Abstract
It is becoming increasingly apparent that long-term potentiation (LTP) of synaptic efficacy in, the hippocampus is not a unitary phenomenon. Most attention has been focussed on the associative form of LTP, which is found in the perforant path projection to granule cells of the dentate gyrus, in the commissural projection to areas CA1 and CA3, and in the Schaffer collateral projection from CA3 to CA1. In the context of LTP, associativity refers to the ability of an active pathway to influence the probability that LTP will occur in another active pathway converging on the same target cells (see Gustafsson and Wigstrom 1991). In all these cases, the induction of the effect is mediated by the NMDA subtype of glutamate receptor, and it is the voltage-dependent properties of the NMDA receptor/channel complex which endows LTP with its associative properties (Collingridge and Bliss 1987). In contrast, LTP in the mossy fibre projection to CA3 cells is not mediated by the NMDA receptor (Harris and Cotman 1986). Although there is disagreement about whether the postsynaptic neurone participates in the induction of mossy-fibre LTP (Jaffe and Johnston 1990; Zalutsky and Nicoll 1990), there have been two reports that this form of LTP is non-associative (Kauer and Nicoll 1988; Chattarji et al. 1989).
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References
Abraham, W. C., Bliss, T. V. P., Goddard, G. V. (1985) Heterosynaptic changes accompany logn-term but not short-term potentiation of the perforant path in the anaesthetized rat. J. Physiol. 363:335–349.
Abraham, W. C., Gustafsson, B., Wigström, H. (1987) Long-term potentiation involves enhanced synaptic excitation relative to synaptic inhibition in guinea pig hippocampus. J. Physiol. 394:367–380.
Andersen, P., Sundberg, S. H., Sveen, O., Wigström, H. (1977) Specific long-lasting potentiation of synaptic transmission in hippocampal slices. Nature 266:736–737.
Andersen, P., Sundberg, S. H., Sveen, O., Sveen, J. W., Wigström H. (1980) Possible mechanisms for long-lasting potentiation of synaptic transmission in hippocampal slices from guinea-pigs. J. Physiol. 302:463–482.
Andersen, P., Avoli, M., Hvalby, O. (1984) Evidence for both pre-and postsynaptic mechanisms during long-term potentiation in hippocampal slices. Exp. Brain Res. Suppl 9:315–324.
Barrionuevo, G., Brown, T. (1983) Associative long-term potentiation in hippocampal slices. Proc. Natl. Acad. Sci. USA 70:7347–7351.
Barrionuevo, G., Kelso, S. R., Johnston, D., Brown T. H. (1986) Conductance mechanism responsible for long-term potentiation in monosynaptic and isolated excitatory synaptic inputs to hippocampus. J. Neurophysiol. 55(3):540–550.
Bilkey, D. K., Goddard, G. V. (1985) Medial septal facilitation of hippocampal granule cell activity is mediated by inhibition of inhibitory interneurones. Brain Res. 361:99–106.
Bliss, T. V. P., Gardner-Medwin, A. R. (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the unanesthetized rabbit following stimulation of the perforant path. J. Physiol. 232:357–374.
Bliss, T. V. P., 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. 232:331–356.
Bliss, T. V. P., Lynch, M. A. (1988) Long-term potentiation of synaptic transmission in the hippocampus: properties and mechanisms. In: Landfield, P. W., Deadwyler, S. A. (eds) Long-term potentiation in the hippocampus: from biophysics to behavior Alan R Liss, New York, pp 3–12.
Bliss, T. V. P., Gardner-Medwin, A. R., Lømo, T (1973) Synaptic plasticity in the hippocampal formation. 193-203.
Bliss, T. V. P., Goddard, G. V., Riives, M. (1983) Reduction of long-term potentiation in the dentate gyrus of the rat following selective depletion of monoamines. J. Physiol. 334:475–491.
Bliss, T. V. P., Errington, M. L., Lynch, M. A. (1987) Calcium-induced long-term potentiation in the dentate gyrus is accompanied by a sustained increase in glutamate release. In: Hicks, T. P., Lodge, D., McLennan, H. (eds) Excitatory amino acid transmission, Alan R. Liss, Inc., New York, pp 337–340.
Chattarji, S., Stanton, P. K., Sejnowski, T. (1989) Commissural synapses, but not mossy fiber synapses, in hippocampal field CA3 exhibit associative long-term potentiation and depression. Brain Res. 495:145–150.
Chavez-Noriega, L. E., Bliss, T. V. P., Halliwell, J. V. (1989) The EPSP-spike (E–S) component of long-term potentiation in the rat hippocampal slice is modulated by GABAergic but not cholinergic mechanisms. Neurosci Lett 104:58–64.
Chavez-Noriega, L. E., Halliwell, J. V., Bliss, T. V. P. (1990) A decrease in firing threshold observed after induction of the EPSP-spike (E–S) component of long-term potentiation in rat hippocampal slices. Exp Brain Res 79:633–641.
Collingridge, G. L., Bliss, T. V. P. (1987) NMDA receptors — their role in long-term potentiation. Trends Neurosci. 10(7):288–293.
Douglas, R. M., Goddard, G. V. (1975) Long-term potentiation of the perforant path-granule cell synapse in the rat hippocampus. Brain Res. 86:205–215.
Errington, M. L., Lynch, M. A., Bliss, T. V. P. (1987) Long-term potentiation in the dentate gyrus: Induction and increased glutamate release are blocked by D(-)aminophosphonovalerate. Neuroscience 20:279–284.
Fantie, B., Goddard, G. V. (1982) Septal modulation of the population spike in the fascia dentata produced by perforant path stimulation in the rat. Brain Res. 252:227–237.
Gustafsson, B., Wigstrom, H. (1991) Associative long-term changes in synaptic efficacy. Seminars Neurosci 1, in press.
Harris, E. W., Cotman, C. W. (1986) Long-term potentiation of guinea pig mossy fiber responses is not blocked by N-methyl-D-aspartate. Neurosci. Lett. 70:132–137.
Jaffe, D., Johnston, D. (1990) Induction of long-term potentiation at hippocampal mossy-fiber synapses follows a Hebbian rule. J Neurosci 64:948–961.
Kauer, J. A., Nicoll, R. A. (1988) In: Haas, H. L., Buzsaki, G. (eds) Synaptic plasticity in the hippocampus. Springer-Verlag, Berlin.
Kelso, S. R., Brown, T. H. (1986) Differential conditioning of associative synaptic enhancement in hippocampal brain slices. Science 232:85–87.
Krnjevic, K., Ropert, N. (1982) Electrophysiological and pharmacological characteristics of facilitation of hippocampal population spikes by stimulation of the medial septum. Neuroscience (9):2165-2183.
Lacaille, J.-C., Harley, C. W. (1985) The action of norepinephrine in the dentate gyrus: Beta-mediated facilitation of evoked potentials in vitro. Brain Res. 358:210–220.
Lynch, M. A., Errington, M. L., Bliss, T. V. P. (1989) Nordihydroguaiaretic acid blocks the synaptic component of long-term potentiation and the associated increases in release of glutamate and arachidonate: an in vivo study in the dentate gyrus of the rat. Neuroscience 30:693–701.
McNaughton, B. L., Barnes, C. A. (1977) Physiological identification and analysis of dentate granule cell responses to stimulation of themedial and lateral perforant pathways in the rat. J. Comp. Neurol. 175(4):439–454.
McNaughton, N., Miller, J. J. (1984) Medial septal projections to the dentate gyrus of the rat: electrophysiological analysis of distribution and plasticity. Exp. Brain Res. 56:243–256.
McNaughton, B. L., Douglas, R. M., Goddard, G. V. (1978) Synaptic enhancement in fascia dentata: cooperativity among coactive afferents. Brain Res. 157:277–293.
Melchers, B. P. C., Pennartz, C. M. A., Hopes da Silva, F. H. (1987) Differential effects of elevated extracellular calcium concentrations on field potentials in dentate gyrus and CA1 of the rat hippocampal slice preparation. Neurosci. Lett. 77:37–42.
Mueller, A. L., Hoffer, B. J., Dunwiddie, T. V. (1981) Noradrenergic responses in rat hippocampus: evidence for mediation by alpha and beta receptors in the in vitro slice. Brain Res. 214:113–126.
Neuman, R. S., Harley, C. W. (1983) Long-lasting potentiation of the dentate gyrus population spike by norepinephrine. Brain Res. 273:162–165.
Olpe, H. R., Laszlo, J., Pozza, M. F., DeHerdt, P., Waldmeier, P. C., Jones, R. S. G. (1986) Glutamate-induced activation of rat locus coeruleus increases CA1 pyramidal cell excitability. Neurosci. Lett. 65:11–16.
Otani, S., Marshall, C. J., Tate, W. P., Goddard, G. V., Abraham, W. C. (1989) Maintenance of long-term potentiation in rat dentate gyrus requires protein synthesis but not messenger RNA synthesis immediately post-tetanization. Neuroscience 28(3):519–526.
Robinson, G. B. (1986) Enhanced long-term potentiation induced in rat dentate gyrus by coactivation of septal and entorhinal inputs: temporal constraints. Brain Res. 379:56–62.
Rovira, C., Ben-Ari, Y., Cherubini, E. (1983) Dual cholinergic modulation of hippocampal somatic and dendritic field potentials by the septo-hippocampal pathway. Exp. Brain. Res. 49:151–155.
Sah, P., Hestrin, S., Nicoll, R. A. (1989) Tonic activation of NMDA receptors by ambient glutamate enhances excitability of neurones. Science 246:815–818.
Stanton, P., Sarvey, J. (1985a) Blockade of norepinephrine-induced long-lasting potentiation in the hippocampal dentate gyrus by an inhibitor or protein synthesis. Brain Res 361:276–283.
Stanton, P. K., Sarvey, J. M., (1985b) Depletion of norepinephrine, but not serotonin, reduces long-term potentiation in the dentate gyrus of rat hippocampal slices. J. Neurosci. 5(8):2169–2176.
Taube, J. S., Schwartzkroin, P. A. (1988) Mechanisms of long-term potentiation: EPSP/spike dissociation, intradendritic recordings and glutamate sensitivity. J. Neurosci. 8:1632–1644.
Turner, R. W., Baimbridge, K. G., Miller, J. J. (1982) Calcium-induced long-term potentiation in the hippocampus. Neuroscience 7:1411–1416.
Williams, J. H., Errington, M. L., Lynch, M. A., Bliss, T. V. P. (1989) Arachidonic acid induces a long-term activity-dependent enhancement of synaptic transmission in the hippocampus. Nature 341:739–742.
Wilson, R. C., Levy, W. B., Steward, O. (1981) Changes in translation of synaptic excitation to dentate granule cell discharge accompanying long-term potentiation. II. An evaluation of mechanisms utilizing dentate gyrus dually innervated by surviving ipsilateral and sprouted crossed temerodentate inputs. J. Neurophysiol. 46:339–355.
Winson, J., Dahl, D. (1985) Action of norepinephrine in the dentate gyrus. II. Iontophoretic studies. Exp. Brain Res. 59:497–506.
Zalutsky, R. A., Nicoll, R. A. (1990) Comparison of two forms of long-term potentiation in single hippocampal neurons. Science 248:1619–248.
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Chavez-Noriega, L.E., Bliss, T.V.P. (1991). Persistent Modulation of Neural Excitability in the Hippocampus: The Role of EPSP-Spike (E–S) Potentiation. In: Ascher, P., Choi, D.W., Christen, Y. (eds) Glutamate, Cell Death and Memory. Research and Perspectives in Neurosciences. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-84526-0_4
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