[en] The aim of the present work was to study the potentiation of the AMPA and NMDA components of minimal excitatory postsynaptic currents (EPSC) evoked by activation of restricted numbers of synapses. EPSC of neurons in field CA1 in hippocampal slices were recorded in whole-call patch-clamp conditions selected such that both (AMPA and NMDA) components were present, and these were measured in parallel using computational methods in combination with pharmacological receptor blockade. There was a quite strong correlation between the amplitudes of the AMPA and NMDA components and this was regarded as evidence that they were generated by the same synapses. In cases producing this correlation, both components showed essentially equal long-term potentiation lasting from 5 min to 2 h after afferent tetanization. The data did not support the postsynaptic hypothesis and were in better agreement with the concept that the major mechanism for the persistence of the initial phase of long-term potentiation (up to 1–2 h) is based on increases in the quantity of transmitter released presynaptically.
A. G. Bragin and O. S. Vinogradova, "Chronic potentiation in the cortical afferent input of pyramidal cells of field CA3 of the hippocampus," in: Physiological Mechanisms of Memory [in Russian], Institute of Biophysics, Academy of Sciences of the USSR, Pushchino-na-Oke (1973), pp. 8-14.
A. L. Byzov, "Regulatable synapses," Priroda, 1, 71-81 (1994).
L. L. Voronin, Analysis of the Plastic Properties of the Central Nervous System [in Russian], Metsniereba, Tbilisi (1982).
L. L. Voronin, "Intrasynaptic ephatic feedback in central synapses," Ros. Fiziol. Zh. im. I. M. Sechenova, 85, No. 6, 729-742 (1999).
L. L. Voronin, I. E. Kudryashov, and S. V. Ioffe, "Posttetanic potentiation in the hippocampus and its relationship with conditioned-reflex mechanisms," Dokl. Akad. Nauk. SSSR, 217, No. 3, 1453-1456 (1974).
L. L. Voronin, U. Kunt, R. G. Davletshin, and G. Gess, "Inefficient synapses in living hippocampal slices," Dokl. Akad. Nauk SSSR, 302, No. 3, 746-749 (1988).
L. L. Voronin, A. V. Rossokhin, and M. V. Sokolov, "Intracellular studies of the interaction between paired facilitation in and the late phase of long-term hippocampal potentiation," Ros. Fiziol. Zh. im. I. M. Sechenova, 84, No. 5-6, 426-435 (1998).
L. L. Voronin, M. V. Sokolov, A. V. Astrelin, T. Benish, and K. G. Raiman, "Quantum analysis does not support increases in the sensitivity of receptors during the late phase of hippocampal long-term potentiation," Dokl. Ros. Akad. Nauk, 358, No. 2, 419-421 (1998).
A. M. Kleshchevnikov, "Long-term potentiation of the NMDA-dependent component of EPSP in the hippocampus," Usp. Fiziol. Nauk., 29, No. 1, 6-23 (1998).
L. G. Magazanik, M. C. Samilova, S. L. Budakova, K. V. Esin, and V. E. Gmiro, "Selective suppression of AMPA/kainate receptors of hippocampal interneurons as a new approach to the study of inhibitory systems," Ros. Fiziol. Zh. im. I. M. Sechenova, 83, No. 5-6, 19-29 (1997)
A. V. Astrelin, M. V. Sokolov, T. Behnisch, K. G. Reymann, and L. L. Voronin, "Principal components analysis of minimal excitatory postsynaptic potentials," J. Neurosci. Meth., 79, 169-186 (1998).
I. Bayazitov and A. Kleschevnikov, "Afferent high-strength tetanizations favour potentiation of the NMDA vs. AMPA receptor-mediated component of field EPSP in Ca1 hippocampal slices of rats," Brain Res., 866, 188-196 (2000).
N. Berretta, A. C. Rossokhin, A. M. Kasyanov, M. V. Sokolov, E. Cherubini, and L. L. Voronin, "Postsynaptic hyperpolarization increases the strength of AMPA mediated synaptic transmission at large synapses between mossy fibers and CA3 pyramidal cells," Neuropharmacology, 39, 2288-2301 (2000).
T. V. P. Bliss and G. L. Collingridge, "A synaptic model for memory:long-term potentiation in the hippocampus," Nature, 361, 31-39 (1993).
T. V. P. Bliss and T. Lomo, "Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path," J. Physiol. (London), 232, 331-356 (1973).
S. L. Buldakova, K. V. Bolshakov, D. B. Tikhonov, and L. G. Magazanik, "Ca2+-dependent desensitization of AMPA receptors," NeuroReport, 11, 1-5 (2000).
K. A. Clark, A. D. Randal, Z. A. Botolotto, Z. A. Bashir, and G. L. Collingridge, "Mechanisms involved in hippocampal LTP: implications for retrograde messengers," Semin. Neurosci., 5, 189-195 (1995).
G. M. Durand, Y. Kovakchuk, and A. Konnerth, "Long-term potentiation and functional synapse induction in developing hippocampus," Nature, 381, 71-75 (1996).
F. A. Edwards, "Anatomy and electrophysiology of fast central synapses lead to a structural model for long-term potentiation," Physiol. Rev., 75, 759-787 (1995).
S. Gasparini, C. Saviane, L. L. Voronin, and E. Cherubini, "Silent synapses in the developing hippocampus: Lack of functional AMPA receptors or low probability of glutamate release?" Proc. Natl. Acad. Sci. USA, 97, 9741-9746 (2000).
J. T. R. Isaac, R. A. Nicoll, and R. C. Malenka, "Evidence for silent synapses. Implications for the expression of LTP," Neuron, 16, 427-434 (1995).
A. M. Kasyanov, V. Maximov, A. L. Byzov, N. Berretta, M. V. Sokolov, S. Gasparini, E. Cherubini, K. Reymann, and L. L. Voronin, "Intrasynaptic ephaptic feedback alters amplitude-voltage relations of mossy fibre responses in rat CA3 hippocampal neurons," Neurosci., 101, 323-336 (2000).
J. A. Kauer, R. C. Malenka, and R. A. Nicoll, "A persistent postsynaptic modification mediates long-term potentiation in the hippocampus," Neuron, 7, 911-917 (1988).
A. M. Kleschevnikov, M. Sokolov, U. Kuhnt, G. S. Dawe, J. D. Stephenson, and L. L. Voronin, "Changes in paired-pulse facilitation correlation with induction of long-term potentiation in area CA1 of rat hippocampal slices," Neurosci., 76, 829-844 (1997).
D. M. Kulmann, "Amplitude fluctuations of dual-component EPSCs in hippocampal pyramidal cells: implications for long-term potentiation," Neuron, 12, 1111-1120 (1994).
D. Liao, N. A. Hessler, and R. Malinow, "Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice," Nature, 375, 400-404 (1995).
L. G. Magazanik, S. L. Buldakova, M. V. Samoilova, V. E. Gmiro, I. R. Mellor, and P. N. R. Usherwood, "Block of open channels of recombinant AMPA receptors and native AMPA/kainate receptors by adamantane derivatives," J. Physiol. (London), 505, 655-663 (1997).
R. C. Malenka and R. A. Nicoll, "Long-term potentiation. A decade of progress?" Science 285, 1870-1874 (1999).
D. Muller, J. Larson, and G. Lynch, "The NMDA receptor-mediated components of resposnes evoked by patterned stimulation is not increased by long-term potentiation," Brain Res., 447, 396-399 (1989).
Z. Nusser, "AMPA and NMDA receptor: similarities and differences in their synaptic distribution," Curr. Opin. Neurobiol., 10, 337-341 (2000).
M. V. Sokolov, A. V. Rossokhin, T. Behnisch, K. G. Reymann, and L. L. Voronin, "Interaction between paired-pulse facilitation and long-term potentiation of minimal EPSPs in rat hippocampal slices: a patch clamp study," Neurosci., 85, 1-13 (1998).
A. M. Thomson and S. Radpour, "Excitatory connections between CA1 pyramidal cells revealed by spike triggered averaging in slices of rat hippocampus are partially NMDA receptor mediated," Eur. J. Neurosci., 3, 587-601 (1991).
L. L. Voronin, Synaptic Modifications and Memory. An Electrophysiological Analysis, Springer, Berlin (1993).
L. L. Voronin, "Quantal analysis of hippocampal long-term potentiation," Rev. Neurosci., 5, 41-170 (1994).
L. Voronin, A. Byzov, A. Kleschevnikov, M. Kozhemyakin, U. Kuhnt, and M. Volgushev, "Neurophysiological analysis of long-term potentiation in mammalian brain," Brain Res., 66, 45-52 (1995).
L. L. Voronin, M. Volgushev, M. Chistiakova, U. Kuhnt, and W. Singer, "Involvement of silent synapses in the induction of LTP and LTD in hippocampal and neocortical neurones," Neurosci., 74, 323-330 (1996).
M.-Y. Xiao, H. Wigstrom, and Y.-P. Niu, "Variability of AMPA and NMDA receptor-mediated responses in CA1 pyramidal cells of young rats," Brain Res., 800, No. 2, 253-259 (1998).