The diverse functional roles and regulation of neuronal gap junctions in the retina

Nature Reviews Neuroscience

Volumn 10, Issue 7, 2009, Pages 495-506

  Bloomfield, Stewart A ^a   Völgyi, Béla ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; NITRIC OXIDE;

CELL INTERACTION; CIRCADIAN RHYTHM; ELECTRIC CURRENT; ELECTRICAL SYNAPSE; GAP JUNCTION; HORIZONTAL CELL; HUMAN; ILLUMINATION; MAMMAL; NERVE; NERVE CELL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE CONDUCTION; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; RETINA CELL; RETINA CONE; RETINA IMAGE; RETINA ROD; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; VISION;

ANIMALS; BIOLOGICAL CLOCKS; CIRCADIAN RHYTHM; CONNEXINS; ELECTRICAL SYNAPSES; HUMANS; NERVE NET; NEURONS; NEUROTRANSMITTER AGENTS; PHOTORECEPTOR CELLS, VERTEBRATE; RETINA; RETINAL GANGLION CELLS; SYNAPTIC TRANSMISSION; VISION, OCULAR;

VERTEBRATA;

EID: 67649476102     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn2636     Document Type: Review

References (169)

1. Furshpan, E. J. & Potter, D. D. Mechanism of nerveimpulse transmission at a crayfish synapse. Nature 180, 342-343 (1957).
2. Watanabe, A. The interaction of electrical activity among neurons of lobster cardiac ganglion. Jpn J. Physiol. 433, 283-305 (1958).
3. Goodenough, D. A. & Revel, J. P. A fine structural analysis of intercellular junctions in the mouse liver. J. Cell Biol. 45, 272-290 (1970).
4. Bennett, M. V. L. in Cellular Biology of Neurons, Handbook of Physiology, The Nervous System (ed. Kandel, E. R.) 357-416 (Williams & Wilkins, Baltimore, 1977).
5. Söhl, G., Maxeiner, S. & Willecke, K. Expression and functions of neuronal gap junctions. Nature Rev. Neurosci. 6, 191-200 (2005).
6. Meier, C. & Dermietzel, R. Electrical synapses-gap junctions in the brain. Results Probl. Cell Differ. 43, 99-128 (2006).
7. Söhl, G. & Willecke, K. An update on connexin genes and their nomenclature in mouse and man. Cell Commun. Adhes. 10, 173-180 (2003).
8. Bloomfield, S. A., Xin, D. & Osborne, T. Light-induced modulation of coupling between AII amacrine cells in the rabbit retina. Vis. Neurosci. 14, 565-576 (1997).
9. Weiler, R., Pottek, M., He, S. & Vaney, D. I. Modulation of coupling between retinal horizontal cells by retinoic acid and endogenous dopamine. Brain Res. Brain Res. Rev. 32, 121-129 (2000).
10. Xin, D. & Bloomfield, S. A. Dark- and light-induced changes in coupling between horizontal cells in mammalian retina. J. Comp. Neurol. 405, 75-87 (1999).
11. Xin, D. & Bloomfield, S. A. Effects of nitric oxide on horizontal cells in the rabbit retina. Vis. Neurosci. 17, 799-811 (2000).
12. Ribelayga, C., Cao, Y. & Mangel, S. C. The circadian clock in the retina controls rod-cone coupling. Neuron 59, 790-801 (2008). This study showed that a circadian clock in the retina controls the extracellular dopamine concentration and thereby the conductance of rod-cone gap junctions.
13. Willecke, K. et al. Structural and functional diversity of connexin genes in the mouse and human genome. Biol. Chem. 383, 725-737 (2002).
14. Lampe, P. D. & Lau, A. F. Regulation of gap junctions by phosphorylation of connexins. Arch. Biochem. Biophys. 384, 205-215 (2000).
15. Lampe, P. D. & Lau, A. F. The effects of connexin phosphorylation on gap junctional communication. Int. J. Biochem. Cell Biol. 36, 1171-1186 (2004).
16. Witkovsky, P. & Dearry, A. Functional roles of dopamine in the vertebrate retina. Prog. Retin. Res. 11, 247-292 (1991).
17. Koistinaho, J., Swanson, R. A., de Vente, J. & Sagar, S. M. NADPH-diaphorase (nitric oxide synthase)-reactive amacrine cells of rabbit retina: putative target cells and stimulation by light. Neuroscience 57, 587-597 (1993).
18. Lasater, E. M. Retinal horizontal cell gap junctional conductance is modulated by dopamine through a cyclic AMP-dependent protein kinase. Proc. Natl Acad. Sci. USA 84, 7319-7323 (1987).
19. DeVries, S. H. & Schwartz, E. A. Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. J. Physiol. 414, 351-375 (1989).
20. Patel, L. S., Mitchell, C. K., Dubinsky, W. P. & O'Brien, J. O. Regulation of gap junction coupling through the neuronal connexin Cx35 by nitric oxide and cGMP. Cell Commun. Adhes. 13, 41-54 (2006).
21. Kothmann, W. W., Massey, S. C. & O'Brien, J. Dopamine D1-receptor-mediated modulation of connexin36 phosphorylation in AII amacrine cells. Invest. Ophthal. Vis. Sci. 49, 1515 (2008).
22. Lasater, E. M. & Dowling, J. E. Dopamine decreases conductance of the electrical junctions between cultured retinal horizontal cells. Proc. Natl Acad. Sci. USA 82, 3025-3029 (1985).
23. Mills, S. L. & Massey, S. C. Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377, 734-737 (1995). This report showed that the gap junctions between AII cells are regulated by dopamine, whereas the gap junctions between AII amacrine cells and ON cone bipolar cells are regulated by nitric oxide.
24. Umino, O., Lee, Y. & Dowling, J. E. Effects of light stimuli on the release of dopamine from interplexiform cells in the white perch retina. Vis. Neurosci. 7, 451-458 (1991).
25. Baldridge, W. H., Weiler, R. & Dowling, J. E. Darksuppression and light-sensitization of horizontal cell responses in the hybrid bass retina. Vis. Neurosci. 12, 611-620 (1995).
26. Bloomfield, S. A. & Völgyi, B. Function and plasticity of homologous coupling between AII amacrine cells. Vision Res. 44, 3297-3306 (2004).
27. Rose, B., Simpson, I. & Loewenstein, W. R. Calcium ion produces graded changes in permeability of membrane channels in cell junction. Nature 267, 625-627 (1977).
28. Peracchia, C. Calcium effects on gap junction structure and cell coupling. Nature 271, 669-671 (1978).
29. Peracchia, C., Wang, X., Li, L. & Peracchia, L. L. Inhibition of calmodulin expression prevents low-pH-induced gap junction uncoupling in Xenopus oocytes. Pflugers Arch. 431, 379-387 (1996).
30. Peracchia, C., Sotkis, A., Wang, X. G., Peracchia, L. L. & Persechini, A. Calmodulin directly gates chemical channels. J. Biol. Chem. 275, 26220-26224 (2000).
31. Török, K., Stauffer, K. & Evans, W. H. Connexin 32 of gap junctions contains two cytoplasmic calmodulinbinding domains. Biochem. J. 326, 479-483 (1997).
32. Lurtz, M. M. & Louis, C. F. Intracellular calcium regulation of connexin43. Am. J. Physiol. Cell Physiol. 293, 1806-1813 (2007).
33. Spray, D. C., Harris, A. L. & Bennett, M. V. Gap junctional conductance is a simple and sensitive function of intracellular pH. Science 211, 712-715 (1981).
34. Church, J. & Baimbridge, K. G. Exposure to high-pH medium increases the conductance and extent of dye coupling between rat hippocampal CA1 pyramidal neurons in vitro. J. Neurosci. 11, 3289-3295 (1991).
35. González, D. et al. Regulation of neuronal connexin-36 channels by pH. Proc. Natl Acad. Sci. USA 105, 17169-17174 (2008).
36. Chesler, M. Regulation and modulation of pH in the brain. Physiol. Rev. 83, 1183-1221 (2003).
37. Spray, D. C., Harris, A. L. & Bennett, M. V. Voltage dependence of junctional conductance in early amphibian embryos. Science 204, 432-434 (1979).
38. Srinivas, M. et al. Voltage dependence of macroscopic and unitary currents of gap junction channels formed by mouse connexin50 expressed in rat neuroblastoma cells. J. Physiol. 517, 673-689 (1999).
39. Moreno, A. P., de Carvalho, A. C., Verselis, V., Eghbali, B. & Spray, D. C. Voltage-dependent gap junction channels are formed by connexin32, the major gap junction protein of rat liver. Biophys. J. 59, 920-925 (1991).
40. Moreno, A. P., Rook, M. B., Fishman, G. I. & Spray, D. C. Gap junction channels: distinct voltage-sensitive and -insensitive conductance states. Biophys. J. 67, 113-119 (1994).
41. Spray, D. C., Chanson, M., Moreno, A. P., Dermietzel, R. & Meda, P. Distinctive gap junction channel types connect WB cells, a clonal cell line derived from rat liver. Am. J. Physiol. 260, 513-527 (1991).
42. Baylor, D. A., Fuortes, M. G. & O'Bryan, P. M. Receptive fields of cones in the retina of the turtle. J. Physiol. 214, 265-294 (1971).
43. Cohen, A. I. Some electron microscopic observations on inter-receptor contacts in the human and macaque retinae. J. Anat. 99, 595-610 (1965).
44. Raviola, E. & Gilula, N. B. Gap junctions between photoreceptor cells in the vertebrate retina. Proc. Natl Acad. Sci. USA 70, 1677-1681 (1973).
45. Kolb, H. The organization of the outer plexiform layer in the retina of the cat: electron microscopic observations. J. Neurocytol. 6, 131-153 (1977).
46. Tsukamoto, Y., Masarachia, P., Schein, S. J. & Sterling, P. Gap junctions between the pedicles of macaque foveal cones. Vision Res. 32, 1809-1815 (1992).
47. Tsukamoto, Y., Morigiwa, K., Ueda, M. & Sterling, P. Microcircuits for the night vision in mouse retina. J. Neurosci. 21, 8616-8623 (2001).
48. Lee, E. J. et al. The immunocytochemical localization of connexin 36 at rod and cone gap junctions in the guinea pig retina. Eur. J. Neurosci. 18, 2925-2934 (2003).
49. Feigenspan, A. et al. Expression of connexin36 in cone pedicles and OFF-cone bipolar cells of the mouse retina. J. Neurosci. 24, 3325-3334 (2004).
50. Li, W. & DeVries, S. H. Separate blue and green cone networks in the mammalian retina. Nature Neurosci. 7, 751-756 (2004).
51. DeVries, S. H., Qi, X., Smith, R., Makous, W. & Sterling, P. Electrical coupling between mammalian cones. Curr. Biol. 12, 1900-1907 (2002). This study showed that coupling between cone photoreceptors results in minor blurring of the image, which is overshadowed by an increased signal-to-noise ratio of cone responses.
52. Hornstein, E. P., Verweij, J., Li, P. H. & Schnapf, J. L. Gap-junctional coupling and absolute sensitivity of photoreceptors in macaque retina. J. Neurosci. 25, 11201-11209 (2005).
53. Dartnell, H. J. A. in The Eye Vol. 2 (ed. Davson, H.) 323-533 (Academic Press, New York, 1962).
54. Hornstein, E. P., Verweij, J. & Schnapf, J. L. Electrical coupling between red and green cones in primate retina. Nature Neurosci. 7, 745-750 (2004).
55. Hsu, A., Smith, R. G., Buchsbaum, G. & Sterling, P. Cost of cone coupling to trichomacy in primate fovea. J. Opt. Soc. Am. A. Opt. Image Sci. Vis. 17, 635-640 (2000).
56. Boycott, B. B. & Kolb, H. The connections between bipolar cells and photoreceptors in the retina of the domestic cat. J. Comp. Neurol. 148, 91-114 (1973).
57. Ghosh, K. K., Bujan, S., Haverkamp, S., Feigenspan, A. & Wässle, H. Types of bipolar cells in the mouse retina. J. Comp. Neurol. 469, 70-82 (2004).
58. Boycott, B. B. & Wässle, H. Morphological classification of bipolar cells of the primate retina. Eur. J. Neurosci. 3, 1069-1088 (1991).
59. Euler, T. & Wässle, H. Immunocytochemical identification of cone bipolar cells in the rat retina. J. Comp. Neurol. 361, 461-478 (1995).
60. Bloomfield, S. A. & Dacheux, R. F. Rod vision: pathways and processing in the mammalian retina. Prog. Retin. Eye Res. 20, 351-384 (2001).
61. Raviola, E. & Gilula, N. B. Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits. J. Cell Biol. 65, 192-222 (1975).
62. Nelson, R. Cat cones have rod input: a comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. J. Comp. Neurol. 172, 109-135 (1977). This study was the first to show that rod signals can be detected in cones, presumably as a result of their interconnecting gap junctions.
63. Schneeweis, D. M. & Schnapf, J. L. Photovoltage of rods and cones in the macaque retina. Science 268, 1053-1056 (1995).
64. DeVries, S. H. & Baylor, D. A. An alternative pathway for signal flow from rod photoreceptors to ganglion cells in mammalian retina. Proc. Natl Acad. Sci. USA 92, 10658-10662 (1995).
65. Völgyi, B., Deans, M. R., Paul, D. L. & Bloomfield, S. A. Convergence and segregation of the multiple rod pathways in mammalian retina. J. Neurosci. 24, 11182-11192 (2004).
66. Blakemore, C. B. & Rushton, W. A. The rod increment threshold during dark adaptation in normal and rod monochromat. J. Physiol. 181, 629-640 (1965).
67. Conner, J. D. The temporal properties of rod vision. J. Physiol. 332, 139-155 (1982).
68. Hess, R. F. & Nordby, K. Spatial and temporal properties of human rod vision in the achromat. J. Physiol. 371, 387-406 (1986).
69. Sharpe, L. T. & Stockman, A. Rod pathways: the importance of seeing nothing. Trends Neurosci. 22, 497-504 (1999).
70. Deans, M. R., Volgyi, B., Goodenough, D. A., Bloomfield, S. A. & Paul, D. L. Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 36, 703-712 (2002). This article showed that Cx36-containing gap junctions form obligatory elements in the transmission of rod signals in the retina.
71. Dunn, F. A., Doan, T., Sampath, A. P. & Rieke, F. Controlling the gain of rod-mediated signals in the mammalian retina. J. Neurosci. 26, 3959-3970 (2006).
72. Smith, R. G., Freed, M. A. & Sterling, P. Microcircuitry of the dark-adapted cat retina: functional architecture of the rod-cone network. J. Neurosci. 6, 3505-3517 (1986).
73. Soucy, E., Wang, Y., Nirenberg, S., Nathans, J. & Meister, M. A novel signaling pathway from rod photoreceptors to ganglion cells in mammalian retina. Neuron 21, 481-493 (1998).
74. Boycott, B. B. & Dowling, J. E. Organization of the primate retina: light microscopy. Philos. Trans. R. Soc. Lond. B Biol. Sci. 255, 109-184 (1969).
75. Hack, I., Peichl, L. & Brandstätter, J. H. An alternative pathway for rod signals in the rodent retina: rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors. Proc. Natl Acad. Sci. USA 96, 14130-14135 (1999).
76. Fyk-Kolodziej, B., Qin, P. & Pourcho, R. G. Identification of a cone bipolar cell in cat retina which has input from both rod and cone photoreceptors. J. Comp. Neurol. 464, 104-113 (2003).
77. Li, W., Keung, J. W. & Massey, S. C. Direct synaptic connections between rods and OFF cone bipolar cells in the rabbit retina. J. Comp. Neurol. 474, 1-12 (2004).
78. Kolb, H. The connections between horizontal cells and photoreceptors in the retina of the cat: electron microscopy of Golgi preparations. J. Comp. Neurol. 155, 1-14 (1974).
79. Yamada, E. & Ishikawa, T. The fine structure of the horizontal cells in some vertebrate retinae. Cold Spring Harb. Symp. Quant. Biol. 30, 383-392 (1965).
80. Vaney, D. Many diverse types of retinal neurons show tracer coupling when injected with biocytin and neurobiotin. Neurosci. Lett. 125, 187-190 (1991). This study was the first to demonstrate that biotinylated tracers permeate gap junctions and can be used to visualize electrical synapses.
81. Bloomfield, S. A., Xin, D. & Persky, S. E. A comparison of receptive field and tracer coupling size of horizontal cells in the rabbit retina. Vis. Neurosci. 12, 985-999 (1995).
82. Dacheux, R. F. & Raviola, E. Horizontal cells in the retina of the rabbit. J. Neurosci. 2, 1486-1493 (1982).
83. Dacey, D. M. Primate retina: cell types, circuits and color opponency. Prog. Retin. Eye Res. 18, 737-763 (1999).
84. Naka, K. I. & Rushton, W. A. The generation and spread of S-potentials in fish (Cyprinidae). J. Physiol. 192, 437-461 (1967).
85. Bloomfield, S. A. & Miller, R. F. A physiological and morphological study of the horizontal cell types in the rabbit retina. J. Comp. Neurol. 208, 288-303 (1982).
86. Hombach, S. et al. Functional expression of connexin57 in horizontal cells of the mouse retina. Eur. J. Neurosci. 19, 2633-2640 (2004).
87. Shelley, J. et al. Horizontal cell receptive fields are reduced in connexin57-deficient mice. Eur. J. Neurosci. 23, 3176-3186 (2006). This report showed that disruption of horizontal cell gap junctions in the connexin57-deficient mouse retina results in a dramatic reduction in their receptive field sizes.
88. Werblin, F. S. & Dowling, J. E. Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J. Neurophysiol. 32, 339-355 (1969).
89. Kaneko, A. Physiological and morphological identification of horizontal, bipolar and amacrine cells in goldfish retina. J. Physiol. 207, 623-633 (1970).
90. Naka, K. I. & Nye, P. W. Role of horizontal cells in organization of the catfish retinal receptive field. J. Neurophysiol. 34, 785-801 (1971).
91. Naka, K. I. & Witkovsky, P. Dogfish ganglion cell discharge resulting from extrinsic polarization of the horizontal cells. J. Physiol. 223, 449-460 (1972).
92. Marchiafava, P. L. Horizontal cells influence membrane potential of bipolar cells in the retina of the turtle. Nature 275, 141-142 (1978).
93. Mangel, S. C. & Miller, R. F. Horizontal cells contribute to the receptive field surround of ganglion cells in the rabbit retina. Brain Res. 414, 182-186 (1987).
94. Kamermans, M. et al. Hemichannel-mediated inhibition in the outer retina. Science 292, 1178-1180 (2001).
95. Dedek, K. et al. Ganglion cell adaptability: does coupling of horizontal cells play a role? PLoS ONE 5, e1714 (2008).
96. Hedden, W. L. & Dowling, J. E. The interplexiform cell system. II. Effects of dopamine on goldfish retinal neurones. Proc. R. Soc. Lond. B Biol. Sci. 201, 27-55 (1978).
97. Piccolino, M., Neyton, J. & Gerschenfeld, H. M. Decrease of gap junction permeability induced by dopamine and cyclic adenosine 3′:5′-monophosphate in horizontal cells of turtle retina. J. Neurosci. 4, 2477-2488 (1984).
98. Baldridge, W. H., Ball, A. K. & Miller, R. G. Dopaminergic regulation of horizontal cell gap junction particle density in goldfish retina. J. Comp. Neurol. 265, 428-436 (1987).
99. McMahon, D. G., Knapp, A. G. & Dowling, J. E. Horizontal cell gap junctions: single-channel conductance and modulation by dopamine. Proc. Natl Acad. Sci. USA 86, 7639-7643 (1989). This report showed that dopamine can directly modulate the conductance of gap junctions connecting neighbouring horizontal cells.
100. Kurz-Isler, G., Voigt, T. & Wolburg, H. Modulation of connexon densities in gap junctions of horizontal cell perikarya and axon terminals in fish retina: effects of light/dark cycles, interruption of the optic nerve and application of dopamine. Cell Tissue Res. 268, 267-275 (1992).
101. McMahon, D. G. & Brown, D. R. Modulation of gapjunction channel gating at zebrafish retinal electrical synapses. J. Neurophysiol. 72, 2257-2268 (1994).
102. DeVries, S. H. & Schwartz, E. A. Hemi-gap-junction channels in solitary horizontal cells of the catfish retina. J. Physiol. 445, 201-230 (1992).
103. Lu, C. & McMahon, D. G. Modulation of hybrid bass retinal gap junctional channel gating by nitric oxide. J. Physiol. 499, 689-699 (1997).
104. Pottek, M., Schultz, K. & Weiler, R. Effects of nitric oxide on the horizontal cell network and dopamine release in the carp retina. Vision Res. 37, 1091-1102 (1997).
105. Hampson, E. C., Weiler, R. & Vaney, D. I. pH-gated dopaminergic modulation of horizontal cell gap junctions in mammalian retina. Proc. Biol. Sci. 255, 67-72 (1994).
106. Mills, S. L. & Massey, S. E. l-Arginine uncouples A-type horizontal cells in rabbit retina. Invest. Ophthalmol. Vis. Sci. (Suppl.) 34, 1382 (1993).
107. Godley, B. F. & Wurtman, R. J. Release of endogenous dopamine from the superfused rabbit retina in vitro: effect of light stimulation. Brain Res. 452, 393-395 (1988).
108. Kirsch, M. & Wagner, H. J. Release pattern of endogenous dopamine in teleost retinae during light adaptation and pharmacological stimulation. Vision Res. 29, 147-154 (1989).
109. Zemel, E., Eyal, O., Lei, B. & Perlman, I. NADPH diaphorase activity in mammalian retinas is modulated by the state of visual adaptation. Vis. Neurosci. 13, 865-871 (1996).
110. Neal, M., Cunningham, J. & Matthews, K. Selective release of nitric oxide from retinal amacrine and bipolar cells. Invest. Ophthalmol. Vis. Sci. 39, 850-853 (1998).
111. Mangel, S. C. & Dowling, J. E. Responsiveness and receptive field size of carp horizontal cells are reduced by prolonged darkness and dopamine. Science 229, 1107-1109 (1985).
112. Mangel, S. C. & Dowling, J. E. The interplexiformhorizontal cell system of the fish retina: effects of dopamine, light stimulation and time in the dark. Proc. R. Soc. Lond. B Biol. Sci. 231, 91-121 (1987).
113. Tornqvist, K., Yang, X. L. & Dowling, J. E. Modulation of cone horizontal cell activity in the teleost fish retina. III. Effects of prolonged darkness and dopamine on electrical coupling between horizontal cells. J. Neurosci. 8, 2279-2288 (1988).
114. Rodieck, R. W. & Stone, J. Analysis of receptive fields of cat retinal ganglion cells. J. Neurophysiol. 28, 832-849 (1965).
115. Peichl, L. & Wässle, H. The structural correlate of the receptive field centre of α cells in the cat retina. J. Physiol. 341, 309-324 (1983).
116. Muller, J. F. & Dacheux, R. F. Alpha ganglion cells of the rabbit retina lose antagonistic surround responses under dark adaptation. Vis. Neurosci. 14, 395-401 (1997).
117. Balboa, R. M. & Grzywacz, N. M. The role of early retinal inhibition: more than maximizing luminance information. Vis. Neurosci. 17, 77-89 (2000).
118. Balboa, R. M. & Grzywacz, N. M. The minimal localasperity hypothesis of early retinal lateral inhibition. Neural Comput. 12, 1485-1517 (2000).
119. Famiglietti, E. V. Jr & Kolb, H. A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Res. 84, 293-300 (1975).
120. Strettoi, E., Dacheux, R. F. & Raviola, E. Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina. J. Comp. Neurol. 295, 449-466 (1990).
121. Feigenspan, A., Teubner, B., Willecke, K. & Weiler, R. Expression of neuronal connexin36 in AII amacrine cells of the mammalian retina. J. Neurosci. 21, 230-239 (2001).
122. Mills, S. L., O'Brien, J. J., Li, W., O'Brien, J. & Massey, S. C. Rod pathways in the mammalian retina use connexin36. J. Comp. Neurol. 436, 336-350 (2001).
123. Lin, B., Jakobs, T. C. & Masland, R. H. Different functional types of bipolar cells use different gapjunctional proteins. J. Neurosci. 25, 6696-6701 (2005).
124. Han, Y. & Massey, S. C. Electrical synapses in retinal ON cone bipolar cells: subtype-specific expression of connexins. Proc. Natl Acad. Sci. USA 102, 13313-13318 (2005).
125. Dedek, K. et al. Localization of the heterotypic gap junctions composed of connexin45 and connexin36 in the rod pathway of the mouse retina. Eur. J. Neurosci. 24, 1675-1686 (2006).
126. Li, X. et al. Connexin45-containing neuronal gap junctions in rodent retina also contain connexin36 in both apposing hemiplaques, forming bihomotypic gap junctions, with scaffolding contributed by zona occludens-1. J. Neurosci. 28, 9769-9789 (2008).
127. Mills, S. L. & Massey, S. C. A series of biotinylated tracers distinguishes three types of gap junction in retina. J. Neurosci. 20, 8629-8636 (2000).
128. Veruki, M. L. & Hartveit, E. Electrical synapses mediate signal transmission in the rod pathway of the mammalian retina. J. Neurosci. 22, 10558-10566 (2002).
129. Güldenagel, M. et al. Visual transmission deficits in mice with targeted disruption of the gap junction gene connexin36. J. Neurosci. 21, 6036-6044 (2001).
130. Xin, D. & Bloomfield, S. A. Comparison of the responses of AII amacrine cells in the dark- and lightadapted rabbit retina. Vis. Neurosci. 16, 653-665 (1999).
131. Smith, R. G. & Vardi, N. Simulation of the AII amacrine cell of mammalian retina: functional consequences of electrical coupling and regenerative membrane properties. Vis. Neurosci. 12, 851-860 (1995).
132. Voigt, T. & Wässle, H. Dopaminergic innervation of AII amacrine cells in mammalian retina. J. Neurosci. 7, 4115-4128 (1987).
133. Hampson, E. C., Vaney, D. I. & Weiler, R. Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. J. Neurosci. 12, 4911-4922 (1992).
134. Urschel, S. et al. Protein kinase A-mediated phosphorylation of connexin36 in mouse retina results in decreased gap junctional communication between AII amacrine cells. J. Biol. Chem. 281, 33163-33171 (2006).
135. Vaney, D. I. Territorial organization of directionselective ganglion cells in rabbit retina. J. Neurosci. 14, 6301-6316 (1994).
136. Xin, D. & Bloomfield, S. A. Tracer coupling pattern of amacrine cells in the rabbit retina. J. Comp. Neurol. 383, 512-528 (1997).
137. Völgyi, B., Chheda, S. & Bloomfield, S. A. Tracer coupling patterns of the ganglion cell subtypes in the mouse retina. J. Comp. Neurol. 512, 664-687 (2009).
138. Bloomfield, S. A. & Xin, D. A comparison of receptivefield and tracer-coupling size of amacrine and ganglion cells in the rabbit retina. Vis. Neurosci. 14, 1153-1165 (1997).
139. Mastronarde, D. N. Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells. J. Neurophysiol. 49, 303-324 (1983).
140. Mastronarde, D. N. Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. J. Neurophysiol. 49, 325-349 (1983).
141. Mastronarde, D. N. Interactions between ganglion cells in cat retina. J. Neurophysiol. 49, 350-365 (1983). This study was the first to report concerted activity between neighbouring ganglion cells, suggesting direct electrical coupling years before gap junctions between ganglion cells were demonstrated.
142. Arnett, D. & Spraker, T. E. Cross-correlation analysis of the maintained discharge of rabbit retinal ganglion cells. J. Physiol. 317, 29-47 (1981).
143. Brivanlou, I. H., Warland, D. K. & Meister, M. Mechanisms of concerted firing among retinal ganglion cells. Neuron 20, 527-539 (1998). This study showed that different types of ganglion cell and amacrine cell electrical coupling result in different patterns of correlated spike activity.
144. DeVries, S. H. Correlated firing in rabbit retinal ganglion cells. J. Neurophysiol. 81, 908-920 (1999).
145. Hu, E. H. & Bloomfield, S. A. Gap junctional coupling underlies the short-latency spike synchrony of retinal α ganglion cells. J. Neurosci. 23, 6768-6777 (2003).
146. Shlens, J., Rieke, F. & Chichilnisky, E. Synchronized firing in the retina. Curr. Opin. Neurobiol. 18, 396-402 (2008).
147. Castelo-Branco, M., Neuenschwander, S. & Singer, W. Synchronization of visual responses between the cortex, lateral geniculate nucleus and retina in the anasthetized cat. J. Neurosci. 18, 6395-63410 (1998).
148. Schnitzer, M. J. & Meister, M. Multineuronal firing patterns in the signal from eye to brain. Neuron 37, 499-511 (2003).
149. Meister, M. & Berry, M. The neural code of the retina. Neuron 22, 435-450 (1999).
150. Alonso, J. M., Usrey, W. M. & Reid, R. C. Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 383, 815-819 (1996).
151. Stevens, C. F. & Zador, A. M. Input synchrony and irregular firing of cortical neurons. Nature Neurosci. 1, 210-217 (1998).
152. Usrey, W. M. & Reid, R. C. Synchronous activity in the visual system. Annu. Rev. Physiol. 61, 435-456 (1999).
153. Singer, W. Neuronal synchrony: a versatile code for the definition of relations? Neuron 24, 49-65 (1999).
154. Mills, S. L. et al. Dopaminergic modulation of tracer coupling in a ganglion-amacrine cell network. Vis. Neurosci. 24, 593-608 (2007).
155. Naus, C. C. & Bani-Yaghoub, M. Gap junctional communication in the developing central nervous system. Cell Biol. Int. 22, 751-763 (1998).
156. Grubb, M. S. & Thompson, I. D. The influence of early experience on the development of sensory systems. Curr. Opin. Neurobiol. 14, 503-512 (2004).
157. Syed, M. M., Lee, S., He, S. & Zhou, Z. J. Spontaneous waves in the ventricular zone of developing mammalian retina. J. Neurophysiol. 91, 1999-2009 (2004).
158. Sernagor, E., Eglen, S. J. & Wong, R. O. Development of retinal ganglion cell structure and function. Prog. Retin. Eye Res. 20, 139-174 (2001).
159. Ackert, J. M. et al. Light induced changes in spike synchronization between coupled ON direction selective ganglion cells in the mammalian retina. J. Neurosci. 26, 4206-4215 (2006). This study showed that changes in the synchronous activity of coupled ON direction-selective ganglion cells provide a mechanism to encode the direction of stimulus motion.
160. Oyster, C. W. The analysis of image motion by the retina. J. Physiol. 199, 613-635 (1968).
161. Oyster, C. W., Simpson, J. I., Takahashi, E. S. & Soodak, R. E. Retinal ganglion cells projecting to the rabbit accessory optic system. J. Comp. Neurol. 190, 49-61 (1980).
162. Buhl, E. H. & Peichl, L. Morphology of rabbit retinal ganglion cells projecting to the medial terminal nucleus of the accessory optic system. J. Comp. Neurol. 253, 163-174 (1986).
163. Pu, M. L. & Amthor, F. R. Dendritic morphologies of retinal ganglion cells projecting to the nucleus of the optic tract in the rabbit. J. Comp. Neurol. 302, 657-674 (1990).
164. Simpson, J. I. The accessory optic sytem. Annu. Rev. Neurosci. 7, 13-41 (1984).
165. Nakase, T. & Nasus, C. C. G. Gap junctions and neurological disorders of the central nervous system. Biochim. Biophys. Acta 1662, 149-158 (2004).
166. O'Brien, J. J. et al. Coupling between A-type horizontal cells is mediated by connexin 50 gap junctions in the rabbit retina. J. Neurosci. 26, 11624-11636 (2006).
167. Schubert, T. et al. Connexin36 mediates gap junctional coupling of alpha-ganglion cells in mouse retina. J. Comp. Neurol. 485, 191-201 (2005).
168. Schubert, T., Maxeiner, S., Krüger, O., Willecke, K. & Weiler, R. Connexin45 mediates gap junctional coupling of bistratified ganglion cells in the mouse retina. J. Comp. Neurol. 490, 29-39 (2005).
169. Völgyi, B., Abrams, J., Paul, D. L. & Bloomfield, S. A. Morphology and tracer coupling of alpha ganglion cells in the mouse retina. J. Comp. Neurol. 492, 66-77 (2005).