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Dopaminergic modulation of tracer coupling in a ganglion-amacrine cell network

Published online by Cambridge University Press:  22 August 2007

STEPHEN L. MILLS
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas at Houston—Health Science Center, Houston, Texas
XIAO-BO XIA
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas at Houston—Health Science Center, Houston, Texas Current address: Department of Ophthalmology, Xiangya Hospital, Central South University, China.
HIDEO HOSHI
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas at Houston—Health Science Center, Houston, Texas
SALLY I. FIRTH
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas at Houston—Health Science Center, Houston, Texas Current address: School of Pharmacy, University of Queensland, St Lucia, Queensland, Australia 4072.
MARGARET E. RICE
Affiliation:
College of Optometry, University of Houston, Houston, Texas
LAURA J. FRISHMAN
Affiliation:
College of Optometry, University of Houston, Houston, Texas
DAVID W. MARSHAK
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas at Houston—Health Science Center, Houston, Texas

Abstract

Many retinal ganglion cells are coupled via gap junctions with neighboring amacrine cells and ganglion cells. We investigated the extent and dynamics of coupling in one such network, the OFF α ganglion cell of rabbit retina and its associated amacrine cells. We also observed the relative spread of Neurobiotin injected into a ganglion cell in the presence of modulators of gap junctional permeability. We found that gap junctions between amacrine cells were closed via stimulation of a D1 dopamine receptor, while the gap junctions between ganglion cells were closed via stimulation of a D2 dopamine receptor. The pairs of hemichannels making up the heterologous gap junctions between the ganglion and amacrine cells were modulated independently, so that elevations of cAMP in the ganglion cell open the ganglion cell hemichannels, while elevations of cAMP in the amacrine cell close its hemichannels. We also measured endogenous dopamine release from an eyecup preparation and found a basal release from the dark-adapted retina of approximately 2 pmol/min during the day. Maximal stimulation with light increased the rate of dopamine release from rabbit retina by 66%. The results suggest that coupling between members of the OFF α ganglion cell/amacrine cell network is differentially modulated with changing levels of dopamine.

Type
Research Article
Copyright
© 2007 Cambridge University Press

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References

REFERENCES

Ackert, J.M., Wu, S.H., Lee, J.C., Abrams, J., Hu, E.H., Perlman, I. & Bloomfield, S.A. (2006). Light-induced changes in spike synchronization between coupled ON direction selective ganglion cells in the mammalian retina. Journal of Neuroscience 26, 42064215.Google Scholar
Bauer, B., Ehinger, B. & Aberg, L. (1980). [3H]-dopamine release from the rabbit retina. Albrecht Von Graefes Archive for Clinical and Experimental Ophthalmology 215, 7178.Google Scholar
Bloomfield, S.A. & Völgyi, B. (2004). Function and plasticity of homologous coupling between AII amacrine cells. Vision Research 44, 32973306.Google Scholar
Bloomfield, S.A., Xin, D. & Osborne, T. (1997). Light-induced modulation of coupling between AII amacrine cells in the rabbit retina. Visual Neuroscience 14, 565576.Google Scholar
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, 164168.Google Scholar
Boatright, J.H., Rubim, N.M. & Iuvone, P.M. (1994). Regulation of endogenous dopamine release in amphibian retina by gamma-aminobutyric acid and glycine. Visual Neuroscience 11, 10031012.Google Scholar
Boelen, M.K., Boelen, M.G. & Marshak, D.W. (1998). Light-stimulated release of dopamine from primate retina is blocked by l-2-amino-4-phosphonobutyric acid (APB). Visual Neuroscience 15, 97103.Google Scholar
Brainard, G.C. & Morgan, W.W. (1987). Light-induced stimulation of retinal dopamine: A dose-response relationship. Brain Research 424, 199203.Google Scholar
Dacey, D.M. & Brace, S. (1992). A coupled network for parasol but not midget ganglion cells in the primate retina. Visual Neuroscience 9, 279290.Google Scholar
DeMonasterio, F.M. (1978). Spectral interactions in horizontal and ganglion cells of isolated and arterially-perfused rabbit retina. Brain Research 150, 239258.Google Scholar
DeVries, S. (1999). Correlated firing in rabbit retinal ganglion cells. Journal of Neurophysiology 81, 908920.Google Scholar
DeVries, S.H. & Baylor, D.A. (1995). An alternative pathway for signal flow from rod photoreceptors to ganglion cells in mammalian retina. Proceedings of the National Academy of Sciences USA. 92, 1065810662.Google Scholar
DeVries, S. & 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, 351375.Google Scholar
Gibson, C.J. (1990). A simple perfusion system for measuring endogenous retinal dopamine release. Journal of Neuroscience Methods 32, 7579.Google Scholar
Gibson, C.J. (1992). Tyrosine augments dopamine release in stimulated rat retina. Brain Research 595, 201205.Google Scholar
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, 393395.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, 49114922.Google Scholar
Hayashida, Y. & Ishida, A.T. (2004). Dopamine receptor activation can reduce voltage-gated Na+ current by modulating both entry into and recovery from inactivation. Journal of Neurophysiology 92, 31343141.Google Scholar
Hidaka, S., Kato, T. & Miyachi, E. (2002). Expression of gap junction connexin36 in adult rat retinal ganglion cells. Journal of Integrative Neuroscience 1, 322.Google Scholar
Hidaka, S., Akahori, Y. & Kurosawa, Y. (2004). Dendrodendritic electrical synapses between mammalian retinal ganglion cells. Journal of Neuroscience 24, 1055310567.Google Scholar
Hoshi, H., O'Brien, J. & Mills, S.L. (2006). A novel fluorescent tracer for visualizing coupled cells in neural circuits of living tissue. Journal of Histochemistry and Cytochemistry 54, 11691176.Google Scholar
Hu, E. & Bloomfield, S.A. (2000). Modulation of the tracer coupling pattern of alpha ganglion cells in the rabbit retina. Investigative Ophthalmology & Visual Science 41, S936.Google Scholar
Hu, E. & Bloomfield, S.A. (2003). Gap junctional coupling underlies the short-latency spike synchrony of retinal alpha ganglion cells. Journal of Neuroscience 23, 67686777.Google Scholar
Jacoby, R., Stafford, D., Kouyama, N. & Marshak, D. (1996). Synaptic inputs to ON parasol ganglion cells in the primate retina. Journal of Neuroscience 16, 80418056.Google Scholar
Krizaj, D., Gabriel, R., Owen, W.G. & Witkovsky, P. (1998). Dopamine D2 receptor-mediated modulation of rod-cone coupling in the Xenopus retina. Journal of Comparative Neurology 398, 529538.Google Scholar
Mangel, S.C. (2001). Circadian clock regulation of neuronal light responses in the vertebrate retina. Progress in Brain Research 131, 505518.Google Scholar
Massey, S.C. & Redburn, D.A. (1982). Tonic gamma-aminobutyric acid-mediated inhibition of cholinergic amacrine cells in rabbit retina. Journal of Neuroscience 2, 633643.Google Scholar
Mastronarde, D.N. (1983a). Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells. Journal of Neurophysiology 49, 303324.Google Scholar
Mastronarde, D.N. (1983b). Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. Journal of Neurophysiology 49, 325349.Google Scholar
McMahon, D.G., Knapp, A.G. & Dowling, J.E. (1989). Horizontal cell gap junctions: Single-channel conductance and modulation by dopamine. Proceedings of the National Academy of Science USA 86, 76397643.Google Scholar
Megaw, P.L., Morgan, I.G. & Boelen, M.K. (1998). Complex dependence of dopamine release on light in chicken retina. Proceedings of the Australian Neuroscience Society 8, 175.Google Scholar
Megaw, P., Morgan, I. & Boelen, M. (2001). Vitreal dihydroxyphenylacetic acid (DOPAC) as an index of retinal dopamine release. Journal of Neurochemistry 76, 16361644.Google Scholar
Meister, M., Lagnado, L. & Baylor, D.A. (1995). Concerted signaling by retinal ganglion cells. Science 270, 12071210.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, 491501.Google Scholar
Mills, S.L. & Massey, S.C. (1995). Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377, 734737.Google Scholar
Mills, S.L. & Massey, S.C. (1998). The kinetics of tracer movement through homologous gap junctions in the rabbit retina. Visual Neuroscience 15, 765777.Google Scholar
Moreno, A.P., Saez, J.C., Fishman, G.I. & Spray, D.C. (1994). Human connexin43 gap junction channels: Regulation of unitary conductances by phosphorylation. Circulation Research 74, 10501057.Google Scholar
Neal, M., Cunningham, J., Lever, I., Pezet, S. & Malcangio, M. (2003). Mechanism by which brain-derived neurotrophic factor increases dopamine release from the rabbit retina. Investigative Ophthalmology and Visual Science 44, 791798.Google Scholar
Nir, I., Haque, R. & Iuvone, P.M. (2000). Diurnal metabolism of dopamine in the mouse retina. Brain Research 870, 118125.Google Scholar
Parkinson, D. & Rando, R.R. (1983). Effect of light on dopamine turnover and metabolism in rabbit retina. Investigative Ophthalmology & Visual Sciences 24, 8488.Google Scholar
Peichl, L., Ott, H. & Boycott, B.B. (1987). Alpha ganglion cells in mammalian retinae. Proceedings of the Royal Society of London B Biological Sciences 231, 169197.Google Scholar
Piccolino, M., Neyton, J. & Gerschenfeld, H.M. (1984). Decrease of gap junction permeability induced by dopamine and cyclic adenosine 3′:5′-monophosphate in horizontal cells of turtle retina. Journal of Neuroscience 4, 24772488.Google Scholar
Raggi, M.A., Sabbioni, C., Casamenti, G., Gerra, G., Calonghi, N. & Masotti, L. (1999). Determination of catecholamines in human plasma by high-performance liquid chromotography with electrochemical detection. Journal of Chromatography B 730, 201211.Google Scholar
Robson, J.G. & Frishman, L.J. (1995). Response linearity and dynamics of the cat retina: The bipolar cell component of the dark-adapted ERG. Visual Neuroscience 12, 837850.Google Scholar
Schubert, T., Maxeiner, S., Kruger, O., Willecke, K. & Weiler, R. (2005a). Connexin45 mediates gap junctional coupling of bistratified ganglion cells in the mouse retina. Journal of Comparative Neurology 490, 2939.Google Scholar
Schubert, T., Degen, J., Willecke, K., Hormuzdi, S.G., Monyer, H. & Weiler, R. (2005b). Connexin36 mediates gap junctional coupling of alpha-ganglion cells in mouse retina. Journal of Comparative Neurology 485, 191201.Google Scholar
Teranishi, T., Negishi, K. & Kato, S. (1984). Regulatory effect of dopamine on spatial properties of horizontal cells in carp retina. Journal of Neuroscience 4, 12711280.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, 187190.Google Scholar
Vaquero, C.F., Pignatelli, A., Partida, G.J. & Ishida, A.T. (2001). A dopamine- and protein kinase A-dependent mechanism for network adaptation in retinal ganglion cells. Journal of Neuroscience 21, 86248635.Google Scholar
Völgyi, B., Abrams, J., Paul, D.L. & Bloomfield, S.A. (2005). Morphology and tracer coupling pattern of alpha ganglion cells in the mouse retina. Journal of Comparative Neurology 492, 6677.Google Scholar
Wightman, R.M. & Robinson, D.L. (2002). Transient changes in mesolimbic dopamine and their association with ‘reward’. Journal of Neurochemistry 82, 721735.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 USA 90, 56675671.Google Scholar
Xia, X.-B. & Mills, S.L. (2004). Gap junctional regulatory mechanisms in the AII amacrine cell of the rabbit retina. Visual Neuroscience 21, 791805.Google Scholar
Xin, D. & Bloomfield, S.A. (1997). Tracer coupling pattern of amacrine and ganglion cells in the rabbit retina. Journal of Comparative Neurology 383, 512528.Google Scholar
Xin, D. & Bloomfield, S.A. (1999). Dark- and light-induced changes in coupling between horizontal cells in mammalian retina. Journal of Comparative Neurology 405, 7587.Google Scholar
Young, H.M. & Vaney, D.I. (1991). Rod-signal interneurons in the rabbit retina: 1. Rod bipolar cells. Journal of Comparative Neurology 310, 139153.Google Scholar
Zhang, D.Q., Zhou, T.R. & McMahon, D.G. (2007). Functional heterogeneity of retinal dopaminergic neurons underlying their multiple roles in vision. Journal of Neuroscience 27, 692699.Google Scholar