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Light-induced modulation of coupling between AII amacrine cells in the rabbit retina

Published online by Cambridge University Press:  02 June 2009

Stewart A. Bloomfield ,
Daiyan Xin  and
Tristan Osborne
Stewart A. Bloomfield
Affiliation:
Department of Ophthalmology, New York University Medical Center, New York Department of Physiology and Neuroscience, New York University Medical Center, New York
Daiyan Xin
Affiliation:
Department of Ophthalmology, New York University Medical Center, New York
Tristan Osborne
Affiliation:
Department of Ophthalmology, New York University Medical Center, New York
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Abstract

The rod-driven, AII amacrine cells in the mammalian retina maintain homologous gap junctions with one another as well as heterologous gap junctions with on-cone bipolar cells. We used background illumination to study whether changes in the adaptational state of the retina affected the permeabilities of these two sets of gap junctions. To access changes in permeability, we injected single AII amacrine cells with the biotinylated tracer, Neurobiotin, and measured the extent of tracer coupling to neighboring AII cells and neighboring cone bipolar cells. We also measured the center-receptive field size of All cells to assess concomitant changes in electrical coupling. Our results indicate that in well dark-adapted retinas, AII cells form relatively small networks averaging 20 amacrine cells and covering about 75 μm. The size of these networks matched closely to the size of AII cell on-center receptive fields. However, over most of their operating range, AII cells formed dramatically larger networks, averaging 326 amacrine cells, which corresponded to an increased receptive-field size. As the retina was light adapted beyond the operating range of the AII cells, they uncoupled to form networks comparable in size to those seen in well dark-adapted retinas. Our results, then, indicate that the adaptational state of the retina has a profound effect on the extent of electrical coupling between AII amacrine cells. Although we observed light-induced changes in the number of tracer-coupled cone bipolar cells, these appeared to be an epiphenomenon of changes in homologous coupling between AII amacrine cells. Therefore, in contrast to the robust changes in AII–AII coupling produced by background illumination, our data provided no evidence of a light-induced modulation of coupling between AII cells and on-cone bipolar cells.

Keywords

RetinaAmacrine cellCone bipolar cellCouplingGap junctions
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 3 , May 1997 , pp. 565 - 576
Copyright
Copyright © Cambridge University Press 1997

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References

REFERENCES

Adams, J.C. (1977). Technical considerations on the use of horseradish peroxidase as a neuronal marker. Neuroscience 2, 141–145.CrossRefGoogle ScholarPubMed
Ames, A. III & Nesbitt, F.B. (1981). In vitro retina as an experimental model of the central nervous system. Journal of Neurochemistry 37, 867–877.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. (1992). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of Neurophysiology 68, 711–725.Google Scholar
Bloomfield, S.A. & Miller, R.F. (1982). A physiological and morphological study of the horizontal cell types in the rabbit retina. Journal of Comparative Neurology 208, 288–303.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Xin, D. (1994). Relationship between tracer-coupling and receptive field size of amacrine and ganglion cells in the rabbit retina. Investigative Ophthalmology and Visual Science (Suppl.) 35, 1822.Google Scholar
Bloomfield, S.A., Xin, D. & Persky, S.E. (1995). A comparison of receptive field and tracer coupling size of horizontal cells in the rabbit retina. Visual Neuroscience 12, 985–999.CrossRefGoogle ScholarPubMed
Boatright, J.H., Hoel, M.J. & Iuvone, P.M. (1989). Stimulation of endogenous dopamine release and metabolism in amphibian retina by light- and K+-evoked depolarization. Brain Research 482, 164–168.Google Scholar
Boos, R., Schneider, H. & Wässle, H. (1993). Voltage- and transmitter-gated currents of All-amacrine cells in a slice preparation of the rat retina. Journal of Neuroscience 13, 2874–2888.CrossRefGoogle Scholar
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: light microscopy. Philosophical Transactions of the Royal Society B (London) 255, 109–184.Google Scholar
Boycott, B.B. & Kolb, H. (1973). The connexions between bipolar cells and photoreceptors in the retina of the domestic cat. Journal of Comparative Neurology 148, 115–140.CrossRefGoogle ScholarPubMed
Cohen, E. & Sterling, P. (1990). Demonstration of cell types among cone bipolar neurons in the cat retina. Philosophical Transactions of the Royal Society B (London) 330, 323–328.Google Scholar
Dacheux, R.F. (1977). A physiological study of the ontological formation of synaptic interactions in the rabbit retina. Ph.D. Thesis. State University of New York.Google Scholar
Dacheux, R.F & Miller, R.F. (1981). An intracellular electrophysiological study of the ontogeny of functional synapses in the rabbit retina. I. Receptors, horizontal, and bipolar cells. Journal of Comparative Neurology 198, 307–326.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331–345.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1989). Light-induced dopamine release from teleost retinas acts acts as a light-adaptive signal to the retinal pigment epithelium. Journal of Neurochemistry 53, 870–878.CrossRefGoogle Scholar
Demonasterio, F.M. (1978). Spectral interactions in horizontal and ganglion cells of the isolated and arterially-perfused rabbit retina. Brain Research 150, 239–258.CrossRefGoogle Scholar
Dolan, R.P. & Schiller, P.H. (1989). Evidence for only depolarizing rod bipolar cells in the primate retina. Visual Neuroscience 2, 421–424.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Famiglietti, E.V. & Kolb, H. (1976). Structural basis for on- and off- center responses in retinal ganglion cells. Science 194, 193–195.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Godley, B.F. & Wurtman, R.J. (1988). Release of endogenous dopamine from the superfused rabbit retina in vitro: Effect of light stimulation. Brain Research 452, 393–395.CrossRefGoogle ScholarPubMed
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
Kaneko, A. (1970). Physiological and morphological identification of horizontal, bipolar and amacrine cells in goldfish retina. Journal of Physiology (London) 207, 623–633.CrossRefGoogle ScholarPubMed
Kaneko, A. (1971). Electrical connexions between horizontal cells in the dogfish retina. Journal of Physiology (London) 213, 95–105.Google Scholar
Kaneko, A. & Stuart, A.E. (1984). Coupling between horizontal cells in carp retina revealed by diffusion of Lucifer yellow. Neuroscience Letters 47, 1–7.CrossRefGoogle ScholarPubMed
Koistinaho, J., Swanson, R.A., De Vente, J. & Sagar, S.M. (1993). NADPH-diaporase (nitric oxide synthase)-reactive amacrine cells of rabbit retina: Putative target cells and stimulation by light. Neuroscience 57, 587–597.Google Scholar
Kolb, H. (1979). The inner plexiform layer in the retína of the cat: Electron microscopic observations. Journal of Neurocytology 8, 295–329.CrossRefGoogle ScholarPubMed
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of the cat retina. Science 186, 47–49.CrossRefGoogle ScholarPubMed
Massey, S.C. & Mills, S.L. (1996). A calbindin-immunoreactive cone bipolar cell type in the rabbit retina. Journal of Comparative Neurology 366, 15–33.Google Scholar
Mills, S.L. & Massey, S.C. (1991). Labeling and distribution of All amacrine cells in the rabbit retina. Journal of Comparative Neurology 304, 491–501.CrossRefGoogle ScholarPubMed
Mills, S.L. & Massey, S.C. (1995). Differential properties of two gap junctional pathways made by All amacrine cells. Nature 377, 734–737.Google Scholar
Müller, F., Wässle, H. & Voigt, T. (1988). Pharmacological modulation of the rod pathway in the cat retina. Journal of Neurophysiology 59, 1657–1672.CrossRefGoogle ScholarPubMed
Nakajima, Y., Iwakabe, H., Akazawa, C., Nawa, H., Shigemoto, R., Mizuno, N. & Nakanishi, S. (1993). Molecular characterization of a novel metabotropic glutamate receptor mGLUR6 with a high selectivity for L-2-amino-4-phosphono butyrate. Journal of Biological Chemistry 268, 11863–11873.Google Scholar
Nawy, S. & Jahr, C.E. (1990). Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature 346, 269–271.Google Scholar
Nawy, S. & Jahr, C.E. (1992). cGMP-gated conductance in retinal bipolar cells is suppressed by the photoreceptor transmitter. Neuron 7, 677–683.Google Scholar
Nelson, R. (1977). Cat cones have rod input: A comparison of response properties of cones and horizontal cell bodies in the retina of the cat. Journal of Comparative Neurology 172, 109–136.CrossRefGoogle ScholarPubMed
Nelson, R. (1982). All amacrine cells quicken time course of rod signals in the cat retina. Journal of Neurophysiology 47, 928–947.Google Scholar
Nelson, R., Kolb, H., Famiglietti, E.V. & Gouras, P. (1976). Neural responses in the rod and cone systems of the cat retina: intracellular records and procion stains. Investigative Ophthalmology 15, 946–953.Google Scholar
Pourcho, R.G. (1980). Uptake of [3H]glycine and [3H]GABA by amacrine cells in the cat retina. Brain Research 198, 333–346.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1985). A combined Golgi and autoradiographic study of [3H]glycine-accumulating amacrine cells in the cat retina. Journal of Comparative Neurology 233, 473–480.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1987). Visualization of endogenous glycine in cat retina: An immunocytochemical study with FAB fragments. Journal of Neuroscience 7, 1189–1197.CrossRefGoogle ScholarPubMed
Pu, M. & Berson, D.M. (1992). A method for reliable and permanent intracellular staining of retinal ganglion cells. Journal of Neuroscience Methods 41, 45–51.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Rushton, W.A.H. (1976). Isolation of rod and cone contributions to cat ganglion cells by a method of light exchange. Journal of Physiology (London) 254, 7759–7773.Google Scholar
Shiells, R.A. & Falk, G. (1990). Glutamate receptors of rod bipolar cells are linked to a cyclic GMP cascade via a G-protein. Proceedings of the Royal Society B (London) 242, 91–94.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, 3505–3517.CrossRefGoogle ScholarPubMed
Smith, R.G. & Vardi, N. (1995). Simulation of the All amacrine cell of mammalian retina: Functional consequences of electrical coupling and regenerative membrane properties. Visual Neuroscience 12, 851–860.CrossRefGoogle ScholarPubMed
Steinberg, R.H. (1969). Rod and cone contributions to S-potentials from the cat retina. Vision Research 9, 1319–1329.Google Scholar
Sterling, P. (1995). Tuning retinal circuits. Nature 377, 676–677.Google Scholar
Sterling, P., Freed, M.A. & Smith, R.G. (1988). Architecture of rod and cone circuits to on-beta ganglion cells. Journal of Neuroscience 8, 623–642.CrossRefGoogle Scholar
Strettoi, E., Daucheux, R.F. & Raviola, E. (1990). Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina. Journal of Comparative Neurology 295, 449–466.Google Scholar
Strettoi, E., Raviola, E. & Dacheux, R.F. (1992). Synaptic connections of the narrow-field, bistratified rod amacrine cell (All) in the rabbit retina. Journal of Comparative Neurology 325, 152–168.Google Scholar
Strettoi, E., Dacheux, R.F. & Raviola, E. (1994). Cone bipolar cells as interneurons in the rod pathway of the rabbit retina. Journal of Comparative Neurology 347, 139–149.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1985). The morphology and topographic distribution of All amacrine cells in the cat retina. Proceedings of the Royal Society B (London) 224, 475–488.Google ScholarPubMed
Vaney, D.I. (1991). Many diverse types of retinal neurons show tracer coupling when injected with biocytin or neurobiotin. Neuroscience Letters 125, 187–190.CrossRefGoogle ScholarPubMed
Vaney, D.I., Gynther, I.C. & Young, H.M. (1991). Rod-cone interactions in the rabbit retina: 2. All amacrine cells. Journal of Comparative Neurology 310, 154–169.CrossRefGoogle Scholar
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recordings. Journal of Neurophysiology 32, 339–355.Google Scholar
Witkovsky, P. & Dearry, A. (1992). Functional roles of dopamine in the vertebrate retina. Progress in Retinal Research 10, 247–292.Google Scholar
Witkovsky, P., Nicholson, C., Rice, M.E., Bohmaker, K. & Meller, E. (1993). Extracellular dopamine concentration in the retina of the clawed frog, Xenopus laevis. Proceedings of the National Academy of Sciences of the U.S.A. 90, 5667–5671.Google Scholar
Witkovksy, P., Owen, W.G. & Woodsworth, M. (1983). Gap-junctions among the perikarya, dendrites and axon terminals of the luminosity-type horizontal cells in the turtle retina. Journal of Comparative Neurology 216, 359–368.Google Scholar
Yamada, E. & Ishikawa, T. (1965). The fine structure of the horizontal cells in some vertebrate retinas. Cold Spring Harbor Symposium on Quantitative Biology 30, 383–392.Google Scholar