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The light-induced reduction of horizontal cell receptive field size in the goldfish retina involves nitric oxide

Published online by Cambridge University Press:  16 February 2011

BRYAN A. DANIELS  and
WILLIAM H. BALDRIDGE
BRYAN A. DANIELS
Affiliation:
Department of Anatomy and Neurobiology, Laboratory for Retina and Optic Nerve Research, Dalhousie University, Halifax, Nova Scotia, Canada
WILLIAM H. BALDRIDGE*
Affiliation:
Department of Anatomy and Neurobiology, Laboratory for Retina and Optic Nerve Research, Dalhousie University, Halifax, Nova Scotia, Canada Department of Ophthalmology and Visual Sciences, Dalhousie University, Halifax, Nova Scotia, Canada
*
*Address correspondence and reprint requests to: Dr. William Baldridge, Department of Anatomy and Neurobiology, Dalhousie University, 5850 College Street, Halifax, Nova Scotia, B3H 1X5 Canada. E-mail: [email protected]
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Abstract

Horizontal cells of the vertebrate retina have large receptive fields as a result of extensive gap junction coupling. Increased ambient illumination reduces horizontal cell receptive field size. Using the isolated goldfish retina, we have assessed the contribution of nitric oxide to the light-dependent reduction of horizontal cell receptive field size. Horizontal cell receptive field size was assessed by comparing the responses to centered spot and annulus stimuli and from the responses to translated slit stimuli. A period of steady illumination decreased the receptive field size of horizontal cells, as did treatment with the nitric oxide donor (Z)-1-[N-(2-aminoethyl)-N-(2-ammonioethyl)amino]diazen-1-ium-1,2-diolate (100 μM). Blocking the endogenous production of nitric oxide with the nitric oxide synthase inhibitor, NG-nitro-l-arginine methyl ester (1 mM), decreased the light-induced reduction of horizontal cell receptive field size. These findings suggest that nitric oxide is involved in light-induced reduction of horizontal cell receptive field size.

Keywords

TeleostLight adaptationNitric oxide synthaseL-NAMEDETA NONOate
Type
Research Articles
Information
Visual Neuroscience , Volume 28 , Issue 2 , March 2011 , pp. 137 - 144
Copyright
Copyright © Cambridge University Press 2011

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References

Angotzi, A.R., Hirano, J., Vallerga, S. & Djamgoz, M.B. (2002). Role of nitric oxide in control of light adaptive cone photomechanical movements in retinas of lower vertebrates: A comparative species study. Nitric Oxide 6, 200–204.CrossRefGoogle ScholarPubMed
Baldridge, W.H. (2001). Triphasic adaptation of teleost horizontal cells. Progress in Brain Research 131, 437–449.CrossRefGoogle ScholarPubMed
Baldridge, W.H. & Ball, A.K. (1991). Background illumination reduces horizontal cell receptive-field size in both normal and 6-hydroxydopamine-lesioned goldfish retinas. Visual Neuroscience 7, 441–450.CrossRefGoogle ScholarPubMed
Baldridge, W.H. & Fischer, A.J. (2001). Nitric oxide donor stimulated increase of cyclic GMP in the goldfish retina. Visual Neuroscience 18, 849–856.CrossRefGoogle ScholarPubMed
Baldridge, W.H., Weiler, R. & Dowling, J.E. (1995). Dark-suppression and light-sensitization of horizontal cell responses in the hybrid bass retina. Visual Neuroscience 12, 611–620.CrossRefGoogle ScholarPubMed
Baylor, D.A., Fuortes, M.G. & O’Bryan, P.M. (1971). Receptive fields of cones in the retina of the turtle. Journal of Physiology 214, 265–294.Google Scholar
Blom, J.J., Blute, T.A. & Eldred, W.D. (2009). Functional localization of the nitric oxide/cGMP pathway in the salamander retina. Visual Neuroscience 26, 275–286.CrossRefGoogle ScholarPubMed
Blute, T.A., Mayer, B. & Eldred, W.D. (1997). Immunocytochemical and histochemical localization of nitric oxide synthase in the turtle retina. Visual Neuroscience 14, 717–729.CrossRefGoogle ScholarPubMed
Blute, T.A., Velasco, P. & Eldred, W.D. (1998). Functional localization of soluble guanylate cyclase in turtle retina: Modulation of cGMP by nitric oxide donors. Visual Neuroscience 15, 485–498.CrossRefGoogle ScholarPubMed
Cheng, N., Tsunenari, T. & Yau, K.W. (2009). Intrinsic light response of retinal horizontal cells of teleosts. Nature 460, 899–903.CrossRefGoogle ScholarPubMed
DeVries, S.H. & Schwartz, E.A. (1989). Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. Journal of Physiology 414, 351–375.CrossRefGoogle ScholarPubMed
Djamgoz, M.B., Petruv, R., Yasui, S., Furukawa, T. & Yamada, M. (1998). Modulation of chromatic difference in receptive field size of H1 horizontal cells in carp retina: Dopamine- and APB-sensitive mechanisms. Neuroscience Research 30, 13–24.CrossRefGoogle ScholarPubMed
Dong, C.J. & McReynolds, J.S. (1991). The relationship between light, dopamine release and horizontal cell coupling in the mudpuppy retina. Journal of Physiology 440, 291–309.CrossRefGoogle ScholarPubMed
Eldred, W.D. & Blute, T.A. (2005). Imaging of nitric oxide in the retina. Vision Research 45, 3469–3486.CrossRefGoogle ScholarPubMed
Furukawa, T., Petruv, R., Yasui, S., Yamada, M. & Djamgoz, M.B. (2002). Nitric oxide controls the light adaptive chromatic difference in receptive field size of H1 horizontal cell network in carp retina. Experimental Brain Research 147, 296–304.CrossRefGoogle ScholarPubMed
Giove, T.J., Deshpande, M.M. & Eldred, W.D. (2009). Identification of alternate transcripts of neuronal nitric oxide synthase in the mouse retina. Journal of Neuroscience Research 87, 3134–3142.Google Scholar
Gotzes, S., de Vente, J. & Muller, F. (1998). Nitric oxide modulates cGMP levels in neurons of the inner and outer retina in opposite ways. Visual Neuroscience 15, 945–955.CrossRefGoogle ScholarPubMed
Greenstreet, E.H. & Djamgoz, M.B. (1994). Nitric oxide induces light-adaptive morphological changes in retinal neurones. Neuroreport 6, 109–112.CrossRefGoogle ScholarPubMed
Haamedi, S.N. & Djamgoz, M.B. (2002). Dopamine and nitric oxide control both flickering and steady-light-induced cone contraction and horizontal cell spinule formation in the teleost (carp) retina: Serial interaction of dopamine and nitric oxide. Journal of Comparative Neurology 449, 120–128.CrossRefGoogle ScholarPubMed
Haverkamp, S. & Eldred, W.D. (1998). Localization of nNOS in photoreceptor, bipolar and horizontal cells in turtle and rat retinas. Neuroreport 9, 2231–2235.CrossRefGoogle ScholarPubMed
Kamermans, M., Haak, J., Habraken, J.B. & Spekreijse, H. (1996). The size of the horizontal cell receptive fields adapts to the stimulus in the light adapted goldfish retina. Vision Research 36, 4105–4119.CrossRefGoogle Scholar
Kamermans, M. & Spekreijse, H. (1999). The feedback pathway from horizontal cells to cones. A mini review with a look ahead. Vision Research 39, 2449–2468.CrossRefGoogle Scholar
Kaneko, A. (1971). Electrical connexions between horizontal cells in the dogfish retina. Journal of Physiology 213, 95–105.Google Scholar
Kourennyi, D.E., Liu, X.D., Hart, J., Mahmud, F., Baldridge, W.H. & Barnes, S. (2004). Reciprocal modulation of calcium dynamics at rod and cone photoreceptor synapses by nitric oxide. Journal of Neurophysiology 92, 477–483.CrossRefGoogle ScholarPubMed
Kurenni, D.E., Thurlow, G.A., Turner, R.W., Moroz, L.L., Sharkey, K.A. & Barnes, S. (1995). Nitric oxide synthase in tiger salamander retina. Journal of Comparative Neurology 361, 525–536.Google Scholar
Levy, H., Twig, G. & Perlman, I. (2004). Nitric oxide modulates the transfer function between cones and horizontal cells during changing conditions of ambient illumination. European Journal of Neuroscience 20, 2963–2974.CrossRefGoogle ScholarPubMed
Liepe, B.A., Stone, C., Koistinaho, J. & Copenhagen, D.R. (1994). Nitric oxide synthase in Muller cells and neurons of salamander and fish retina. Journal of Neuroscience 14, 7641–7654.CrossRefGoogle ScholarPubMed
Lu, C. & McMahon, D.G. (1997). Modulation of hybrid bass retinal gap junctional channel gating by nitric oxide. Journal of Physiology 499(Pt 3), 689–699.CrossRefGoogle ScholarPubMed
Naka, K.I. & Nye, P.W. (1971). Role of horizontal cells in organization of the catfish retinal receptive field. Journal of Neurophysiology 34, 785–801.Google Scholar
Naka, K.I. & Rushton, W.A. (1967). The generation and spread of S-potentials in fish (Cyprinidae). Journal of Physiology 192, 437–461.CrossRefGoogle ScholarPubMed
Naka, K.I. & Witkovsky, P. (1972). Dogfish ganglion cell discharge resulting from extrinsic polarization of the horizontal cells. Journal of Physiology 223, 449–460.CrossRefGoogle ScholarPubMed
Neal, M., Cunningham, J. & Matthews, K. (1998). Selective release of nitric oxide from retinal amacrine and bipolar cells. Investigative Ophthalmology & Visual Science 39, 850–853.Google Scholar
Negishi, K. & Drujan, B.D. (1978). Effects of catecholamines on the horizontal cell membrane potential in the fish retina. Sensory Processes 2, 388–395.Google Scholar
Negishi, K. & Drujan, B.D. (1979). Effects of catecholamines and related compounds on horizontal cells in the fish retina. Journal of Neuroscience Research 4, 311–334.CrossRefGoogle ScholarPubMed
Pang, J.J., Gao, F. & Wu, S.M. (2010). Light responses and morphology of bNOS-immunoreactive neurons in the mouse retina. Journal of Comparative Neurology 518, 2456–2474.CrossRefGoogle ScholarPubMed
Piehl, L., Capani, F., Facorro, G., Lopez, E.M., de Celis, E.R., Pustovrh, C., Hager, A., Coirini, H. & Lopez-Costa, J.J. (2007). Nitric oxide increases in the rat retina after continuous illumination. Brain Research 1156, 112–119.Google Scholar
Pottek, M., Schultz, K. & Weiler, R. (1997). Effects of nitric oxide on the horizontal cell network and dopamine release in the carp retina. Vision Research 37, 1091–1102.CrossRefGoogle ScholarPubMed
Pottek, M. & Weiler, R. (2000). Light-adaptive effects of retinoic acid on receptive field properties of retinal horizontal cells. European Journal of Neuroscience 12, 437–445.CrossRefGoogle ScholarPubMed
Ribelayga, C. & Mangel, S.C. (2003). Absence of circadian clock regulation of horizontal cell gap junctional coupling reveals two dopamine systems in the goldfish retina. Journal of Comparative Neurology 467, 243–253.Google Scholar
Ribelayga, C. & Mangel, S.C. (2007). Tracer coupling between fish rod horizontal cells: Modulation by light and dopamine but not the retinal circadian clock. Visual Neuroscience 24, 333–344.CrossRefGoogle Scholar
Savchenko, A., Barnes, S. & Kramer, R.H. (1997). Cyclic-nucleotide-gated channels mediate synaptic feedback by nitric oxide. Nature 390, 694–698.Google Scholar
Schmidt, H.H., Pollock, J.S., Nakane, M., Forstermann, U. & Murad, F. (1992). Ca2+/calmodulin-regulated nitric oxide synthases. Cell Calcium 13, 427–434.Google Scholar
Sekaran, S., Cunningham, J., Neal, M.J., Hartell, N.A. & Djamgoz, M.B. (2005). Nitric oxide release is induced by dopamine during illumination of the carp retina: Serial neurochemical control of light adaptation. European Journal of Neuroscience 21, 2199–2208.CrossRefGoogle ScholarPubMed
Shigematsu, Y. & Yamada, M. (1988). Effects of dopamine on spatial properties of horizontal cell responses in the carp retina. Neuroscience Research. Supplement 8, S69–S80.CrossRefGoogle ScholarPubMed
Stell, W.K. & Lightfoot, D.O. (1975). Color-specific interconnections of cones and horizontal cells in the retina of the goldfish. Journal of Comparative Neurology 159, 473–502.Google Scholar
Stell, W.K., Lightfood, D.O., Wheeler, T.G. & Leeper, H.F. (1975). Goldfish retina: Functional polarization of cone horizontal cell dendrites and synapses. Science 190, 989–990.CrossRefGoogle ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1983). Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina. Nature 301, 243–246.CrossRefGoogle ScholarPubMed
Thoreson, W.B., Babai, N. & Bartoletti, T.M. (2008). Feedback from horizontal cells to rod photoreceptors in vertebrate retina. Journal of Neuroscience 28, 5691–5695.CrossRefGoogle ScholarPubMed
Umino, O., Lee, Y. & Dowling, J.E. (1991). Effects of light stimuli on the release of dopamine from interplexiform cells in the white perch retina. Visual Neuroscience 7, 451–458.Google Scholar
Weiler, R., He, S. & Vaney, D.I. (1999). Retinoic acid modulates gap junctional permeability between horizontal cells of the mammalian retina. European Journal of Neuroscience 11, 3346–3350.CrossRefGoogle ScholarPubMed
Weiler, R. & Kewitz, B. (1993). The marker for nitric oxide synthase, NADPH-diaphorase, co-localizes with GABA in horizontal cells and cells of the inner retina in the carp retina. Neuroscience Letters 158, 151–154.CrossRefGoogle ScholarPubMed
Weiler, R., Pottek, M., He, S. & Vaney, D.I. (2000). Modulation of coupling between retinal horizontal cells by retinoic acid and endogenous dopamine. Brain Research. Brain Research Reviews 32, 121–129.Google Scholar
Weiler, R., Schultz, K., Pottek, M., Tieding, S. & Janssen-Bienhold, U. (1998). Retinoic acid has light-adaptive effects on horizontal cells in the retina. Proceedings of the National Academy of Sciences of the United States of America 95, 7139–7144.CrossRefGoogle ScholarPubMed
Xin, D. & Bloomfield, S.A. (1999). Dark- and light-induced changes in coupling between horizontal cells in mammalian retina. Journal of Comparative Neurology 405, 75–87.Google Scholar
Xin, D. & Bloomfield, S.A. (2000). Effects of nitric oxide on horizontal cells in the rabbit retina. Visual Neuroscience 17, 799–811.CrossRefGoogle ScholarPubMed
Yamada, M., Fraser, S.P., Furukawa, T., Hirasawa, H., Katano, K., Djamgoz, M. & Yasui, S. (1999). Effects of nitric oxide, light adaptation and APB on spectral characteristics of H1 horizontal cells in carp retina. Neuroscience Research 35, 309–319.Google Scholar
Yang, X.L., Tornqvist, K. & Dowling, J.E. (1988). Modulation of cone horizontal cell activity in the teleost fish retina. I. Effects of prolonged darkness and background illumination on light responsiveness. Journal of Neuroscience 8, 2259–2268.Google Scholar
Yang, X.L. & Wu, S.M. (1991). Feedforward lateral inhibition in retinal bipolar cells: Input-output relation of the horizontal cell-depolarizing bipolar cell synapse. Proceedings of the National Academy of Sciences of the United States of America 88, 3310–3313.CrossRefGoogle ScholarPubMed
Zemel, E., Eyal, O., Lei, B. & Perlman, I. (1996). NADPH diaphorase activity in mammalian retinas is modulated by the state of visual adaptation. Visual Neuroscience 13, 863–871.CrossRefGoogle ScholarPubMed