Cellular and Molecular Neurobiology

, Volume 18, Issue 5, pp 461–475 | Cite as

The Relationship Between Adhesion Molecules and Neuronal Plasticity

  • Keith B. Hoffman


1. It is presently widely assumed that structural reorganization of synaptic architectures subserves the functional gains that define certain neuronal plasticities.

2. While target molecules thought to participate in such morphological dynamics are not well defined, growing evidence suggests a pivotal role for cell adhesion molecules.

3. Herein, brief discussions are presented on (i) the history of how adhesion molecules became implicated in plasticity and memory processes, (ii) the general biology of some of the major classes of such molecules, and (iii) the future of the adhesion molecule/plasticity relationship.

neural cell adhesion NCAM L1 integrins synaptic plasticity LTP memory history 


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  1. Albelda, S. M., and Buck, C. A. (1990). Integrins and other cell adhesion molecules. FASEB J. 4:2868–2880.PubMedGoogle Scholar
  2. Ambros-Ingerson, J., and Lynch, G. (1993). Channel gating kinetics and synaptic efficacy: A hypothesis for expression of long-term potentiation. Proc. Natl. Acad. Sci. USA 90:7903–7907.PubMedGoogle Scholar
  3. Ambros-Ingerson, J., Larson, J., Xiao, P., and Lynch, G. (1991). LTP changes the waveform of synaptic responses. Synapse 9:314–316.PubMedGoogle Scholar
  4. Ambros-Ingerson, J., Xiao, P., Larson, J., and Lynch, G. (1993). Waveform analysis suggests that LTP alters the kinetics of synaptic receptor channels. Brain Res. 620:237–244.CrossRefPubMedGoogle Scholar
  5. Arai, A., Larson, J., and Lynch, G. (1990). Anoxia reveals a vulnerable period in the development of long-term potentiation. Brain Res. 511:353–357.CrossRefPubMedGoogle Scholar
  6. Arami, S., Jucker, M., Schachner, M., and Welzl, H. (1996). The effect of continuous intraventricular infusion of L1 and NCAM antibodies on spatial learning in rats. Behav. Brain Res. 81:81–87.CrossRefPubMedGoogle Scholar
  7. Bahr, B. A., and Lynch, G. (1992). Purification of an Arg-Gly-Asp selective matrix receptor from brain synaptic plasma membranes. Biochem. J. 281:137–142.PubMedGoogle Scholar
  8. Bahr, B. A., Staubli, U., Xiao, P., Chun, D., Ji, Z., Esteban, E. T., and Lynch, G. (1997). Arg-Gly-Asp-Ser selective adhesion and the stabilization of LTP: Pharmacological studies and the characterization of a candidate matrix receptor. J. Neurosci. 17:1320–1329.PubMedGoogle Scholar
  9. Barrionuevo, G., Schottler, F., and Lynch, G. (1980). The effects of repetitive low frequency stimulation on control and “potentiated” synaptic responses in the hippocampus. Life Sci. 27:2385–2391.CrossRefPubMedGoogle Scholar
  10. Bliss, T. V. P., and Collingridge, G. L. (1993). A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361:31–39.CrossRefPubMedGoogle Scholar
  11. Bliss, T. V. P., and Lomo, T. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232:331–356.PubMedGoogle Scholar
  12. Brackenbury, R., Thiery, J. P., Rutishauser, U., and Edelman, G. M. (1977). Adhesion among neural cells of the chick embryo. I. An immunological assay for molecules involved in cell-cell binding. J. Biol. Chem. 252:6835–6840.PubMedGoogle Scholar
  13. Bronner-Fraser, M., Wolf, J. J., and Murray, B. A. (1992). Effects of antibodies against N-cadherin and N-CAM on the cranial neural crest and neural tube. Dev. Biol. 153:291–301.CrossRefPubMedGoogle Scholar
  14. Buchs, P. A., and Muller, D. (1996). Induction of long-term potentiation is associated with major ultrastructural changes of activated synapses. Proc. Natl. Acad. Sci. USA 93:8040–8045.CrossRefPubMedGoogle Scholar
  15. Calverley, R. K. S., and Jones, D. G. (1992). Contributions of dendritic spines and perforated synapses to synaptic plasticity. Brain Res. Rev. 15:215–249.CrossRefGoogle Scholar
  16. Chang, F. L., and Greenough, W. T. (1984). Transient and enduring morphological correlates of synaptic activity and efficacy change in the rat hippocampal slice. Brain Res. 309:35–46.CrossRefPubMedGoogle Scholar
  17. Changeux, J. P., and Danchin, A. (1976). Selective stabilization of developing synapses as a mechanism for the specification of neuronal networks. Nature 264:705–712.PubMedGoogle Scholar
  18. Collingridge, G. L., Kehl, S. J., and McLennan, H. (1983). Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J. Physiol. 334:33–46.PubMedGoogle Scholar
  19. Cotman, C. W., and Nieto-Sampedro, M. (1984). Cell biology of synaptic plasticity. Science 225:1287–1294.PubMedGoogle Scholar
  20. Cremer, H., Lange, R., Christoph, A., Plomann, M., Vopper, G., Roes, J., Brown, R., Baldwin, S., Kraemer, P., Scheff, S., et al. (1994). Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367:455–459.CrossRefPubMedGoogle Scholar
  21. Cunningham, B. A., Hoffman, S.; Rutishauser, U., Hemperly, J. J., and Edelman, G. M. (1983). Molecular topography of the neural cell adhesion molecule N-CAM: surface orientation and location of sialic acid-rich and binding regions. Proc. Natl. Acad. Sci. USA 80:3116–3120.PubMedGoogle Scholar
  22. de la Rosa, E. J., Kayyem, J. F., Roman, J. M., Stierhof, Y. D., Dreyer, W. J., and Schwarz, U. (1990). Topologically restricted appearance in the developing chick retinotectal system of Bravo, a neural surface protein: experimental modulation by environmental cues. J. Cell Biol. 11:3087–3096.CrossRefGoogle Scholar
  23. Desmond, N. L., and Levy, W. B. (1986a). Changes in the numerical density of synaptic contacts with long-term potentiation in the hippocampal dentate gyrus. J. Comp. Neurol. 253:466–475.PubMedGoogle Scholar
  24. Desmond, N. L., and Levy, W. B. (1986b). Changes in the postsynaptic density with long-term potentiation in the dentate gyrus. J. Comp. Neurol. 253:476–482.PubMedGoogle Scholar
  25. Desmond, N. L., and Levy, W. B. (1990). Morphological correlates of long-term potentiation imply the modification of existing synapses, not synaptogenesis, in the hippocampal dentate gyrus. Synapse 5:139–143.PubMedGoogle Scholar
  26. Doherty, P., and Walsh, F. S. (1992). Cell adhesion molecules, second messengers and axonal growth. Curr. Opin. Neurobiol. 2:595–601.CrossRefPubMedGoogle Scholar
  27. Doherty, P., Cohen, J., and Walsh, F. S. (1990). Neurite outgrowth in response to transfected N-CAM changes during development and is modulated by polysialic acid. Neuron 5:209–219.CrossRefPubMedGoogle Scholar
  28. Doherty, P., Ashton, S. V., Moore, S. E., and Walsh, F. S. (1991). Morphoregulatory activities of NCAM and N-cadherin can be accounted for by G protein-dependent activation of L-and N-type neuronal Ca2+ channels. Cell 67:21–33.CrossRefPubMedGoogle Scholar
  29. Doherty, P., Fazeli, M. S., and Walsh, F. S. (1995). The neural cell adhesion molecule and synaptic plasticity. J. Neurobiol. 26:437–446.PubMedGoogle Scholar
  30. Doyle, E., Nolan, P. M., Bell, B., and Regan, C. M. (1992a). Intraventricular infusions of anti-neural cell adhesion molecules in a discrete posttraining period impair consolidation of a passive avoidance response in the rat. J. Neurochem. 59:1570–1573.PubMedGoogle Scholar
  31. Doyle, E., Nolan, P. M., Bell, R., and Regan, C. M. (1992b). Hippocampal NCAM180 transiently increases sialyation during the acquisition and consolidation of a passive avoidance response in the adult rat. J. Neurosci. Res. 31:513–523.PubMedGoogle Scholar
  32. Edelman, G. M., and Crossin, K. L. (1991). Cell adhesion molecules: implications for a molecular histology. Annu. Rev. Biochem. 60:155–190.CrossRefPubMedGoogle Scholar
  33. Edwards, F. A. (1995). Anatomy and electrophysiology of fast central synapses lead to a structural model for long-term potentiation. Physiol. Rev. 75:759–787.PubMedGoogle Scholar
  34. Fazeli, M. S., Breen, K., Errington, M. L., and Bliss, T. V. P. (1994). Increase in extracellular NCAM and amyloid precursor protein following induction of long-term potentiation in the dentate gyrus of anaesthetized rats. Neurosci. Lett. 169:77–80.CrossRefPubMedGoogle Scholar
  35. Fields, R. D., and Itoh, K. (1996). Neural cell adhesion molecules in activity-dependent development and synaptic plasticity. TINS 19:473–483.PubMedGoogle Scholar
  36. Fischer, G., Kunemund, V., and Schachner, M. (1986). Neurite outgrowth patterns in cerebellar microexplant cultures are affected by antibodies to the cell surface glycoprotein L1. J. Neurosci. 6:605–612.PubMedGoogle Scholar
  37. Fox, G. B., O'Connell, A. W., Murphy, K. J., and Regan, C. M. (1995). Memory consolidation induces a transient and time-dependent increase in the frequency of neural cell adhesion molecule polysialylated cells in the adult rat hippocampus. J. Neurochem. 65:2796–2799.PubMedGoogle Scholar
  38. Fujii, S., Saito, K., Miyakawa, H., Ito, K., and Kato, H. (1991). Reversal of long-term potentiation (depotentiation) induced by tetanus stimulation of the input to CA1 neurons of guinea pig hippocampal slices. Brain Res. 555:112–122.CrossRefPubMedGoogle Scholar
  39. Geinisman, Y., deToledo-Morell, L., Morrell, F., Heller, R. E., Rossi, M., and Parshall, R. F. (1993). Structural synaptic correlates of long-term potentiation: Formation of axospinous synapses with multiple, completely partitioned transmission zones. Hippocampus 3:435–556.PubMedGoogle Scholar
  40. Geinisman, Y., deToledo-Morell, L., Morrell, F., Persina, I. S., and Beatty, M. A. (1996). Synapse restructuring associated with the maintenance phase of hippocampal long-term potentiation. J. Comp. Neurol. 368:413–423.PubMedGoogle Scholar
  41. Goridis, C., and Brunet, J. F. (1992). NCAM: Structural diversity, function and regulation of expression. Semin. Cell Biol. 3:189–197.PubMedGoogle Scholar
  42. Grooms, S. Y., Terracio, L., and Jones, L. S. (1993). Anatomical localization of β1 integrin-like immunoreactivity in rat brain. Exp. Neurol. 122:253–259.CrossRefPubMedGoogle Scholar
  43. Grumet, M., Hoffman, S., Chuong, C.-M., and Edelman, G. M. (1984). Polypeptide components and binding functions of neuron-glia cell adhesion molecules. Proc. Natl. Acad. Sci. USA 81:7989–7993.PubMedGoogle Scholar
  44. Grumet, M., Mauro, V., Burgoon, M. P., Edelman, G. M., and Cunningham, B. A. (1991). Structure of a new nervous system glycoprotein, Nr-CAM, and its relationship to subgroups of neural cell adhesion molecules. J. Cell Biol. 113:1399–1412.CrossRefPubMedGoogle Scholar
  45. Gustafsson, B., Asztely, F., Hanse, E., and Wigstrom, H. (1989). Onset characteristics of long-term potentiation in the guinea pig hippocampal CA1 region in vitro. Eur. J. Neurosci. 1:382–394.PubMedGoogle Scholar
  46. Hall, R. A., Kessler, M., and Lynch, G. (1992). Evidence that high-and low-affinity AMPA binding sites reflect membrane-dependent states of a single receptor. J. Neurochem. 59:1997–2004.PubMedGoogle Scholar
  47. Hall, R. A., Quan, A., Kessler, M., and Lynch, G. (1996). Ultraviolet radiation, thiol reagents, and solubilization enhance AMPA receptor binding affinity via a common mechanism. Neurochem. Res. 21:969–974.PubMedGoogle Scholar
  48. Harris, E. W., Ganong, A. H., and Cotman, C. W. (1984). Long-term potentiation in the hippocampus involves activation of N-methyl-D-aspartate receptors. Brain Res. 323:132–137.CrossRefPubMedGoogle Scholar
  49. Heidemann, S. R. (1993). A new twist on integrins and the cytoskeleton. Science 260:1080–1081.PubMedGoogle Scholar
  50. Hoffman, K. B., Kessler, M., and Lynch, G. (1997). Sialic acid residues indirectly modulate the binding properties of AMPA-type glutamate receptors. Brain Res. 753:309–314.CrossRefPubMedGoogle Scholar
  51. Hoffman, K. B., Kessler, M., Ta, J., Lam, L., and Lynch, G. (1998). Mannose-specific lectins modulate ligand binding to AMPA-type glutamate receptors. Brain Res. 795:105–111.CrossRefPubMedGoogle Scholar
  52. Hoffman, S., and Edelman, G. M. (1983). Kinetics of homophilic binding by embryonic and adult forms of the neural cell adhesion molecule. Proc. Natl. Acad. Sci. USA 80:5762–5766.PubMedGoogle Scholar
  53. Honore, T., and Nielsen, M. (1985). Complex structure of quisqualate-sensitive glutamate receptors in rat cortex. Neurosci. Lett. 54:27–32.PubMedGoogle Scholar
  54. Horstkorte, R., Schachner, M., Magyar, J. P., Vorherr, T., and Schmitz, B. (1993). The fourth immunoglobulin-like domain of NCAM contains a carbohydrate recognition domain for oligomannosidic glycans implicated in association with L1 and neurite outgrowth. J. Cell Biol. 121:1409–1421.CrossRefPubMedGoogle Scholar
  55. Hortsch, M. (1996). The L1 family of neural cell adhesion molecules: old proteins performing new tricks. Neuron 17:587–593.CrossRefPubMedGoogle Scholar
  56. Hynes, R. O. (1992). Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 69:11–25.CrossRefPubMedGoogle Scholar
  57. Itoh, K., Stevens, B., Schachner, M., and Fields, R. D. (1995). Regulated expression of the neural cell adhesion molecule L1 by specific patterns of neural impulses. Science 270:1369–1372.PubMedGoogle Scholar
  58. Izquierdo, I., and Medina, J. H. (1995). Correlation between the pharmacology of long-term potentiation and the pharmacology of memory. Neurobiol. Learn. Memory 63:19–32.CrossRefGoogle Scholar
  59. Jacque, C., Jorgensen, O. S., and Bock, E. (1974). Quantitative studies of the brain specific antigen S-100, GFA, 14-3-2, D1, D2, D3 and C1 in quaking mouse. FEBS Lett. 49:264–266.CrossRefPubMedGoogle Scholar
  60. Jacque, C. M., Jorgensen, O. S., Baumann, N. A., and Bock, E. (1976a). Brain specific antigens in the quaking mouse during ontogeny. J. Neurochem. 27:905–909.PubMedGoogle Scholar
  61. Jacque, C. M., Baumann, N. A., and Bock, E. (1976b). Quantitative studies of the brain specific antigens GFA, 14-3-2, synaptin—C1, D1, D2, D3 and D5 in Jimpy mouse. Neurosci. Lett. 3:41–44.CrossRefGoogle Scholar
  62. Jones, L. S. (1996). Integrins: Possible functions in the adult CNS. TINS 19:68–72.PubMedGoogle Scholar
  63. Jorgensen, O. S., and Bock, E. (1974). Brain specific synaptosomal membrane proteins demonstrated by crossed immunoelectrophoresis. J. Neurochem. 23:879–880.PubMedGoogle Scholar
  64. Jorgensen, O. S., and Bock, E. (1975). Synaptic plasma membrane antigen D2 measured in human cerebrospinal fluid by rocket-line immunoelectrophoresis. Determination in psychiatric and neurological patients. Scand. J. Immunol. 4:25–30.PubMedGoogle Scholar
  65. Jorgensen, O. S., Bock, E., Beck, P., and Rafaelsen, O. J. (1977). Synaptic membrane protein D2 in the cerebrospinal fluid of manic-melancholic patients. Acta. Psychiat. Scand. 56:50–56.PubMedGoogle Scholar
  66. Jorgensen, O. S. (1995). Neural cell adhesion molecule (NCAM) as a quantitative marker is synaptic remodeling. Neurochem. Res. 20:533–547.PubMedGoogle Scholar
  67. Jung, M. W., Larson, J., and Lynch, G. (1991). Evidence that changes in spine neck resistance are not responsible for expression of LTP. Synapse 7:216–220.PubMedGoogle Scholar
  68. Kadom, G., Kowitz, A., Altevogt, P., and Schachner, M. (1990). Functional cooperation between the neural cell adhesion molecules L1 and N-CAM is carbohydrate dependent. J. Cell Biol. 110:209–218.CrossRefPubMedGoogle Scholar
  69. Kayyem, J. F., Roman, J. M., de la Rosa, E. J., Schwarz, U., and Dreyer, W. J. (1992). Bravo/Nr-CAM is closely related to the cell adhesion molecules L1 and Ng-CAM and has similar heterodimer structure. J. Cell Biol. 118:1259–1270.CrossRefPubMedGoogle Scholar
  70. Kobiler, D., Fuchs, S., and Samuel, D. (1976). The effect of antisynaptosomal plasma membrane antibodies on memory. Brain Res. 115:129–138.CrossRefPubMedGoogle Scholar
  71. Koch, C., and Poggio, T. (1983a). Electrical properties of dendritic spines. TINS 6:80–83.Google Scholar
  72. Koch, C., and Poggio, T. (1983b). A theoretical analysis of electrical properties of spines. Proc. Roy. Soc. Lond. 218:455–477.Google Scholar
  73. Kolta, A., Lynch, G., and Ambros-Ingerson, J. (1998). Effects of antiracetam after LTP induction are suggestive of interactions on the kinetics of the AMPA receptor channel. Brain Res. 788:269–286.CrossRefPubMedGoogle Scholar
  74. Larson, J., and Lynch, G. (1986). Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. Science 232:985–988.PubMedGoogle Scholar
  75. Larson, J., and Lynch, G. (1988). Role of N-Methyl-D-Aspartate receptors in the induction of synaptic potentiation by burst stimulation patterned after the hippocampal theta rhythm. Brain Res. 441:111–118.CrossRefPubMedGoogle Scholar
  76. Larson, J., and Lynch, G. (1991). A test of the spine resistance hypothesis for LTP expression. Brain Res. 538:347–350.CrossRefPubMedGoogle Scholar
  77. Larson, J., Xiao, P., and Lynch, G. (1993). Reversal of LTP by theta frequency stimulation. Brain Res. 600:697–702.CrossRefGoogle Scholar
  78. Lee, K. S., Schottler, F., Oliver, M., and Lynch, G. (1980). Brief bursts of high-frequency stimulation produce two types of structural change in rat hippocampus. Neurophysiology 44:247–258.PubMedGoogle Scholar
  79. Lee, K., Oliver, M., Schottler, F., and Lynch, G. (1981). Electron microscopic studies of brain slices: The effects of high frequency stimulation on dendritic ultrastructure. In Kerkut, G., and Wheal, H. V. (eds.), Electrical Activity in Isolated Mammalian C.N.S. Preparations, Academic Press, New York, pp. 189–212.Google Scholar
  80. Linnemann, D., and Bock, E. (1989). Cell adhesion molecules in neural development. Dev. Neurosci. 11:149–173.PubMedGoogle Scholar
  81. Lomo, T. (1966). Frequency potentiation of excitatory synaptic activity in the dentate area of the hippocampal formation. Acta Physiol. Scand. 68:128.Google Scholar
  82. Luthi, A., Parent, J.-P., Figurov, D., Muller, D., and Schachner, M. (1994). Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM. Nature 372:777–779.CrossRefPubMedGoogle Scholar
  83. Luthi, A., Mohajeri, H., Schachner, M., and Laurent, J.-P. (1996). Reduction of hippocampal long-term potentiation in transgenic mice ectopically expressing the neural cell adhesion molecule L1 in astrocytes. J. Neurosci. Res. 46:1–6.CrossRefPubMedGoogle Scholar
  84. Lynch, G., Larson, J., Staubli, U., and Granger, R. (1991a). Variants of synaptic potentiation and different types of memory operations in hippocampus and related structures. In Squire, L. R., Weinberger, N. M., Lynch, G., and McGaugh, J. L. (eds.), Memory: Organization and Locus of Change, Oxford University Press, New York, pp. 330–363.Google Scholar
  85. Lynch, G., Bahr, B. A., and Vanderklish, P. W. (1991b). Induction and stabilization of long-term potentiation. In Ascher, P., Choi, D. W., and Christen, Y. (ed.), Glutamate Cell-Death and Memory, Springer-Verlag, Berlin/Heidelberg, pp. 45–60.Google Scholar
  86. Malenka, R. C. (1991). Postsynaptic factors control the duration of synaptic enhancement in area CA1 of the hippocampus. Neuron 6:53–60.CrossRefPubMedGoogle Scholar
  87. Maren, S., and Baudry, M. (1995). Properties and mechanisms of long-term synaptic plasticity in the mammalian brain: Relationships to learning and memory. Neurobiol. Learn. Memory 63:1–18.CrossRefGoogle Scholar
  88. Mayer, M. L., and Vyklicky, L., Jr. (1989). Concanavalin A selectively reduces desensitization of mammalian neuronal quisqualate receptors. Proc. Natl. Acad. Sci. USA 86:1411–1415.PubMedGoogle Scholar
  89. Mayford, M., Barzilai, A., Keller, F., Schacher, M., and Kandel, E. (1992). Modulation of an NCAM-related adhesion molecule with long-term synaptic plasticity in Aplysia. Science 256:638–644.PubMedGoogle Scholar
  90. Montgomery, A. M. P., Becker, J. C., Chi-Hung Siu, Lemmon, V. P., Cheresh, D. A., Pancook, J. D., Zhao, X., and Reisfeld, R. A. (1996). Human neural cell adhesion molecule L1 and rat homologue NILE are ligands for integrin αvβy. J. Cell Biol. 132:475–485.CrossRefPubMedGoogle Scholar
  91. Muller, D., and Lynch, G. (1988). Long-term potentiation differentially affects two components of synaptic responses in hippocampus. Proc. Natl. Acad. Sci. USA 85:9346–9350.PubMedGoogle Scholar
  92. Muller, D., Wang, C., Skibo, G., Toni, N., Cremer, H., Calaora, V., Rougon, G., and Kiss, J. Z. (1996). PSA-NCAM is required for activity-induced synaptic plasticity. Neuron 17:413–422.CrossRefPubMedGoogle Scholar
  93. Murphy, K. J., O'Connell, A. W., and Regan, C. M. (1996). Repetitive and transient increases in hippocampal neural cell adhesion molecule polysialylation state following multitrail spatial training. J. Neurochem. 67:1268–1274.PubMedGoogle Scholar
  94. O'Connell, C., O'Malley, A., and Regan, C. M. (1997). Transient, learning-induced ultrastructural change in spatially-clustered dentate granule cells of the adult rat hippocampus. Neuroscience 76:55–62.CrossRefPubMedGoogle Scholar
  95. Pavalko, F. M., Otey, C. A., Simon, K. O., and Burridge, K. (1991). Alpha-actinin: A direct link between actin and integrins. Biochem. Soc. Trans. 19:1065–1069.PubMedGoogle Scholar
  96. Persohn, E., Pollerberg, G. E., and Schachner, M. (1989). Immunoelectron-microscopic localization of the 180 kD component of the neural cell adhesion molecule N-CAM in postsynaptic membranes. Comp. Neurol. 288:92–100.Google Scholar
  97. Pollerberg, E., Burridge, K., Krebs, S., Goodman, S., and Schachner, M. (1987). The 180 kD component of the neural cell adhesion molecule N-CAM is involved in cell-cell contacts and cytoskeleton-membrane interactions. Cell Tissue Res. 250:227–236.CrossRefPubMedGoogle Scholar
  98. Rall, W. (1974). Dendritic spines, synaptic potency and neuronal plasticity. In Woody, C. D., Brown, K. A., Crow, T. J., Jr., and Knispel, J. D. (eds.), Cellular Mechanisms Subserving Changes in Neuronal Activity, University of California Press, Los Angeles, 1974, pp. 13–21.Google Scholar
  99. Rathjen, F. G., and Schachner, M. (1984). Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J. 3:1–10.PubMedGoogle Scholar
  100. Regan, C. M. (1991). Regulation of neural cell adhesion molecule sialyation state. Int. J. Biochem. 23:513–523.CrossRefPubMedGoogle Scholar
  101. Ronn, L. C. B., Bock, E. Linnemann, D., and Jahnsen, H. (1995). NCAM antibodies modulate induction of long-term potentiation in rat hippocampal CA1. Brain Res. 677:145–151.CrossRefPubMedGoogle Scholar
  102. Rosales, C., and Juliano, R. L. (1995). Signal transduction by cell adhesion receptors in leukocytes. J. Leukocyte Biol. 57:189–198.PubMedGoogle Scholar
  103. Rose, S. P. (1995). Glycoproteins and memory formation. Behav. Brain Res. 66:73–78.CrossRefPubMedGoogle Scholar
  104. Ruoslahti, E., and Pierschbacher, M. D. (1987). New perspectives in cell adhesion: RGD and integrins. Science 238:491–497.PubMedGoogle Scholar
  105. Ruppert, M., Aigner, S., Hubbe, M., Yagita, H., and Altevogt, P. (1995). The L1 adhesion molecule is a cellular ligand for VLA-5. J. Cell Biol. 131:1881–1891.CrossRefPubMedGoogle Scholar
  106. Rutishauser, U. (1992). NCAM and its polysialic acid moiety: A mechanism for pull/push regulation of cell interactions during development? Development Suppl. 99–104.Google Scholar
  107. Rutishauser, U., and Landmesser, L. (1996). Polysialic acid in the vertebrate nervous system: A promoter of plasticity in cell-cell interactions. Trends Neurosci. 19:422–427.PubMedGoogle Scholar
  108. Rutishauser, U., Theiry, J. P., Brackenbury, R., Sela B. A., and Edelman, G. M. (1976). Mechanisms of adhesion among cells from neural tissues of the chick embryo. Proc. Natl. Acad. Sci. USA 73:577–581.PubMedGoogle Scholar
  109. Rutishauser, U., Hoffman, S., and Edelman, G. M. (1982). Binding properties of a cell adhesion molecule from neural tissue. Proc. Natl. Acad. Sci. USA 79:685–689.PubMedGoogle Scholar
  110. Rutishauser, U., Acheson, A., Hall, A. K., Mann, D. M., and Sunshine, J. (1988). The neural cell adhesion molecule (NCAM) as a regulator of cell-cell interactions. Science 240:53–57.PubMedGoogle Scholar
  111. Sadoul, R., Hirn, M., Deagostini-Bazin, H., Rougon, G., and Goridis, C. (1983). Adult and embryonic mouse neural cell adhesion molecules have different binding properties. Nature 304:347–349.PubMedGoogle Scholar
  112. Salton, S. R. J., Richter-Landsberg, C., Greene, L. A., and Shelanski, M. L. (1983). Nerve growth factor-inducible large external (NILE) glycoprotein: Studies of a central and peripheral neuronal marker. J. Neurosci. 3:441–454.PubMedGoogle Scholar
  113. Scholey, A. B., Rose, S. P. R., Zamani, M. R., Bock, E., and Schachner, M. (1993). A role for the neural cell adhesion molecule in a late, consolidating phase of glycoprotein synthesis 6 hours following passive avoidance training of the young chick. Neuroscience 52:393–401.CrossRefPubMedGoogle Scholar
  114. Schuster, C. M., Davis, G. W., Fetter, R. D., and Goodman, C. S. (1996). Genetic dissection of structural and functional components of synaptic plasticity. II. Fasciclin II controls presynaptic structural plasticity. Neuron 17:655–667.CrossRefPubMedGoogle Scholar
  115. Seki, T., and Arai, Y. (1993). Distribution and possible roles of the highly polysialyated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system. Neurosci. Res. 17:265–290.CrossRefPubMedGoogle Scholar
  116. Staubli, U. (1995). Parallel properties of long-term potentiation and memory. In McGaugh, J., Weinberger, N., and Lynch, G. (eds.), Brain and Memory: Modulation and Mediation of Neuroplasticity, 1995, pp. 303–318.Google Scholar
  117. Staubli, U., and Lynch, G. (1987). Stable hippocampal long-term potentiation elicited by “theta” pattern stimulation. Brain Res. 435:227–234.CrossRefPubMedGoogle Scholar
  118. Staubli, U., Vanderklish, P., and Lynch, G. (1990). An inhibitor of integrin receptors blocks long-term potentiation. Behav. Neural Biol. 53:1–5.PubMedGoogle Scholar
  119. Staubli, U., Rogers, G., and Lynch, G. (1994). Facilitation of glutamate receptors enhances memory. Proc. Natl. Acad. Sci. USA 91:777–781.PubMedGoogle Scholar
  120. Thiery, J.-P., Brackenbury, R., Rutishauser, U., and Edelman, G. M. (1977). Adhesion among neural cells of the chick embryo. J. Biol. Chem. 252:6841–6845.PubMedGoogle Scholar
  121. Thio, L. L., Clifford, D. B., and Zorumski, C. F. (1992a). Blockade of ionotropic quisqualate receptor desensitization by wheat germ agglutinin in cultured postnatal rat hippocampal neurons. J. Neurophys. 68:1917–1929.Google Scholar
  122. Thio, L. L., Clark, G. D., Clifford, D. B., and Zorumski, C. F. (1992b). Wheat germ agglutinin enhances EPSCs in cultured postnatal rat hippocampal neurons by blocking ionotropic quisqualate receptor desensitization. J. Neurophys. 68:1930–1938.Google Scholar
  123. Vyklicky, L., Jr., Patneau, D. K., and Mayer, M. L. (1991). Modulation of excitatory synaptic transmission by drugs that reduce desensitization at AMPA/kainate receptors. Neuron 7:971–984.CrossRefPubMedGoogle Scholar
  124. Wang, N., Butler, J. P., and Ingber, D. E. (1993). Mechanotransduction across the cell surface and through the cytoskeleton. Science 260:1124–1127.PubMedGoogle Scholar
  125. Wenzel, J., Kammerer, E., Kirsche, W., Matthies, H., and Wenzel, M. (1980). Electron microscopic and morphometric studies on synaptic plasticity in the hippocampus of the rat following conditioning. J. Hirnforschung 21:647–654.Google Scholar
  126. Xiao, P., Bahr, B. A., Staubli, U., Vanderklish, P. W., and Lynch, G. (1991). Evidence that matrix recognition contributes to stabilization but not induction of LTP. Neuroreport 2:461–464.PubMedGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1998

Authors and Affiliations

  • Keith B. Hoffman
    • 1
  1. 1.Ancile PharmaceuticalsLa Jolla

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