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Oligodendrocyte-mediated myelin plasticity and its role in neural synchronization

Temporal synchrony of signals arriving from different neurons or brain regions is essential for proper neural processing. Nevertheless, it is not well understood how such synchrony is achieved and maintained in a complex network of time-delayed neural interactions. Myelin plasticity, accomplished by...

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Autores principales: Pajevic, Sinisa, Plenz, Dietmar, Basser, Peter J, Fields, R Douglas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10132807/
https://www.ncbi.nlm.nih.gov/pubmed/36976252
http://dx.doi.org/10.7554/eLife.81982
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author Pajevic, Sinisa
Plenz, Dietmar
Basser, Peter J
Fields, R Douglas
author_facet Pajevic, Sinisa
Plenz, Dietmar
Basser, Peter J
Fields, R Douglas
author_sort Pajevic, Sinisa
collection PubMed
description Temporal synchrony of signals arriving from different neurons or brain regions is essential for proper neural processing. Nevertheless, it is not well understood how such synchrony is achieved and maintained in a complex network of time-delayed neural interactions. Myelin plasticity, accomplished by oligodendrocytes (OLs), has been suggested as an efficient mechanism for controlling timing in brain communications through adaptive changes of axonal conduction velocity and consequently conduction time delays, or latencies; however, local rules and feedback mechanisms that OLs use to achieve synchronization are not known. We propose a mathematical model of oligodendrocyte-mediated myelin plasticity (OMP) in which OLs play an active role in providing such feedback. This is achieved without using arrival times at the synapse or modulatory signaling from astrocytes; instead, it relies on the presence of global and transient OL responses to local action potentials in the axons they myelinate. While inspired by OL morphology, we provide the theoretical underpinnings that motivated the model and explore its performance for a wide range of its parameters. Our results indicate that when the characteristic time of OL’s transient intracellular responses to neural spikes is between 10 and 40 ms and the firing rates in individual axons are relatively low (10 Hz), the OMP model efficiently synchronizes correlated and time-locked signals while latencies in axons carrying independent signals are unaffected. This suggests a novel form of selective synchronization in the CNS in which oligodendrocytes play an active role by modulating the conduction delays of correlated spike trains as they traverse to their targets.
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spelling pubmed-101328072023-04-27 Oligodendrocyte-mediated myelin plasticity and its role in neural synchronization Pajevic, Sinisa Plenz, Dietmar Basser, Peter J Fields, R Douglas eLife Neuroscience Temporal synchrony of signals arriving from different neurons or brain regions is essential for proper neural processing. Nevertheless, it is not well understood how such synchrony is achieved and maintained in a complex network of time-delayed neural interactions. Myelin plasticity, accomplished by oligodendrocytes (OLs), has been suggested as an efficient mechanism for controlling timing in brain communications through adaptive changes of axonal conduction velocity and consequently conduction time delays, or latencies; however, local rules and feedback mechanisms that OLs use to achieve synchronization are not known. We propose a mathematical model of oligodendrocyte-mediated myelin plasticity (OMP) in which OLs play an active role in providing such feedback. This is achieved without using arrival times at the synapse or modulatory signaling from astrocytes; instead, it relies on the presence of global and transient OL responses to local action potentials in the axons they myelinate. While inspired by OL morphology, we provide the theoretical underpinnings that motivated the model and explore its performance for a wide range of its parameters. Our results indicate that when the characteristic time of OL’s transient intracellular responses to neural spikes is between 10 and 40 ms and the firing rates in individual axons are relatively low (10 Hz), the OMP model efficiently synchronizes correlated and time-locked signals while latencies in axons carrying independent signals are unaffected. This suggests a novel form of selective synchronization in the CNS in which oligodendrocytes play an active role by modulating the conduction delays of correlated spike trains as they traverse to their targets. eLife Sciences Publications, Ltd 2023-03-28 /pmc/articles/PMC10132807/ /pubmed/36976252 http://dx.doi.org/10.7554/eLife.81982 Text en https://creativecommons.org/publicdomain/zero/1.0/This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication (https://creativecommons.org/publicdomain/zero/1.0/) .
spellingShingle Neuroscience
Pajevic, Sinisa
Plenz, Dietmar
Basser, Peter J
Fields, R Douglas
Oligodendrocyte-mediated myelin plasticity and its role in neural synchronization
title Oligodendrocyte-mediated myelin plasticity and its role in neural synchronization
title_full Oligodendrocyte-mediated myelin plasticity and its role in neural synchronization
title_fullStr Oligodendrocyte-mediated myelin plasticity and its role in neural synchronization
title_full_unstemmed Oligodendrocyte-mediated myelin plasticity and its role in neural synchronization
title_short Oligodendrocyte-mediated myelin plasticity and its role in neural synchronization
title_sort oligodendrocyte-mediated myelin plasticity and its role in neural synchronization
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10132807/
https://www.ncbi.nlm.nih.gov/pubmed/36976252
http://dx.doi.org/10.7554/eLife.81982
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AT plenzdietmar oligodendrocytemediatedmyelinplasticityanditsroleinneuralsynchronization
AT basserpeterj oligodendrocytemediatedmyelinplasticityanditsroleinneuralsynchronization
AT fieldsrdouglas oligodendrocytemediatedmyelinplasticityanditsroleinneuralsynchronization