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...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2023-03-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/81982 |
| _version_ | 1797838924787220480 |
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| author | Sinisa Pajevic Dietmar Plenz Peter J Basser R Douglas Fields |
| author_facet | Sinisa Pajevic Dietmar Plenz Peter J Basser R Douglas Fields |
| author_sort | Sinisa Pajevic |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-09T15:48:44Z |
| format | Article |
| id | doaj.art-9f906abe307043a9bb92552c49551c2c |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-09T15:48:44Z |
| publishDate | 2023-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-9f906abe307043a9bb92552c49551c2c2023-04-26T14:32:24ZengeLife Sciences Publications LtdeLife2050-084X2023-03-011210.7554/eLife.81982Oligodendrocyte-mediated myelin plasticity and its role in neural synchronizationSinisa Pajevic0https://orcid.org/0000-0002-8880-3320Dietmar Plenz1https://orcid.org/0000-0002-0008-3657Peter J Basser2https://orcid.org/0000-0003-4795-6088R Douglas Fields3Section on Critical Brain Dynamics, National Institute of Mental Health, NIH, Bethesda, United StatesSection on Critical Brain Dynamics, National Institute of Mental Health, NIH, Bethesda, United StatesSection on Quantitative Imaging and Tissue Sciences, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, United StatesNervous System Development and Plasticity Section, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, United StatesTemporal 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.https://elifesciences.org/articles/81982neural synchronizationmyelin plasticityoligodendrocytemodeling |
| spellingShingle | Sinisa Pajevic Dietmar Plenz Peter J Basser R Douglas Fields Oligodendrocyte-mediated myelin plasticity and its role in neural synchronization eLife neural synchronization myelin plasticity oligodendrocyte modeling |
| 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 | neural synchronization myelin plasticity oligodendrocyte modeling |
| url | https://elifesciences.org/articles/81982 |
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