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Stratification of ON and OFF ganglion cell dendrites depends on glutamate-mediated afferent activity in the developing retina

Abstract

A FUNDAMENTAL attribute of the vertebrate visual system is the segregation of ON and OFF pathways signalling increments and decrements of light1–4. In the mature retina, dendrites of ON- and OFF-centre retinal ganglion cells (RGCs) stratify in different sublaminae of the inner plexiform layer (IPL), and are differentially innervated by two types of bipolar cells which depolarize and hyperpolarize on exposure to light5–10. This stratification of ON and OFF RGCs is achieved by the gradual restriction of their dendrites which ramify throughout the IPL early in development11–14. The factors underlying this regressive event are unknown. Dendritic stratification occurs around the time that bipolar cells form synapses in the IPL15,16, which raises the possibility that synaptic activity is involved in this process. Here we test this hypothesis by treating the developing cat retina with the glutamate analogue 2-amino-4-phosphonobutyric acid (APR), which hyper-polarizes ON cone bipolar and rod bipolar cells, thereby preventing their release of glutamate17–19. We report that intraocular injection of APB during the period when dendritic stratification normally occurs prevents the formation of structurally segregated ON and OFF retinal pathways. These results provide evidence that glutamate-mediated afferent activity regulates the remodelling of RGC dendrites during development.

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References

  1. Hartline, H. K. Am. J. Physiol. 121, 400–415 (1938).

    Google Scholar 

  2. Kuffler, S. W. J. Neurophysiol. 16, 37–68 (1953).

    Article  CAS  Google Scholar 

  3. Barlow, H. B. J. Physiol. 119, 69–88 (1953).

    Article  CAS  Google Scholar 

  4. Schiller, P. H. Trends Neurosci. 15, 86–92 (1992).

    Article  CAS  Google Scholar 

  5. Nelson, R. & Kolb, H. Vision Res. 23, 1183–1195 (1983).

    Article  CAS  Google Scholar 

  6. Famiglietti, E. V. Jr & Kolb, H. Science 194, 193–195 (1976).

    Article  ADS  Google Scholar 

  7. Nelson, R., Famiglietti, E. V. Jr & Kolb, H. J. Neurophysiol. 41, 472–483 (1978).

    Article  CAS  Google Scholar 

  8. Wässle, H., Boycott, B. B. & Illing, R. B. Proc. R. Soc. Lond. B212, 177–195 (1981).

    ADS  PubMed  Google Scholar 

  9. McGuire, B. A., Stevens, J. K. & Sterling, P. J. Neurosci. 6, 907–918 (1986).

    Article  CAS  Google Scholar 

  10. Wässle, H. & Boycott, B. B. Physiol. Rev. 71, 447–480 (1991).

    Article  Google Scholar 

  11. Maslim, J., Webster, M. & Stone, J. J. comp. Neurol. 254, 382–402 (1986).

    Article  CAS  Google Scholar 

  12. Maslim, J. & Stone, J. Devl Br. Res. 44, 87–93 (1988).

    Article  CAS  Google Scholar 

  13. Ramoa, A. S., Campbell, G. & Shatz, C. J. J. Neurosci. 8, 4239–4261 (1988).

    Article  CAS  Google Scholar 

  14. Dann, J. F., Buhl, E. H. & Peichl, L. J. Neurosci. 8, 1485–1499 (1988).

    Article  CAS  Google Scholar 

  15. Maslim, J. & Stone J. Brain Res. 373, 35–48 (1986).

    Article  CAS  Google Scholar 

  16. Maslim, J. & Stone J. Devl Br. Res. 44, 87–93 (1988).

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  18. Bolz, J., Wässle, H. & Thier, P. Neurosci. 12, 875–885 (1984).

    Article  CAS  Google Scholar 

  19. Müller, F., Wässle, H. & Voigt, T. J. Neurophysiol. 59, 1657–1672 (1988).

    Article  Google Scholar 

  20. Wässle, H., Boycott, B. B. & Illing R. B. Proc. R. Soc. Lond. B 212, 177–195 (1981).

    ADS  PubMed  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  22. Famiglietti, E. V. & Kolb, H. Brain Res. 84, 293–300 (1975).

    Article  Google Scholar 

  23. McGuire, B. A., Stevens, J. K. & Sterling, P. J. Neurosci. 4, 2920–2938 (1984).

    Article  CAS  Google Scholar 

  24. McGuire, B. A., Stevens, J. K. & Sterling, P. J. Neurosci. 6, 907–918 (1986).

    Article  CAS  Google Scholar 

  25. Wässle, H., Yamashita, M., Greferath, U., Grünert, U. & Müller, F. Vis. Neurosci. 7, 99–112 (1991).

    Article  Google Scholar 

  26. Movshon, J. A. & van Sluyters, R. C. A. Rev. Psychol. 32, 477–522 (1981).

    Article  CAS  Google Scholar 

  27. Sherman, S. M. & Spear, P. D. Physiol. Rev. 62, 740–855 (1982).

    Article  Google Scholar 

  28. Shatz, C. J. & Stryker, M. P. Science 242, 87–89 (1988).

    Article  ADS  CAS  Google Scholar 

  29. Sretavan, D. W., Shatz, C. J. & Stryker, M. P. Nature 336, 468–471 (1988).

    Article  ADS  CAS  Google Scholar 

  30. Shatz, C. J. Neuron 5, 745–756 (1990).

    Article  CAS  Google Scholar 

  31. Hahm, J. O., Langdon R. B. & Sur, M. Nature 351, 568–570 (1991).

    Article  ADS  CAS  Google Scholar 

  32. Wong, R. O. L., Herrmann, K. & Shatz, C. J. J. Neurobiol. 22, 685–697 (1991).

    Article  CAS  Google Scholar 

  33. Dubin, M. W., Stark, L. A. & Archer, S. M. J. Neurosci. 6, 1021–1036 (1986).

    Article  CAS  Google Scholar 

  34. Leventhal, A. G. & Hirsch, H. V. B. J. Neurosci. 3, 332–344 (1983).

    Article  CAS  Google Scholar 

  35. Lau, K. C., So, K. F. & Tay, D. J. comp. Neurol. 300, 583–592 (1990).

    Article  CAS  Google Scholar 

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Bodnarenko, S., Chalupa, L. Stratification of ON and OFF ganglion cell dendrites depends on glutamate-mediated afferent activity in the developing retina. Nature 364, 144–146 (1993). https://doi.org/10.1038/364144a0

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