Relations Between Long‐term Synaptic Modifications and Paired‐pulse Interactions in the Rat Neocortex

The phenomenon of paired‐pulse facilitation (PPF) was exploited to investigate the role of presynaptic mechanisms in the induction and maintenance of long‐term synaptic plasticity in the neocortex. Long‐term potentiation (LTP) and depression (LTD) were induced without afferent activation by applying tetani of intracellular pulses. Our results show that synaptic modifications closely resembling LTP and LTD can be induced by postsynaptic activation alone. The polarity of these synaptic modifications depends on initial properties of the input, as indicated by a correlation between initial PPF ratio and post‐tetanic amplitude changes: inputs exhibiting strong PPF, which might be associated with low release probability tend to be potentiated, while inputs with small PPF are more likely to show depression. Maintenance of both LTP and LTD involve presynaptic mechanisms, as indicated by changes in PPF ratios and in failure rate after LTP or LTD induction. Presynaptic mechanisms could include changes in release probability and/or in the number of active release sites. Because induction was postsynaptic, this supports the notion of a retrograde signal. The relative contribution of pre‐ and postsynaptic mechanisms in the maintenance of long‐term synaptic modifications depends on the initial state of the synaptic input and on LTP magnitude. PPF changes were especially pronounced in inputs which had initially high PPF and underwent strong potentiation. Since LTP and LTD are associated with changes of PPF ratios these synaptic modifications do not only alter the gain but also the temporal properties of synaptic transmission. Because of the LTP associated reduction of PPF, potentiated inputs profit less from temporal summation, favouring transmission of synchronized, low frequency activity.

[1]  B. Katz,et al.  The role of calcium in neuromuscular facilitation , 1968, The Journal of physiology.

[2]  B L McNaughton,et al.  Long‐term synaptic enhancement and short‐term potentiation in rat fascia dentata act through different mechanisms , 1982, The Journal of physiology.

[3]  L. Voronin,et al.  Long-term potentiation in the hippocampus , 1983, Neuroscience.

[4]  Robert K. S. Wong,et al.  Latent synaptic pathways revealed after tetanic stimulation in the hippocampus , 1987, Nature.

[5]  Graham L. Collingridge,et al.  Temporally distinct pre- and post-synaptic mechanisms maintain long-term potentiation , 1989, Nature.

[6]  Gary Lynch,et al.  Evidence that changes in presynaptic calcium currents are not responsible for long-term potentiation in hippocampus , 1989, Brain Research.

[7]  R. Llinás,et al.  Postsynaptic Hebbian and non-Hebbian long-term potentiation of synaptic efficacy in the entorhinal cortex in slices and in the isolated adult guinea pig brain. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[8]  R. Nicoll,et al.  Comparison of two forms of long-term potentiation in single hippocampal neurons. , 1990, Science.

[9]  J Larson,et al.  Mossy fiber potentiation and long‐term potentiation involve different expression mechanisms , 1990, Synapse.

[10]  W. Singer,et al.  Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex , 1990, Nature.

[11]  Ulrich Kuhnt,et al.  Long-term potentiation affects facilitation ratio of EPSPs recorded from CA1 pyramidal cells in the guinea pig hippocampal slice. , 1990 .

[12]  B. McNaughton,et al.  Long‐term enhancement of CA1 synaptic transmission is due to increased quantal size, not quantal content , 1991, Hippocampus.

[13]  Hiroshi Kato,et al.  Reversal of long-term potentiation (depotentiation) induced by tetanus stimulation of the input to CA1 neurons of guinea pig hippocampal slices , 1991, Brain Research.

[14]  A. Marty,et al.  Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents , 1991, Neuron.

[15]  Dimitri M. Kullmann,et al.  Ca2+ Entry via postsynaptic voltage-sensitive Ca2+ channels can transiently potentiate excitatory synaptic transmission in the hippocampus , 1992, Neuron.

[16]  K. Stratford,et al.  Presynaptic release probability influences the locus of long-term potentiation , 1992, Nature.

[17]  U Kuhnt,et al.  Presynaptic calcium transients evoked by paired‐pulse stimulation in the hippocampal slice , 1992, Neuroreport.

[18]  C. Armstrong,et al.  Inhibitory synaptic currents in rat cerebellar Purkinje cells: modulation by postsynaptic depolarization. , 1992, The Journal of physiology.

[19]  Tadaharu Tsumoto,et al.  Long-term potentiation and long-term depression in the neocortex , 1992, Progress in Neurobiology.

[20]  Y. Ben-Ari,et al.  Biochemical correlates of long-term potentiation in hippocampal synapses. , 1993, International review of neurobiology.

[21]  W. Singer,et al.  Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation , 1993, Trends in Neurosciences.

[22]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[23]  R. Nicoll,et al.  NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms , 1993, Trends in Neurosciences.

[24]  R. Nicoll,et al.  Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. , 1993, Journal of neurophysiology.

[25]  J. Sweatt,et al.  Nitric oxide synthase-independent long-term potentiation in area CA1 of hippocampus. , 1993, Neuroreport.

[26]  Yy Huang,et al.  Examination of TEA-induced synaptic enhancement in area CA1 of the hippocampus: the role of voltage-dependent Ca2+ channels in the induction of LTP , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  L. Voronin.  Quantal Analysis of Hippocampal Long-Term Potentiation , 1994, Reviews in the neurosciences.

[28]  Y. Komatsu,et al.  Age-dependent long-term potentiation of inhibitory synaptic transmission in rat visual cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  B L McNaughton,et al.  Persistent increase of hippocampal presynaptic axon excitability after repetitive electrical stimulation: dependence on N-methyl-D-aspartate receptor activity, nitric-oxide synthase, and temperature. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[30]  P. Saggau,et al.  Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  U. Kuhnt,et al.  Interaction between paired-pulse facilitation and long-term potentiation in area ca1 of guinea-pig hippocampal slices: Application of quantal analysis , 1994, Neuroscience.

[32]  D. Johnston,et al.  Changes in paired-pulse facilitation suggest presynaptic involvement in long-term potentiation , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  Y. Yoshimura,et al.  Dependence of LTP induction on postsynaptic depolarization: a perforated patch-clamp study in visual cortical slices of young rats. , 1994, Journal of neurophysiology.

[34]  W. Abraham,et al.  Differential regulation of paired-pulse plasticity following LTP in the dentate gyrus. , 1994, Neuroreport.

[35]  W Singer,et al.  Induction of LTP and LTD in visual cortex neurones by intracellular tetanization , 1994, Neuroreport.

[36]  U. Kuhnt,et al.  Long term enhancement of synaptic transmission in the hippocampus after tetanization of single neurons by short intracellular current pulses , 1994 .

[37]  R. Tsien,et al.  Presynaptic component of long-term potentiation visualized at individual hippocampal synapses. , 1995, Science.

[38]  Y Otsu,et al.  Hebbian induction of LTP in visual cortex: perforated patch-clamp study in cultured neurons. , 1995, Journal of neurophysiology.

[39]  B. Alger,et al.  GABAergic and developmental influences on homosynaptic LTD and depotentiation in rat hippocampus , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  W Singer,et al.  All‐or‐none Excitatory Postsynaptic Potentials in the Rat Visual Cortex , 1995, The European journal of neuroscience.

[41]  Frances A. Edwards,et al.  LTP — a structural model to explain the inconsistencies , 1995, Trends in Neurosciences.

[42]  M. Volgushev,et al.  Neurophysiological analysis of long-term potentiation in mammalian brain , 1995, Behavioural Brain Research.

[43]  S. Siegelbaum,et al.  Regulation of hippocampal transmitter release during development and long-term potentiation. , 1995, Science.

[44]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[45]  D. Linden,et al.  Long-term synaptic depression. , 1995, Annual review of neuroscience.

[46]  W. Singer.  Development and plasticity of cortical processing architectures. , 1995, Science.

[47]  Robert S. Zucker,et al.  Postsynaptic Levels of [Ca2+]i Needed to Trigger LTD and LTP , 1996, Neuron.

[48]  L. Bindman,et al.  Intracellular studies of heterosynaptic long‐term depression (LTD) in CA1 of hippocampal slices , 1996, Hippocampus.

[49]  H. Markram,et al.  Redistribution of synaptic efficacy between neocortical pyramidal neurons , 1996, Nature.

[50]  W. Singer,et al.  Modification of discharge patterns of neocortical neurons by induced oscillations of the membrane potential , 1998, Neuroscience.