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Differential properties of two gap junctional pathways made by AII amacrine cells

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

  1. Hampson, E. C. G. M., Vaney, D. I. & Weiler, R. J. Neurosci. 12, 4911–4922 (1992).

    Article  CAS  Google Scholar 

  2. Kolb, H. & Famiglietti, E. V. Science 186, 47–49 (1974).

    Article  ADS  CAS  Google Scholar 

  3. Strettoi, E., Raviola, E. & Dacheux, R. F. J. comp. Neurol. 325, 152–168 (1992).

    Article  CAS  Google Scholar 

  4. Sterling, P. A. Rev. Neurosci. 6, 149–185 (1983).

    Article  CAS  Google Scholar 

  5. Bennett, M. V. L. et al. Neuron 6, 305–320 (1991).

    Article  CAS  Google Scholar 

  6. Beyer, E. C., Paul, D. L. & Goodenough, D. A. J. Membr. Biol. 116, 187–194 (1990).

    Article  CAS  Google Scholar 

  7. Rae, J. L. Curr. Top. Eye Res. 1, 37–90 (1979).

    CAS  PubMed  Google Scholar 

  8. Swenson, K. L., Jordan, J. R., Beyer, E. C. & Paul, D. L. Cell 57, 145–155 (1989).

    Article  CAS  Google Scholar 

  9. Werner, R., Levine, E., Rabadan-Diehl, C. & Dahl, G. Proc. natn. Acad. Sci. U.S.A. 86, 5380–5384 (1989).

    Article  ADS  CAS  Google Scholar 

  10. Bruzzone, R., White, T. W. & Paul, D. L. J. Cell Sci. 107, 955–967 (1994).

    CAS  PubMed  Google Scholar 

  11. Flagg-Newton, J., Simpson, I. & Loewenstein, W. R. Science 205, 406–407 (1979).

    Article  ADS  Google Scholar 

  12. Brink, P. & Dewey, M. M. Nature 285, 101–102 (1980).

    Article  ADS  CAS  Google Scholar 

  13. Zimmerman, A. L. & Rose, B. J. Membr. Biol. 84, 269–283 (1985).

    Article  CAS  Google Scholar 

  14. Veenstra, R. D., Wang, H.-Z., Beyer, E. C. & Brink, P. R. Circ. Res. 75, 483–490 (1994).

    Article  CAS  Google Scholar 

  15. Törk, I. & Stone, J. Brain Res. 169, 261–273 (1979).

    Article  Google Scholar 

  16. Voigt, T. & Wässle, H. J. Neurosci. 7, 4115–4128 (1987).

    Article  CAS  Google Scholar 

  17. Witkovsky, P. & Dearry, A. Progr. Ret. Res. 11, 247–292 (1991).

    Article  CAS  Google Scholar 

  18. Koistinaho, J., Swanson, R. A., De Vente, J. & Sagar, S. M. Neuroscience 57, 587–597 (1993).

    Article  CAS  Google Scholar 

  19. Massey, S. C., Mills, S. L. & De Vente, J. Invest. Ophthal. Vis. Sci. (suppl.) 34, 1382 (1993).

    Google Scholar 

  20. Vaney, D. I. Progr. Ret. Res. 13, 301–355 (1994).

    Article  Google Scholar 

  21. Yamamoto, R., Bredt, D. S., Snyder, S. H. & Stone, R. A. Neuroscience 54, 189–200 (1993).

    Article  CAS  Google Scholar 

  22. Shiells, R. & Falk, G. Neuroreport 3, 845–848 (1992).

    Article  CAS  Google Scholar 

  23. Slaughter, M. M. & Miller, R. F. Science 211, 182–185 (1981).

    Article  ADS  CAS  Google Scholar 

  24. Shiells, R. & Falk, G. Proc. R. Soc. Lond. B 242, 91–94 (1990).

    Article  ADS  CAS  Google Scholar 

  25. Nawy, S. & Jahr, C. E. Nature 346, 269–271 (1990).

    Article  ADS  CAS  Google Scholar 

  26. Yamashita, M. & Wassle, H. J. Neurosci. 11, 2372–2382 (1991).

    Article  CAS  Google Scholar 

  27. Nomura, A. et al. Cell 77, 361–369 (1994).

    Article  CAS  Google Scholar 

  28. Tian, N. & Slaughter, M. M. J. Neurophysiol. 71, 2258–2268 (1994).

    Article  CAS  Google Scholar 

  29. Mills, S. L. & Massey, S. C. J. comp. Neurol. 304, 491–501 (1991).

    Article  CAS  Google Scholar 

Download references

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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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