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Gap junctional regulatory mechanisms in the AII amacrine cell of the rabbit retina

Published online by Cambridge University Press:  01 September 2004

XIAO-BO XIA  and
STEPHEN L. MILLS
XIAO-BO XIA
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas at Houston—Health Science Center, Houston
STEPHEN L. MILLS
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas at Houston—Health Science Center, Houston
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Abstract

Gap junctions are commonplace in retina, often between cells of the same morphological type, but sometimes linking different cell types. The strength of coupling between cells derives from the properties of the connexins, but also is regulated by the intracellular environment of each cell. We measured the relative coupling of two different gap junctions made by AII amacrine cells of the rabbit retina. Permeability to the tracer Neurobiotin was measured at different concentrations of the neuromodulators dopamine, nitric oxide, or cyclic adenosine monophosphate (cAMP) analogs. Diffusion coefficients were calculated separately for the gap junctions between pairs of AII amacrine cells and for those connecting AII amacrine cells with ON cone bipolar cells. Increased dopamine caused diffusion rates to decline more rapidly across the AII–AII gap junctions than across the AII–bipolar cell gap junctions. The rate of decline at these sites was well fit by a model proposing that dopamine modulates two independent gates in AII–AII channels, but only a single gate on the AII side of the AII–bipolar channel. However, a membrane-permeant cAMP agonist modulated both types of channel equally. Therefore, the major regulator of channel closure in this network is the local cAMP concentration within each cell, as regulated by dopamine, rather than different cAMP sensitivity of their respective gates. In contrast, nitric oxide preferentially reduced AII–bipolar cell permeabilities. Coupling from AII amacrine cells to the different bipolar cell subtypes was differentially affected by dopamine, indicating that light adaptation acting via dopamine release alters network coupling properties in multiple ways.

Keywords

Electrical couplingGap junctionRetina
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 5 , September 2004 , pp. 791 - 805
Copyright
2004 Cambridge University Press

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References

REFERENCES

Bloomfield, S.A., Xin, D., & Osborne, T. (1997). Light-induced modulation of coupling between AII amacrine cells in the rabbit retina. Visual Neuroscience 14, 565–576.Google Scholar
Chow, C.C. & Kopell, N. (2000). Dynamics of spiking neurons with electrical coupling. Neural Computation 12, 1643–1678.Google Scholar
Cohen, E. & Sterling, P. (1990). Demonstration of cell types among cone bipolar neutrons of cat retina. Philosophical Transactions of the Royal Society B (London) 330, 305–321.Google Scholar
Condorelli, D.F., Parenti, R., Spinella, F., Trovato Salinaro, A., Belluardo, N., Cardile, V., & Cicirata, F. (1998). Cloning of a new gap junction gene (Cx36) highly expressed in mammalian brain neurons. European Journal of Neuroscience 10, 1202–1208.Google Scholar
Deans, M.R., Volgyi, B., Goodenough, D.A., Bloomfield, S.A., & Paul, D.L. (2002). Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 36, 703–712.Google Scholar
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293–300.Google Scholar
Feigenspan, A., Teubner, B., Willecke, K., & Weiler, R. (2001). Expression of neuronal connexin36 in AII amacrine cells of the mammalian retina. Journal of Neuroscience 21, 230–239.Google Scholar
Freed, M.A. (2000). Rate of quantal excitation to a retinal ganglion cell evoked by sensory input. Journal of Neurophysiology 83, 2956–2966.Google Scholar
Freed, M.A., Smith, R.G., & Sterling, P. (1987). Rod bipolar array in the cat retina: Pattern of input from rods and GABA-accumulating amacrine cells. Journal of Comparative Neurology 266, 445–455.Google Scholar
Galarreta, M. & Hestrin, S. (2001). Electrical synapses between GABA-releasing interneurons. Nature Reviews: Neuroscience 2, 425–433.Google Scholar
Hampson, E.C.G.M., Vaney, D.I., & Weiler, R. (1992). Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. Journal of Neuroscience 12, 4911–4922.Google Scholar
Harris, A.L. (2001). Emerging issues of connexin channels: Biophysics fills the gap. Quarterly Review of Biophysics 34, 325–472.Google Scholar
Jacoby, R.A. & Marshak, D.W. (2000). Synaptic connections of DB3 diffuse bipolar cell axons in macaque retina. Journal of Comparative Neurology 416, 19–29.Google Scholar
Kirsch, T., Schubert, T., Janssen-Bienhold, U., Soehl, G., Maxeiner, S., Willecke, K., & Weiler, R. (2003). Cellular expression of Cx45 in the mouse retina. Investigative Ophthalmology and Visual Science 44, E-Abstract 4133.Google Scholar
Kolb, H. (1979). The inner plexiform layer in the retina of the cat: Electron microscopic observations. Journal of Neurocytology 8, 295–329.Google Scholar
Kwak, B.R., van Veen, T.A.B, Analber, L.J.S., & Jongsma, H.J. (1995). TPA increases conductance but decreases permeability in neonatal rat cardiomyocyte gap junction channels. Experimental Cell Research 200, 456–463.Google Scholar
Landisman, C.E., Long, M.A., Beierlein, M., Deans, M.R., Paul, D.L., & Connors, B.W. (2002). Electrical synapses in the thalamic reticular nucleus. Journal of Neuroscience 22, 1002–1009.Google Scholar
Lee, B.B., Smith, V.C., Pokorny, J., & Kremers, J. (1997). Rod inputs to macaque ganglion cells. Vision Research 37, 2813–2828.Google Scholar
Lewis, T.J. & Rinzel, J. (2003). Dynamics of spiking neurons connected by both inhibitory and electrical coupling. Journal of Computational Neuroscience 14, 283–309.Google Scholar
Loewenstein, Y., Yarom, Y., & Sompolinsky, H. (2001). The generation of oscillations in networks of electrically coupled cells. Proceedings of the National Academy of Sciences of the U.S.A. 98, 8095–8100.Google Scholar
Lu, C. & McMahon, D.G. (1997). Modulation of hybrid bass retinal gap junctional channel gating by nitric oxide. Journal of Physiology (London) 499, 689–699.Google Scholar
Lu, C., Zhang, D.-Q., & McMahon, D.G. (1998). Differential modulation by SNP and dopamine of Vj-dependent and Vj-independent electrical synapses in retinal horizontal cells. Society for Neuroscience Abstracts 24, 135.Google Scholar
Massey, S.C. & Mills, S.L. (1996). A calbindin-immunoreactive bipolar cell type in the rabbit retina. Journal of Comparative Neurology 366, 15–33.Google Scholar
Massey, S.C. & Mills, S.L. (1999). Gap junctions between AII amacrine cells and calbindin-positive bipolar cells in the rabbit retina. Visual Neuroscience 16, 181–189.Google Scholar
Massey, S.C., Kittila, C.A., & See, T.P. (1996). ON α ganglion cells receive potential input from calbindin cone bipolar cells in the rabbit retina. Investigative Ophthalmology and Visual Science (Suppl.) 37, S950.Google Scholar
McMahon, D.G. & Schmidt, K.F. (1999). Horizontal cell glutamate receptor modulation by NO: Mechanisms and functional implications for the first visual synapse. Visual Neuroscience 16, 425–433.Google Scholar
Mills, S.L. (1999). Unusual coupling properties of a cone bipolar cell in mammalian retina. Visual Neuroscience 16, 1029–1035.Google Scholar
Mills, S.L. & Massey, S.C. (1991). Labeling and distribution of AII amacrine cells in the rabbit retina. Journal of Comparative Neurology 304, 491–501.Google Scholar
Mills, S.L. & Massey, S.C. (1995). Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377, 734–737.Google Scholar
Mills, S.L. & Massey, S.C. (1998). The kinetics of tracer movement through homologous retinal gap junctions. Visual Neuroscience 15, 765–777.Google Scholar
Mills, S.L. & Massey, S.C. (2000). A series of biotinylated tracers distinguishes three types of gap junction in retina. Journal of Neuroscience 20, 8629–8636.Google Scholar
Mills, S.L., O'Brien, J.J., Li, W., O'Brien, J., & Massey, S.C. (2001). Rod pathways in the mammalian retina use connexin36. Journal of Comparative Neurology 436, 336–350.Google Scholar
Mitropoulou, G. & Bruzzone, R. (2003). Modulation of perch connexin35 hemichannels by cyclic AMP requires a protein kinase A phosphorylation site. Journal of Neuroscience Research 72, 147–157.Google Scholar
Moreno, A.P., Fishman, G.I., & Spray, D.C. (1992). Phosphorylation shifts unitary conductance and modifies voltage dependent kinetics of human connexin43 gap junction channels. Biophysical Journal 62, 51–53.Google Scholar
Smith, R.G., Freed, M.A., & Sterling, P. (1986). Microcircuitry of the dark-adapted cat retina: Functional architecture of the rod–cone network. Journal of Neuroscience 6, 3605–3617.Google Scholar
Srinivas, M., Rozental, R., Kojima, T., Dermietzel, R., Mehler, M., Condorelli, D.F., Kessler, J.A., & Spray, D.C. (1999). Functional properties of channels formed by the neuronal gap junction protein connexin36. Journal of Neuroscience 19, 9848–9855.Google Scholar
Sterling, P., Freed, M.A., & Smith, R.G. (1988). Architecture of rod and cone circuits to the on-beta ganglion cell. Journal of Neuroscience 8, 623–642.Google Scholar
Strettoi, E., Dacheux, R.F., & Raviola, E. (1992). Synaptic connections of the narrow-field, bistratified rod amacrine cell (AII) in the rabbit retina. Journal of Comparative Neurology 325, 152–168.Google Scholar
Teubner, B., Degen, J., Söhl, G., Güldenagel, M., Bukauskas, F.F., Trexler, E.B., Verselis, V.K., De Zeeux, C.I., Lee, C.G., Kozak, C.A., Petrasch-Parwez, E., Dermietzel, R., & Willecke, K. (2000). Functional expression of the murine connexin36 gene coding for a neuron-specific gap junctional protein. Journal of Membrane Biology 176, 249–262.Google Scholar
Trexler, E.B., Li, W., Mills, S.L., & Massey, S.C. (2001). Coupling from AII amacrine cells to ON cone bipolar cells is bi-directional. Journal of Comparative Neurology 437, 408–422.Google Scholar
Umino, O., Maehara, M., Hidaka, S., Kita, S., & Hashimoto, Y. (1994). The network properties of bipolar-bipolar cell coupling in the retina of teleost fishes. Visual Neuroscience 11, 533–548.Google Scholar
Vaney, D.I. (1991). Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Journal of Neuroscience Letters 125, 187–190.Google Scholar
Vaney, D.I., Nelson, J.C., & Pow, D.V. (1998). Neurotransmitter coupling through gap junctions in the retina. Journal of Neuroscience 18, 10594–10602.Google Scholar
van Veen, T.A., van Rijen, H.V., & Jongsma, H.J. (2000). Electrical conductance of mouse connexin45 gap junction channels is modulated by phosphorylation. Cardiovascular Research 46, 496–510.Google Scholar
Veruki, M.L. & Hartveit, E. (2002a). AII (Rod) amacrine cells form a network of electrically coupled interneurons in the mammalian retina. Neuron 33, 935–946.Google Scholar
Veruki, M.L. & Hartveit, E. (2002b). Electrical synapses mediate signal transmission in the rod pathway of the Mammalian retina. Journal of Neuroscience 22, 10558–10566.Google Scholar
Winbow, V., O'Brien, J., & Mills, S.L. (2001). Mutations in retinal connexin35 in the intracellular loop or carboxyl terminus block or decrease direct phosphorylation by protein kinase A. Investigative Ophthalmology and Visual Science (Suppl) 42, S193.Google Scholar
Witkovsky, P. & Dearry, A. (1991). Functional roles of dopamine in the vertebrate retina. Progress in Retinal Research 11, 247–292.Google Scholar
Xin, D. & Bloomfield, S.A. (1999). Comparison of the responses of AII amacrine cells in the dark- and light-adapted rabbit retina. Visual Neuroscience 16, 653–665.Google Scholar
Zimmerman, A.L. & Rose, B. (1985). Permeability properties of cell-to-cell channels: Kinetics of fluorescent tracer diffusion through a cell junction. Journal of Membrane Biology 84, 269–283.Google Scholar