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Visual input induces long-term potentiation of developing retinotectal synapses

Nature Neuroscience volume 3, pages 708–715 (2000)Cite this article

Abstract

Early visual experience is essential in the refinement of developing neural connections. In vivo whole-cell recording from the tectum of Xenopus tadpoles showed that repetitive dimming-light stimulation applied to the contralateral eye resulted in persistent enhancement of glutamatergic inputs, but not GABAergic or glycinergic inputs, on tectal neurons. This enhancement can be attributed to potentiation of retinotectal synapses. It required spiking of postsynaptic tectal cells as well as activation of NMDA receptors, and effectively occluded long-term potentiation (LTP) of retinotectal synapses induced by direct electrical stimulation of retinal ganglion cells. Thus, LTP-like synaptic modification can be induced by natural visual inputs and may be part of the underlying mechanism for the activity-dependent refinement of developing connections.

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Figure 1: CSCs recorded in tectal neurons in response to visual stimuli in developing Xenopus tadpoles.
Figure 2: Three major types of tectal responses triggered by the dimming stimulus.
Figure 3: Enhancement of light evoked responses by repetitive dimming stimuli.
Figure 4: Involvement of postsynaptic spiking and NMDA receptors in synaptic modification by dimming stimuli.
Figure 5: Induction of LTP at retinotectal synapses by repetitive dimming stimuli.
Figure 6: Occlusion of electrically induced LTP by dimming stimuli.

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References

  1. Katz, L. C. & Shatz, C. J. Synaptic activity and the construction of cortical circuits. Science 274, 1133–1138 (1996).

    Article  CAS  Google Scholar 

  2. Penn, A. A., Riquelme, P. A., Feller, M. B. & Shatz, C. J. Competition in retinogeniculate patterning driven by spontaneous activity. Science 279, 2108–2112 (1998).

    Article  CAS  Google Scholar 

  3. Crowley, J. C. & Katz, L. C. Development of ocular dominance columns in the absence of retinal input. Nat. Neurosci. 2, 1125–1130 (1999).

    Article  CAS  Google Scholar 

  4. Wiesel, T. N. & Hubel, D. H. Single cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26, 1003–1017 (1963).

    Article  CAS  Google Scholar 

  5. LeVay, S., Stryker, M. P. & Shatz, C. J. Ocular dominance columns and their development in layer IV of the cat's visual cortex: a quantitative study. J. Comp. Neurol. 179, 223–244 (1978).

    Article  CAS  Google Scholar 

  6. LeVay, S., Wiesel, T. N. & Hubel, D. The development of ocular dominance columns in normal and visually deprived monkeys. J. Comp. Neurol. 191, 1–51 (1980).

    Article  CAS  Google Scholar 

  7. Stryker, M. P. & Harris, W. A. Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. J. Neurosci. 6, 2117–2133 (1986).

    Article  CAS  Google Scholar 

  8. Weliky, M. & Katz, L. C. Disruption of orientation tuning in visual cortex by artificially correlated neuronal activity. Nature 386, 680–685 (1997).

    Article  CAS  Google Scholar 

  9. Crair, M. C., Gillespie, D. C. & Stryker, M. P. The role of visual experience in the development of columns in cat visual cortex. Science 279, 566–570 (1998).

    Article  CAS  Google Scholar 

  10. Rittenhouse, C. D., Shouval, H. Z., Paradiso, M. A. & Bear, M. F. Monocular deprivation induces homosynaptic long-term depression in visual cortex. Nature 397, 347–350 (1999).

    Article  CAS  Google Scholar 

  11. Fawcett, J. W. & Willshaw, D. J. Compound eyes project stripes on the optic tectum in Xenopus. Nature 296, 350–351 (1982).

    Article  CAS  Google Scholar 

  12. Udin, S. B. Abnormal visual input leads to development of abnormal axon trajectories in frogs. Nature 301, 336–338 (1983).

    Article  CAS  Google Scholar 

  13. Reh, T. A. & Constantine-Paton, M. Eye-specific segregation requires neural activity in three-eyed Rana pipiens. J. Neurosci. 5, 1132–1143 (1985).

    Article  CAS  Google Scholar 

  14. Schmidt, J. T. & Buzzard, M. Activity-driven sharpening of the retinotectal projection in goldfish: development under stroboscopic illumination prevents sharpening. J. Neurobiol. 24, 384–99 (1993).

    Article  CAS  Google Scholar 

  15. Bliss, T. V. & Lømo, T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. (Lond.) 232, 331–356 (1973).

    Article  CAS  Google Scholar 

  16. Malenka, R. C. & Nicoll, R. A. Long-term potentiation—a decade of progress? Science 285, 1870–1874 (1999).

    Article  Google Scholar 

  17. Perkins, A. T. & Teyler, T. J. A critical period for long term potentiation in the developing rat visual cortex. Brain Res. 439, 222–229 (1988).

    Article  Google Scholar 

  18. Komatsu, Y., Fujii, K., Maeda, J., Sakaguchi, H. & Toyama, K. Long-term potentiation of synaptic transmission in kitten visual cortex. J. Neurophysiol. 59, 124–141 (1988).

    Article  CAS  Google Scholar 

  19. Artola, A., Bröcher, S. & Singer, W. Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature 347, 69–72 (1990).

    Article  CAS  Google Scholar 

  20. Mooney, R., Madison, D. V. & Shatz, C. J. Enhancement of transmission at the developing retinogeniculate synapse. Neuron 10, 815–825 (1993).

    Article  CAS  Google Scholar 

  21. Crair, M. C. & Malenka, R. C. A critical period for long-term potentiation at thalamo-cortical synapses. Nature 375, 325–328 (1995).

    Article  CAS  Google Scholar 

  22. Zhang, L. I., Tao, H. W., Holt, C. E., Harris, W. A. & Poo, M. A critical window for cooperation and competition among developing retinotectal synapses. Nature 395, 37–44 (1998).

    Article  CAS  Google Scholar 

  23. Cline, H. T. & Constantine-Paton, M. NMDA receptor antagonists disrupt the retinotectal topographic map. Neuron 3, 413–426 (1989).

    Article  CAS  Google Scholar 

  24. Scherer, W. J. & Udin, S. B. N-methyl-D-aspartate antagonists prevent interaction of binocular maps in Xenopus tectum. J. Neurosci. 9, 3837–3843 (1989).

    Article  CAS  Google Scholar 

  25. Bear, M. F., Kleinschmidt, A., Gu, Q. A. & Singer, W. Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist. J. Neurosci. 10, 909–925 (1990).

    Article  CAS  Google Scholar 

  26. Schmidt, J. T. Long-term potentiation and activity-dependent retinotopic sharpening in the regenerating retinotectal projection of goldfish: common sensitive period and sensitivity to NMDA blockers. J. Neurosci. 10, 233–246 (1990).

    Article  CAS  Google Scholar 

  27. Hahm, J. O., Langdon, R. B. & Sur, M. Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors. Nature 351, 568–570 (1991).

    Article  CAS  Google Scholar 

  28. Simon, D. K., Prusky, G. T., O'Leary, D. D. & Constantine-Paton, M. N-methyl-d-aspartate receptor antagonists disrupt the formation of a mammalian neural map. Proc. Natl. Acad. Sci. USA 89 10593–10597 (1992).

    Article  CAS  Google Scholar 

  29. Schlaggar, B. L., Fox, K. & O'Leary, D. D. Postsynaptic control of plasticity in developing somatosensory cortex. Nature 364, 623–626 (1993).

    Article  CAS  Google Scholar 

  30. Li, Y., Erzurumlu, R. S., Chen, C., Jhaveri, S. & Tonegawa, S. Whisker-related neuronal patterns fail to develop in the trigeminal brainstem nuclei of NMDAR1 knockout mice. Cell 76, 427–437 (1994).

    Article  CAS  Google Scholar 

  31. Aamodt, S. M. & Constantine-Paton, M. The role of neural activity in synaptic development and its implications for adult brain function. Adv. Neurol. 79, 133–144 (1999).

    CAS  PubMed  Google Scholar 

  32. Kirkwood, A., Rioult, M. C. & Bear, M. F. Experience-dependent modification of synaptic plasticity in visual cortex. Nature 381, 526–528 (1996).

    Article  CAS  Google Scholar 

  33. Kirkwood, A., Lee, H. K. & Bear, M. F. Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience. Nature 375, 328–331 (1995).

    Article  CAS  Google Scholar 

  34. Rogan, M. T., Staubli, U. V. & LeDoux, J. E. Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390, 604–607 (1997).

    Article  CAS  Google Scholar 

  35. Oda, Y., Kawasaki, K., Morita, M., Korn, H. & Matsui, H. Inhibitory long-term potentiation underlies auditory conditioning of goldfish escape behaviour. Nature 394, 182–185 (1998).

    Article  CAS  Google Scholar 

  36. Moser, E. I., Krobert, K. A., Moser, M.-B. & Morris, R. G. M. Impaired spatial learning after saturation of long-term potentiation. Science 281, 2038–2042 (1998).

    Article  CAS  Google Scholar 

  37. Rioult-Pedotti, M. S., Friedman, D., Hess, G. & Donoghue, J. P. Strengthening of horizontal cortical connections following skill learning. Nat. Neurosci. 1, 230–234 (1998).

    Article  CAS  Google Scholar 

  38. Xu, L., Anwyl, R. & Rowan, M. J. Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature 394, 891–894 (1998).

    Article  CAS  Google Scholar 

  39. Hamill, O. P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391, 85–100 (1981).

    Article  CAS  Google Scholar 

  40. Rae, J., Cooper, K., Gates, P. & Watsky, M. Low access resistance perforated patch recordings using amphotericin B. J. Neurosci. Methods 37, 15–26 (1991).

    Article  CAS  Google Scholar 

  41. Nieuwkoop, P. D. & Faber, J. Normal Table of Xenopus Laevis 2nd edn. (North Holland, Amsterdam, 1967).

    Google Scholar 

  42. Gaze, R. M., Keating, M. J. & Chung, S. H. The evolution of the retinotectal map during development in Xenopus. Proc. R. Soc. Lond. B. 185, 301–330 (1974).

    Article  CAS  Google Scholar 

  43. Holt, C. E. & Harris, W. A. Order in the initial retinotectal map in Xenopus: a new technique for labelling growing nerve fibres. Nature 301, 150–152 (1983).

    Article  CAS  Google Scholar 

  44. Edwards, J. A. & Cline, H. T. Light-induced calcium influx into retinal axons is regulated by presynaptic nicotinic acetylcholine receptor activity in vivo. J. Neurophysiol. 81, 895–907 (1999).

    Article  CAS  Google Scholar 

  45. Ben-Ari, Y., Khazipov, R., Leinekugel, X., Caillard, O. & Gaiarsa, J. L. GABAA, NMDA and AMPA receptors: a developmentally regulated ‘ménage à trois’. Trends Neurosci. 20, 523–529 (1997).

    Article  CAS  Google Scholar 

  46. Lettvin, J. Y., Maturana, H. R., McCulloch, W. S. & Pitts, W. H. What the frog's eye tells the frog's brain. Proc. Inst. Radio Eng. 47, 1950–1961 (1959).

    Google Scholar 

  47. Bi, G.-q. & Poo, M.-m. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18, 10464–10472 (1998).

    Article  CAS  Google Scholar 

  48. Engert, F. & Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66–70 (1999).

    Article  CAS  Google Scholar 

  49. Maletic-Savatic, M., Malinow, R. & Svoboda, K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283, 1923–1927 (1999).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank G. Bi, Y. Dan, W. Harris, C. Holt and F. Engert for suggestions. This work was supported by a grant from the National Science Foundation.

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Author notes

  1. Li I. Zhang and Hui-zhong W. Tao: The first two authors contributed equally to this work.

Authors and Affiliations

  1. Department of Biology, University of California at San Diego, La Jolla, 92093-0357, California, USA

    Li I. Zhang, Hui-zhong W. Tao & Mu-ming Poo

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Correspondence to Mu-ming Poo.

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Zhang, L., Tao, Hz. & Poo, Mm. Visual input induces long-term potentiation of developing retinotectal synapses. Nat Neurosci 3, 708–715 (2000). https://doi.org/10.1038/76665

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