Persistent sodium channel activity mediates subthreshold membrane potential oscillations and low-threshold spikes in rat entorhinal cortex layer V neurons
Section snippets
Slice preparation
The procedures for slice preparation and intracellular recording were followed according to previously published procedures.1 All efforts were made to minimize both the suffering and the number of animals used, and all the experiments were carried out in accordance with the Canadian Council on Animal Care guidelines on the ethical use of animals. In brief, young adult male Long–Evans rats (postnatal days 35–50; Charles River, Quebec, Canada) were decapitated, the brains were removed and a block
Current-clamp analysis of low-threshold, tetrodotoxin-sensitive responses in entorhinal cortex layer V neurons
In a recent study, we have shown that although principal neurons in layer V of the medial EC can be grouped into three distinct morphological categories, the three categories of cells share a number of electrophysiological attributes. The latter include inward rectification in the depolarizing direction and the ability of many of the cells to generate rhythmic, subthreshold membrane potential oscillations and/or slow low-threshold depolarizing potentials that can trigger spike doublets.20
It has
Discussion
The results of the present study demonstrate that the subthreshold intrinsic excitability of EC layer V neurons is largely dominated by a low-threshold sustained sodium current (INaP), which appears to be mainly due to “persistent” sodium channel activity similar to that described previously in EC layer II principal cells.38 Under current-clamp conditions, this voltage-gated “persistent” sodium channel activity causes pronounced inward rectification in the depolarizing direction and is
Acknowledgements
This work has been supported by the Canadian Institutes of Health Research, HFSPO and the North Atlantic Treaty Organization.
References (71)
- et al.
Structure and function of the beta 2 subunit of brain sodium channels, a transmembrane glycoprotein with a CAM motif
Cell
(1995) - et al.
Synchronous discharges in the rat entorhinal cortex in vitro: site of initiation and the role of excitatory amino acid receptors
Neuroscience
(1990) - et al.
Cloning, localization, and functional expression of sodium channel beta1A subunits
J. biol. Chem.
(2000) - et al.
Persistent sodium currents through brain sodium channels induced by G protein betagamma subunits
Neuron
(1997) - et al.
Epileptiform activity induced by pilocarpine in the rat hippocampal–entorhinal slice preparation
Neuroscience
(1996) - et al.
Sodium channels as molecular targets for antiepileptic drugs
Brain Res. Rev.
(1998) - et al.
Subthreshold membrane potential oscillations in neurons of deep layers of the entorhinal cortex
Neuroscience
(1998) Memory systems
C. r. hebd Séanc. Acad. Sci. III
(1998)- et al.
Negative slope conductance due to a persistent subthreshold sodium current in cat neocortical neurons in vitro
Brain Res.
(1982) - et al.
Reverberatory seizure discharges in hippocampal–parahippocampal circuits
Expl Neurol.
(1992)
Na+ currents that fail to inactivate
Trends Neurosci.
Na+ channels as targets for neuroprotective drugs
Trends pharmac. Sci.
Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections
Brain Res.
Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region
Prog. Neurobiol.
Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II
J. Neurophysiol.
Subthreshold Na+-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II
Nature
Modal gating of Na+ channels as a mechanism of persistent Na+ current in pyramidal neurons from rat and cat sensorimotor cortex
J. Neurosci.
Responses of the superficial entorhinal cortex in vitro in slices from naive and chronically epileptic rats
J. Neurophysiol.
Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat
J. comp. Neurol.
The hippocampo-neocortical dialogue
Cerebral Cortex
Hippocampus–entorhinal cortex loop and seizure generation in the young rodent limbic system
J. Neurophysiol.
High-frequency oscillations in the output networks of the hippocampal–entorhinal axis of the freely behaving rat
J. Neurosci.
H.M.’s medial temporal lobe: findings from magnetic resonance imaging
J. Neurosci.
Persistent sodium current in mammalian central neurons
A. Rev. Physiol.
Muscarinic induction of synchronous population activity in the entorhinal cortex
J. Neurosci.
Properties and role of I(h) in the pacing of subthreshold oscillations in entorhinal cortex layer II neurons
J. Neurophysiol.
Entorhinal cortex of the rat: organization of intrinsic connections
J. comp. Neurol.
Entorhinal cortex of the rat: topographic organization of the cells of origin of the perforant path projection to the dentate gyrus
J. comp. Neurol.
Regional and time dependent variations of low Mg2+ induced epileptiform activity in rat temporal cortex slices
Expl Brain Res.
Kinetics of slow inactivation of persistent sodium current in layer V neurons of mouse neocortical slices
J. Neurophysiol.
A voltage-dependent persistent sodium current in mammalian hippocampal neurons
J. gen. Physiol.
Subthreshold inward membrane currents in guinea-pig frontal cortex neurons
Neuroscience
Subthreshold oscillations and resonant frequency in guinea-pig cortical neurons: physiology and modeling
J. Physiol., Lond.
Morphological and electrophysiological characteristics of layer V neurons of the rat medial entorhinal cortex
J. comp. Neurol.
Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches
Pflügers Arch.
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Permanent address: Dipartimento di Scienze Fisiologiche-Farmacologiche-Cellulari-Molecolari, Sezione di Fisiologia Generale e Biofisica Cellulare, Università degli Studi di Pavia, via Forlanini 6, 27100 Pavia, Italy.