Computer simulations of EPSP-spike (E-S) potentiation in hippocampal CA1 pyramidal cells

Wathey, John C.; Lytton, William W.; Jester, Jennifer M.; Sejnowski, Terrence J.

doi:10.1523/jneurosci.12-02-00607.1992

Cited by 44 publications

(20 citation statements)

References 61 publications

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“…We show here that changes in excitability accompany modifications in synaptic efficacy and therefore follow the Bienenstock, Cooper, and Munrow rule (29). E-S P and E-S depotentiation were found to be specific to the stimulated pathway, suggesting that the underlying changes in intrinsic excitability are probably restricted to the active dendritic area (30). Thus, the input specificity conferred by synaptic efficacy is respected and the functional contrast between active and inactive synaptic inputs is not subsequently altered by modifications in the intrinsic excitability.…”

Section: Discussionsupporting

confidence: 56%

Bidirectional plasticity of excitatory postsynaptic potential (EPSP)-spike coupling in CA1 hippocampal pyramidal neurons

Daoudal

Hanada

Debanne

2002

Proc. Natl. Acad. Sci. U.S.A.

137

152

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Integration of synaptic excitation to generate an action potential (excitatory postsynaptic potential-spike coupling or E-S coupling) determines the neuronal output. Bidirectional synaptic plasticity is well established in the hippocampus, but whether active synaptic integration can display potentiation and depression remains unclear. We show here that synaptic depression is associated with an N-methyl-D-aspartate receptor-dependent and long-lasting depression of E-S coupling. E-S depression is input-specific and is expressed in the presence of ␥-aminobutyric acid type A and B receptor antagonists. In single neurons, E-S depression is observed without modification of postsynaptic passive properties. We conclude that a decrease in intrinsic excitability underlies E-S depression and is synergic with glutamatergic long-term depression.I ntegration of synaptic inputs to produce an action potential at the axon hillock is a complex operation that depends on two critical factors: the distribution of voltage-gated ion channels in the dendrites and the passive electrical properties upon which these active channels are superimposed (1). Synaptic potentials have been shown to be shaped by intrinsic voltage-gated conductances located in the dendrites and the soma (2), but the dynamics of active synaptic integration remains poorly understood. We addressed here the question as to whether synaptic integration is modified after induction of long-term synaptic potentiation and depotentiation.In the area CA1, homosynaptic long-term potentiation (LTP) of excitatory synaptic transmission is induced by high-frequency stimulation (HFS, 100 Hz) of the afferent fibers (3). In parallel, the probability of discharge of the postsynaptic neurons in response to a given excitatory postsynaptic potential (EPSP) is enhanced (4-7). This second component has been called EPSPto-Spike potentiation (E-S potentiation, E-S P) which is complementary to LTP and functionally important. The reversal of LTP preserves a potential for network plasticity and appears essential for any model of memory (8). Long-term synaptic depotentiation has been reported in the area CA1 (9), but the reversal of E-S P has never been clearly established (10, 11). We show here that E-S depression (E-S D) is expressed concomitantly with long-term depression (LTD). E-S D is largely independent of synaptic inhibition but requires N-methyl-D-aspartate (NMDA) receptor (NMDAR) activation for its induction. We provide evidence for an activity-dependent decrease of the intrinsic excitability of CA1 pyramidal neurons that acts in synergy with LTD. MethodsSlice Preparation. Hippocampal slices (400 m) were obtained from 3-to 6-week-old rats according to institutional guidelines. Slices were cut in a solution (280 mM sucrose͞26 mM NaHCO 3 ͞10 mM D-glucose͞1.3 mM KCl͞1 mM CaCl 2 ͞10 mM MgCl 2 ), and were maintained for 1 h at room temperature in oxygenated (95% O 2 ͞5% CO 2 ) artificial cerebrospinal fluid (ACSF; 125 mM NaCl͞2.5 mM KCl͞0.8 mM NaH 2 PO 4 ͞26 mM NaHCO 3 ͞3 mM CaCl 2 ͞2 mM Mg...

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Section: Discussionsupporting

confidence: 56%

Bidirectional plasticity of excitatory postsynaptic potential (EPSP)-spike coupling in CA1 hippocampal pyramidal neurons

Daoudal

Hanada

Debanne

2002

Proc. Natl. Acad. Sci. U.S.A.

137

152

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“…In preliminary experiments of this kind (S. Chattarji, unpublished data ; see also ref 36) tetanization of a proximal input to CAI neurons causes potentiation of the population spikes elicited through both the tetanized input and a distal untetanized input, in agreement with the prediction . Recently evidence of a nonspecific component of LTP in CAI neurons has also been reported (37) but it cannot be seen if the tetanized and untetanized inputs are segregated to basal and apical dendrites, respectively, consistent with the simulation results of Figure 9C .…”

Section: Examplessupporting

confidence: 76%

“…does not change ( Figure 8A We used a model to investigate some of the consequences of the hypothesis that E-S potentiation is caused by an increase in postsynaptic excitability . 11 The cellular morphology used in these simulations was identical to that in Figure 2 . The axon and soma were excitable but the dendrites were initially passive .…”

Section: Examplesmentioning

confidence: 99%

Realistic single-neuron modeling

Lytton¹,

Wathey²

1992

Seminars in Neuroscience

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Realistic single-neuron modeling organizes and clarifies physiological hypotheses. It extends the experimenter's intuition and leads to testable predictions . A powerful new algorithm, several user friendly software packages and the advent offast, cheap computers have together made this tool accessible to a broad range of neurobiologists . Equally dramatic advances in experimental findings have increased the level of sophistication of the models . Here we provide a guide to singleneuron modeling, illustrate its power with a few examples and speculate on possible future directions for this rapidly growing field.Key words : computer model / compartmental model / cable model / channel kinetics ALL NEUROPHYSIOLOGISTS are modelers . They may explain the bursting behavior of a neuron in terms of voltage-sensitive calcium currents and a calcium-activated potassium conductance . They may conclude from a complex spike waveform that the cell has excitable dendrites . They may choose to voltage-clamp the cell body to study synaptic currents. Behind each of their experimental designs and interpretations of results lies an implicit hypothesis, a model, of how the neuron works .Here we describe a tool with which these mental models can be transformed into precise and explicit computer simulations . This transformation is in itself a valuable exercise, because it requires a complete list of the relevant biophysical parameters . Compiling this list may immediately reveal important gaps in knowledge . Of far greater value, however, is the expansion of intuition that comes with running many simulations over wide ranges of parameter values .Realistic models at the single-neuron level are primarily concerned with local changes in membrane current and voltage, caused by such things as synaptic input and voltage-sensitive conductances, and with the propagation of these local changes over spatially extensive dendrites and axons . With recent What follows is not a comprehensive review of the subject but rather an overview for the uninitiated . We begin with some intuitive explanations of the biophysical processes being simulated and a guide to the latest simulation software. We then describe a few illustrative models, taken largely from our own work, and conclude with speculations on the future directions of this rapidly growing field . A guide to realistic single-neuron modelsModeling membrane mechanisms Biophysical processes that cause local changes in membrane potential, such as synaptic activation and voltage sensitive conductances, are most easily modeled in a patch of membrane that is spatially isopotential . This is an appropriate model for preparations such as the space-clamped squid axons or neurons that lack dendrites . 2 Such models are best understood in terms of a parallel conductance circuit (Figure 1) . The capacitor represents the electrical capacitance of the membrane, the batteries represent the reversal potentials of the various ionic channels in the membrane and the resistors symbolize the conductances of those chan...

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“…In CA1 hippocampal pyramidal neurons, after induction of LTP, postsynaptic spike firing increases more than would be expected from synaptic LTP, a phenomenon referred to as EPSP-to-spike (E-S) potentiation (Bliss and Lomo, 1973;Andersen et al, 1980). E-S potentiation has been reported to depend on disinhibition (Abraham et al, 1987;Chavez-Noriega et al, 1990), but later studies have suggested a change in the intrinsic excitability (Wathey et al, 1992;Pugliese et al, 1994;Jester et al, 1995;Wang et al, 2003). More recent studies suggest that full expression of E-S potentiation requires both GABA A receptor-mediated disinhibition and intrinsic potentiation (Daoudal et al, 2002;Staff and Spruston, 2003).…”

Section: Introductionmentioning

confidence: 99%

Activity-Dependent Long-Term Potentiation of Intrinsic Excitability in Hippocampal CA1 Pyramidal Neurons

Kang²,

Jiang³

et al. 2005

J. Neurosci.

159

178

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The efficiency of neural circuits is enhanced not only by increasing synaptic strength but also by increasing intrinsic excitability. In contrast to the detailed analysis of long-term potentiation (LTP), less attention has been given to activity-dependent changes in the intrinsic neuronal excitability. By stimulating hippocampal CA1 pyramidal neurons with synaptic inputs correlating with postsynaptic neuronal spikes, we elicited an LTP of intrinsic excitability (LTP-IE) concurring with synaptic LTP. LTP-IE was manifested as a decrease in the action potential threshold that was attributable to a hyperpolarized shift in the activation curve of voltage-gated sodium channels (VGSCs) rather than activity-dependent changes in synaptic inputs or A-type K ϩ channels. Cell-attached patch recording of VGSC activities indicated such an activity-dependent change in VGSCs. Induction of LTP-IE was blocked by the NMDA receptor antagonist APV, intracellular BAPTA, the CaM kinase inhibitors KN-62 and autocamtide-2-related inhibitory peptide, and the protein synthesis inhibitors emetine and anisomycin. The results suggest that induction of LTP-IE shares a similar signaling pathway with the late phase of synaptic LTP and requires activation of the NMDA glutamate receptor subtype, Ca 2ϩ influx, activity of CaM kinase II, and function of the protein synthesis. This new form of hippocampal neuronal plasticity could be a cellular correlate of learning and memory besides synaptic LTP.

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Computer simulations of EPSP-spike (E-S) potentiation in hippocampal CA1 pyramidal cells

Cited by 44 publications

References 61 publications

Bidirectional plasticity of excitatory postsynaptic potential (EPSP)-spike coupling in CA1 hippocampal pyramidal neurons

Bidirectional plasticity of excitatory postsynaptic potential (EPSP)-spike coupling in CA1 hippocampal pyramidal neurons

Realistic single-neuron modeling

Activity-Dependent Long-Term Potentiation of Intrinsic Excitability in Hippocampal CA1 Pyramidal Neurons

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