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Unique functional properties of the APB sensitive and insensitive rod pathways signaling light decrements in mouse retinal ganglion cells

Published online by Cambridge University Press:  09 March 2006

GUO-YONG WANG
Affiliation:
Department of Structural and Cellular Biology, School of Medicine, Tulane University, New Orleans, Louisiana

Abstract

Light decrements are mediated by two distinct groups of rod pathways in the dark-adapted retina that can be differentiated on the basis of their sensitivity to the glutamate agonist DL-2-amino-phosphonobutyric (APB). By means of the APB sensitive pathway, rods transmit light decrements via rod bipolar cells to AII amacrine cells, then to Off cone bipolar cells, which in turn innervate the dendrites of Off ganglion cells. APB hyperpolarizes rod bipolar cells, thus blocking this rod pathway. With APB insensitive pathways, rods either directly synapse onto Off cone bipolar cells, or rods pass light decrement signal to cones by gap junctions. In the present study, whole-cell patch-clamp recordings were made from ganglion cells in the dark-adapted mouse retina to investigate the functional properties of APB sensitive and insensitive rod pathways. The results revealed several clear-cut differences between the APB sensitive and APB insensitive rod pathways. The latency of Off responses to a flashing spot of light was significantly shorter for the APB insensitive pathways than those for the APB sensitive pathway. Moreover, Off responses of the APB insensitive pathways were found to be capable of following substantially higher stimulus frequencies. Nitric oxide was found to selectively block Off responses in the APB sensitive rod pathway. Collectively, these results provide evidence that the APB sensitive and insensitive rod pathways can convey different types of information signaling light decrements in the dark-adapted retina.

Type
Research Article
Copyright
2006 Cambridge University Press

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References

REFERENCES

Ashmore, J.F. & Copenhagen, D.R. (1980). Different postsynaptic events in two types of retinal bipolar cell. Nature 288, 8486.Google Scholar
Baylor, D.A. (1987). Photoreceptor signals and vision. Proctor lecture. Investigative Ophthalmology and Visual Science 28, 3449.Google Scholar
Blakemore, C.B. & Rushton, W.A. (1965a). Dark adaptation and increment threshold in a rod monochromat. The Journal of Physiology 181, 612628.Google Scholar
Blakemore, C.B. & Rushton, W.A. (1965b). The rod increment threshold during dark adaptation in normal and rod monochromat. Journal of Physiology 181, 629640.Google Scholar
Brainard, D.H. (1997). The Psychophysics Toolbox. Spatial Vision 10, 433436.Google Scholar
Bredt, D.S., Hwang, P.M., & Snyder, S.H. (1990). Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347, 768770.Google Scholar
Conner, J.D. (1982). The temporal properties of rod vision. Journal of Physiology 332, 139155.Google Scholar
Dawson, T.M., Bredt, D.S., Fotuhi, M., Hwang, P.M., & Snyder, S.H. (1991). Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proceedings of the National Academy of Sciences of the U.S.A. 88, 77977801.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, 703712.Google Scholar
Demb, J.B., Haarsma, L., Freed, M.A., & Sterling, P. (1999). Functional circuitry of the retinal ganglion cell's nonlinear receptive field. Journal of Neuroscience 19, 97569767.Google Scholar
Doi, M., Uji, Y., & Yamamura, H. (1995). Morphological classification of retinal ganglion cells in mice. Journal of Comparative Neurology 356, 368386.Google Scholar
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, Massachusetts: Belknap Press of Harvard University Press.
Field, G.D. & Rieke, F. (2002). Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron 34, 773785.Google Scholar
Goureau, O., Lepoivre, M., Becquet, F., & Courtois, Y. (1993). Differential regulation of inducible nitric oxide synthase by fibroblast growth factors and transforming growth factor beta in bovine retinal pigmented epithelial cells: Inverse correlation with cellular proliferation. Proceedings of the National Academy of Sciences of the U.S.A. 90, 42764280.Google Scholar
Hack, I., Peichl, L., & Brandstatter, J.H. (1999). An alternative pathway for rod signals in the rodent retina: Rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors. Proceedings of the National Academy of Sciences of the U.S.A. 96, 1413014135.Google Scholar
Hirooka, K., Kourennyi, D.E., & Barnes, S. (2000). Calcium channel activation facilitated by nitric oxide in retinal ganglion cells. Journal of Neurophysiology 83, 198206.Google Scholar
Howes, K.A., Pennesi, M.E., Sokal, I., Church-Kopish, J., Schmidt, B., Margolis, D., Frederick, J.M., Rieke, F., Palczewski, K., Wu, S.M., Detwiler, P.B., & Baehr, W. (2002). GCAP1 rescues rod photoreceptor response in GCAP1/GCAP2 knockout mice. EMBO Journal 21, 15451554.Google Scholar
Koistinaho, J., Swanson, R.A., De Vente, J., & Sagar, S.M. (1993). NADPH-diaphorase (nitric oxide synthase)-reactive amacrine cells of rabbit retina: Putative target cells and stimulation by light. Neuroscience 57, 587597.Google Scholar
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, 76417654.Google Scholar
Neal, M., Cunningham, J., & Matthews, K. (1997). Nitric oxide enhancement of cholinergic amacrine activity by inhibition of glycine release. Investigative Ophthalmolology and Visual Science 38, 16341639.Google Scholar
Pelli, D.G. (1997). The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spatial Vision 10, 437442.Google Scholar
Protti, D.A., Flores-Herr, N., Li, W., Massey, S.C., & Wässle, H. (2005). Light signaling in scotopic conditions in the rabbit, mouse and rat retina: A physiological and anatomical study. Journal of Neurophysiology 93, 34793488.Google Scholar
Robinson, D.W. & Chalupa, L.M. (1997). The intrinsic temporal properties of alpha and beta retinal ganglion cells are equivalent. Current Biology 7, 366374.Google Scholar
Schiller, P.H. (1992). The ON and OFF channels of the visual system. Trends in Neurosciences 15, 8692.Google Scholar
Sharpe, L.T. & Stockman, A. (1999). Rod pathways: The importance of seeing nothing. Trends in Neurosciences 22, 497504.Google Scholar
Soucy, E., Wang, Y., Nirenberg, S., Nathans, J., & Meister, M. (1998). A novel signaling pathway from rod photoreceptors to ganglion cells in mammalian retina. Neuron 21, 481493.Google Scholar
Sterling, P. (2003). Retina. In The Synaptic Organization of the Brain, ed. Shepherd, G.M., pp. 205254. New York: Oxford University Press.
Völgyi, B., Deans, M.R., Paul, D.L., & Bloomfield, S.A. (2004). Convergence and segregation of the multiple rod pathways in mammalian retina. Journal of Neuroscience 24, 1118211192.Google Scholar
Wang, G.Y., Ratto, G., Bisti, S., & Chalupa, L.M. (1997). Functional development of intrinsic properties in ganglion cells of the mammalian retina. Journal of Neurophysiology 78, 28952903.Google Scholar
Wang, G.Y., Liets, L.C., & Chalupa, L.M. (2001). Unique functional properties of on and off pathways in the developing mammalian retina. Journal of Neuroscience 21, 43104317.Google Scholar
Wang, G.Y., Liets, L.C., & Chalupa, L.M. (2003). Nitric oxide differentially modulates ON and OFF responses of retinal ganglion cells. Journal of Neurophysiology 90, 13041313.Google Scholar
Yamamoto, R., Bredt, D.S., Snyder, S.H., & Stone, R.A. (1993). The localization of nitric oxide synthase in the rat eye and related cranial ganglia. Neuroscience 54, 189200.Google Scholar
Yu, D. & Eldred, W.D. (2005). Nitric oxide stimulates gamma-aminobutyric acid release and inhibits glycine release in retina. Journal of Comparative Neurology 483, 278291.Google Scholar