What can the Long-Term Potentiation Procedure Tell us about the Neural Mechanisms of Learning and Memory?

  • Serge Laroche
Part of the Advances in Behavioral Biology book series (ABBI, volume 28)


The theoretical background of most physiological models of learning and memory rests on the idea that persistent synaptic modifications in neural networks are the basis of information storage. The neurophysiological approaches to the study of learning and memory have thus long been concerned with such guestions as how and under what circumstances do synaptic changes occur in the brain, as well as what could be the nature of the change itself.


Dendritic Spine Classical Conditioning Hippocampal Slice Population Spike Perforant Path 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Andersen, P., Bliss, T.V.P., and Skrede, K.K., 1971, Unit analysis of hippocampal population spikes, Exp. Brain Res., 13:208.Google Scholar
  2. Andersen, P., Sundberg, S.H., Sveen, O., and Wigstrom, H., 1977, Specific long-lasting potentiation of synaptic transmission in hippocampal slices, Nature, 266:736.CrossRefGoogle Scholar
  3. Bär, P.R., Schotman, P., Gispen, W.H., Tielen, A.M., and Lopes da Silva, F.H., 1980, Changes in synaptic membrane phosphorylation after tetanic stimulation in the dentate area of the rat hippocampal slice, Brain Res., 198:478.CrossRefGoogle Scholar
  4. Barnes, C.A., 1979, Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat, J. Comp. Physiol. Psychol., 93:74.CrossRefGoogle Scholar
  5. Barnes, C.A., and McNaughton, B.L., 1980, Spatial memory and hippocampal synaptic plasticity in senescent and middle-aged rats, in: “The Psychobiology of Aging: Problems and Perspectives”, D. Stein, ed., Elsevier, Amsterdam.Google Scholar
  6. Baudry, M., Oliver, M., Creager, R., Wieraszko, A., and Lynch, C., 1980, Increase in glutamate receptors following repetitive electrical stimulation in hippocampal slices, Life Sci., 27:325.CrossRefGoogle Scholar
  7. Berger, T.W., Alger, B., and Thompson, R.F., 1976, Neuronal substrate of classical conditioning in the hippocampus, Science, 192:483.CrossRefGoogle Scholar
  8. Berger, T.W., 1984, Long-term potentiation of hippocampal synaptic transmission affects rate of behavioral learning, Science, 224:627.CrossRefGoogle Scholar
  9. Bliss, T.V.P., and Dolphin, A.C., 1982, What is the mechanism of long-term potentiation in the hippocampus ?, Trends Neurosci., 5:289.CrossRefGoogle Scholar
  10. Bliss, T.V.P., and Gardner-Medwin, A.R., 1973, Long-lasting potentiation of synaptic transmission in the dentate area of the unanaesthetized rabbit following stimulation of the perforant path, J. Physiol. (Lond.), 232:357.Google Scholar
  11. Bliss, T.V.P., and Lømo, T., 1973, 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.Google Scholar
  12. Bloch, V., 1970, Facts and hypotheses concerning memory consolidation processes, Brain Res., 24:561.CrossRefGoogle Scholar
  13. Bloch, V., Denti, A., and Schmaltz, C., 1966, Effets de la stimulation réticulaire sur la phase de consolidation de la trace mnésique, J. Physiol. (Paris), 58:469.Google Scholar
  14. Bloch, V., Deweer, B., and Hennevin, E., 1970, Suppression de l’amnésie rétrograde et consolidation d’un apprentissage à essai unique par stimulation réticulaire, Physiol. Behav., 5:1235.CrossRefGoogle Scholar
  15. Bloch, V., and Laroche, S., 1981, Conditioning of hippocampal cells: its acceleration and long-term facilitation by post-trial reticular stimulation, Behav. Brain Res., 3:23.CrossRefGoogle Scholar
  16. Bloch, V., and Laroche, S., 1984, Facts and hypotheses related to the search of the engram, in: “Neurobiology of Learning and Memory”, G. Lynch, J.L. McGaugh, and N.M. Weinberger, eds., Guilford, New York.Google Scholar
  17. Bloch, V., and Laroche, S., 1985, Enhancement of long-term potentiation in the rat dentate gyrus by post-trial stimulation of the reticular formation, J. Physiol. (Lond.), in press.Google Scholar
  18. Bottjer, S.W., and Arnold, A.P., 1984, Hormones and structural plasticity in the adult brain, Trends Neurosci., 7:168.CrossRefGoogle Scholar
  19. Brown, T.H., and McAfee, D.A., 1982, Long-term synaptic potentiation in the superior cervical ganglion, Science, 215:1411.CrossRefGoogle Scholar
  20. Browning, M., Dunwiddie, T., Bennett, W.F., Gispen, W.H., and Lynch, G., 1979, Synaptic phosphoproteins: specific changes after repetitive stimulation of the hippocampal slice, Science, 203:60.CrossRefGoogle Scholar
  21. Buzsáki, G., 1984, Long-term changes of hippocampal sharp-waves following high frequency afferent activation, Brain Res., 300:179.CrossRefGoogle Scholar
  22. Buzsâki, G., Grastyán, E., Czopf, J., Kellényi, L., and Prohaska, O., 1981, Changes in neuronal transmission in the rat hippocampus during behavior, Brain Res., 225:235.CrossRefGoogle Scholar
  23. Chang, F.F., and Greenough, W.T., 1982, Lateralized effects of monocular training on dendritic branching in adult split-brain rats, Brain Res., 232:283.CrossRefGoogle Scholar
  24. Chepkova, A.N., and Skrebitsky, V.G., 1982, Effects of some adrenergic drugs and neuropeptides on long-term potentiation in hippocampal slices, in: “Neuronal Plasticity and Memory Formation”, IBRO Monograph Series, Vol. 9, C. Ajmone Marsan, and H. Matthies, eds., Raven, New York.Google Scholar
  25. Cotman, C.W., and Neito-Sampedro, M., 1982, Brain function, synapse renewal, and plasticity, Ann. Rev. Psychol., 33:371.CrossRefGoogle Scholar
  26. de Jonge, M.C., and Racine, R.J., 1983, Effects of repetitive induction of long-term potentiation in the dentate gyrus of the rat, Soc. Neurosci. Abstr., 9:102.Google Scholar
  27. Desmond, N.L., and Levy, W.B., 1983, Synaptic correlates of associative potentiation/depression: an ultrastructural study in the hippocampus, Brain Res., 265:21.CrossRefGoogle Scholar
  28. Deweer, B., 1976, Selective facilitative effect of post-trial reticular stimulation in discriminative learning in the rat, Behav. Proc., 1:243.CrossRefGoogle Scholar
  29. Dolphin, A.C., Errington, M.L., and Bliss, T.V.P., 1982, Long-term potentiation of the perforant path in vivo is associated with increased glutamate release, Nature, 297:496.CrossRefGoogle Scholar
  30. Douglas, R.M., 1977, Long-lasting synaptic potentiation in the rat dentate gyrus following brief high-frequency stimulation, Brain Res., 126:361.CrossRefGoogle Scholar
  31. Douglas, R.M., and Goddard, G.V., 1975, Long-term potentiation of the perforant path-granule cell synapse in the rat hippocampus, Brain Res., 86:205.CrossRefGoogle Scholar
  32. Dudek, F.E., Andrew, R.D., MacVicar, B.A., Snow, R.W., and Taylor, C.P., 1983, Recent evidence for and possible significance of gap junctions and electronic synapses in the mammalian brain, in: “Basic Mechanisms of Neuronal Hyperexcitability”, Alan R. Liss, New York.Google Scholar
  33. Duffy, C., Teyler, T.J., and Shashoua, V.E., 1981, Long-term potentiation in the hippocampal slice: evidence for stimulated secretion of newly synthetized proteins, Science, 212:1148.CrossRefGoogle Scholar
  34. Eccles, J.C., 1983, Calcium in long-term potentiation as a model for memory, Neurosci., 10:1071.CrossRefGoogle Scholar
  35. Fessard, A., and Szabo, T.H., 1961, La facilitation de post-activation omme facteur de plasticité dans l’établissement des liaisons emporaires, in: “Brain Mechanisms and Learning”, A. Fessard, R.W. Gerard, J. Konorski, and J.F. Delafresnaye, eds., Blackwell, Oxford.Google Scholar
  36. Fifkova, E., Anderson, C.L., Young, S.J, and Van Harreveld, A., 1982, Effect of anisomycin on stimulation-induced changes in dendritic spines of the dentate granule cells, J. Neurocytol., 11:183.CrossRefGoogle Scholar
  37. Fifkova, E., and Van Harreveld, A., 1978, Changes in dendritic spines of the dentate molecular layer during conditioning, Soc. Neurosci. Abstr., 4:257.Google Scholar
  38. Gerren, R.A., and Weinberger, N.M., 1983, Long term potentiation in the magnocellular medial geniculate nucleus of the anesthetized cat, Brain Res., 265:138.CrossRefGoogle Scholar
  39. Goddard, G.V., 1981, Progress on the physiological bases of memory, in: “Brain and Behaviour”, Advances in Physiological Sciences, Vol. 17, G. Adam, I. Meszaros, and E.I. Banyai, eds., Pergamon, Akademiai Kiado, Budapest.Google Scholar
  40. Gold, P.E., Delanoy, R.L., and Merrin, J., 1984, Modulation of long-term potentiation by peripherally administered amphetamine and epinephrine, Brain Res., 305:103.CrossRefGoogle Scholar
  41. Greenough, W.T., 1984, Structural correlates of information storage in the mammalian brain: a review and hypothesis, Trends Neurosci., 7:229.CrossRefGoogle Scholar
  42. Hebb, D.O., 1949, “The Organization of Behavior”, Wiley, New York.Google Scholar
  43. Hesse, G.W., and Teyler, T.J., 1976, Reversible loss of hippocampal long-term potentiation following electroconvulsive seizures, Nature, 264:562.CrossRefGoogle Scholar
  44. Horn, G., 1981, Neural mechanisms of learning: an analysis of imprinting in the domestic chick, Proc. R. Soc. Lond., 213:101.CrossRefGoogle Scholar
  45. Jaffard, R., and Jeantet, Y., 1981, Posttraining changes in excitability of the commissural path-CAl pyramidal cell synapses in the hippocampus of mice, Brain Res., 220:167.CrossRefGoogle Scholar
  46. John, E.R., 1972, Switchboard versus statistical theories of learning and memory, Science, 177:850.CrossRefGoogle Scholar
  47. Komatsu, Y., Toyama, K., Maeda, J., and Sakaguchi, H., 1981, Long-term potentiation investigated in a slice preparation of striate cortex of young kittens, Neurosci. Lett., 26:269.CrossRefGoogle Scholar
  48. Kosaka, T., 1983, Axon initial segments of the granule cell in the rat dentate gyrus: synaptic contacts on bundles of axon initial segments, Brain Res., 274:129.CrossRefGoogle Scholar
  49. Laroche, S., Bergis, O.-E., and Bloch, V., 1983, Posttrial reticular facilitation of dentate multiunit conditioning is followed by an increased long-term potentiation, Soc. Neurosci. Abstr., 9:645.Google Scholar
  50. Laroche, S., and Bloch, V., 1982, Conditioning of hippocampal cells and long-term potentiation: an approach to mechanisms of post-trial memory facilitation, in: “Neuronal Plasticity and Memory Formation”, IBRO Monograph Series, Vol. 9, C. Ajmone Marsan, and H. Matthies, eds., Raven, New York.Google Scholar
  51. Laroche, S., Falcou, R., and Bloch, V., 1983, Post-trial reticular facilitation of associative changes in multiunit activity: comparison between dentate gyrus and entorhinal cortex, Behav. Brain Res., 9:381.CrossRefGoogle Scholar
  52. Lee, K.S., 1982, Sustained enhancement of evoked potentials following brief, high-frequency stimulation of the cerebral cortex in vitro, Brain Res., 239:617.CrossRefGoogle Scholar
  53. Lee, K.S., 1983, Cooperativity among afferents for the induction of long-term potentiation in the CA1 region of the hippocampus, J. Neurosci., 3:1369.Google Scholar
  54. 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, J. Neurophysiol., 44:247.Google Scholar
  55. Levy, W.B., and Steward, O., 1979, Synapses as associative memory elements in the hippocampal formation, Brain Res., 175:233.CrossRefGoogle Scholar
  56. Lewis, D., Teyler, T., and Shashoua, V., 1981, Development of long-term potentiation in the in vitro goldfish optic tectum, Soc. Neurosci. Abstr.,7:66.Google Scholar
  57. Lewis, D.D., 1979, Psychobiology of active and inactive memory, Psychol. Bull., 86:1054.CrossRefGoogle Scholar
  58. Lømo, T., 1971, Patterns of activation in a monosynaptic cortical pathway: the perforant path input to the dentate area of the hippocampal formation, Exp. Brain Res., 12:18.Google Scholar
  59. McNaughton, B.L., and Barnes, C.A., 1977, Physiological identification and analysis of dentate granule cell responses to stimulation of the medial and lateral perforant pathway in the rat, J. Comp. Neurol., 175:439.CrossRefGoogle Scholar
  60. McNaughton, B.L., Douglas, R.M., and Goddard, G.V., 1978, Synaptic enhancement in fascia dentata: cooperativity among coactive afferents, Brain Res., 157:277.CrossRefGoogle Scholar
  61. Misgeld, U., Sarvey, J.M., and Klee, M.R., 1979, Heterosynaptic postactivation potentiation in hippocampal CA3 neurons: long-term changes in the postsynaptic potentials, Exp. Brain Res., 37:217.CrossRefGoogle Scholar
  62. Olds, J., Disterhoft, J.F., Segal, M., Kornblith, C.L., and Hirsh, R., 1972, Learning centers of rat brain mapped by measuring latencies of conditioned unit responses, J. Neurophysiol., 35:202.Google Scholar
  63. Ott, T., Ruthrich, H., Reymann, K., Lindenau, L., and Matthies, H., 1982, Direct evidence for the participation of changes in synaptic efficacy in the development of behavioral plasticity, in: “Neuronal Plasticity and Memory Formation”, IBRO Monograph Series, Vol. 9, C. Ajmone Marsan, and H. Matthies, eds., Raven, New York.Google Scholar
  64. Racine, R.J., Milgram, N.W., and Hafner, S., 1983, Long-term potentiation phenomena in the rat limbic forebrain. Brain Res., 260:217.CrossRefGoogle Scholar
  65. Ranck, J.B., 1973, Studies in single neurons in dorsal hippocampal formation and septum in unrestrained rats, Exp. Neurol., 41:461.CrossRefGoogle Scholar
  66. Reymann, K.G., and Ott, T., 1983, Footshock-induced modification of a monosynaptic evoked potential in the hippocampus, Physiol. Behav., 31:615.Google Scholar
  67. Richardson, T.L., Turner, R.W., and Miller, J. J., 1984, Extracellular fields influence transmembrane potentials and synchronization of hippocampal neuronal activity, Brain Res., 294:255.CrossRefGoogle Scholar
  68. Roney, K.J., Scheibel, A.B., and Shaw, G.L., 1979, Dendritic bundles: survey of anatomical experiments and physiological theories, Brain Res. Rev., 1:225.CrossRefGoogle Scholar
  69. Rosenzweig, M.R., and Bennett, E.L., 1976, Enriched environments: facts, factors and fantasies, in: “Knowing, Thinking and Believing”, J.L. McGaugh, and L. Petrinovich, eds., Plenum, New York.Google Scholar
  70. Rüthrich, H., Matthies, H., and Ott, T., 1982, Long-term changes in synaptic excitability of hippocampal cell populations as a result of training, in: “Neuronal Plasticity and Memory Formation”, IBRO Monograph Series, Vol. 9, C. Ajmone Marsan, and H. Matthies, eds., Raven, New York.Google Scholar
  71. Segal, M., 1977, Excitability changes in rat hippocampus during conditioning, Exp. Neurol., 55:67.CrossRefGoogle Scholar
  72. Serfling, R., and Schuster, T., 1983, Light-microscopic investigations on the problem of a dendritic bundling in the rat hippocampus, J. Hirnforsch., 24:1.Google Scholar
  73. Shaw, G.L., 1978, Space-time correlations of neuronal firing related to memory storage capacity, Brain Res. Bull., 3:107.CrossRefGoogle Scholar
  74. Shaw, G.L., Harth, E., and Scheibel, A.B., 1982, Cooperatiyity in brain function: assemblies of approximately 30 neurons, Exp. Neurol., 77:324.CrossRefGoogle Scholar
  75. Spear, N.E., 1978, “The Processing of Memories: Forgetting and Retention”, Erlbaum, Hillsdale.Google Scholar
  76. Swanson, L.W., Teyler, T.J., and Thompson, R.F., 1982, Hippocampal long-term potentiation: mechanisms and implications for memory, Neurosci. Res. Prog. Bull., 20:613.Google Scholar
  77. Teyler, T.J., and Discenna, P., 1984, Long-term potentiation as a candidate mnemonic device, Brain Res. Rev., 7:15.CrossRefGoogle Scholar
  78. Thompson, R.F., 1982, Increases in the monosynaptic population spike response of dentate gyrus during classical conditioning, Neurosci. Res. Prog. Bull., 20:693.Google Scholar
  79. Thompson, R.F., Berger, T.W., and Madden IV, J., 1983, Cellular processes of learning and memory in the mammalian CNS, Ann. Rev. Neurosci., 6:447.CrossRefGoogle Scholar
  80. Thompson, R.F., Manounas, L.A., Lynch, G., and Baudry, M., 1983, Increased glutamate receptor binding in hippocampus following classical conditioning of the rabbit eyelid response, Soc. Neurosci. Abstr., 9:830.Google Scholar
  81. Tsukahara, N., 1981, Synaptic plasticity in the mammalian central nervous system, Ann. Rev. Neurosci., 4:351.CrossRefGoogle Scholar
  82. Underwood, B.J., 1969, “Attributes of memory”, Psychol. Rev., 76:559–573.CrossRefGoogle Scholar
  83. Van Harreveld, A., and Fifkova, E., 1975, Swelling of dendritic spines in the fascia dentata after stimulation of the perforant fibers as a mechanism of post-tetanic potentiation, Exp. Neurol., 49:736.CrossRefGoogle Scholar
  84. Voronin, L.L., 1983, Long-term potentiation in the hippocampus, Neurosci., 10:1051.CrossRefGoogle Scholar
  85. Vrensen, G., and Cardozo, J.N., 1981, Changes in size and shape of synaptic connections after visual training: an ultrastructural approach of synaptic plasticity, Brain Res., 218:79.CrossRefGoogle Scholar
  86. Weinberger, N.M., 1980, Neurophysiological studies of learning in association with the pupillary dilatation conditioned reflex, in: “Neural Mechanisms of Goal-Directed Behavior and Learning”, R.F. Thompson, L.H. Hicks, and V.B. Shvyrkov, eds., Academic, New York.Google Scholar
  87. Wenzel, S., 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. Hirnforsch., 21:647.Google Scholar
  88. Wilson, D.A., and Racine, R.J., 1981, Transient and long-term potentiation in the neocortex of the rat, Soc. Neurosci. Abstr., 7:69.Google Scholar
  89. Yamamoto, C., and Chujo, T., 1978, Long-term potentiation in thin hippocampal section studied by intracellular and extracellular recordings, Exp. Neurol., 58:242.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1985

Authors and Affiliations

  • Serge Laroche
    • 1
  1. 1.Département de Psychophysiologie, LPN 2C.N.R.SGif-sur-YvetteFrance

Personalised recommendations