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Persistent barrage firing in cortical interneurons can be induced in vivo and may be important for the suppression of epileptiform activity

Neural circuits are typically maintained in a state of dynamic equilibrium by balanced synaptic excitation and inhibition. However, brain regions that are particularly susceptible to epilepsy may have evolved additional specialized mechanisms for inhibiting over-excitation. Here we identify one such...

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Autores principales: Suzuki, Norimitsu, Tang, Clara S.-M., Bekkers, John M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3952511/
https://www.ncbi.nlm.nih.gov/pubmed/24659955
http://dx.doi.org/10.3389/fncel.2014.00076
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author Suzuki, Norimitsu
Tang, Clara S.-M.
Bekkers, John M.
author_facet Suzuki, Norimitsu
Tang, Clara S.-M.
Bekkers, John M.
author_sort Suzuki, Norimitsu
collection PubMed
description Neural circuits are typically maintained in a state of dynamic equilibrium by balanced synaptic excitation and inhibition. However, brain regions that are particularly susceptible to epilepsy may have evolved additional specialized mechanisms for inhibiting over-excitation. Here we identify one such possible mechanism in the cerebral cortex and hippocampus of mice. Recently it was reported that some types of GABAergic interneurons can slowly integrate excitatory inputs until eventually they fire persistently in the absence of the original stimulus. This property, called persistent firing or retroaxonal barrage firing (BF), is of unknown physiological importance. We show that two common types of interneurons in cortical regions, neurogliaform (NG) cells and fast-spiking (FS) cells, are unique in exhibiting BF in acute slices (~85 and ~23% success rate for induction, respectively). BF can also be induced in vivo, although the success rate for induction is lower (~60% in NG cells). In slices, BF could reliably be triggered by trains of excitatory synaptic input, as well as by exposure to proconvulsant bath solutions (elevated extracellular K(+), blockade of GABA(A) receptors). Using pair recordings in slices, we confirmed that barrage-firing NG cells can produce synaptic inhibition of nearby pyramidal neurons, and that this inhibition outlasts the original excitation. The ubiquity of NG and FS cells, together with their ability to fire persistently following excessive excitation, suggests that these interneurons may function as cortical sentinels, imposing an activity-dependent brake on undesirable neuronal hyperexcitability.
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spelling pubmed-39525112014-03-21 Persistent barrage firing in cortical interneurons can be induced in vivo and may be important for the suppression of epileptiform activity Suzuki, Norimitsu Tang, Clara S.-M. Bekkers, John M. Front Cell Neurosci Neuroscience Neural circuits are typically maintained in a state of dynamic equilibrium by balanced synaptic excitation and inhibition. However, brain regions that are particularly susceptible to epilepsy may have evolved additional specialized mechanisms for inhibiting over-excitation. Here we identify one such possible mechanism in the cerebral cortex and hippocampus of mice. Recently it was reported that some types of GABAergic interneurons can slowly integrate excitatory inputs until eventually they fire persistently in the absence of the original stimulus. This property, called persistent firing or retroaxonal barrage firing (BF), is of unknown physiological importance. We show that two common types of interneurons in cortical regions, neurogliaform (NG) cells and fast-spiking (FS) cells, are unique in exhibiting BF in acute slices (~85 and ~23% success rate for induction, respectively). BF can also be induced in vivo, although the success rate for induction is lower (~60% in NG cells). In slices, BF could reliably be triggered by trains of excitatory synaptic input, as well as by exposure to proconvulsant bath solutions (elevated extracellular K(+), blockade of GABA(A) receptors). Using pair recordings in slices, we confirmed that barrage-firing NG cells can produce synaptic inhibition of nearby pyramidal neurons, and that this inhibition outlasts the original excitation. The ubiquity of NG and FS cells, together with their ability to fire persistently following excessive excitation, suggests that these interneurons may function as cortical sentinels, imposing an activity-dependent brake on undesirable neuronal hyperexcitability. Frontiers Media S.A. 2014-03-13 /pmc/articles/PMC3952511/ /pubmed/24659955 http://dx.doi.org/10.3389/fncel.2014.00076 Text en Copyright © 2014 Suzuki, Tang and Bekkers. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Suzuki, Norimitsu
Tang, Clara S.-M.
Bekkers, John M.
Persistent barrage firing in cortical interneurons can be induced in vivo and may be important for the suppression of epileptiform activity
title Persistent barrage firing in cortical interneurons can be induced in vivo and may be important for the suppression of epileptiform activity
title_full Persistent barrage firing in cortical interneurons can be induced in vivo and may be important for the suppression of epileptiform activity
title_fullStr Persistent barrage firing in cortical interneurons can be induced in vivo and may be important for the suppression of epileptiform activity
title_full_unstemmed Persistent barrage firing in cortical interneurons can be induced in vivo and may be important for the suppression of epileptiform activity
title_short Persistent barrage firing in cortical interneurons can be induced in vivo and may be important for the suppression of epileptiform activity
title_sort persistent barrage firing in cortical interneurons can be induced in vivo and may be important for the suppression of epileptiform activity
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3952511/
https://www.ncbi.nlm.nih.gov/pubmed/24659955
http://dx.doi.org/10.3389/fncel.2014.00076
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