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T‐type calcium channels contribute to NMDA receptor independent synaptic plasticity in hippocampal regular‐spiking oriens‐alveus interneurons

KEY POINTS: Regular‐spiking interneurons in the hippocampal stratum oriens exhibit a form of long‐term potentiation of excitatory transmission that is independent of NMDA receptors but requires co‐activation of Ca(2+)‐permeable AMPA receptors and group I metabotropic glutamate receptors. We show tha...

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Autores principales: Nicholson, Elizabeth, Kullmann, Dimitri M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5451714/
https://www.ncbi.nlm.nih.gov/pubmed/28134447
http://dx.doi.org/10.1113/JP273695
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author Nicholson, Elizabeth
Kullmann, Dimitri M.
author_facet Nicholson, Elizabeth
Kullmann, Dimitri M.
author_sort Nicholson, Elizabeth
collection PubMed
description KEY POINTS: Regular‐spiking interneurons in the hippocampal stratum oriens exhibit a form of long‐term potentiation of excitatory transmission that is independent of NMDA receptors but requires co‐activation of Ca(2+)‐permeable AMPA receptors and group I metabotropic glutamate receptors. We show that T‐type Ca(2+) channels are present in such interneurons. Blockade of T‐type currents prevents the induction of long‐term potentiation, and also interferes with long‐lasting potentiation induced either by postsynaptic trains of action potentials or by pairing postsynaptic hyperpolarization with activation of group I metabotropic receptors. Several Ca(2+) sources thus converge on the induction of NMDA receptor independent synaptic plasticity. ABSTRACT: NMDA receptor independent long‐term potentiation (LTP) in hippocampal stratum oriens‐alveus (O/A) interneurons requires co‐activation of postsynaptic group I metabotropic glutamate receptors (mGluRs) and Ca(2+)‐permeable AMPA receptors. The rectification properties of such AMPA receptors contribute to the preferential induction of LTP at hyperpolarized potentials. A persistent increase in excitatory transmission can also be triggered by exogenous activation of group I mGluRs at the same time as the interneuron is hyperpolarized, or by postsynaptic trains of action potentials in the absence of presynaptic stimulation. In the present study, we identify low‐threshold transient (T‐type) channels as a further source of Ca(2+) that contributes to synaptic plasticity. T‐type Ca(2+) currents were detected in mouse regular‐spiking O/A interneurons. Blocking T‐type currents pharmacologically prevented LTP induced by high‐frequency stimulation of glutamatergic axons, or by application of the group I mGluR agonist dihydroxyphenylglycine, paired with postsynaptic hyperpolarization. T‐type current blockade also prevented synaptic potentiation induced by postsynaptic action potential trains. Several sources of Ca(2+) thus converge on NMDA receptor independent LTP induction in O/A interneurons.
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spelling pubmed-54517142017-06-02 T‐type calcium channels contribute to NMDA receptor independent synaptic plasticity in hippocampal regular‐spiking oriens‐alveus interneurons Nicholson, Elizabeth Kullmann, Dimitri M. J Physiol Neuroscience ‐ Cellular/Molecular KEY POINTS: Regular‐spiking interneurons in the hippocampal stratum oriens exhibit a form of long‐term potentiation of excitatory transmission that is independent of NMDA receptors but requires co‐activation of Ca(2+)‐permeable AMPA receptors and group I metabotropic glutamate receptors. We show that T‐type Ca(2+) channels are present in such interneurons. Blockade of T‐type currents prevents the induction of long‐term potentiation, and also interferes with long‐lasting potentiation induced either by postsynaptic trains of action potentials or by pairing postsynaptic hyperpolarization with activation of group I metabotropic receptors. Several Ca(2+) sources thus converge on the induction of NMDA receptor independent synaptic plasticity. ABSTRACT: NMDA receptor independent long‐term potentiation (LTP) in hippocampal stratum oriens‐alveus (O/A) interneurons requires co‐activation of postsynaptic group I metabotropic glutamate receptors (mGluRs) and Ca(2+)‐permeable AMPA receptors. The rectification properties of such AMPA receptors contribute to the preferential induction of LTP at hyperpolarized potentials. A persistent increase in excitatory transmission can also be triggered by exogenous activation of group I mGluRs at the same time as the interneuron is hyperpolarized, or by postsynaptic trains of action potentials in the absence of presynaptic stimulation. In the present study, we identify low‐threshold transient (T‐type) channels as a further source of Ca(2+) that contributes to synaptic plasticity. T‐type Ca(2+) currents were detected in mouse regular‐spiking O/A interneurons. Blocking T‐type currents pharmacologically prevented LTP induced by high‐frequency stimulation of glutamatergic axons, or by application of the group I mGluR agonist dihydroxyphenylglycine, paired with postsynaptic hyperpolarization. T‐type current blockade also prevented synaptic potentiation induced by postsynaptic action potential trains. Several sources of Ca(2+) thus converge on NMDA receptor independent LTP induction in O/A interneurons. John Wiley and Sons Inc. 2017-03-22 2017-06-01 /pmc/articles/PMC5451714/ /pubmed/28134447 http://dx.doi.org/10.1113/JP273695 Text en © 2017 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society This is an open access article under the terms of the Creative Commons Attribution (http://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Neuroscience ‐ Cellular/Molecular
Nicholson, Elizabeth
Kullmann, Dimitri M.
T‐type calcium channels contribute to NMDA receptor independent synaptic plasticity in hippocampal regular‐spiking oriens‐alveus interneurons
title T‐type calcium channels contribute to NMDA receptor independent synaptic plasticity in hippocampal regular‐spiking oriens‐alveus interneurons
title_full T‐type calcium channels contribute to NMDA receptor independent synaptic plasticity in hippocampal regular‐spiking oriens‐alveus interneurons
title_fullStr T‐type calcium channels contribute to NMDA receptor independent synaptic plasticity in hippocampal regular‐spiking oriens‐alveus interneurons
title_full_unstemmed T‐type calcium channels contribute to NMDA receptor independent synaptic plasticity in hippocampal regular‐spiking oriens‐alveus interneurons
title_short T‐type calcium channels contribute to NMDA receptor independent synaptic plasticity in hippocampal regular‐spiking oriens‐alveus interneurons
title_sort t‐type calcium channels contribute to nmda receptor independent synaptic plasticity in hippocampal regular‐spiking oriens‐alveus interneurons
topic Neuroscience ‐ Cellular/Molecular
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5451714/
https://www.ncbi.nlm.nih.gov/pubmed/28134447
http://dx.doi.org/10.1113/JP273695
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