β-Adrenergic Mechanisms in Long-Term Potentiation and Norepinephrine-Induced Long-Lasting Potentiation

  • John M. Sarvey


A brief train of high-frequency, repetitive electrical stimulation to the perforant path results in long-term potentiation (LTP) of the response to low-frequency stimulation of that pathway. In the dentate gyrus, LTP is manifested as an increased amplitude of the extracellularly recorded synchronous action potentials (population spike) of granule cells, a decrease in the latency of the population spike, and a steepening of the initial slope of the extracellularly recorded excitatory postsynaptic potential (EPSP) in response to stimulation of the perforant path (Bliss and Lømo, 1973; Bliss and Gardner-Medwin, 1973). Long-term potentiation has also been demonstrated in hippocampal fields CA1 and CA3 (Schwartzkroin and Wester, 1975; Alger and Teyler, 1976). In intracellular recordings, LTP is manifested primarily as an increased EPSP amplitude (Andersen et al., 1977, 1980; Yamamoto and Chujo, 1978; Misgeld et al., 1979; Wigström and Gustafsson, 1985; Barrionuevo et al., 1986).


Dentate Gyrus Locus Coeruleus Hippocampal Slice Population Spike Repetitive Stimulation 
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. Abrams, T. W., 1985, Activity-dependent presynaptic facilitation: An associative mechanism in Aplysia, Cell. Mol. Neurobiol. 5: 123–145.PubMedCrossRefGoogle Scholar
  2. Alger, B. E., and Teyler, T. J., 1976, Long-term and short-term plasticity in the CA1, CA3 and dentate regions of the rat hippocampal slice, Brain Res. 110: 463–480.PubMedCrossRefGoogle Scholar
  3. Andersen, P., Sundberg, S. H., Sveen, O., and Wigström, H., 1977, Specific long-lasting potentiation of synaptic transmission in hippocampal slices, Nature 266: 736–737.PubMedCrossRefGoogle Scholar
  4. Andersen, P., Sundberg, S. H., Sveen, O., Swann, J. W., and Wigström, H., 1980, Possible mechanism for long-term potentiation of synaptic transmission in hippocampal slices from guinea-pig, J. Physiol. (Lond.) 302: 463–482.Google Scholar
  5. Ashe, J. H., 1984, A possible enabling and enhancing function for catecholamines in neuronal plasticity, in: Memory Systems of the Brain ( N. M. Weinberger, J. L. McGaugh, and G. Lynch, eds.), Guilford, New York, pp. 107–119.Google Scholar
  6. 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: 478–484.PubMedCrossRefGoogle Scholar
  7. Barrionuevo, G., Kelso, S. R., Johnston, D., and Brown, T. H., 1986, Conductance mechanism responsible for long-term potentiation in monosynaptic and isolated excitatory synaptic inputs to hippocampus, J. Neurophysiol. 55: 540–550.PubMedGoogle Scholar
  8. Bliss, T. V. P., and Gardner-Medwin, A. R., 1973, Long-lasting potentiation of synaptic transmission in the dentate area of unanaesthetized rabbit following stimulation of the perforant path, J. Physiol. (Lond.) 232: 357–374.Google Scholar
  9. 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: 331–356.Google Scholar
  10. Bliss, T. V. P., Goddard, G. V., and Riives, M., 1983, Reduction of long-term potentiation in the dentate gyms of the rat following selective depletion of monoamines, J. Physiol. (Lond.) 334: 475–491.Google Scholar
  11. Browning, M., Bennett, W. F., Kelly, P., and Lynch, G., 1981, Evidence that the 40,000 M r phosphoprotein influenced by high frequency synaptic stimulation is the alpha subunit of pyruvate dehydrogenase, Brain Res. 218: 255–266.PubMedCrossRefGoogle Scholar
  12. Collingridge, G. L., 1985, Long term potentiation in the hippocampus: Mechanisms of initiation and modulation by neurotransmitters, Trends Pharmacol. Sci. 6: 407–411.CrossRefGoogle Scholar
  13. 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. (Lond.) 334: 33–46.Google Scholar
  14. Dahl, D., and Winson, J., 1985, Action of norepinephrine in the dentate gyrus. I. Stimulation of the locus coeruleus, Exp. Brain Res. 59: 491–496.PubMedCrossRefGoogle Scholar
  15. Dingledine, R., 1983, N-Methyl aspartate activates voltage-dependent calcium conductance in rat hippocampal pyramidal cells, J. Physiol. (Lond.) 343: 385–405.Google Scholar
  16. Dingledine, R., 1986, NMDA receptors: What do they do? Trends Neurosci. 9: 47–49.CrossRefGoogle Scholar
  17. Duffy, C., Teyler, T. J., and Shashoua, V. E., 1981, Long-term potentiation in the hippocampal slice: Evidence for stimulated secretion of newly synthesized proteins, Science 212: 1148–1151.PubMedCrossRefGoogle Scholar
  18. Dunwiddie, T. V., and Lynch, G., 1979, The relationship between extracellular calcium concentrations and the induction of hippocampal long-term potentiation, Brain Res. 169: 103–110.PubMedCrossRefGoogle Scholar
  19. Dunwiddie, T., Madison, D., and Lynch, G., 1978, Synaptic transmission is required for initiation of longterm potentiation, Brain Res. 150: 413–417.PubMedCrossRefGoogle Scholar
  20. Eiden, L. E., Girand, P., Affolter, H. U., Herbert, E., and Hotchkiss, A. J., 1984, Alternative modes of enkephalin biosynthesis regulation by reserpine and cyclic AMP in cultured chromaffin cells, Proc. Natl. Acad. Sci. U.S.A. 81: 3949–3953.PubMedCrossRefGoogle Scholar
  21. Fifkova, E., and Van Harreveld, A., 1977, Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area, J. Neurocytol. 6: 211–230.PubMedCrossRefGoogle Scholar
  22. 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: 183–210.PubMedCrossRefGoogle Scholar
  23. Foster, A. C., and Fagg, G. E., 1984, Acidic amino acid binding sites in mammalian neuronal membranes: Their characteristics and relationship to synaptic receptors, Brain Res. Rev. 7: 103–164.CrossRefGoogle Scholar
  24. Gribkoff, V. K., and Ashe, J. H., 1984, Modulation by dopamine of population responses and cell membrane properties of hippocampal CAI neurons in vitro, Brain Res. 292: 327–338.PubMedCrossRefGoogle Scholar
  25. Harley, C. W., and Milway, J. S., 1986, Glutamate ejection in the locus coeruleus enhances the perforant path-evoked population spike in the dentate gyrus, Exp. Brain Res. 63: 143–150.PubMedCrossRefGoogle Scholar
  26. Harris, E. W., and Cotman, C. W., 1986, Long-term potentiation of guinea pig mossy fiber responses is not blocked by N-methyl D-aspartate antagonists, Neurosci. Lett. 70: 132–137.PubMedCrossRefGoogle Scholar
  27. 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.PubMedCrossRefGoogle Scholar
  28. Hoch, D. B., Dingledine, R. J., and Wilson, J. E., 1984, Long-term potentiation in the hippocampal slice: Possible involvement of pyruvate dehydrogenase, Brain Res. 302: 125–134.PubMedCrossRefGoogle Scholar
  29. Kelso, S. R., Ganong, A. H., and Brown, T. H., 1986, Hebbian synapses in hippocampus, Proc. Natl. Acad. Sci. U.S.A. 83: 5326–5330.PubMedCrossRefGoogle Scholar
  30. Krug, M., Lössner, B., and Ott, T., 1984, Anisomycin blocks the late phase of long-term potentiation in the dentate gyms of freely moving rats, Brain Res. Bull. 13: 39–42.PubMedCrossRefGoogle Scholar
  31. Lacaille, J.-C., and Harley, C. W., 1985, The action of norepinephrine in the dentate gyms: Beta-mediated facilitation of evoked potentials in vitro, Brain Res. 358: 210–220.PubMedCrossRefGoogle Scholar
  32. Lynch, G. S., and Baudry, M., 1984, The biochemistry of memory: A new and specific hypothesis, Science 224: 1057–1063.PubMedCrossRefGoogle Scholar
  33. Lynch, G., Larson, J., Kelso, S., Barrionuevo, G., and Schottler, F., 1983, Intracellular injections of EGTA block induction of hippocampal long-term potentiation, Nature 305: 719–721.PubMedCrossRefGoogle Scholar
  34. Lynch, M. A., and Bliss, T. V. P., 1986, Noradrenaline modulates the release of [14Clglutamate from dentate but not from CA1/CA3 slices of rat hippocampus, Neuropharmacology 25: 493–498.PubMedCrossRefGoogle Scholar
  35. MacDermott, A. B., Mayer, M. L., Westbrook, G. L., Smith, S. J., and Barker, J.L., 1986, NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones, Nature 321: 519–522.PubMedCrossRefGoogle Scholar
  36. Malenka, R. C., Madison, D. V., and Nicoll, R. A., 1986, Potentiation of synaptic transmission in the hippocampus by phorbol esters, Nature 321: 175–177.PubMedCrossRefGoogle Scholar
  37. Malinow, R., and Miller, J. P., 1986, Postsynaptic hyperpolarization during conditioning reversibly blocks induction of long-term potentiation, Nature 320: 529–530.PubMedCrossRefGoogle Scholar
  38. Mayer, M. L., Westbrook, G. L., and Guthrie, P. B., 1984, Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones, Nature 309: 261–263.PubMedCrossRefGoogle Scholar
  39. McNaughton, B. L., 1982, Long-term enhancement and short-term potentiation in rat fascia dentata act through different mechanisms, J. Physiol. (Lond.) 324: 249–262.Google Scholar
  40. Misgeld, U., Sarvey, J. M., and Klee, M. R., 1979, Heterosynaptic postactivation potentiation in hippocampal CA 3 neurons: Long-term changes of the postsynaptic potentials, Exp. Brain Res. 37: 217–229.PubMedCrossRefGoogle Scholar
  41. Montminy, M. R., Low, J. M., Tapia-Arancibia, L., Reichlin, S., Mandel, G., and Goodman, R, H., 1986, Cyclic AMP regulates somatostatin mRNA accumulation in primary diencephalic cultures and in transfected fibroblast cells, J. Neurosci. 6: 1171–1176.PubMedGoogle Scholar
  42. Morris, R., and Baker, M., 1984, Does long-term potentiation/synaptic enhancement have anything to do with learning or memory? in: Neurobiology of Learning and Memory ( G. Lynch, J. L., McGaugh, and N. M. Weinberger, eds.), Guilford, New York, pp. 521–535.Google Scholar
  43. Moskal, J. R., Schaffner, A. E., and Koller, K. J., 1985, The identification and partial characterization of a cell surface protein that modulates REM in neonatal rats and long term synapse plasticity in hippocampal slice preparations, Soc. Neurosci. Abstr. 11: 838.Google Scholar
  44. Murdoch, G. H., Rosenfeld, M. G., and Evans, R. M., 1982, Eukaryotic transcriptional regulation and chromatin associated protein phosphorylation by cyclic AMP, Science 218: 1315–1317.PubMedCrossRefGoogle Scholar
  45. Neuman, R. S., and Harley, C. W., 1983, Long-lasting potentiation of the dentate gyms population spike by norepinephrine, Brain Res. 273: 162–165.PubMedCrossRefGoogle Scholar
  46. Nicoletti, F., Meek, J. L., ladorola, M. J., Chuang, D. M., Roth, B. L., and Costa, E., 1986a, Coupling of inositol phospholipid metabolism with excitatory amino acid recognition sites in rat hippocampus, J. Neurochem. 46: 40–46.PubMedCrossRefGoogle Scholar
  47. Nicoletti, F., Wroblewski, J. T., Novelli, A., Alho, H., Guidotti, A., and Costa, E., 1986b, The activation of inositol phospholipid metabolism as a signal-transducing system for excitatory amino acids in primary cultures of cerebellar granule cells, J. Neurosci. 6: 1905–1911.PubMedGoogle Scholar
  48. Nowak, L., Bregestovski, P., Ascher, P., Hebet, A., and Prochiantz, A., 1984, Magnesium gates glutamate-activated channels in mouse central neurones, Nature 307: 462–465.PubMedCrossRefGoogle Scholar
  49. Rasmussen, H., 1986a, The calcium messenger system (first of two parts), N. Engl. J. Med. 314: 1094–1101.PubMedCrossRefGoogle Scholar
  50. Rasmussen, H., 1986b, The calcium messenger system (second of two parts), N. Engl. J. Med. 314: 1164–1170.PubMedCrossRefGoogle Scholar
  51. Robinson, B. G., and Racine, R. J., 1985, Long-term potentiation in the dentate gyros: Effects of noradrenaline depletion in the awake rat, Brain Res. 325: 71–78.PubMedCrossRefGoogle Scholar
  52. Routtenberg, A., Colley, P., Linden, D., Lovinger, D., Murakami, K., and Sheu, F.-S., 1986, Phorbol ester promotes growth of synaptic plasticity, Brain Res. 378: 374–378.PubMedCrossRefGoogle Scholar
  53. Scharfman, H. E., and Sarvey, J. M., 1985a, Postsynaptic firing during repetitive stimulation is required for long-term potentiation in hippocampus, Brain Res. 331: 267–274.PubMedCrossRefGoogle Scholar
  54. Scharfman, H. E., and Sarvey, J. M., 1985b, -y-Aminobutyrate sensitivity does not change during long-term potentiation in rat hippocampal slices, Neuroscience 15: 695–702.Google Scholar
  55. Schwartzkroin, P. A., 1975, Characteristics of CAI neurons recorded intracellularly in the hippocampal in vitro slice preparation, Brain Res. 84: 424–436.Google Scholar
  56. Schwartzkroin, P. A., and Wester, K., 1975, Long-lasting facilitation of the synaptic potential following tetanization in the in vitro hippocampal slice, Brain Res. 89: 107–119.PubMedCrossRefGoogle Scholar
  57. Seamon, K. B., Padgett, W., and Daly, J. W., 1981, Forskolin: Unique diterpine activator of adenylate cyclase in membranes and in intact cells, Proc. Natl. Acad. Sci. U.S.A. 78: 3363–3367.PubMedCrossRefGoogle Scholar
  58. Stanton, P. K., and Sarvey, J. M., 1984, Blockade of long-term potentiation in rat hippocampal CAI region by inhibitors of protein synthesis, J. Neurosci. 4: 3080–3088.PubMedGoogle Scholar
  59. Stanton, P. K., and Sarvey, J. M., 1985a, Depletion of norepinephrine, but not serotonin, reduces long-term potentiation in the dentate gyros of rat hippocampal slices, J. Neurosci. 5: 2169–2176.PubMedGoogle Scholar
  60. Stanton, P. K., and Sarvey, J. M., 1985b, The effect of high-frequency electrical stimulation and norepinephrine on cyclic AMP levels in normal versus norepinephrine-depleted rat hippocampal slices, Brain Res. 358: 343348.Google Scholar
  61. Stanton, P. K., and Sarvey, J. M., 1985c, Blockade of norepinephrine-induced long-lasting potentiation in the hippocampal dentate gyros by an inhibitor of protein synthesis, Brain Res. 361: 276–283.PubMedCrossRefGoogle Scholar
  62. Stanton, P. K., and Sarvey, J. M., 1987, Norepinephrine regulates long-term potentiation of both the population spike and dendritic EPSP in hippocampal dentate gyros, Brain. Res. Bull. 18: 115–119.PubMedCrossRefGoogle Scholar
  63. Stanton, P. K., Sarvey, J. M., and Moskal, J. R., 1985, A monoclonal antibody (MAb) to a cell-surface antigen which inhibits both production and maintenance of long-term potentiation (LTP) in rat hippocampal slice, Soc. Neurosci. Abstr. 11: 838.Google Scholar
  64. 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: 613–769.Google Scholar
  65. Watkins, J. C., and Evans, R. H., 1981, Excitatory amino acid transmitters, Annu. Rev. Pharmacol. Toxicol. 21: 165–204.PubMedCrossRefGoogle Scholar
  66. Wigström, H., and Gustafsson, B., 1984, A possible correlate of the postsynaptic condition for long-lasting potentiation in the guinea pig hippocampus in vitro, Neurosci. Lett. 44: 327–332.PubMedCrossRefGoogle Scholar
  67. Wigström, H., and Gustafsson, B., 1985, Facilitation of hippocampal long-lasting potentiation by GABA antagonists, Acta Physiol. Scand. 125: 159–172.PubMedCrossRefGoogle Scholar
  68. Wigström, H., McNaughton, B. L., and Barnes, C. A., 1982, Long-term enhancement in hippocampus is not regulated by postsynaptic membrane potential, Brain Res. 233: 195–199.PubMedCrossRefGoogle Scholar
  69. Winson, J., and Dahl, D., 1985, Action of norepinephrine in the dentate gyros. Il. Iontophoretic studies, Exp. Brain Res. 59: 497–506.PubMedCrossRefGoogle Scholar
  70. Worley, P. F., Baraban, J. M., De Sousa, E. B., and Snyder, S. H., 1986a, Mapping second messenger systems in the brain: Differential locations of adenylate cyclase and protein kinase C, Proc. Natl. Acad. Sci. U.S.A. 83: 4053–4057.PubMedCrossRefGoogle Scholar
  71. Worley, P. F., Baraban, J. M., and Snyder, S. H., 1986b, Heterogeneous localization of protein kinase C in rat brain: Autoradiographic analysis of phorbol ester receptor binding, J. Neurosci. 6: 199–207.PubMedGoogle Scholar
  72. Yamamoto, C., and Chujo, T., 1978, Long-term potentiation in thin hippocampal sections studied by intracellular and extracellular recordings, Exp. Neurol. 58: 242–250.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1988

Authors and Affiliations

  • John M. Sarvey
    • 1
  1. 1.Department of PharmacologyUniformed Services University of the Health SciencesBethesdaUSA

Personalised recommendations