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      Myelinating satellite oligodendrocytes are integrated in a glial syncytium constraining neuronal high-frequency activity

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          Abstract

          Satellite oligodendrocytes (s-OLs) are closely apposed to the soma of neocortical layer 5 pyramidal neurons but their properties and functional roles remain unresolved. Here we show that s-OLs form compact myelin and action potentials of the host neuron evoke precisely timed Ba 2+-sensitive K + inward rectifying (Kir) currents in the s-OL. Unexpectedly, the glial K + inward current does not require oligodendrocytic Kir4.1. Action potential-evoked Kir currents are in part mediated by gap–junction coupling with neighbouring OLs and astrocytes that form a syncytium around the pyramidal cell body. Computational modelling predicts that glial Kir constrains the perisomatic [K +] o increase most importantly during high-frequency action potentials. Consistent with these predictions neurons with s-OLs showed a reduced probability for action potential burst firing during [K +] o elevations. These data suggest that s-OLs are integrated into a glial syncytium for the millisecond rapid K + uptake limiting activity-dependent [K +] o increase in the perisomatic neuron domain.

          Abstract

          Satellite oligodendrocytes (s-OLs) are characterised by their close proximity to neocortical pyramidal cells. Here, the authors find that s-OLs myelinate axons and activity of host neurons evokes inward K + currents in s-OLs which may work to modulate action potential burst firing by buffering extracellular K + levels.

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          Most cited references 51

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          Myelination and support of axonal integrity by glia.

          The myelination of axons by glial cells was the last major step in the evolution of cells in the vertebrate nervous system, and white-matter tracts are key to the architecture of the mammalian brain. Cell biology and mouse genetics have provided insight into axon-glia signalling and the molecular architecture of the myelin sheath. Glial cells that myelinate axons were found to have a dual role by also supporting the long-term integrity of those axons. This function may be independent of myelin itself. Myelin abnormalities cause a number of neurological diseases, and may also contribute to complex neuropsychiatric disorders.
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            Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus.

            Fast excitatory neurotransmission in the central nervous system occurs at specialized synaptic junctions between neurons, where a high concentration of glutamate directly activates receptor channels. Low-affinity AMPA (alpha-amino-3-hydroxy-5-methyl isoxazole propionic acid) and kainate glutamate receptors are also expressed by some glial cells, including oligodendrocyte precursor cells (OPCs). However, the conditions that result in activation of glutamate receptors on these non-neuronal cells are not known. Here we report that stimulation of excitatory axons in the hippocampus elicits inward currents in OPCs that are mediated by AMPA receptors. The quantal nature of these responses and their rapid kinetics indicate that they are produced by the exocytosis of vesicles filled with glutamate directly opposite these receptors. Some of these AMPA receptors are permeable to calcium ions, providing a link between axonal activity and internal calcium levels in OPCs. Electron microscopic analysis revealed that vesicle-filled axon terminals make synaptic junctions with the processes of OPCs in both the young and adult hippocampus. These results demonstrate the existence of a rapid signalling pathway from pyramidal neurons to OPCs in the mammalian hippocampus that is mediated by excitatory, glutamatergic synapses.
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              A cellular mechanism for cortical associations: an organizing principle for the cerebral cortex.

              A basic feature of intelligent systems such as the cerebral cortex is the ability to freely associate aspects of perceived experience with an internal representation of the world and make predictions about the future. Here, a hypothesis is presented that the extraordinary performance of the cortex derives from an associative mechanism built in at the cellular level to the basic cortical neuronal unit: the pyramidal cell. The mechanism is robustly triggered by coincident input to opposite poles of the neuron, is exquisitely matched to the large- and fine-scale architecture of the cortex, and is tightly controlled by local microcircuits of inhibitory neurons targeting subcellular compartments. This article explores the experimental evidence and the implications for how the cortex operates. Copyright © 2012 Elsevier Ltd. All rights reserved.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                10 May 2016
                2016
                : 7
                Affiliations
                [1 ]Axonal Signalling Group, Netherlands Institute for Neuroscience, Royal Academy of Arts and Sciences , Meibergdreef 47, 1105 BA Amsterdam, The Netherlands
                [2 ]Cell Biology, Department of Biology, Faculty of Science, University of Utrecht , 3584 CH Utrecht, The Netherlands
                Author notes
                Article
                ncomms11298
                10.1038/ncomms11298
                4866043
                27161034
                Copyright © 2016, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

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