Advertisement

Activity-Driven Mechanisms for Sharpening Retinotopic Projections: Correlated Activity, NMDA Receptors, Calcium Entry, and Beyond

  • John T. Schmidt

Abstract

The precise organization of visual projections develops by selective stabilization of appropriate synapses from a more diffuse set of initial connections, a process that requires normal patterns of activity during the sensitive period. This chapter covers research on the establishment of retinotopic precision in the direct retinal map on tectum of fish and frog. This research grew out of two separate lines of inquiry: early demonstrations of plasticity in both developing and adult retinotectal projection, and studies of the effects of experience on development of visual cortex in mammals. Of course, Mike Gaze was the leader in demonstrating plasticity within the retinotectal projection, which initially had been thought to be rigidly specified (Sperry, 1963).

Keywords

NMDA Receptor Ocular Dominance NMDA Receptor Blocker Monocular Deprivation Retinal Axon 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adamson J, Burke J, Grobstein P (1984): Recovery of the ipsilateral oculotectal projection following nerve crush in the frog: Evidence that retinal afferents make synapses at abnormal tectal locations. J Neurosci 4: 2635–2649Google Scholar
  2. Bear MF, Kleinschmidt A, Gu Q, Singer W (1990): Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist. J Neurosci 10: 909–925Google Scholar
  3. Bekkers JM, Stevens CF (1990): Presynaptic mechanism for long-term potentiation in the hippocampus. Nature 346: 724–728CrossRefGoogle Scholar
  4. Benowitz LI, Routtenberg A (1987): A membrane phosphoprotein associated with neural development, axonal regeneration, phospholipid metabolism, and synaptic plasticity. Trends Neurosci 10: 527–532CrossRefGoogle Scholar
  5. Benowitz LI, Schmidt JT (1987): Activity dependent sharpening of the regenerating retinotectal projection in goldfish: Relationship to the expression of growth associated protein. Brain Res 417: 118–112CrossRefGoogle Scholar
  6. Boss VC, Schmidt JT (1984): Activity and the formation of ocular dominance patches in dually innervated tectum of goldfish. J Neurosci 4: 2891–2905Google Scholar
  7. Brink DL, Meyer RL (1986): Locally correlated spontaneous activity in the goldfish optic tectum after nerve crush. Neurosci Abstr 12: 438Google Scholar
  8. Cine HT (1991): Activity-dependent plasticity in the visual system of frogs and fish. Trends Neurosci 14: 104–111CrossRefGoogle Scholar
  9. Cline HT, Constantine-Paton M (1989): NMDA receptor antagonists disrupt the retinotectal topographic map. Neuron 3: 413–426CrossRefGoogle Scholar
  10. Cline HT, Constantine-Paton M (1990): The differential influence of protein kinase inhibitors on retinal arbor morphology and eye-specific stripes in the frog retinotectal system. Neuron 4: 899–908CrossRefGoogle Scholar
  11. Cline HT, Debski EA, Constantine-Paton M (1987): N-Methyl-D-aspartate receptor antagonist desegregates eye specific stripes. Proc Natl Acad Sci USA 84: 4342–4345CrossRefGoogle Scholar
  12. Cline HT, Debski EA, Constantine-Paton M (1990): NMDA receptor agonists and antagonists alter retinal ganglion cell arbor structure in the developing frog retinotectal projection. J Neurosci 10: 1197–1215Google Scholar
  13. Collingridge GL, Bliss TVP (1987): NMDA receptors—their role in long term potentiation. Trends Neurosci 10: 288–293CrossRefGoogle Scholar
  14. Cook JE, Becker DL (1988): Retinotopic refinement of the regenerating goldfish optic tract is not linked to activity-dependent refinement of the retinotectal map. Development 104:321–329Google Scholar
  15. Cook JE, Rankin ECC (1986): Impaired refinement of the regenerated retinotectal projection of the goldfish in stroboscopic light: A quantitative WGA-HRP study. Exp Brain Res 63: 421–430CrossRefGoogle Scholar
  16. Dorman RV, Schwartz MA, Terrian DM (1988): Depolarization induced [3H]arachidonic acid accumulation: Effects of external Ca++ and phospholipase inhibitors. Brain Res Bull 21: 445–450CrossRefGoogle Scholar
  17. Drapeau C, Pellerin L, Wolfe LS, Avoli M (1990): Long-term changes of synaptic transmission induced by arachidonic acid in the CA1 subfield of the rat hippocampus. Neurosci Lett 115: 286–292CrossRefGoogle Scholar
  18. Dubin MW, Stark LA, Archer SM (1986): A role for action potential activity in the development of neuronal connections in the kitten retinogeniculate pathway. J Neurosci 6: 1021–1036Google Scholar
  19. Dumuis A, Sebben M, Haynes L, Pin J-P, Bockaert J (1988): NMDA receptors activate the arachidonic acid cascade system in striatal neurons. Nature 336: 68–70CrossRefGoogle Scholar
  20. Eisele LE, Schmidt JT (1988): Activity sharpens the regenerating retinotectal projection in goldfish: Sensitive period for strobe illumination and lack of effect on synaptogenesis and on ganglion cell receptive field properties. J Neurobiol 19: 395–411CrossRefGoogle Scholar
  21. Freeman EJ, Terrian DM, Dorman RV (1990): Presynaptic facilitation of glutamate release from isolated hippocampal mossy fiber endings by arachidonic acid. Neurochem Res 15: 743–750CrossRefGoogle Scholar
  22. Fujisawa H (1987): Mode of growth of retinal axons within the tectum of Xenopus tadpoles, and implications in the ordered neuronal connection between the retina and the tectum. J Comp Neurol 260: 127–139CrossRefGoogle Scholar
  23. Gaze RM, Sharma SC (1970): Axial differences in the reinnervation of the goldfish optic tectum by regenerating optic nerve fibres. Exp Brain Res 10: 171–181CrossRefGoogle Scholar
  24. Gaze RM, Keating MJ, Chung SH (1974): The evolution of the retinotectal map during development in Xenopus. Proc R Soc Lond B 185: 301–330CrossRefGoogle Scholar
  25. Gu Q, Bear M, Singer W (1989): Blockade of NMDA receptors prevents ocularity changes in kitten visual cortex after reversed monocular deprivation. Dev Brain Res 47: 281–288CrossRefGoogle Scholar
  26. Hahm J-O, Langdon RB, Sur M (1991): Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors. Nature 351: 568–570CrossRefGoogle Scholar
  27. Hartlieb E, Stuermer CAO (1987): Preferential loss of collaterals from goldfish retinal axons in the optic tract is delayed by tetrodotoxin. Neurosci Lett 79: 1–5CrossRefGoogle Scholar
  28. Hayes WP, Meyer RL (1989): Impulse blockade by intraocular tetrodotoxin during optic regeneration in goldfish: HRP-EM evidence that the formation of normal numbers of optic synapses and the elimination of exuberant optic fibers is activity independent. J Neurosci 9: 1414–1423Google Scholar
  29. Hebb DO (1949): The Organization of Behavior. New York: John Wiley and SonsGoogle Scholar
  30. Hirsch HVB, Tieman SB (1987): Perceptual development and experience-dependent changes in cat visual cortex. In: Sensitive Periods in Development: Interdisciplinary Perspectives, Bernstein M, ed. Hillsdale, NJ: Lawrence Erlbaum AssocGoogle Scholar
  31. Humphrey MF, Beazley LD (1982): An electrophysiological study of early retinotectal projection patterns during optic nerve regeneration in Hyla moorei. Brain Res 239: 595–602CrossRefGoogle Scholar
  32. Kageyama GH, Meyer RL (1988): Regenerating optic axons form transient topographically inappropriate synapses in goldfish tectum: A WGA-HRP study. Neurosci Abstr 14:674Google Scholar
  33. Keating MJ, Grant S, Dawes EA, Nanchanal K (1986): Visual deprivation of the retinotectal projection in Xenopus laevis. J Embryol Exp Morphol 91: 101–115Google Scholar
  34. Keyser DO, Alger BE (1991): Synergistic activation of protein kinase C by arachidonic acid and diacyl glycerol in hippocampal neurons. Neurosci Abstr 17: 16Google Scholar
  35. Kleinschmidt A, Bear MF, Singer W (1987): Blockade of “NMDA” receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238: 355–357CrossRefGoogle Scholar
  36. Komatsu Y, Fujii K, Maeda J, Sakaguchi H, Toyoma K (1988): Long term potentiation of synaptic transmission in kitten visual cortex. J Neurophysiol 59: 124–141Google Scholar
  37. Langdon RB, Freeman JA (1986): Antagonists of glutaminergic neurotransmission block retinotectal transmission in goldfish. Brain Res 398: 169–174CrossRefGoogle Scholar
  38. MacDermott AB, Mayer ML, Westbrook GL, Smith SJ, Barker JL (1986): NMDA- receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321: 519–522CrossRefGoogle Scholar
  39. Madison DV, Malenka RC, Nicoll RA (1991): Mechanisms underlying long-term potentiation of synaptic transmission. Ann Rev Neurosci 14: 379–397CrossRefGoogle Scholar
  40. Massicotte G, Oliver MW, Lynch G, Baudry M (1990): Effect of bromophenacyl bromide, a phospholipase A2 inhibitor, on the induction and maintenance of LTP in hippocampal slices. Brain Res 537: 49–53CrossRefGoogle Scholar
  41. Mastronarde DN (1989): Correlated firing of retinal ganglion cells. Trends Neurosci 12: 75–80CrossRefGoogle Scholar
  42. Matsumoto N, Kometani M, Nagano K (1987): Regenerating retinal fibers of the goldfish make temporary and unspecific but functional synapses before forming the final retinotopic projection. Neuroscience 22: 1103–1110CrossRefGoogle Scholar
  43. Meyer RL (1982): Tetrodotoxin blocks the formation of ocular dominance columns in goldfish. Science 218: 589–591CrossRefGoogle Scholar
  44. Murray M (1982): A quantitative study of regenerative sprouting by optic axons in goldfish. J Comp Neurol 209: 352–362CrossRefGoogle Scholar
  45. Nakamura H, O’Leary DDM (1989): Inaccuracies in initial growth and arborization of chick retinotectal axons followed by course corrections and axon remodelling to develop topographic order. J Neurosci 9: 3776–3795Google Scholar
  46. Norden JJ, Lettes A, Costello B, Lin LH, Wouters B, Bock S, Freeman JA (1991): Possible role of GAP-43 in calcium regulation/neurotransmitter release. Ann NY Acad Sci 627: 75–93CrossRefGoogle Scholar
  47. Nowak L, Bregestovski P, Ascher P, Herbert A, Prochianz A (1984): Magnesium gates glutamate activated channels in mouse central neurons. Nature 307: 462–465CrossRefGoogle Scholar
  48. Okada D, Yamagishi S, Sugiyama H (1989): Differential effects of phospholipase inhibitors in long-term potentiation in the rat hippocampal mossy fiber synapses and schaffer/commissural synapses. Neurosci Lett 100: 141–146CrossRefGoogle Scholar
  49. O’Leary DDM, Fawcett JW, Cowan WM (1986): Topographic targeting errors in the retinocollicular projection and their elimination by selective ganglion cell death. J Neurosci 6: 3692–3705Google Scholar
  50. Reh TA, Constantine-Paton M (1985): Eye-specific segregation requires neural activity in three-eyed Rana pipiens. J Neurosci 5: 1132–1143Google Scholar
  51. Sachs GM, Jacobson M, Caviness VS (1986): Postnatal changes in arborization patterns of murine retinocollicular axons. J Comp Neurol 246: 395–408CrossRefGoogle Scholar
  52. Sakaguchi DS, Murphey RK (1985): Map formation in the developing Xenopus retinotectal system: An examination of ganglion cell terminal arborizations. J Neurosci 5: 3229–3245Google Scholar
  53. Sanfeliu C, Hunt A, Patel AJ (1990): Exposure to N-methyl-D-aspartate increased release of arachidonic acid in primary cultures of rat hippocampal neurones and not in astrocytes. Brain Res 526: 241–248CrossRefGoogle Scholar
  54. Schmidt JT (1982): The formation of retinotectal projections. Trends Neurosci 5: 111–116CrossRefGoogle Scholar
  55. Schmidt JT (1990): 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: 233–246Google Scholar
  56. Schmidt JT (1991a): Long-term potentiation during the activity-dependent sharpening of the retinotopic map in goldfish. Ann NY Acad Sci 627:10–25CrossRefGoogle Scholar
  57. Schmidt JT (1991b): Kinase manipulations disrupt activity-driven retinotopic sharpening in goldfish tectum. Neurosci Abstr 17:215Google Scholar
  58. Schmidt JT (1992): The roles of activity, competition and continued growth in the formation and stabilization of retinotectal connections in fish and frog. In: Advances in Neural and Behavioral Development, Vol. 4, Casagrande VA, ed. Norwood, NJ: AblemanGoogle Scholar
  59. Schmidt JT, Buzzard M (1990): Activity-driven sharpening of the regenerating retinotectal projection: Effects of blocking or synchronizing activity on the morphology of individual optic regenerating arbors. J Neurobiol 21: 900–917CrossRefGoogle Scholar
  60. Schmidt JT, Edwards DL (1983): Activity sharpens the map during the regeneration of the retinotectal projection in goldfish. Brain Res 269: 29–39CrossRefGoogle Scholar
  61. Schmidt JT, Eisele LE (1985): Stroboscopic illumination and dark rearing block the sharpening of the regenerated retinotectal map in goldfish. Neuroscience 14: 535–546CrossRefGoogle Scholar
  62. Schmidt JT, Edwards DL, Steurmer CAO (1983): The reestablishment of synaptic transmission by regenerating optic axons in goldfish: Time course and effects of blocking activity by intraocular injection of tetrodotoxin. Brain Res 269: 15–27CrossRefGoogle Scholar
  63. Schmidt JT, Turcotte JC, Buzzard M, Tieman DG (1988): Staining of regenerated optic arbors in goldfish tectum: Progressive changes in immature arbors and a comparison of mature regenerated arbors with normal arbors. J Comp Neurol 269: 565–591CrossRefGoogle Scholar
  64. Schneider GE, Rava L, Sachs GM, Jhaveri S (1981): Widespread branching of retinotectal axons: Transient in normal development and anomalous in adults with neonatal lesions. Neurosci Abstr 7: 732Google Scholar
  65. Shapira R, Silberberg SD, Ginsberg S, Rahaminoff R (1987): Activation of protein kinase C augments evoked transmitter release. Nature 325: 58–60CrossRefGoogle Scholar
  66. Shatz CJ (1990): Competitive interactions between retinal ganglion cells during prenatal development. J Neurobiol 21: 197–211CrossRefGoogle Scholar
  67. Shearman MS, Naor Z, Sekiguchi A, Kishimoto A, Nishizuka (1989): Selective activation of the gamma subspecies of protein kinase C from bovine cerebellum by arachidonic acid and its lipoxygenase metabolities. FEBS Lett. 243: 177–182CrossRefGoogle Scholar
  68. Simon DK, O’Leary DDM (1990): Limited topographic specificity in the targeting and branching of mammalian retinal axons. Dev Biol 137: 125–134CrossRefGoogle Scholar
  69. Sperry RW (1963): Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc Natl Acad Sci USA 50: 703–709CrossRefGoogle Scholar
  70. Stryker MP, Harris WA (1986): Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. J Neurosci 6: 2117–2133Google Scholar
  71. Stryker MP, Strickland SL (1984): Physiological segregation of ocular dominance columns depends upon the pattern of afferent electrical activity. Invest Ophthalmol Vis Sci (Suppl) 25: 278Google Scholar
  72. Stuermer CAO (1988a): Trajectories of regenerating retinal axons in the goldfish tectum: II. Exploratory branches and growth cones on axons at early regeneration stages. J Comp Neurol 267: 69–91CrossRefGoogle Scholar
  73. Stuermer CAO (1988b): Retinotopic organization of the developing retinotectal projection in the zebrafish embryo. J Neurosci 8: 4513–4530Google Scholar
  74. Stuermer CAO (1990): Development of the retinotectal projection in zebrafish embryos under TTX-induced neural-impulse blockade. J Neurosci 10: 3615–3626Google Scholar
  75. Stuermer CAO, Easter SS (1984): A comparison of the normal and regenerated retinotectal pathways of goldfish. J Comp Neurol 223: 57–76CrossRefGoogle Scholar
  76. Stuermer CAO, Raymond PA (1989): Developing retinotectal projection in larval goldfish. J Comp Neurol 281: 630–640CrossRefGoogle Scholar
  77. Sur M, Humphrey AL, Sherman SM (1982): Monocular deprivation affects X- and Y-cell retinogeniculate terminations in cats. Nature 300: 183–185CrossRefGoogle Scholar
  78. Tsumoto T, Kimura F, Nishigori A (1990): A role for NMDA receptors and Ca++ influx in synaptic plasticity in the developing visual cortex. In: Excitatory Amino Acids and Neuronal Plasticity, Ben-Ari Y, ed. New York: Plenum PressGoogle Scholar
  79. Walter J, Henke-Fahle S, Bonhoeffer F (1987): Avoidance of posterior tectal membranes by temporal retinal axons. Development 101: 909–913Google Scholar
  80. Wiesel TN (1982): Postnatal development of the visual cortex and the influence of environment. Nature 299: 583–591CrossRefGoogle Scholar
  81. Williams JH, Bliss TVP (1988): Induction but not maintenance of calcium-induced long term potentiation in dentate gyrus and area CA 1 of the hippocampal slice is blocked by nordihydroguaiaretic acid. Neurosci Lett 88: 81–85CrossRefGoogle Scholar
  82. Williams JH, Errington ML, Lynch MA, Bliss TVP (1989): Arachidonic acid induces a long-term activity-dependent enhancement of synaptic transmission in hippocampus. Nature 341:139–742Google Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • John T. Schmidt

There are no affiliations available

Personalised recommendations