Circuit Functions of Gap Junctions in the Mammalian Retina

The Senses: A Comprehensive Reference

Volumn 1, Issue , 2008, Pages 457-471

  Massey, S C ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Amacrine cells; Ganglion cells; Gap junction; Horizontal cells; Photoreceptors; Retina

Indexed keywords

EID: 84882535134     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-012370880-9.00399-6     Document Type: Chapter

References (96)

1. Ackert J.M., Wu S.H., Lee J.C., Abrams J., Hu E.H., Perlman I., Bloomfield S.A. Light-induced changes in spike synchronization between coupled ON direction selective ganglion cells in the mammalian retina. J. Neurosci. 2006, 26:4206-4215.
2. Ahnelt P.K., Pflug R. Telodendrial contacts between foveolar cone pedicles in the human retina. Experientia 1986, 42:298-300.
3. Ahnelt P., Keri C., Kolb H. Identification of pedicles of putative blue-sensitive cones in the human retina. J. Comp. Neurol. 1990, 293:39-53.
4. Baylor D.A., Nunn B.J., Schnapf J.L. Spectral sensitivity of cones of the monkey Macaca fascicularis. J. Physiol. 1987, 390:145-160.
5. Bloomfield S.A., Dacheux R.F. Rod vision: pathways and processing in the mammalian retina. Prog. Retin. Eye Res. 2001, 20:351-384.
6. Bloomfield S.A., Volgyi B. Function and plasticity of homologous coupling between AII amacrine cells. Vision Res. 2004, 44:3297-3306.
7. 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. 1995, 12:985-999.
8. Cadetti L., Thoreson W.B. Feedback effects of horizontal cell membrane potential on cone calcium currents studied with simultaneous recordings. J. Neurophysiol. 2006, 95:1992-1995.
9. Cohen E., Sterling P. Accumulation of (3H)glycine by cone bipolar neurons in the cat retina. J. Comp. Neurol. 1986, 250:1-7.
10. Cusato K., Zakevicius J., Ripps H. An experimental approach to the study of gap-junction-mediated cell death. Biol. Bull. 2003, 205:197-199.
11. Dacheux R.F., Raviola E. Horizontal cells in the retina of the rabbit. J. Neurosci. 1982, 2:1486-1493.
12. Deans M.R., Paul D.L. Mouse horizontal cells do not express connexin26 or connexin36. Cell. Adhes. Commun. 2001, 8:361-366.
13. 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 2002, 36:703-712.
14. DeBoer D.J., Vaney D.I. Gap-junction communication between subtypes of direction-selective ganglion cells in the developing retina. J. Comp. Neurol. 2005, 482:85-93.
15. Dedek K., Schultz K., Pieper M., Dirks P., Maxeiner S., Willecke K., Weiler R., Janssen-Bienhold U. Localization of heterotypic gap junctions composed of connexin45 and connexin36 in the rod pathway of the mouse retina. Eur. J. Neurosci. 2006, 24:1675-1686.
16. DeVries S.H. Correlated firing in rabbit retinal ganglion cells. J. Neurophysiol. 1999, 81:908-920.
17. 2+ current in mammalian cone photoreceptors. Neuron 2001, 32:1107-1117.
18. DeVries S.H., Qi X., Smith R., Makous W., Sterling P. Electrical coupling between mammalian cones. Curr. Biol. 2002, 12:1900-1907.
19. Dunn F.A., Doan T., Sampath A.P., Rieke F. Controlling the gain of rod-mediated signals in the mammalian retina. J. Neurosci. 2006, 26:3959-3970.
20. Famiglietti E.V., Kolb H. A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Res. 1975, 84:293-300.
21. Feigenspan A., Janssen-Bienhold U., Hormuzdi S., Monyer H., Degen J., Sohl G., Willecke K., Ammermuller J., Weiler R. Expression of connexin36 in cone pedicles and OFF-cone bipolar cells of the mouse retina. J. Neurosci. 2004, 24:3325-3334.
22. Feigenspan A., Teubner B., Willecke K., Weiler R. Expression of neuronal connexin36 in AII amacrine cells of the mammalian retina. J. Neurosci. 2001, 21:230-239.
23. Galarreta M., Hestrin S. Electrical synapses between GABA-releasing interneurons. Nat. Rev. Neurosci. 2001, 2:425-433.
24. Guldenagel M., Sohl G., Plum A., Traub O., Teubner B., Weiler R., Willecke K. Expression patterns of connexin genes in mouse retina. J. Comp. Neurol. 2000, 425:193-201.
25. Hampson E.C., Vaney D.I., Weiler R. Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. J. Neurosci. 1992, 12:4911-4922.
26. Hampson E.C., Weiler R., Vaney D.I. pH-gated dopaminergic modulation of horizontal cell gap junctions in mammalian retina. Proc. R. Soc. Lond. Ser B Biol. Sci. 1994, 255:67-72.
27. Han Y., Massey S.C. Electrical synapses in retinal ON cone bipolar cells: subtype-specific expression of connexins. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:13313-13318.
28. He S., Weiler R., Vaney D.I. Endogenous dopaminergic regulation of horizontal cell coupling in the mammalian retina. J. Comp. Neurol. 2000, 418:33-40.
29. Hidaka S., Akahori Y., Kurosawa Y. Dendrodendritic electrical synapses between mammalian retinal ganglion cells. J. Neurosci. 2004, 24:10553-10567.
30. Hombach S., Janssen-Bienhold U., Sohl G., Schubert T., Bussow H., Ott T., Weiler R., Willecke K. Functional expression of connexin57 in horizontal cells of the mouse retina. Eur. J. Neurosci. 2004, 19:2633-2640.
31. Hornstein E.P., Verweij J., Schnapf J.L. Electrical coupling between red and green cones in primate retina. Nat. Neurosci. 2004, 7:745-750.
32. Hornstein E.P., Verweij J., Li P.H., Schnapf J.L. Gap-junctional coupling and absolute sensitivity of photoreceptors in macaque retina. J. Neurosci. 2005, 25:11201-11209.
33. Hoshi H., O'Brien J., Mills S.L. A novel fluorescent tracer for visualizing coupled cells in neural circuits of living tissue. J. Histochem. Cytochem. 2006, 54:1169-1176.
34. Hsu A., Smith R.G., Buchsbaum G., Sterling P. Cost of cone coupling to trichromacy in primate fovea. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 2000, 17:635-640.
35. Hu E.H., Bloomfield S.A. Gap junctional coupling underlies the short-latency spike synchrony of retinal alpha ganglion cells. J. Neurosci. 2003, 23:6768-6777.
36. Kamasawa N., Furman C.S., Davidson K.G., Sampson J.A., Magnie A.R., Gebhardt B.R., Kamasawa M., Yasumura T., Zumbrunnen J.R., Pickard G.E., Nagy J.I., Rash J.E. Abundance and ultrastructural diversity of neuronal gap junctions in the OFF and ON sublaminae of the inner plexiform layer of rat and mouse retina. Neuroscience 2006, 142:1093-1117.
37. Kamermans M., Spekreijse H. The feedback pathway from horizontal cells to cones. A mini review with a look ahead. Vision Res. 1999, 39:2449-2468.
38. Kamermans M., Fahrenfort I., Schultz K., Janssen-Bienhold U., Sjoerdsma T., Weiler R. Hemichannel-mediated inhibition in the outer retina. Science 2001, 292:1178-1180.
39. Kolb H. The organization of the outer plexiform layer in the retina of the cat: electron microscopic observations. J. Neurocytol. 1977, 6:131-153.
40. Lee E.J., Han J.W., Kim H.J., Kim I.B., Lee M.Y., Oh S.J., Chung J.W., Chun M.H. The immunocytochemical localization of connexin 36 at rod and cone gap junctions in the guinea pig retina. Eur. J. Neurosci. 2003, 18:2925-2934.
41. Li W., DeVries S.H. Separate blue and green cone networks in the mammalian retina. Nat. Neurosci. 2004, 7:751-756.
42. Lin B., Jakobs T.C., Masland R.H. Different functional types of bipolar cells use different gap-junctional proteins. J. Neurosci. 2005, 25:6696-6701.
43. Marc R.E., Jones B.W. Molecular phenotyping of retinal ganglion cells. J. Neurosci. 2002, 22:413-427.
44. Massey S.C., O'Brien J.J., Trexler E.B., Li W., Keung J.W., Mills S.L., O'Brien J. Multiple neuronal connexins in the mammalian retina. Cell Commun. Adhes. 2003, 10:425-430.
45. Maxeiner S., Dedek K., Janssen-Bienhold U., Ammermuller J., Brune H., Kirsch T., Pieper M., Degen J., Kruger O., Willecke K., Weiler R. Deletion of connexin45 in mouse retinal neurons disrupts the rod/cone signaling pathway between AII amacrine and ON cone bipolar cells and leads to impaired visual transmission. J. Neurosci. 2005, 25:566-576.
46. McGuire B.A., Stevens J.K., Sterling P. Microcircuitry of bipolar cells in cat retina. J. Neurosci. 1984, 4:2920-2938.
47. Meister M. Multineuronal codes in retinal signaling. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:609-614.
48. Menichella D.M., Goodenough D.A., Sirkowski E., Scherer S.S., Paul D.L. Connexins are critical for normal myelination in the CNS. J. Neurosci. 2003, 23:5963-5973.
49. Mills S.L., Massey S.C. Distribution and coverage of A- and B-type horizontal cells stained with Neurobiotin in the rabbit retina. Vis. Neurosci. 1994, 11:549-560.
50. Mills S.L., Massey S.C. Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 1995, 377:734-737.
51. Mills S.L., Massey S.C. A series of biotinylated tracers distinguishes three types of gap junction in retina. J. Neurosci. 2000, 20:8629-8636.
52. 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. 2001, 436:336-350.
53. 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. 1977, 172:109-135.
54. O'Brien J.J., Li W., Pan F., Keung J., O'Brien J., Massey S.C. Coupling between A-type horizontal cells is mediated by connexin 50 gap junctions in the rabbit retina. J. Neurosci. 2006, 26:11624-11636.
55. O'Brien J., Nguyen H.B., Mills S.L. Cone photoreceptors in bass retina use two connexins to mediate electrical coupling. J. Neurosci. 2004, 24:5632-5642.
56. Pan F., Massey S.C. Rod and cone input to horizontal cells in the rabbit retina. J. Comp. Neurol. 2007, 500:815-831.
57. Pang J.J., Abd-El-Barr M.M., Gao F., Bramblett D.E., Paul D.L., Wu S.M. Relative contributions of rod and cone bipolar cell inputs to AII amacrine cell light responses. J. Physiol. 2007, 580:397-410.
58. Peichl L., Gonzalez-Soriano J. Morphological types of horizontal cell in rodent retinae: a comparison of rat, mouse, gerbil, and guinea pig. Vis. Neurosci. 1994, 11:501-517.
59. Raviola E., Gilula N.B. Gap junctions between photoreceptor cells in the vertebrate retina. Proc. Natl. Acad. Sci. U. S. A. 1973, 70:1677-1681.
60. 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. 1975, 65:192-222.
61. Ripps H. Cell death in retinitis pigmentosa: gap junctions and the 'bystander' effect. Exp. Eye Res. 2002, 74:327-336.
62. Schneeweis D.M., Schnapf J.L. Photovoltage of rods and cones in the macaque retina. Science 1995, 268:1053-1056.
63. Schneeweis D.M., Schnapf J.L. The photovoltage of macaque cone photoreceptors: adaptation, noise, and kinetics. J. Neurosci. 1999, 19:1203-1216.
64. Schubert T., Degen J., Willecke K., Hormuzdi S.G., Monyer H., Weiler R. Connexin36 mediates gap junctional coupling of alpha-ganglion cells in mouse retina. J. Comp. Neurol. 2005, 485:191-201.
65. Schubert T., Maxeiner S., Kruger O., Willecke K., Weiler R. Connexin45 mediates gap junctional coupling of bistratified ganglion cells in the mouse retina. J. Comp. Neurol. 2005, 490:29-39.
66. Shields C.R., Klooster J., Claassen Y., Kamermans M., Zoidl G., Dermietzel R. Horizontal cell-specific expression of connexin 52.6 & connexin 55.5 in the zebrafish retina. Invest. Ophthalmol. Vis. Sci. 2005, 46. e-abstract 599.
67. Shlens J., Field G.D., Gauthier J.L., Grivich M.I., Petrusca D., Sher A., Litke A.M., Chichilnisky E.J. The structure of multi-neuron firing patterns in primate retina. J. Neurosci. 2006, 26:8254-8266.
68. 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. 1995, 12:851-860.
69. Smith R.G., Freed M.A., Sterling P. Microcircuitry of the dark-adapted cat retina: functional architecture of the rod-cone network. J. Neurosci. 1986, 6:3505-3517.
70. Srinivas M., Costa M., Gao Y., Fort A., Fishman G.I., Spray D.C. Voltage dependence of macroscopic and unitary currents of gap junction channels formed by mouse connexin50 expressed in rat neuroblastoma cells. J. Physiol. (Lond.) 1999, 517:673-689.
71. Strettoi E., Dacheux R.F., Raviola E. Cone bipolar cells as interneurons in the rod pathway of the rabbit retina. J. Comp. Neurol. 1994, 347:139-149.
72. Strettoi E., Raviola E., Dacheux R.F. Synaptic connections of the narrow-field, bistratified rod amacrine cell (AII) in the rabbit retina. J. Comp. Neurol. 1992, 325:152-168.
73. Teranishi T., Negishi K., Kato S. Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina. Nature 1983, 301:243-246.
74. Teranishi T., Negishi K., Kato S. Regulatory effect of dopamine on spatial properties of horizontal cells in carp retina. J. Neurosci. 1984, 4:1271-1280.
75. Thompson R.J., Zhou N., MacVicar B.A. Ischemia opens neuronal gap junction hemichannels. Science 2006, 312:924-927.
76. Trexler E.B., Li W., Massey S.C. Simultaneous contribution of two rod pathways to AII amacrine and cone bipolar cell light responses. J. Neurophysiol. 2005, 93:1476-1485.
77. Trexler E.B., Li W., Mills S.L., Massey S.C. Coupling from AII amacrine cells to ON cone bipolar cells is bidirectional. J. Comp. Neurol. 2001, 437:408-422.
78. Tsukamoto Y., Masarachia P., Schein S.J., Sterling P. Gap junctions between the pedicles of macaque foveal cones. Vision Res. 1992, 32:1809-1815.
79. Tsukamoto Y., Morigiwa K., Ueda M., Sterling P. Microcircuits for night vision in mouse retina. J. Neurosci. 2001, 21:8616-8623.
80. Usrey W.M., Reppas J.B., Reid R.C. Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus. Nature 1998, 395:384-387.
81. Vaney D.I. Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neurosci. Lett. 1991, 125:187-190.
82. Vaney D.I. The coupling pattern of axon-bearing horizontal cells in the mammalian retina. Proc. R. Soc. Lond. Ser. B Biol. Sci. 1993, 252:93-101.
83. Vaney D.I. Territorial organization of direction-selective ganglion cells in rabbit retina. J. Neurosci. 1994, 14:6301-6316.
84. Vaney D.I., Nelson J.C., Pow D.V. Neurotransmitter coupling through gap junctions in the retina. J. Neurosci. 1998, 18:10594-10602.
85. Vardi N., Smith R.G. The AII amacrine network: coupling can increase correlated activity. Vision Res. 1996, 36:3743-3757.
86. Veruki M.L., Hartveit E. AII (Rod) amacrine cells form a network of electrically coupled interneurons in the mammalian retina. Neuron 2002, 33:935-946.
87. Veruki M.L., Hartveit E. Electrical synapses mediate signal transmission in the rod pathway of the mammalian retina. J. Neurosci. 2002, 22:10558-10566.
88. Vessey J.P., Lalonde M.R., Mizan H.A., Welch N.C., Kelly M.E., Barnes S. Carbenoxolone inhibition of voltage-gated Ca channels and synaptic transmission in the retina. J. Neurophysiol. 2004, 92:1252-1256.
89. Vessey J.P., Stratis A.K., Daniels B.A., Da Silva N., Jonz M.G., Lalonde M.R., Baldridge W.H., Barnes S. Proton-mediated feedback inhibition of presynaptic calcium channels at the cone photoreceptor synapse. J. Neurosci. 2005, 25:4108-4117.
90. Volgyi B., Abrams J., Paul D.L., Bloomfield S.A. Morphology and tracer coupling pattern of alpha ganglion cells in the mouse retina. J. Comp. Neurol. 2005, 492:66-77.
91. Volgyi B., Deans M.R., Paul D.L., Bloomfield S.A. Convergence and segregation of the multiple rod pathways in mammalian retina. J. Neurosci. 2004, 24:11182-11192.
92. Wässle H. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 2004, 5:747-757.
93. Wassle H., Grunert U., Chun M.H., Boycott B.B. The rod pathway of the macaque monkey retina: identification of AII-amacrine cells with antibodies against calretinin. J. Comp. Neurol. 1995, 361:537-551.
94. Willecke K., Eiberger J., Degen J., Eckardt D., Romualdi A., Guldenagel M., Deutsch U., Sohl G. Structural and functional diversity of connexin genes in the mouse and human genome. Biol. Chem. 2002, 383:725-737.
95. Xin D., Bloomfield S.A. Dark- and light-induced changes in coupling between horizontal cells in mammalian retina. J. Comp. Neurol. 1999, 405:75-87.
96. Xin D., Bloomfield S.A. Comparison of the responses of AII amacrine cells in the dark- and light-adapted rabbit retina. Vis. Neurosci. 1999, 16:653-665.