Abstract
THE retina is sensitive to light stimuli varying over more than 12 log units in intensity. It accomplishes this, in part, by switching between rod-dominated circuits designed for maximum utilization of scarce photons and cone circuits designed for greater acuity. Rod signals are integrated into the cone pathways through AII amacrine cells, which are connected by gap junctions both to other AII amacrine cells and to cone bipolar cells. To determine the relative permeabilities of the two junctional pathways, we have measured the distribution of biotinylated tracers across this heterologous cell assembly after injecting a single AII amacrine cell. We found that neurobiotin (relative molecular mass, 286) passed easily through both types of gap junctions, but that biotin-X cadaverine (relative molecular mass, 442) passed through AII/bipolar cell gap junctions poorly compared to AII/AII gap junctions. Thus, the AII /bipolar cell channel has a lower permeability to large molecules than does the AII/AII amacrine cell channel. The two pathways are also regulated differently. Dopamine and cyclic AMP agonists, known to diminish AII–AII coupling1, did not change the relative labelling intensity of AII to bipolar cells. However, nitric oxide and cGMP agonists selectively reduced labelling in bipolar cells relative to AII amacrine cells, perhaps by acting at the bipolar side of this gap junction. This suggests that increased cGMP controls the network switching between rod and cone pathways associated with light adaptation.
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References
Hampson, E. C. G. M., Vaney, D. I. & Weiler, R. J. Neurosci. 12, 4911–4922 (1992).
Kolb, H. & Famiglietti, E. V. Science 186, 47–49 (1974).
Strettoi, E., Raviola, E. & Dacheux, R. F. J. comp. Neurol. 325, 152–168 (1992).
Sterling, P. A. Rev. Neurosci. 6, 149–185 (1983).
Bennett, M. V. L. et al. Neuron 6, 305–320 (1991).
Beyer, E. C., Paul, D. L. & Goodenough, D. A. J. Membr. Biol. 116, 187–194 (1990).
Rae, J. L. Curr. Top. Eye Res. 1, 37–90 (1979).
Swenson, K. L., Jordan, J. R., Beyer, E. C. & Paul, D. L. Cell 57, 145–155 (1989).
Werner, R., Levine, E., Rabadan-Diehl, C. & Dahl, G. Proc. natn. Acad. Sci. U.S.A. 86, 5380–5384 (1989).
Bruzzone, R., White, T. W. & Paul, D. L. J. Cell Sci. 107, 955–967 (1994).
Flagg-Newton, J., Simpson, I. & Loewenstein, W. R. Science 205, 406–407 (1979).
Brink, P. & Dewey, M. M. Nature 285, 101–102 (1980).
Zimmerman, A. L. & Rose, B. J. Membr. Biol. 84, 269–283 (1985).
Veenstra, R. D., Wang, H.-Z., Beyer, E. C. & Brink, P. R. Circ. Res. 75, 483–490 (1994).
Törk, I. & Stone, J. Brain Res. 169, 261–273 (1979).
Voigt, T. & Wässle, H. J. Neurosci. 7, 4115–4128 (1987).
Witkovsky, P. & Dearry, A. Progr. Ret. Res. 11, 247–292 (1991).
Koistinaho, J., Swanson, R. A., De Vente, J. & Sagar, S. M. Neuroscience 57, 587–597 (1993).
Massey, S. C., Mills, S. L. & De Vente, J. Invest. Ophthal. Vis. Sci. (suppl.) 34, 1382 (1993).
Vaney, D. I. Progr. Ret. Res. 13, 301–355 (1994).
Yamamoto, R., Bredt, D. S., Snyder, S. H. & Stone, R. A. Neuroscience 54, 189–200 (1993).
Shiells, R. & Falk, G. Neuroreport 3, 845–848 (1992).
Slaughter, M. M. & Miller, R. F. Science 211, 182–185 (1981).
Shiells, R. & Falk, G. Proc. R. Soc. Lond. B 242, 91–94 (1990).
Nawy, S. & Jahr, C. E. Nature 346, 269–271 (1990).
Yamashita, M. & Wassle, H. J. Neurosci. 11, 2372–2382 (1991).
Nomura, A. et al. Cell 77, 361–369 (1994).
Tian, N. & Slaughter, M. M. J. Neurophysiol. 71, 2258–2268 (1994).
Mills, S. L. & Massey, S. C. J. comp. Neurol. 304, 491–501 (1991).
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Mills, S., Massey, S. Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377, 734–737 (1995). https://doi.org/10.1038/377734a0
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DOI: https://doi.org/10.1038/377734a0
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