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Ontogeny of kainate-induced gamma oscillations in the rat CA3 hippocampus in vitro

GABAergic inhibition, which is instrumental in the generation of hippocampal gamma oscillations, undergoes significant changes during development. However, the development of hippocampal gamma oscillations remains largely unknown. Here, we explored the developmental features of kainate-induced oscil...

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Autores principales: Tsintsadze, Vera, Minlebaev, Marat, Suchkov, Dimitry, Cunningham, Mark O., Khazipov, Roustem
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4438719/
https://www.ncbi.nlm.nih.gov/pubmed/26041996
http://dx.doi.org/10.3389/fncel.2015.00195
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author Tsintsadze, Vera
Minlebaev, Marat
Suchkov, Dimitry
Cunningham, Mark O.
Khazipov, Roustem
author_facet Tsintsadze, Vera
Minlebaev, Marat
Suchkov, Dimitry
Cunningham, Mark O.
Khazipov, Roustem
author_sort Tsintsadze, Vera
collection PubMed
description GABAergic inhibition, which is instrumental in the generation of hippocampal gamma oscillations, undergoes significant changes during development. However, the development of hippocampal gamma oscillations remains largely unknown. Here, we explored the developmental features of kainate-induced oscillations (KA-Os) in CA3 region of rat hippocampal slices. Up to postnatal day P5, the bath application of kainate failed to evoke any detectable oscillations. KA-Os emerged by the end of the first postnatal week; these were initially weak, slow (20–25 Hz, beta range) and were poorly synchronized with CA3 units and synaptic currents. Local field potential (LFP) power, synchronization of units and frequency of KA-Os increased during the second postnatal week to attain gamma (30–40 Hz) frequency by P15–21. Both beta and gamma KA-Os are characterized by alternating sinks and sources in the pyramidal cell layer, likely generated by summation of the action potential—associated currents and GABAergic synaptic currents, respectively. Blockade of GABA(A) receptors with gabazine completely suppressed KA-Os at all ages indicating that GABAergic mechanisms are instrumental in their generation. Bumetanide, a NKCC1 chloride co-transporter antagonist which renders GABAergic responses inhibitory in the immature hippocampal neurons, failed to induce KA-Os at P2–4 indicating that the absence of KA-Os in neonates is not due to depolarizing actions of GABA. The linear developmental profile, electrographic features and pharmacological properties indicate that CA3 hippocampal beta and gamma KA-Os are fundamentally similar in their generative mechanisms and their delayed onset and developmental changes likely reflect the development of perisomatic GABAergic inhibition.
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spelling pubmed-44387192015-06-03 Ontogeny of kainate-induced gamma oscillations in the rat CA3 hippocampus in vitro Tsintsadze, Vera Minlebaev, Marat Suchkov, Dimitry Cunningham, Mark O. Khazipov, Roustem Front Cell Neurosci Neuroscience GABAergic inhibition, which is instrumental in the generation of hippocampal gamma oscillations, undergoes significant changes during development. However, the development of hippocampal gamma oscillations remains largely unknown. Here, we explored the developmental features of kainate-induced oscillations (KA-Os) in CA3 region of rat hippocampal slices. Up to postnatal day P5, the bath application of kainate failed to evoke any detectable oscillations. KA-Os emerged by the end of the first postnatal week; these were initially weak, slow (20–25 Hz, beta range) and were poorly synchronized with CA3 units and synaptic currents. Local field potential (LFP) power, synchronization of units and frequency of KA-Os increased during the second postnatal week to attain gamma (30–40 Hz) frequency by P15–21. Both beta and gamma KA-Os are characterized by alternating sinks and sources in the pyramidal cell layer, likely generated by summation of the action potential—associated currents and GABAergic synaptic currents, respectively. Blockade of GABA(A) receptors with gabazine completely suppressed KA-Os at all ages indicating that GABAergic mechanisms are instrumental in their generation. Bumetanide, a NKCC1 chloride co-transporter antagonist which renders GABAergic responses inhibitory in the immature hippocampal neurons, failed to induce KA-Os at P2–4 indicating that the absence of KA-Os in neonates is not due to depolarizing actions of GABA. The linear developmental profile, electrographic features and pharmacological properties indicate that CA3 hippocampal beta and gamma KA-Os are fundamentally similar in their generative mechanisms and their delayed onset and developmental changes likely reflect the development of perisomatic GABAergic inhibition. Frontiers Media S.A. 2015-05-20 /pmc/articles/PMC4438719/ /pubmed/26041996 http://dx.doi.org/10.3389/fncel.2015.00195 Text en Copyright © 2015 Tsintsadze, Minlebaev, Suchkov, Cunningham and Khazipov. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution and 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
Tsintsadze, Vera
Minlebaev, Marat
Suchkov, Dimitry
Cunningham, Mark O.
Khazipov, Roustem
Ontogeny of kainate-induced gamma oscillations in the rat CA3 hippocampus in vitro
title Ontogeny of kainate-induced gamma oscillations in the rat CA3 hippocampus in vitro
title_full Ontogeny of kainate-induced gamma oscillations in the rat CA3 hippocampus in vitro
title_fullStr Ontogeny of kainate-induced gamma oscillations in the rat CA3 hippocampus in vitro
title_full_unstemmed Ontogeny of kainate-induced gamma oscillations in the rat CA3 hippocampus in vitro
title_short Ontogeny of kainate-induced gamma oscillations in the rat CA3 hippocampus in vitro
title_sort ontogeny of kainate-induced gamma oscillations in the rat ca3 hippocampus in vitro
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4438719/
https://www.ncbi.nlm.nih.gov/pubmed/26041996
http://dx.doi.org/10.3389/fncel.2015.00195
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