Summary
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1.
In rabbits, initially anaesthetized by urethane/chloralose and maintained on urethane alone, the perforant path, contacting the apical dendrites of the dentate granule cells by way of boutons en-passage, was activated by paired stimuli. The effect of the first conditioning stimulus was studied by recording the extracellular field response and the extra- and intracellular responses of single granule cells to a second test stimulus.
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2.
The monosynaptic test EPSP recorded extra- as well as intracellularly was potentiated by a preceding volley in the perforant path. The rate of rise and the amplitude of the extracellular test EPSP increased by as much as 100% at an optimal conditioning-test interval of about 25 msec. The total duration of the potentiation was 200–300 msec. Sometimes the potentiation was followed by a slight subnormal phase.
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3.
The EPSP potentiation was not due to a larger presynaptic test volley since (1) the size of the presynaptic fibre potential was not effected, and (2) removal of the entorhinal area did not reduce the effect.
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4.
The potentiation was not due to the recurrent inhibitory hyperpolarization of the postsynaptic membrane because (1) weak conditioning volleys potentiated the EPSPs without discharging the granule cells or producing any inhibition. (2) Conditioning antidromic volleys produced marked inhibition and IPSPs but had no effect on the test perforant path EPSP.
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5.
Different mechanisms that may be responsible for the EPSP potentiation are discussed. The potentiation is compared with that observed in other types of synapses. Potentiation of EPSPs may be an important mechanism behind the frequency potentiation of mass responses characteristic of the hippocampal formation.
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References
Andersen, P.: Interhippocampal impulses. II. Apical dendritic activation of CAl neurons. Acta physiol. scand. 48, 178–208 (1960).
—, Holmqvist, B., Voorhoeve, P.E.: Entorhinal activation of dentate granule cells. Acta physiol. scand. 66, 448–460 (1966).
Andersen, P. Lømo, T.: Control of hippocampal output by afferent volley frequency. In: Progress in Brain Research. Vol. 27, pp. 400–412. Structure and function of the limbic system. Ed.: W. B. Adey and T. Tokizane. Elsevier Publ. Co. 1967.
Blackstad, T.W., Dahl, H.A.: Quantitative evaluation of structures in contact with neuronal somata. An electron microscopic study on the fascia dentata of the rat. Acta morph. neerl-scand. 4, 329–343 (1962).
Braun, M., Schmidt, R.F., Zimmermann, M.: Facilitation of the frog neuromuscular junction during and after repetitive stimulation. Pflügers Arch. ges. Physiol. 287, 41–55 (1966).
Creutzfeldt, O.D., Lux, H.D.: Zur Unterscheidung von „spezifischen” und „unspezifischen” Synapsen an corticalen Nervenzellen. Naturwissenschaften 51, 89–90 (1964).
Curtis, D.R., Eccles, J.C.: Synaptic action during and after repetitive stimulation. J. Physiol. (Lond.) 150, 374–398 (1960).
Eccles, J.C.: Synaptic potentials and transmission in sympathetic ganglion. J. Physiol. (Lond.) 101, 465–483 (1943).
—: The physiology of synapses, 316 pp. Berlin-Göttingen-Heidelberg-New York: Springer 1964.
—, Katz, B., Kuffler, S.W.: Nature of the “endplate potential” in curarized muscle. J. Neurophysiol. 4, 362–387 (1941).
—, Llinás, R., Sasaki, K.: The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum. J. Physiol. (Lond.) 182, 268–296 (1966a).
—: Parallel fiber stimulation and the responses induced thereby in the Purkinje cells of the cerebellum. Exp. Brain Res. 1, 17–39 (1966b).
Euler, C. von, Green, J.D.: Excitation, inhibition and rhythmical activity in hippocampal pyramidal cells in rabbit. Acta physiol. scand. 48, 110–125 (1960).
Gloor, P., Vera, C.L., Sperti, L.: Electrophysiological studies of hippocampal neurons. III. Responses of hippocampal neurons to repetitive perforant path volleys. Electroenceph. clin. Neurophysiol. 17, 353–370 (1964).
Hubbard, J.I.: Post-activation changes at the mammalian neuromuscular junction. Nature (Lond.) 184, 1945–1947 (1959).
—: Repetitive stimulation at the mammalian neuromuscular junction, and the mobilization of transmitter. J. Physiol. (Lond.) 169, 641–662 (1963).
Job, C., Lundberg, A.: On the significance of post- and presynaptic events for facilitation and inhibition in the sympathetic ganglion of the cat. Acta physiol. scand. 28, 14–28 (1953).
Laatsch, R.H., Cowan, W.M.: Electron microscopic studies of the dentate gyrus of the rat. I. Normal structure with special reference to synaptic organization. J. comp. Neurol. 128, 359–396 (1966).
Liley, A.W., North, K.A.K.: An electrical investigation of effects of repetitive stimulation on mammalian neuromuscular junction. J. Neurophysiol. 16, 509–527 (1953).
Lundberg, A., Quilisch, H.: Presynaptic potentiation and depression of neuro-muscular transmission in frog and rat. Acta physiol. scand. 30 (suppl. 111), 111–120 (1953).
Lømo, T.: Frequency potentiation of excitatory synaptic activity in the dentate area of the hippocampal formation. Acta physiol. scand. 68 (suppl. 277), 128 (1966).
Lømo, T.: Potentiation of monosynaptic EPSPs in cortical cells by single and repetitive afferent volleys. J. Physiol. (Lond.) 194, 84–85P (1968).
—: Nature and distribution of inhibition in a simple cortex (Dentate Area). Acta Physiol. scand. 74, 8–9 A (1968).
—: Patterns of activation in a monosynaptic cortical pathway: the perforant path input to the dentate area of the hippocampal formation. Exp. Brain Res. 12, 18–45 (1971).
Mallart, A., Martin, A.R.: An analysis of facilitation of transmitter release at the neuromuscular junction of the frog. J. Physiol. (Lond.) 193, 679–694 (1967).
—: The relation between quantum content and facilitation at the neuromuscular junction of the frog. J. Physiol. (Lond.) 196, 593–604 (1968).
Nacimiento, A.C., Lux, H.D., Creutzfeldt, O.D.: Postsynaptische Potentiale von Nervenzellen des motorischen Cortex nach elektrischer Reizung spezifischer und unspezifischer Thalamuskerne. Pflügers Arch. ges. Physiol. 281, 152–169 (1964).
Rall, W.: Cable properties of dendrites and effects of synaptic location, pp. 175–187. In: Andersen, P. and Jansen, J.K.S. (eds.) Excitatory synaptic mechanisms. Oslo: Universitetsforlaget 1970.
Takeuchi, A., Takeuchi, N.: Active phase of frog's end-plate potential. J. Neurophysiol. 22, 395–411 (1959).
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Lømo, T. Potentiation of monosynaptic EPSPs in the perforant path-dentate granule cell synapse. Exp Brain Res 12, 46–63 (1971). https://doi.org/10.1007/BF00234415
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DOI: https://doi.org/10.1007/BF00234415