Tupaia belangeri. Vis. Neurosci. 15:541-552.
27. Schneeweis, D. M., and D. L. Schnapf. 2000. Noise and light adaptation in rods of the macaque monkey. Vis. Neurosci. 17:659-666.
28. Nawy, S. 1999. The metabotropic receptor mGluR6 may signal through G(o), but not phosphodiesterase, in retinal bipolar cells. J. Neurosci. 19:2938-2944.
29. Nawy, S. 2004. Desensitization of the mGluR6 transduction current in tiger salamander On bipolar cells. J. Physiol. (Lond.). 558:137-146.
30. Dhingra, A., M. Jiang, T. L. Wang, A. Lyubarsky, A. Savchenko, T. Bar-Yehuda, P. Sterling, L. Birnbaumer, and N. Vardi. 2002. Light response of retinal ON bipolar cells requires a specific splice variant of Gα(o). J. Neurosci. 22:4878-4884.
31. o and accelerates an expressed metabotropic glutamate receptor 6 cascade. J. Neurosci. 24:5684-5693.
32. Slaughter, M. M., and R. F. Miller. 1981. 2-Amino-4-phosphonobutyric acid: a new pharmacological tool for retina research. Science. 211:182-185.
33. Nakajima, Y., H. Iwakabe, C. Akazawa, H. Nawa, R. Shigemoto, N. Mizuno, and S. Nakanishi. 1993. Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. J. Biol. Chem. 268:11868-11873.
34. Nomura, A., R. Shigemoto, Y. Nakamura, N. Okamoto, N. Mizuno, and S. Nakanishi. 1994. Developmentally-regulated postsynaptic localization of a metabotropic glutamate-receptor in rat rod bipolar cells. Cell. 77:361-369.
35. Pin, J. P., and R. Duvoisin. 1995. The metabotropic glutamate receptors: structure and functions. Neuropharmacology. 34:1-26.
36. Vardi, N., and K. Morigiwa. 1997. ON cone bipolar cells in rat express the metabotropic receptor mGluR6. Vis. Neurosci. 14:789-794.
37. Nelson, R. 1973. A comparison of electrical properties of neurons in Necturus retina. J. Neurophysiol. 36:519-535.
38. Toyoda, J. 1973. Membrane resistance changes underlying the bipolar cell response in the carp retina. Vision Res. 13:283-294.
39. Nawy, S., and C. E. Jahr. 1990. Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature. 346:269-271.
40. Shiells, R. A., and G. Falk. 1990. Glutamate receptors of rod bipolar cells are linked to a cyclic GMP cascade via a G-protein. Proc. R. Soc. Lond. B Biol. Sci. 242:91-94.
41. Shiells, R. A., and G. Falk. 1992. Properties of the cGMP-activated channel of retinal on-bipolar cells. Proc. R. Soc. Lond. B Biol. Sci. 247:21-25.
42. de la Villa, P., T. Kurahashi, and A. Kaneko. 1995. L-glutamate-induced responses and cGMP-activated channels in three subtypes of retinal bipolar cells dissociated from the cat. J. Neurosci. 15:3571-3582.
43. Euler, T., H. Schneider, and H. Wässle. 1996. Glutamate responses of bipolar cells in a slice preparation of the rat retina. J. Neurosci. 16:2934-2944.
44. Walters, R. J., R. H. Kramer, and S. Nawy. 1998. Regulation of cGMP-dependent current in On bipolar cells by calcium/calmodulin-dependent kinase. Vis. Neurosci. 15:257-261.
45. 2+ underlies light adaptation in dogfish retinal "on" bipolar cells. J. Physiol. (Lond.). 514:343-350.
46. 2+- calmodulin kinase II induces desensitization by background light in dogfish retinal "on" bipolar cells. J. Physiol. (Lond.). 528:327-338.
47. Shiells, R.A., and G. Falk. 2001. Rectification of cGMP-activated channels induced by phosphorylation in dogfish retinal "on" bipolar cells. J. Physiol. (Lond.). 535:697-702.
48. 2+. J. Neurosci. 20:4471-4479.
49. Snellman, J., and S. Nawy. 2002. Regulation of the retinal bipolar cell mGluR6 pathway by calcineurin. J. Neurophysiol. 88:1088-1096.
50. Shiells, R.A., and G. Falk. 2002. Potentiation of "on" bipolar cell flash responses by dim background light and cGMP in dogfish retinal slices. J. Physiol. (Lond.). 542:211-220.
51. Snellman, J., and S. Nawy. 2004. cGMP-dependent kinase regulates response sensitivity of the mouse on bipolar cell. J. Neurosci. 24:6621-6628.
52. Taylor, W. R., and R. G. Smith. 2004. Transmission of scotopic signals from the rod to rod-bipolar cell in the mammalian retina. Vision Res. 44:3269-3276.
53. Berntson, A., R. G. Smith, and W. R. Taylor. 2004. Transmission of single photon signals through a binary synapse in the mammalian retina. Vis. Neurosci. 21:693-702.
54. Fain, G. 2003. Sensory Transduction. Sinauer, Sunderland, MA. 173, 180.
55. Shiells, R. A., G. Falk, and S. Naghshineh. 1981. Action of glutamate and aspartate analogues on rod horizontal and bipolar cells. Nature. 294:592-594.
56. Nawy, S., and D. R. Copenhagen. 1987. Multiple classes of glutamate receptor on depolarizing bipolar cells in retina. Nature. 325:56-58.
57. Sampath, A., K. Strissel, R. Elias, V. Arshavsky, J. McGinnis, J. Chen, S. Kawamura, R. Rieke, and J. Hurley. 2005. Recoverin improves rod-mediated vision by enhancing signal transmission in the mouse retina. Neuron. 46:413-420.