A clockwork hypothesis: Synaptic release by rod photoreceptors must be regular

Biophysical Journal

Volumn 89, Issue 6, 2005, Pages 3931-3949

  Schein, Stan ^a   Ahmad, Kareem M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTRANSMITTER; RHODOPSIN; VOLTAGE GATED CALCIUM CHANNEL;

ARTICLE; HYPERPOLARIZATION; HYPOTHESIS; LIGHT ABSORPTION; LIGHT INTENSITY; NEUROTRANSMITTER RELEASE; PHOTORECEPTOR; RETINA ROD; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC MEMBRANE;

MAMMALIA;

EID: 28444452299     PISSN: 00063495     EISSN: 00063495     Source Type: Journal    
DOI: 10.1529/biophysj.105.070623     Document Type: Article

References (110)

1. 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. Chapter 5.
2. Rodieck, R. W. 1998. The First Steps in Seeing. Sinauer, Sunderland, MA. Chapter 7.
3. Hecht, S., S. Shlaer, and M. H. Pirenne. 1942. Energy quanta and vision. J. Gen. Physiol. 25:819-840.
4. van der Velden, H. A. 1946. The number of quanta necessary for the perception of light in the human eye. Ophthalmologica. 111:321-331.
5. Sakitt, B. 1972. Counting every quantum. J. Physiol. 223:131-150.
6. Schneeweis, D. M., and J. L. Schnapf. 1995. Photovoltage of rods and cones in the macaque retina. Science. 268:1053-1056.
7. Schneeweis, D. M., and J. L. Schnapf. 2000. Noise and light adaptation in rods of the macaque monkey. Vis. Neurosci. 17:659-666.
8. Field, G. D., and F. Rieke. 2002a. Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron. 34:773-785.
9. Robson, J. G., H. Maeda, S. M. Saszik, and L. J. Frishman. 2004. In vivo studies of signaling in rod pathways of the mouse using the electroretinogram. Vision Res. 44:3253-3268.
10. Sampath, A. P., and F. Rieke. 2004. Selective transmission of single photon responses by saturation at the rod-to-rod bipolar synapse. Neuron. 41:431-443.
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. 357:575-607.
12. van Rossum, M. C., and R. G. Smith. 1998. Noise removal at the rod synapse of mammalian retina. Vis. Neurosci. 15:809-821.
13. Falk, G., and P. Fatt. 1972. Physical changes induced by light in the rod outer segment of vertebrates. In Handbook of Sensory Physiology, Vol. VII/I. H. J. A. Dartnall, editor. Springer-Verlag. Berlin. 200-244.
14. Fatt, P., and B. Katz. 1952. Spontaneous subthreshold activity at motor nerve endings. J. Physiol. 117:109-128.
15. del Castillo, J., and J. B. Katz. 1953. Statistical nature of facilitation at a single nerve-muscle junction. Nature. 171:1016-1017.
16. Katz, B., and R. Miledi. 1965. The measurement of synaptic delay, and the time course of acetylcholine release at the neuromuscular junction. Proc. R. Soc. Land. B Biol. Sci. 161:483-495.
17. Katz, B. 1969. The release of neural transmitter substances. Liverpool University Press, Liverpool.
18. Barrett, E. F., and C. F. Stevens. 1972. The kinetics of transmitter release at the frog neuromuscular junction. J. Physiol. 227:691-708.
19. Allen, C., and C. F. Stevens. 1994. An evaluation of causes for unreliability of synaptic transmission. Proc. Natl. Acad. Sci. USA. 91:10380-10383.
20. Bekkers, J. M., and C. F. Stevens. 1994. The nature of quantal transmission at central excitatory synapses. Adv. Second Messenger Phosphoprotein Res. 29:261-273.
21. Rao-Mirotznik, R., G. Buchsbaum, and P. Sterling. 1998. Transmitter concentration at a three-dimensional synapse. J. Neurophysiol. 80:3163-3172.
22. Baylor, D. 1996. How photons start vision. Proc. Natl. Acad. Sci. USA. 93:560-565.
23. 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. 331:253-284.
24. 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. 354:557-575.
25. Rieke, F., and E. A. Schwartz. 1996. Asynchronous transmitter release: control of exocytosis and endocytosis at the salamander rod synapse. J. Physiol. 493:1-8.
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. Hille, B. 1984. Ionic channels of excitable membranes. Sinauer Associates: Sunderland, MA.
28. Rieke, F., and E. A. Schwartz. 1994. A cGMP-gated current can control exocytosis at cone synapses. Neuron. 13:863-873.
29. Wilkinson, M. F., and S. Barnes. 1996. The dihydropyridine-sensitive calcium channel subtype in cone photoreceptors. J. Gen. Physiol. 107:621-630.
30. Schmitz, Y., and P. Witkovsky. 1997. Dependence of photoreceptor glutamate release on a dihydropyridine-sensitive calcium channel. Neuroscience. 78:1209-1216.
31. Witkovsky, P., Y. Schmitz, A. Akopian, D. Krizaj, and D. Tranchina. 1997. Gain of rod to horizontal cell synaptic transfer: relation to glutamate release and a dihydropyridine-sensitive calcium current. J. Neurosci. 17:7297-7306.
32. Nachman-Clewner, M., R. St. Jules, and E. Townes-Anderson. 1999. L-type calcium channels in the photoreceptor ribbon synapse: localization and role in plasticity. J. Comp. Neurol. 415:1-16.
33. Wässle, H., S. Haverkamp, U. Grünert, and C. W. Morgans. 2003. The cone pedicle, the first synapse in the retina. In The Neural Basis of Early Vision. A. Kaneko, editor. Springer Verlag, Tokyo. 19-38.
34. 2+ currents and synaptic transmission in amphibian photoreceptors. J. Neurophysiol. 77:2175-2190.
35. Armstrong-Gold, C. E., and F. Rieke. 2003. Bandpass filtering at the rod to second-order cell synapse in salamander (Ambystoma tigrinum) retina. J. Neurosci. 23:3796-3806.
36. 2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron. 42:595-605.
37. 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.
38. 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.
39. Rieke, F., and D. A. Baylor. 1996. Molecular origin of continuous dark noise in rod photoreceptors. Biophys. J. 71:2553-2572.
40. Graham, C. H., and R. Margaria. 1935. Area and the intensity-time relation in the peripheral retina. Am. J. Physiol. 113:299-305.
41. Barlow, H. B. 1957. Increment thresholds at low intensities considered as signal/noise discrimination. J. Physiol. 136:469-488.
42. Sperling, H. G., and C. L. Jolliffe. 1965. Intensity-time relationships at threshold for spectral stimuli in human vision. J. Opt. Soc. Am. 55:191-199.
43. Baumgardt, E., and B. Hillmann. 1961. Duration and size as determinants of peripheral retinal response. J. Opt. Soc. Am. 51:340-344.
44. Robson, J. G., and L. J. Frishman. 1999. Dissecting the dark-adapted electroretinogram. Doc. Ophthalmol. 95:187-215.
45. Baylor, D. A., G. Matthews, and K.-W. Yau. 1980. Two components electrical dark noise in toad rod outer segments. J. Physiol. 309:591-621.
46. Mastronarde, D. N. 1983. Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. J. Neurophysiol. 49:325-349.
47. Copenhagen, D. R., K. Donner, and T. Reuter. 1987. Ganglion cell performance at absolute threshold in toad retina: Effects of dark events in rods. J. Physiol. 393:667-680.
48. Barlow, H. B. 1956. Retinal noise and absolute threshold. J. Opt. Soc. Am. 8:634-639.
49. Donner, K. 1992. Noise and the absolute thresholds of cone and rod vision. Vision Res. 32:853-866.
50. Belgum, J. H., and D. R. Copenhagen. 1988. Synaptic transfer of rod signals to horizontal and bipolar cells in the retina of the toad (Bufo marinus). J. Physiol. 396:225-245.
51. Walraven, J., C. Enroth-Cugell, D. C. Hood, D. I. A. MacLeod, and J. L. Schnapf. 1990. Control of visual sensitivity. In Visual Perception: The Neurophysiological Foundations. L. Spillman, and J. S. Werner, editors. Academic Press, San Diego. 53-101.
52. Field, G. D., A. P. Sampath, and F. 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.
53. 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.
54. Rieke, F., and D. Warland, R. R. de Ruyter van Steveninck, and W. Bialek. 1997. Spikes: Exploring the Neural Code. MIT Press, Cambridge, MA.
55. Green, D. M., and J. A. Swets. 1966. Signal Detection Theory and Psychophysics. John Wiley, New York. 151-179.
56. 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.
57. 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.
58. Berry, M. J., and M. Meister. 1998. Refractoriness and neural precision. J. Neurosci. 18:2200-2211.
59. Uzzell, V. J., and E. J. Chichilnisky. 2004. Precision of spike trains in primate retinal ganglion cells. J. Neurophysiol. 92:780-789.
60. Stevens, C. F., and Y. Wang. 1995. Facilitation and depression at single central synapses. Neuron. 14:795-802.
61. Korn, H., A. Mallet, A. Triller, and D. S. Faber. 1982. Transmission at a central inhibitory synapse. II. Quantal description of release, with a physical correlate for binomial n. J. Neurophysiol. 48:679-707.
62. Redman, S. 1990. Quantal analysis of synaptic potentials in neurons of the central nervous system. Physiol. Rev. 70:165-198.
63. Korn, H., and D. S. Faber. 1991. Quantal analysis and synaptic efficacy in the CNS. Trends Neurosci. 14:439-445.
64. Schikorski, T., and C. F. Stevens. 1997. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J. Neurosci. 17:5858-5867.
65. Hjelmstad, G. O., R. A. Nicoll, and R. C. Malenka. 1997. Synaptic refractory period provides a measure of probability of release in the hippocampus. Neuron. 19:1309-1318.
66. Rieke, F., and D. A. Baylor. 1998. Origin of reproducibility in the responses of retinal rods to single photons. Biophys. J. 75:1836-1857.
67. Field, G. D., and F. Rieke. 2002b. Mechanisms regulating variability of the single photon responses of mammalian rod photoreceptors. Neuron. 35:733-747.
68. Hamer, R. D., S. C. Nicholas, D. Tranchina, P. A. Liebman, and T. D. Lamb. 2004. Multiple steps of phosphorylation of activated rhodopsin can account for the reproducibility of vertebrate rod single-photon responses. J. Gen. Physiol. 122:419-444.
69. 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.
70. Picaud, S., H. P. Larsson, D. P. Wellis, H. Lecar, and F. Werblin. 1995. Cone photoreceptors respond to their own glutamate release in the tiger salamander. Proc. Natl. Acad. Sci. USA. 92:9417-9421.
71. Koulen, P. 1999. Clustering of neurotransmitter receptors in the mammalian retina. J. Membr. Biol. 171:97-105.
72. Barnes, S., and Q. Bui. 1991. Modulation of calcium-activated chloride current via pH-induced changes of calcium channel properties in cone photoreceptors. J. Neurosci. 11:4015-4023.
73. Barnes, S., V. Merchant, and F. Mahmud. 1993. Modulation of transmission gain by protons at the photoreceptor output synapse. Proc. Natl. Acad. Sci. USA. 90:10081-10085.
74. DeVries, S. H. 2001. Exocytosed protons feedback to suppress the Ca2+ current in mammalian cone photoreceptors. Neuron. 32:1107-1117.
75. Hirasawa, H., and A. Kaneko. 2003. pH changes in the invaginating synaptic cleft mediate feedback from horizontal cells to cone photoreceptors by modulating Ca2+ channels. J. Gen. Physiol. 122:657-671.
76. Miesenbock, G., D. A. De Angelis, and J. E. Rothman. 1998. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature. 394:192-195.
77. Gandhi, S. P., and C. F. Stevens. 2003. Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature. 423:607-613.
78. Aravanis, A. M., J. L. Pyle, and R. W. Tsien. 2003. Single synaptic vesicles fusing transiently and successively without loss of identity. Nature. 423:643-647.
79. von Gersdorff, H., and G. Matthews. 1994. Dynamics of synaptic vesicle exocytosis and membrane retrieval in synaptic terminals. Nature. 367:735-739.
80. von Gersdorff, H., N. Vardi, G. Matthews, and P. Sterling. 1996. Evidence that vesicles on the synaptic ribbon of retinal bipolar neurons can be rapidly released. Neuron. 16:1221-1227.
81. Herr, S., K. Klug, P. Sterling, and S. Schein. 2003. Inner S-cone bipolar cells provide all of the central elements for S cones in Macaque retina. J. Comp. Neurol. 457:185-201.
82. 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.
83. Vardi, N., and K. Morigiwa. 1997. ON cone bipolar cells in rat express the metabotropic receptor mGluR6. Vis. Neurosci. 14:789-794.
84. Haverkamp, S., U. Grünert, and H. Wässle. 2001. The synaptic architecture of AMPA receptors at the cone pedicle of the primate retina. J. Neurosci. 21:2488-2500.
85. Bemtson, A., and W. R. Taylor. 2003. The unitary event amplitude of mouse retinal on-cone bipolar cells. Vis. Neurosci. 20:621-626.
86. Laughlin, B., and R. R. de Ruyter van Steveninck. 1996. Measurements of signal transfer and noise suggest new model for graded transmission at an adapting retinal synapse. J. Physiol. 494:19.
87. Fain, G. 2003. Sensory Transduction. Sinauer Associates, Sunderland, MA.
88. Geisler, C. D. 1998. From Sound to Synapse. Physiology of the Mammalian Ear. Oxford University Press, New York.
89. Glowatzki, E., and P. A. Fuchs. 2002. Transmitter release at the hair cell ribbon synapse. Nat. Neurosci. 5:147-154.
90. Siegel, J. H. 1992. Spontaneous synaptic potentials from afferent terminals in the guinea pig cochlea. Hear. Res. 59:85-92.
91. Liberman, M. C. 1980. Morphological differences among radial afferent fibers in the cat cochlea: an electron-microscopic study of serial sections. Hear. Res. 3:45-63.
92. Liberman, M. C. 1982. Single-neuron labeling in the cat auditory nerve. Science. 216:1239-1241.
93. Sewell, W. F. 1990. Synaptic potentials in afferent fibers innervating hair cells of the lateral line organ in Xenopus laevis. Hear. Res. 44:71-81.
94. Tricas,T. C., and S. M. Highstein. 1991. Action of the octavolateralis efferent system upon the lateral line of free-swimming toadfish, Opsanus tau. J. Comp. Physiol. [A]. 169:25-37.
95. von Gersdorff, H. 2001. Synaptic ribbons: versatile signal transducers. Neuron. 29:7-10.
96. Sterling, P., and G. Matthews. 2005. Structure and function of ribbon synapses. Trends Neurosci. 28:20-29.
97. Auger, C., and A. Marty. 2000. Quantal currents at single-site central synapses. J. Physiol. 526:3-11.
98. Edmonds, B. W., F. D. Gregory, and F. E. Schweizer. 2004. Evidence that fast exocytosis can be predominantly mediated by vesicles not docked at active zones in frog saccular hair cells. J. Physiol. 560:439-450.
99. Parsons, T. D., and P. Sterling. 2003. Synaptic ribbon: conveyor belt or safety belt? Neuron. 37:379-382.
100. Heidelberger, R., C. Heinemann, E. Neher, and G. Matthews. 1994. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature. 371:513-515.
101. Singer, J. H., L. Lassova, N. Vardi, and J. S. Diamond. 2004. Coordinated multivesicular release at a mammalian ribbon synapse. Nat. Neurosci. 7:826-833.
102. Douglass, J. K., L. Wilkens, L. Pantazelou, and F. Moss. 1993. Noise enhancement of information transfer in crayfish mechanoreceptors by stochastic resonance. Nature. 365:337-340.
103. Gammaitoni, L., P. M. Hanggi, P. Jung, and F. Marchesoni. 1998. Stochastic resonance. Rev. Mod. Phys. 70:223-287.
104. Kara, P., P. Reinagel, and R. C. Reid. 2000. Low response variability in simultaneously recorded retinal, thalamic, and cortical neurons. Neuron. 27:635-646.
105. Barlow, H. B., W. R. Levick, and M. Yoon. 1971. Responses to single quanta of light in retinal ganglion cells of the cat. Vision Res. S3:87-101.
106. Cox, D. R. 1962. Renewal Theory. Methuen, London.
107. Wickens, T. D. 1982. Models for Behavior: Stochastic Processes in Psychology. W. H. Freeman, San Francisco.
108. Morlat, G., and É. Borel. 1952. Sur une géné ralisation de loi de Poisson. Comptes Rendus. 234:933-935.
109. Johnson, N. L., S. Kotz, and A. W. Kemp. 1992. Univariate Discrete Distributions, 2nd ed. Wiley Interscience. John Wiley & Sons, New York.
110. Horowitz, P., and W. Hill. 1980. The Art of Electronics. Cambridge University Press, Cambridge.