Membrane potential‐dependent integration of synaptic inputs in entorhinal stellate neurons

Economo, Michael N.; Martínez, Joan José; White, John A.

doi:10.1002/hipo.22329

Cited by 12 publications

(18 citation statements)

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“…EPSP amplification was observed upon the injection of both an artificial I NaP or a linear negative conductance after TTX application, using the dynamic clamp method (Ceballos et al 2017;Economo et al 2014). Further evidence supporting the hypothesis that the negative slope conductance of I NaP prolongs EPSP decay is provided by the recently proposed quasi-active cable theory approximation (Remme and Rinzel 2011).…”

Section: Negative Slope Conductance Amplifies Postsynaptic Potentialsmentioning

confidence: 64%

“…The amplification of EPSPs by I NaP has been extensively observed in neurons from the neocortex (Andreasen and Lambert 1999;Carter et al 2012;Deisz et al 1991;Fricker and Miles 2000;González-Burgos and Barrionuevo 2001;Hirsch and Gilbert 1991;Lipowsky et al 1996;Rotaru et al 2007;Schwindt and Crill 1995;Stafstrom et al 1985;Stuart and Sakmann 1995;Thomson et al 1988;Zsiros and Hestrin 2005), hippocampus (Ceballos et al 2017;Urban et al 1998;Vervaeke et al 2006), entorhinal cortex (Economo et al 2014;Rosenkranz and Johnston 2007), dorsal cochlear nucleus (Hirsch and Oertel 1988), subthalamic nucleus (Farries et al 2010), hypothalamus (Branco et al 2016), olfactory bulb (Liu and Shipley 2008), dorsal horn of the spinal cord (Prescott and De Koninck 2005), medial superior olive and substantia nigra pars compacta (Yamashita and Isa 2004). In most of these experiments, blocking I NaP with TTX abolished the voltage dependence of the EPSP amplitude and area.…”

Section: Negative Slope Conductance Amplifies Postsynaptic Potentialsmentioning

confidence: 99%

“…For example, I NaP amplifies IPSPs in neocortical pyramidal neurons (Stuart 1999;Williams and Stuart 2003), hippocampal pyramidal neurons (Hardie and Pearce 2006) and stellate cells of the medial entorhinal cortex (Economo et al 2014). Ca ++ currents also amplify IPSPs in cat motoneurons (Bui et al 2008).…”

Section: Negative Slope Conductance Amplifies Postsynaptic Potentialsmentioning

confidence: 99%

“…It has been observed that I NaP increases the impedance of neurons (Boehlen et al 2012;Curti et al 2008;Economo et al 2014;Gutfreund and Segev 1995;Hu et al 2002;Hutcheon et al 1996a;Hutcheon et al 1996b;Jacobson et al 2005;Klink and Alonso 1997;Manuel et al 2007;Pape and Driesang 1998;Saint Mleux and Moore 2000;Sun et al 2014;Wu et al 2001;Wu et al 2005;Yang et al 2009;Yaron-Jakoubovitch et al 2008). This increase in the membrane impedance is thus a function of membrane voltage, increasing as the neuron is depolarized towards the spike threshold.…”

mentioning

confidence: 99%

“…It has been observed in several types of neurons that R m and τ m increase in a voltage-dependent manner and that this effect is abolished by tetrodotoxin (TTX) application (Agrawal et al 2001;Curti et al 2008;Economo et al 2014;Fernandez et al 2015;Hirsch and Oertel 1988;Klink and Alonso 1993;Stafstrom et al 1982;Yamada-Hanff and Bean 2015). The authors of these studies suggested that the negative slope conductance region generated by I NaP caused this paradoxical increase in R m .…”

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confidence: 99%

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The role of negative conductances in neuronal subthreshold properties and synaptic integration

2017

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Based on passive cable theory, an increase in membrane conductance produces a decrease in the membrane time constant and input resistance. Unlike the classical leak currents, voltage-dependent currents have a nonlinear behavior which can create regions of negative conductance, despite the increase in membrane conductance (permeability). This negative conductance opposes the effects of the passive membrane conductance on the membrane input resistance and time constant, increasing their values and thereby substantially affecting the amplitude and time course of postsynaptic potentials at the voltage range of the negative conductance. This paradoxical effect has been described for three types of voltage-dependent inward currents: persistent sodium currents, L-and T-type calcium currents and ligand-gated glutamatergic N-methyl-D-aspartate currents. In this review, we describe the impact of the creation of a negative conductance region by these currents on neuronal membrane properties and synaptic integration. We also discuss recent contributions of the quasi-active cable approximation, an extension of the passive cable theory that includes voltage-dependent currents, and its effects on neuronal subthreshold properties.

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Section: Negative Slope Conductance Amplifies Postsynaptic Potentialsmentioning

confidence: 64%

Section: Negative Slope Conductance Amplifies Postsynaptic Potentialsmentioning

confidence: 99%

Section: Negative Slope Conductance Amplifies Postsynaptic Potentialsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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The role of negative conductances in neuronal subthreshold properties and synaptic integration

2017

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A Negative Slope Conductance of the Persistent Sodium Current Prolongs Subthreshold Depolarizations

Ceballos

Roque

Leão

2017

Biophysical Journal

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Neuronal subthreshold voltage-dependent currents determine membrane properties such as the input resistance (R) and the membrane time constant (τ) in the subthreshold range. In contrast with classical cable theory predictions, the persistent sodium current (I), a non-inactivating mode of the voltage-dependent sodium current, paradoxically increases R and τ when activated. Furthermore, this current amplifies and prolongs synaptic currents in the subthreshold range. Here, using a computational neuronal model, we showed that the creation of a region of negative slope conductance by I activation is responsible for these effects and the ability of the negative slope conductance to amplify and prolong R and τ relies on the fast activation of I. Using dynamic clamp in hippocampal CA1 pyramidal neurons in brain slices, we showed that the effects of I on R and τ can be recovered by applying an artificial I after blocking endogenous I with tetrodotoxin. Furthermore, we showed that injection of a pure negative conductance is enough to reproduce the effects of I on R and τ and is also able to prolong artificial excitatory post synaptic currents. Since both the negative slope conductance and the almost instantaneous activation are critical for producing these effects, the I is an ideal current for boosting the amplitude and duration of excitatory post synaptic currents near the action potential threshold.

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The Creation of A Negative Slope Conductance Region by the activation of The Persistent Sodium Current Prolongs Near-Threshold Synaptic Potentials

Ceballos

Roque

Leão

2016

Preprint

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A change of the input resistance (R in ) of the neuron involves a change in the membrane conductances by opening and closing of ion channels. In passive membranes, i.e., membranes with only linear leak conductances, the increase or decrease of these conductances leads to a decrease or increase of the R in and the membrane time constant (τ m ). However, the presence of subthreshold voltage dependent currents can produce non-linear effects generating deviations from this relationship, especially the contradictory effect of negative conductances, as produced by the sodium-persistent current (I NaP ), on the R in . In this work we aimed to analyze experimentally and theoretically the impact of the negative conductance produced by I NaP on R in . Experiments of whole-cell patch-clamp conducted in CA1 hippocampus pyramidal cells from brain slices showed a paradoxical voltage-dependent decrease of the R in and the τ m in subthreshold membrane potentials close to the firing threshold after the perfusion with TTX, which inhibits I NaP . This effect is postulated to be a result of the negative slope conductance in the subthreshold region produced by this conductance. The analysis of the experimental data, together with simulations found that the slope conductance of I NaP is negative for subthreshold membrane potentials and its magnitude is voltage dependent in the same range observed for the voltage-dependence of R in and τ m . The injection of an artificial I NaP using dynamic-clamp in the presence of TTX restored the R in and τ m to its original values.Additionally the injection of an artificial leak current with a negative conductance in the presence of TTX restored the R in and τ m as the artificial I nap did. On the other hand, the injection of an artificial leak current

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Membrane potential‐dependent integration of synaptic inputs in entorhinal stellate neurons

Cited by 12 publications

References 82 publications

The role of negative conductances in neuronal subthreshold properties and synaptic integration

The role of negative conductances in neuronal subthreshold properties and synaptic integration

A Negative Slope Conductance of the Persistent Sodium Current Prolongs Subthreshold Depolarizations

The Creation of A Negative Slope Conductance Region by the activation of The Persistent Sodium Current Prolongs Near-Threshold Synaptic Potentials

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