Contribution of near-threshold currents to intrinsic oscillatory activity in rat medial entorhinal cortex layer II stellate cells

Boehlen, Anne; Henneberger, Christian; Heinemann, Uwe; Erchova, Irina

doi:10.1152/jn.00743.2011

Cited by 40 publications

(40 citation statements)

References 89 publications

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“…The presence of G NaP necessarily contributes a nonlinearity to the subthreshold response properties of these neurons: membrane impedance is thus a function of membrane voltage, increasing as a neuron is depolarized towards spike threshold. Here, our results are consistent with prior findings showing the characteristic membrane impedance spectrum of entorhinal stellate cells (Erchova et al, ; Nolan et al, ) and the role of TTX‐sensitive currents in the impedance spectrum (Boehlen et al, ).…”

Section: Resultssupporting

confidence: 93%

“…In agreement with previous studies (Erchova et al, ; Nolan et al, ; Boehlen et al, ), we have demonstrated that the subthreshold impedance of stellate neurons in the MEC Layer II is sensitive to voltage and that this dependence is brought about by the successive activation of increasing numbers of non‐inactivating, “persistent” sodium channels in response to membrane depolarization. The effect of this nonlinearity is an increase in membrane impedance, particularly near the theta frequency band, as spike threshold is approached (Fig.…”

Section: Discussionsupporting

confidence: 93%

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

2014

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Stellate cells (SCs) of the medial entorhinal cortex exhibit robust spontaneous membrane-potential oscillations (MPOs) in the theta (4–12 Hz) frequency band as well as theta-frequency resonance in their membrane impedance spectra. Past experimental and modeling work suggests that these features may contribute to the phase-locking of SCs to the entorhinal theta rhythm and may be important for forming the hexagonally tiled grid cell place fields exhibited by these neurons in vivo. Among the major biophysical mechanisms contributing to MPOs is a population of persistent (non-inactivating or slowly inactivating) sodium channels. The resulting persistent sodium conductance (GNaP) gives rise to an apparent increase in input resistance as the cell approaches threshold. In this study, we used dynamic clamp to test the hypothesis that this increased input resistance gives rise to voltage-dependent, and thus MPO phase-dependent, changes in the amplitude of excitatory and inhibitory post-synaptic potential (PSP) amplitudes. We find that PSP amplitude depends on membrane potential, exhibiting a 5–10% increase in amplitude per mV depolarization. The effect is larger than—and sums quasi-linearly with—the effect of the synaptic driving force, V – Esyn. Given that input-driven MPOs 10 mV in amplitude are commonly observed in MEC stellate cells in vivo, this voltage- and phase-dependent synaptic gain is large enough to modulate PSP amplitude by over 50% during theta-frequency MPOs. Phase-dependent synaptic gain may therefore impact the phase locking and phase precession of grid cells in vivo to ongoing network oscillations.

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Section: Resultssupporting

confidence: 93%

Section: Discussionsupporting

confidence: 93%

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

2014

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“…; Boehlen et al . ). We found that the independent presence of NaP channels altered the CDW and modulated the STA and its weak delta‐frequency selectivity that is mediated by the spike‐generating conductances (Das & Narayanan, ).…”

Section: Resultsmentioning

confidence: 99%

“…We next turned our attention to the NaP channels, which are important regulators of neuronal excitability and temporal summation in several neuronal subtypes, including the hippocampal CA1 pyramidal neurons (French et al 1990;Crill, 1996;Andreasen & Lambert, 1999;Astman et al 2006;Vervaeke et al 2006;Royeck et al 2008). NaP channels are regenerative conductances that are known to amplify subthreshold resonance and facilitate intrinsic oscillations when co-expressed with resonating conductances (Hutcheon et al 1994(Hutcheon et al , 1996Hu et al 2002;Boehlen et al 2013). We found that the independent presence of NaP channels altered the CDW and modulated the STA and its weak delta-frequency selectivity that is mediated by the spike-generating J Physiol 593.16 conductances (Das & Narayanan, 2014).…”

Section: Nap Channels Sharpened the Coincidence Detection Window And mentioning

confidence: 99%

Active dendrites mediate stratified gamma‐range coincidence detection in hippocampal model neurons

Das

Narayanan

2015

The Journal of Physiology

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Key pointsr Quantitative metrics for the temporal window of integration/coincidence detection, based on the spike-triggered average, were employed to assess the emergence and dependence of gamma-range coincidence detection in hippocampal pyramidal neurons on various ion channel combinations.r The presence of hyperpolarization-activated cyclic nucleotide-gated (HCN) channels decreased the coincidence detection window (CDW) of the neuronal compartment to the gamma frequency range. Interaction of HCN channels with T-type calcium channels and persistent sodium channels further reduced the CDW, whereas interaction with A-type potassium channels broadened the CDW.r When multiple channel gradients were co-expressed, the high density of resonating conductances in the distal dendrites led to a slow gamma CDW in the proximal dendrites and a fast-gamma CDW in the distal dendrites.r The presence of resonating and spike-generating conductances serve as a mechanism underlying the emergence of stratified gamma-range coincidence detection in the dendrites of CA1 pyramidal neurons, enabling them to perform behaviour-and state-dependent gamma frequency multiplexing.Abstract Hippocampal pyramidal neurons exhibit gamma-phase preference in their spikes, selectively route inputs through gamma frequency multiplexing and are considered part of gamma-bound cell assemblies. How do these neurons exhibit gamma-frequency coincidence detection capabilities, a feature that is essential for the expression of these physiological observations, despite their slow membrane time constant? In this conductance-based modelling study, we developed quantitative metrics for the temporal window of integration/coincidence detection based on the spike-triggered average (STA) of the neuronal compartment. We employed these metrics in conjunction with quantitative measures for spike initiation dynamics to assess the emergence and dependence of coincidence detection and STA spectral selectivity on various ion channel combinations. We found that the presence of resonating conductances (hyperpolarization-activated cyclic nucleotide-gated or T-type calcium), either independently or synergistically when expressed together, led to the emergence of spectral selectivity in the spike initiation dynamics and a significant reduction in the coincidence detection window (CDW). The presence of A-type potassium channels, along with resonating conductances, reduced the STA characteristic frequency and broadened the CDW, but persistent sodium channels sharpened the CDW by strengthening the spectral selectivity in the STA. Finally, in a morphologically precise model endowed with experimentally constrained channel gradients, we found that somatodendritic compartments expressed functional maps of strong theta-frequency selectivity in spike initiation dynamics and gamma-range CDW. Our results reveal the heavy expression of resonating and spike-generating conductances as the mechanism underlying the robust emergence of stratified gamma-range coincidence detection in the dendrites o...

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“…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.…”

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confidence: 99%

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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Contribution of near-threshold currents to intrinsic oscillatory activity in rat medial entorhinal cortex layer II stellate cells

Cited by 40 publications

References 89 publications

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

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

Active dendrites mediate stratified gamma‐range coincidence detection in hippocampal model neurons

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

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