Abstract
Electrophysiological laboratory studies on rat visual cortex and hippocampus slices are reviewed. The aim was to confirm the existence of positive feedback in central synapses operating by an electrical (ephaptic) mechanism, as suggested by Byzov. Byzov's hypothesis holds that artificial hyperpolarization of the postsynaptic membrane potential should increase the amplitude of the excitatory postsynaptic current (EPSC) and potential (EPSP) in some central synapses not only by means of increases in the electromotive force (EMF), but also by means of increases in transmitter release from the presynaptic apparatus. Some experiments showed that hyperpolarization altered the parameters of presynaptic transmitter release, i.e., the quantity of “failed” responses N0, the coefficient of variation CV, and the quantum compositionm of minimal EPSC and EPSP. The effect was particularly marked for EPSP in giant synapses formed by mossy fibers on neurons in field CA3. “Supralinear” functions were observed for these synapses in the relationship between EPSC amplitude and membrane potential in conditions of hyperpolarization of membrane potentials and in the relationship between presynaptic paired-stimulus facilitation and membrane potential. All of these “non-classical” effects disappeared when summed rather than minimal EPSC were evoked. The results are in agreement with computer experiments based on the Byzov model and are regarded as support for Byzov's hypothesis. Regardless of their explanation, the data obtained here demonstrate a new feedback mechanism for central synapses, which allows the postsynaptic neuron to control the efficiency of some synapses via changes in membrane potential. This mechanism can significantly increase the efficiency of large (“perforated”) synapses and explains the increase in the number of this type of synapse after various experimental manipulations, such as those inducing long-term potentiation or forming conditioned reflexes.
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References
A. L. Byzov, “Regulatable synapses,”Priroda,1, 71–81 (1994).
A. L. Byzov and V. V. Maksimov, “Electrical feedback in chemical synapses,”Ros. Fiziol. Zh. im. I. M. Sechenova,84, No. 10, 1074–1084 (1998).
O. S. Vinogradova,The Hippocampus and Memory [in Russian], Nauka, Moscow (1975).
L. L. Voronin,Analysis of the Plastic Properties of the Central Nervous System [in Russian], Metsniereba, Tbilisi (1982).
L. L. Voronin, U. Kunt, R. G. Davletshin, and G. Khess, “Non-effective 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 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. Behnisch, and K. G. Reymann, “Quantum analysis does not support an increase in the sensitivity of postsynaptic receptors during the late phase of hippocampal long-term potentiation,”Dokl. Ros. Akad. Nauk,358, No. 3, 419–421 (1998).
L. L. Voronin, M. V. Volgushev, A. V. Sokolov, M. V. Kas'yanov, and M. Chistyakova, “The effects of postsynaptic hyperpolarization support the existence of intrasynaptic ephaptic feedback in central synapses,”Dokl. Ros. Akad. Nauk, in press (1999).
B. Katz,Nerve, Muscle, and Synapse [Russian translation], Inostrannaya Literatura (Foreign Literature Press), Moscow (1967).
A. V. Astrelin, M. V. Sokolov, T. Behnisch, K. G. Reymann, and L. L. Voronin, “Noise deconvolution based on the L1-metric and decomposition of discrete distributions of presynaptic responses,”J. Neurosci. Meth.,73, 17–27 (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).
G. Barrionuevo, S. R. Kelso, D. Johnston, and T. H. Brown, “Conductance mechanism responsible for long-term potentiation in monosynaptic and isolated excitatory synaptic inputs to hippocampus,”J. Neurophysiol.,55, 540–550 (1986).
N. Berretta, A. V. Rossokhin, E. Cherubini, A. V. Astrelin, and L. L. Voronin, “Long-term synaptic changes induced by intracellualr tetanization of CA3 pyramidal neurons in the hippocampal slice from juvenile rats,”Neuroscience, in press (1999).
T. V. P. Bliss and G. L. Collingridge “A synaptic model for memory: long-term potentiation in the hippocampus,”Nature,361, 31–39 (1993).
A. L. Byzov and T. M. Shura-Bura, “Electrical feedback mechanism in the processing of signals in the outer plexiform layer of the retina,”Vision Res.,26, 33–34 (1986).
R. K. S. Calverley and D. G. Jones, “Contributions of dendritic spines and perforated synapses to synaptic plasticity,”Brain Res. Rev.,15, 215–249 (1990).
K. A. Clark, A. D. Randall, and G. L. Collingridge, “A comparison of paired-pulse facilitation of AMPA and NMDA receptor-mediated excitatory postsynaptic currents in the hippocampus,”Exp. Brain Res.,104, 272–278 (1994).
Y. Geinisman, L. de Toledo-Morell, F. Morell, R. E. Heller, M. Rossi, and R. F. Parshall, “Structural synaptic correlate of long-term potentiation: formation of axospinous synapses with multiple, completely partitioned transmission zones,”Hippocampus,3, 435–446 (1993).
M. Glitsch, I. Llano, and A. Marty, “Glutamate as a candidate retrograde messenger at interneurone-Purkinje cell synapses of rat cerebellum,”J. Physiol. (London),497, 531–537 (1996).
D. Johnston, S. Williams, D. Jagge, and R. Gray, “NMDA-receptor independent long-term potentiation,”Ann. Rev. Physiol.,54, 489–505 (1992).
P. Jonas and N. Burnashev, “Molecular mechanisms controlling calcium entry through AMPA-type glutamate receptor channels,”Neuron,15, 987–990 (1995).
P. Jonas, G. Major, and B. Sakmann, “Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus,”J. Physiol. (London),472, 615–663 (1993).
H. Kamiya, H. Shinozaki, and C. Yamamoto, “Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fibre synapses,”J. Physiol. (London),493, 447–455 (1996).
A. M. Kasyanov, V. V. Maximov, A. L. Byzov, N. Berretta, M. V. Sokolov, S. Gasparini, E. Cherubini, K. G. Reymann, and L. L. Voronin, “Intrasynaptic ephaptic feedback alters amplitude-voltage relations of mossy fibre responses I rat CA3 hippocampal neurones,”J. Physiol. (London), in press (1999).
T. Mannabe, D. J. A. Wyllie, D. J. Perkel, and R. A. Nicoll, “Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus,”J. Neurophysiol.,70, 1451–1459 (1993).
V. V. Petukhov and V. L. Popov, “Quantitative analysis of ultrastructural changes in synapses of the rat hippocampal field CA3 in vitro in different functional states,”Neuroscience,18, 823–835 (1986).
M. Scanziani, P. A. Salin, K. E. Vogt, R. S. Malenka, and R. A. Nicoll, “Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors,”Nature,385, 630–634 (1997).
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,”Neuroscience,85, 1–13 (1998).
A. Takeuchi and N. Takeuchi, “Changes in potassium concentration around motor nerve terminals, produced by current flow, and their effects on neuromuscular transmission,”J. Physiol. (London),155, 46–58 (1961).
M. Volgushev, L. L. Voronin, M. Chistiakova, A. Artola, and W. Singer, “All-or-none excitatory postsynaptic potentials in the rat visual cortex,”Eur. J. Neurosci.,7, 1751–1760 (1995).
M. Volguschev, L. L. Voronin, M. Chistiakova, and W. Singer, “Relations between long-term synaptic modifications and paired-pulse interactions in the rat neocortex,”Eur. J. Neurosci.,9, 1656–1665 (1997).
L. L. Voronin,Synaptic Modifications and Memory, Springer, Berlin (1993).
L. L. Voronin, “On the quantal analysis of hippocampal long-term potentiation and related phenomena of synaptic plasticity,”Neuroscience,56, 275–304 (1993).
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, U. Kuhnt, G. Hess, A. G. Gusev, and V. Roschin, “Quantal parameters of ‘minimal’ excitatory postsynaptic potentials in guinea pig hippocampal slices: binomial approach,”Exp. Brain Res.,89, 248–264 (1992).
L. L. Voronin, M. Volgushev, M. Sokolov, A. Kasyanov, M. Chistiakova, and K. G. Reymann, “Evidence for an electrical feedback in cortical synapses: postsynaptic hyperpolarization alters the number of response failures and quantal content,”Neuroscience, in press (1999).
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Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 85, No. 6, pp. 729–742, June, 1999.
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Voronin, L.L. Intrasynaptic ephaptic feedback in central synapses. Neurosci Behav Physiol 30, 575–585 (2000). https://doi.org/10.1007/BF02462618
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DOI: https://doi.org/10.1007/BF02462618