Abstract
Heterosynaptic facilitation (HF), analyzed first by Kandel and Tauc (1965), is an activity-dependent, lasting amplification of synaptic transmission in convergent neural pathways. As a cellular associative mechanism, HF can account for the temporal specificity and stimulus—response specificity of classical conditioning in Aplysia (Kandel and Tauc, 1965; Kandel, 1976). Heterosynaptic facilitation is a presynaptic phenomenon in molluscs, and action potential generation in the postsynaptic neuron is neither necessary nor sufficient for HF induction in these species (Wurtz et al., 1967; Carew et al., 1984). This finding is at odds with Hebb’s postulate (Hebb, 1949) proposing that synaptic transmission is enhanced only when the presynaptic stimulus occurs in conjunction with action potential generation in the postsynaptic cell. Apart from Aplysia, plastic synaptic changes in agreement with the Hebb model have been documented in vertebrate ganglion cells (Schulman and Weight, 1976; Kumamoto and Kuba, 1983; Mochida and Libet, 1985), in the hippocampus (McNaughton et al., 1978; Levy and Steward, 1979; Lynch et al., 1983; Kuhnt, 1984; Scharfman and Sarvey, 1985; Wigstrom and Gustafsson, 1985; Wigstrom et al., 1986; Kelso et al., 1986; Malinow and Miller, 1986), and in the visual cortex (Hubel and Wiesel, 1965; Rauschecker and Singer, 1981; Bienenstock et al., 1983; Fregnac and Imbert, 1984; Bear and Singer, 1986).
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References
Alkon, D. L., 1984, Calcium mediated reduction of ionic currents: A biophysical memory trace, Science 226: 1037–1045.
Baranyi, A., and Chase, M. H., 1984, Ethanol-induced modulation of the membrane potential and synaptic activity of trigeminal motoneurons during sleep and wakefulness, Brain Res. 307: 233–245.
Baranyi, A., and Feher, 0., 1978, Conditioned changes of synaptic transmission in the motor cortex of the cat, Exp. Brain Res. 33: 283–298.
Baranyi, A., and Feher, O., 1981a, Selective facilitation of synapses in the neocortex by heterosynaptic activation, Brain Res. 212: 164–168.
Baranyi, A., and Feher, O., 1981b, Intracellular studies on cortical synaptic plasticity: Conditioning effect of antidromic activation of test-EPSPs, Exp. Brain Res. 41: 124–134.
Baranyi, A., and Feher, O., 1981c, Synaptic facilitation requires paired activation of convergent pathways in the neocortex, Nature 290: 413–415.
Baranyi, A., and Feher, O., 1981d, Long-term facilitation of excitatory synaptic transmission in single motor cortex neurons of the cat produced by repetitive pairing of synaptic potentials and action potentials following intracellular stimulation, Neurosci. Lett. 23: 303–308.
Baranyi, A., and Szente, M., 1986, The effect of intracellular colchicine and EGTA injection on the hetero-synaptic facilitation of cortical neurons, Acta Physiol. Hung. 68: 353 (Absr.).
Baux, G., Simonneau, M., and Tauc, L., 1981, Action of colchicine on membrane currents and synaptic transmission in Aplysia ganglion cells, J. Neurobiol. 12: 75–85.
Bear, M. F., and Singer, W., 1986, Modulation of visual cortical plasticity by acetylcholine and noradrenaline, Nature 320: 172–176.
Bienenstock, E. L., Fregnac, Y., and Thorpe, S., 1983, Iontophoretic clamp of activity in visual cortical neurons in the cat: A test of Hebb’s hypothesis, J. Physiol. (Lond.) 345: 123 P.
Bindman, L. J., Lippold, O. C. J., and Milne, A. R., 1979, Prolonged changes in excitability of pyramidal tract neurons in the cat: A postsynaptic mechanism, J . Physiol. (Lond.) 286: 457–477.
Black-Cleworth, P., Woody, C. D., and Nieman, J. A., 1975, Conditioned eyeblink obtained by using electrical stimulation of the facial nerve as unconditioned stimulus, Brain Res. 90: 44–56.
Brindley, G. S., 1969, Nerve net models of plausible size that perform many simple learning tasks, Proc. R. Soc. (Lond.) 174: 173–191.
Byrne, J. H., 1985, Neuronal and molecular mechanisms underlying information storage in Aplysia: Implications for learning and memory, Trends Neurosci. 9: 478–482.
Carew, T. J., Hawkins, R. D., Abrams, T. W., and Kandel, E. R., 1984, A test of Hebb’s postulate at identified synapses which mediate classical conditioning in Aplysia, J. Neurosci. 4:1217–1224.
Carlson, N. R., Laxer, K. D., and Mason, M. A., 1983, Intracerebral infusions of colchicine abolish kindled epileptogenic foci in cats, Soc. Neurosci. Abstr. 9: 764.
Deschenes, M., Landry, P., and Clercq, M., 1982, Reanalysis of the ventrolateral input in slow and fast pyramidal tract neurons of the cat motor cortex, Neuroscience 7: 2149–2157.
Fambrough, M. D., and Devreotes, P. M., 1978, Newly synthetized acetylcholine receptors are located in the Golgi apparatus, J. Cell. Biol. 76: 237–244.
Fregnac, Y., and Imbert, M., 1984, Development of neuronal selectivity in primary visual cortex of cat, Physiol. Rev. 64: 325–434.
Gardner-Medwin, A. R., 1976, The recall of events through the learning of associations between their parts, Proc. R. Soc. (Lond.) [Biol.] 194: 375–402.
Gardner-Medwin, A. R., 1978, The possible significance for learning of some different types of synaptic modification, Biochem. Soc. Trans. 6: 841–844.
Goelet, P., Castellucci, V. F., Schacher, S., and Kandel, E. R., 1986, The long and the short of long-term memory—a molecular framework, Nature 322: 419–422.
Gustafsson, B., and Wigstrom, H., 1986, Hippocampal long-lasting potentiation produced by pairing single volleys and brief conditioning tetani evoked in separate afferents, J. Neurosci. 6: 1575–1582.
Hebb, D. 0., 1949, The Organization of Behavior, John Wiley & Sons, New York.
Holmes, W. R., and Woody, C. D., 1987, Effects of uniform and nonuniform synaptic “activation-distributions” on the cable properties of modeled cortical pyramidal neurons, J. Neurophysiol. (in press).
Hubel, D. H., and Wiesel, T. N., 1965, Binocular interaction in striate cortex of kittens reared with artificial squint, J. Neurophysiol. 28: 1041–1049.
Kandel, E. R., 1976, Cellular Basis of Behavior, W. H. Freeman, San Francisco.
Kandel, E. R., and Tauc, L., 1965, Mechanism of heterosynaptic facilitation in the giant cell of the abdominal ganglion of Aplysia depilans, J. Physiol. (Lond.) 181: 28–47.
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.
Kreutzberg, G. W., 1981, Parameters of dendritic transport, Neurosci. Res. Prog. Bull. 20: 45–55.
Kuhnt, U., 1984, Long-lasting changes of synaptic excitability induced by repetitive intracellular current injection in hippocampal neurons, Neurosci. Lett. Suppl. 18: S27.
Kumamoto, E., and Kuba, K., 1983, Sustained rise in ACh sensitivity of sympathetic ganglion cell induced by postsynaptic electrical activities, Nature 305: 145–146.
Levy, W. B., and Steward, O., 1979, Synapses as associative elements in the hippocampal formation, Brain Res. 175: 233–245.
Libet, B., 1984, Heterosynaptic interaction at a sympathetic neuron as a model for induction and storage of a postsynaptic memory trace, in: Neurobiology of Learning and Memory ( G. Lynch, J. L. McGaugh, and N. M. Weinberger, eds.), Guilford Press, New York, pp. 405–430.
Lynch, G., and Baudry, T., 1984, The biochemistry of memory: A new and specific hypothesis, Science 224: 1057–1063.
Lynch, G., Larson, J., Kelso, S., Barrionuevo, G., and Shottler, F., 1983, Intracellular injections of EGTA block induction of hippocampal long-term potentiation, Nature 305: 719–721.
Malinow, R., and Miller, J. P., 1986, Postsynaptic hyperpolarization during conditioning reversibly block induction of long-term potentiation, Nature 320: 529–530.
Man, D. A., 1970, A theory for cerebral neocortex, Proc. R. Soc. Lond. [Biol.] 176: 164–234.
Martin, G. K., Land, T., and Thompson, R. F., 1980, Classical conditioning of the rabbit (Oryctolagus cuniculus) nicticating membrane response with electrical brain stimulation, J. Comp. Physiol. Psychol. 94: 216–226.
McCabe, B., 1976, An after-effect of local stimulation of neurons in the cerebral cortex of the unanaesthetized tat, J. Physiol. (Lond.) 263: 140–141.
McNaughton, B. L., Douglas, P. M., and Goddard, G. V., 1978, Synaptic enhancement in fascia dentata: Cooperativity among coactive afferents, Brain Res. 157: 277–293.
Mochida, S., and Libet, B., 1985, Synaptic long-term enhancement (LTE) induced by heterosynaptic neuronal input, Brain Res. 39: 360–363.
Nestler, E. J., Walaas, J. S., and Greengard, P., 1984, Neuronal phosphoproteins. Physiological and clinical implications, Science 225: 1357–1365.
O’Brien, J. H., Wilder, M. B., and Stevens, C. D., 1977, Conditioning of cortical neurons in cats with antidromic activation as the unconditioned stimulus, J. Comp. Physiol. Psychol. 91: 918–929.
Olds, J., 1980, Thoughts on cerebral function: The cortex as an action system, in: Biology of Reinforcement, Facets of Brain-Stimulation Reward ( A. Routtenberg, ed.), Academic Press, New York, pp. 149–167.
Palm, G., 1982, Neural Assemblies: An Alternative Approach to Artificial Intelligence Studies of Brain Function, Vol. 7, Spinger-Verlag, Berlin, Heidelberg, New York.
Peters, A., and Jones, E. G., 1984, Cellular Components of the Cerebral Cortex, Plenum Press, New York, London.
Pumain, R., and Heinemann, H., 1985, Stimulus and aminoacid-induced calcium and potassium changes in rat neocortex, J. Neurophysiol. 53: 1–16.
Purpura, D. P., 1972, Intracellular studies on synaptic organizations in mammalian brain, in: Structure and Function of Synapses ( D. P. Purpura and G. D. Pappas, eds.), Raven Press, New York, pp. 253–302.
Quinn, K. J., and O’Brien, J. H., 1983, Cortical motor neuron activity in the cat during classical conditioning with central stimulation as the CS and US, Behay. Neurosci. 97: 28–41.
Rauschecker, J. P., and Singer, W., 1981, The effects of early visual experience and their possible explanation by Hebb synapses, J. Pysiol. (Lond.) 310: 215–239.
Scharfman, H., and Sarvey, J. M., 1985, Postsynaptic firing during repetitive stimulation is required for longterm potentiation in hippocampus, Brain Res. 331: 267–274.
Schulman, J. A., and Weight, F. F., 1976, Synaptic transmission: Long-lasting potentiation by a postsynaptic mechanism, Science 194: 1434–1439.
Sutula, T., Goldsmith, R., and Steward, 0., 1982, Effect of colchicine on synaptic transmission and longterm potentiation in the dentate gyms, Soc. Neurosci. Absr. 9: 240.
Takahashi, K., Kubota, K., and Uno, M., 1967, Recurrent facilitation in cat pyramidal tract cells, J. Neurophysiol. 30: 22–34.
Tzebelikos, E., and Woody, C. D., 1979, Intracellularly studies on excitability changes in coronal—pericruciate neurons following low-frequency stimulation of the corticobulbar tract, Brain Res. Bull. 4: 635–641.
Wigstrom, H., and Gustaffson, B., 1985, On long-lasting potentiation in the hippocampus: A proposed mechanism for its dependence on coincident pre-and postsynaptic activity, Acta Physiol. Scand. 123: 519–522.
Wigstrom, H., Gustafsson, B., Huang, Y. Y., and Abraham, W. C., 1986, Hippocampal long-term potentiation is induced by pairing single afferent valleys with intracellularly injected depolarizing current pulse, Acta Physiol. Scand. 126: 317–319.
Woody, C. D., Buerger, J. A., Ungar, R. A., and Levine, D. S., 1977, Modelling aspects of learning by altering biophysical properties of a simulated neuron, Biol. Cybernet. 23: 73–82.
Woody, C. D., Alkon, D. L., and Hay, B., 1984, Depolarization-induced effects of Ca’ -calmodulin-dependent protein kinase injection, in vivo, in single neurons of cat motor cortex, Brain Res. 321: 192–197.
Woody, C. D., Bartfai, T., Gruen, E., and Nairn, A. C., 1986, Intracellular injection of cGMP-dependent protein kinase results in increase input resistance in neurons of the mammalian motor cortex, Brain Res. 386: 379–385.
Wurtz, R. H., Castellucci, V. F., and Nusrala, J. M., 1967, Synaptic plasticity: The effect of the action potential in the postsynaptic neuron, Exp. Neurol. 18: 350–368.
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Baranyi, A., Szente, M.B. (1988). Postsynaptic Activity-Dependent Facilitation of Excitatory Synaptic Transmission in the Neocortex. In: Woody, C.D., Alkon, D.L., McGaugh, J.L. (eds) Cellular Mechanisms of Conditioning and Behavioral Plasticity. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-9610-0_36
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