Activity-dependent myelination: a glial mechanism of oscillatory self-organization in large-scale brain networks
Open accessAbstract
Communication and oscillatory synchrony between distributed neural populations are believed to play a key role in multiple cognitive and neural functions. These interactions are mediated by long-range myelinated axonal fiber bundles, collectively termed as white matter. While traditionally considered to be static after development, white matter properties have been shown to change in an activity-dependent way through learning and behavior-a phenomenon known as white matter plasticity. In the central nervous system, this plasticity stems from oligodendroglia, which form myelin sheaths to regulate the conduction of nerve impulses across the brain, hence critically impacting neural communication. We here shift the focus from neural to glial contribution to brain synchronization and examine the impact of adaptive, activity-dependent changes in conduction velocity on the large-scale phase synchronization of neural oscillators. Using a network model based on primate large-scale white matter neuroanatomy, our computational and mathematical results show that such plasticity endows white matter with self-organizing properties, where conduction delay statistics are autonomously adjusted to ensure efficient neural communication. Our analysis shows that this mechanism stabilizes oscillatory neural activity across a wide range of connectivity gain and frequency bands, making phase-locked states more resilient to damage as reflected by diffuse decreases in connectivity. Critically, our work suggests that adaptive myelination may be a mechanism that enables brain networks with a means of temporal self-organization, resilience, and homeostasis.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Even small changes in myelination can exert profound effects on neural circuit dynamics and consequently on cognitive function.
“even small changes in myelination can exert profound effects on neural circuit dynamics and consequently on cognitive function (Steadman et al., 2020; Noori et al., 2020; Pajevic et al., 2014).”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Noori et al., 2020
Cites
Chemical Oscillations, Waves, and Turbulence
Kuramoto, Y. (1984) · Springer series in synergetics · doi:10.1007/978-3-642-69689-3 · Cited by 7,242 · see citing works
The brainweb: phase synchronization and large-scale integration
Varela, F., Lachaux, J.-P., Rodriguez, E., & Martinerie, J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35067550 · Cited by 4,761 · see citing works
A mechanism for cognitive dynamics: neuronal communication through neuronal coherence.
Fries, P. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2005.08.011 · Cited by 4,284 · see citing works
Strogatz, S. H. (2000) · Physica D Nonlinear Phenomena · doi:10.1016/s0167-2789(00)00094-4 · Cited by 3,094 · see citing works
Neurophysiological and Computational Principles of Cortical Rhythms in Cognition
Wang, X.-J. (2010) · Physiological Reviews · doi:10.1152/physrev.00035.2008 · Cited by 1,939 · see citing works
Training induces changes in white-matter architecture
Scholz, J., Klein, M. C., Behrens, T. E. J., & Johansen-Berg, H. (2009) · Nature Neuroscience · doi:10.1038/nn.2412 · Cited by 1,508 · see citing works
Neuronal activity promotes oligodendrogenesis and adaptive myelination in the mammalian brain
Gibson, E. M., Purger, D., Mount, C. W., Goldstein, A. K., Lin, G. L., Wood, L. S., Inema, I., Miller, S. E., Bieri, G., Zuchero, J. B., et al. (2014) · Science · doi:10.1126/science.1252304 · Cited by 1,472 · see citing works
Fiber composition of the human corpus callosum
Aboitiz, F., Scheibel, A. B., Fisher, R. S., & Eran Zaidel, B. (1992) · Brain Research · doi:10.1016/0006-8993(92)90178-c · Cited by 1,467 · see citing works
Spectral fingerprints of large-scale neuronal interactions
Siegel, M., Donner, T. H., & Engel, A. K. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3137 · Cited by 1,295 · see citing works
Variability, compensation and homeostasis in neuron and network function
Marder, E., & Goaillard, J.-M. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1949 · Cited by 1,212 · see citing works
Motor skill learning requires active central myelination
McKenzie, I. A., Ohayon, D., Li, H., Paes de Faria, J., Emery, B., Tohyama, K., & Richardson, W. D. (2014) · Science · doi:10.1126/science.1254960 · Cited by 1,177 · see citing works
A critical period for social experience-dependent oligodendrocyte maturation and myelination
Makinodan, M., Rosen, K. M., Ito, S., & Corfas, G. (2012) · Science · doi:10.1126/science.1220845 · Cited by 922 · see citing works
A new mechanism of nervous system plasticity: activity-dependent myelination
Fields, R. D. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn4023 · Cited by 794 · see citing works
Key role of coupling, delay, and noise in resting brain fluctuations
Deco, G., Jirsa, V., McIntosh, A. R., Sporns, O., & Kötter, R. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901831106 · Cited by 756 · see citing works
Impaired adult myelination in the prefrontal cortex of socially isolated mice
Liu, J., Dietz, K., DeLoyht, J. M., Pedre, X., Kelkar, D., Kaur, J., Vialou, V., Lobo, M. K., Dietz, D. M., Nestler, E. J., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3263 · Cited by 685 · see citing works
Induction of myelination in the central nervous system by electrical activity
Demerens, C., Stankoff, B., Logak, M., Anglade, P., Allinquant, B., Couraud, F., Zalc, B., & Lubetzki, C. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.18.9887 · Cited by 678 · see citing works
Time Delay in the Kuramoto Model of Coupled Oscillators
Yeung, M. K. S., & Strogatz, S. H. (1999) · Physical Review Letters · doi:10.1103/physrevlett.82.648 · Cited by 614 · see citing works
Myelin remodeling through experience-dependent oligodendrogenesis in the adult somatosensory cortex
Hughes, E. G., Orthmann-Murphy, J. L., Langseth, A. J., & Bergles, D. E. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0121-5 · Cited by 540 · see citing works
Role of local network oscillations in resting-state functional connectivity
Cabral, J., Hugues, E., Sporns, O., & Deco, G. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.04.010 · Cited by 515 · see citing works
Generative Models of Cortical Oscillations: Neurobiological Implications of the Kuramoto Model
Breakspear, M. J., Heitmann, S., & Daffertshofer, A. (2010) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2010.00190 · Cited by 513 · see citing works
Rapid production of new oligodendrocytes is required in the earliest stages of motor-skill learning
Xiao, L., Ohayon, D., McKenzie, I. A., Sinclair-Wilson, A., Wright, J. L., Fudge, A. D., Emery, B., Li, H., & Richardson, W. D. (2016) · Nature Neuroscience · doi:10.1038/nn.4351 · Cited by 507 · cited 1× · see citing works
“than the myelin formation reported in animals, which stabilizes after a few hours (48).”
BackgroundChomiak, T., & Hu, B. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007754 · Cited by 446 · see citing works
Disruption of oligodendrogenesis impairs memory consolidation in adult mice
Steadman, P. E., Xia, F., Ahmed, M., Mocle, A. J., Penning, A. R. A., Geraghty, A. C., Steenland, H. W., Monje, M., Josselyn, S. A., & Frankland, P. W. (2020) · Neuron · doi:10.1016/j.neuron.2019.10.013 · Cited by 426 · see citing works
Self-citationHuman brain networks function in connectome-specific harmonic waves
Atasoy, S., Donnelly, I., & Pearson, J. (2016) · Nature Communications · doi:10.1038/ncomms10340 · Cited by 381 · see citing works
Role of myelin plasticity in oscillations and synchrony of neuronal activity
Pajevic, S., Basser, P. J., & Fields, R. D. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.11.007 · Cited by 378 · see citing works
Advanced database methodology for the Collation of Connectivity data on the Macaque brain (CoCoMac)
Stephan, K. E., Kamper, L., Bozkurt, A., Burns, G., Young, M. P., & Kötter, R. (2001) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2001.0908 · Cited by 369 · see citing works
Pharmacogenetic stimulation of neuronal activity increases myelination in an axon-specific manner
Mitew, S., Gobius, I., Fenlon, L. R., McDougall, S. J., Hawkes, D. J., Xing, Y. L., Bujalka, H., Gundlach, A. L., Richards, L. J., Kilpatrick, T. J., et al. (2018) · Nature Communications · doi:10.1038/s41467-017-02719-2 · Cited by 345 · see citing works
Variability, compensation, and modulation in neurons and circuits
Marder, E. E. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010674108 · Cited by 341 · see citing works
Dynamical relaying can yield zero time lag neuronal synchrony despite long conduction delays
Vicente, R., Gollo, L. L., Mirasso, C. R., Fischer, I., & Pipa, G. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809353105 · Cited by 341 · see citing works
Distributed Delays Facilitate Amplitude Death of Coupled Oscillators
Atay, F. M. (2003) · Physical Review Letters · doi:10.1103/physrevlett.91.094101 · Cited by 321 · see citing works
Salami, M., Itami, C., Tsumoto, T., & Kimura, F. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0937380100 · Cited by 314 · see citing works
Cabral, J., Luckhoo, H., Woolrich, M. W., Joensson, M., Mohseni, H., Baker, A. P., Kringelbach, M. L., & Deco, G. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.11.047 · Cited by 312 · see citing works
Node of Ranvier length as a potential regulator of myelinated axon conduction speed
Arancibia‐Cárcamo, I. L., Ford, M. C., Cossell, L., Ishida, K., Tohyama, K., & Attwell, D. (2017) · eLife · doi:10.7554/elife.23329 · Cited by 306 · see citing works
Ford, M. C., Alexandrova, O., Cossell, L., Stange-Marten, A., Sinclair, J., Kopp‐Scheinpflug, C., Pecka, M., Attwell, D., & Grothe, B. (2015) · Nature Communications · doi:10.1038/ncomms9073 · Cited by 295 · see citing works
Loss of adaptive myelination contributes to methotrexate chemotherapy-related cognitive impairment
Geraghty, A. C., Gibson, E. M., Ghanem, R. A., Greene, J. J., Ocampo, A., Goldstein, A. K., Ni, L., Yang, T., Marton, R. M., Paşca, S. P., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.04.032 · Cited by 288 · see citing works
Resting-State Temporal Synchronization Networks Emerge from Connectivity Topology and Heterogeneity
Ponce‐Alvarez, A., Deco, G., Hagmann, P., Romani, G. L., Mantini, D., & Corbetta, M. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004100 · Cited by 234 · see citing works
Regulation of conduction time along axons
Seidl, A. H. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.06.047 · Cited by 231 · see citing works
On Myelinated Axon Plasticity and Neuronal Circuit Formation and Function
Almeida, R. G., & Lyons, D. A. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.3185-16.2017 · Cited by 221 · see citing works
Modulation of Impulse Conduction Along the Axonal Tree
Swadlow, H. A., Kocsis, J. D., & Waxman, S. G. (1980) · Annual Review of Biophysics and Bioengineering · doi:10.1146/annurev.bb.09.060180.001043 · Cited by 206 · see citing works
Regulation of myelin structure and conduction velocity by perinodal astrocytes
Dutta, D. J., Woo, D. H., Lee, P. R., Pajevic, S., Bukalo, O., Huffman, W. C., Wake, H., Basser, P. J., SheikhBahaei, S., Lazarevic, V., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1811013115 · Cited by 198 · see citing works
Oscillator death in populations of “all to all” coupled nonlinear oscillators
Ermentrout, G. B. (1990) · Physica D Nonlinear Phenomena · doi:10.1016/0167-2789(90)90124-8 · Cited by 190 · see citing works
Modeling the outcome of structural disconnection on resting-state functional connectivity
Cabral, J., Hugues, E., Kringelbach, M. L., & Deco, G. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.06.007 · Cited by 182 · see citing works
Uhlhaas, P. J., & Singer, W. (2011) · Schizophrenia Bulletin · doi:10.1093/schbul/sbr034 · Cited by 176 · see citing works
Myelination and Oligodendrocyte Functions in Psychiatric Diseases
Nave, K.-A., & Ehrenreich, H. (2014) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2014.189 · Cited by 157 · see citing works
Intrinsic and adaptive myelination—A sequential mechanism for smart wiring in the brain
Bechler, M. E., Swire, M., & ffrench‐Constant, C. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22518 · Cited by 149 · see citing works
Mapping brains without coordinates
Kötter, R., & Wanke, E. (2005) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2005.1625 · Cited by 137 · see citing works
Aboitiz, F., Morales, D., & Montiel, J. F. (2003) · Behavioral and Brain Sciences · doi:10.1017/s0140525x03000128 · Cited by 135 · see citing works
Transmission time delays organize the brain network synchronization
Petkoski, S., & Jirsa, V. (2019) · Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences · doi:10.1098/rsta.2018.0132 · Cited by 131 · see citing works
Evidence for Myelin Sheath Remodeling in the CNS Revealed by In Vivo Imaging
Auer, F., Vagionitis, S., & Czopka, T. (2018) · Current Biology · doi:10.1016/j.cub.2018.01.017 · Cited by 112 · see citing works
Myelin plasticity and behaviour — connecting the dots
Kaller, M. S., Lazari, A., Blanco‐Duque, C., Sampaio‐Baptista, C., & Johansen‐Berg, H. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.09.014 · Cited by 102 · see citing works
Perturbation of whole-brain dynamics in silico reveals mechanistic differences between brain states
Deco, G., Cabral, J., Saenger, V. M., Boly, M., Tagliazucchi, E., Laufs, H., Someren, E. J. W. V., Jobst, B., Stevner, A. B. A., & Kringelbach, M. L. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.12.009 · Cited by 98 · see citing works
Bakiri, Y., Káradóttir, R. T., Cossell, L., & Attwell, D. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.201376 · Cited by 97 · see citing works
Endothelin signalling mediates experience-dependent myelination in the CNS
Swire, M., Kotelevtsev, Y. V., Webb, D. J., Lyons, D. A., & ffrench‐Constant, C. (2019) · eLife · doi:10.7554/elife.49493 · Cited by 90 · see citing works
A macaque connectome for large-scale network simulations in TheVirtualBrain
Shen, K., Bezgin, G., Schirner, M., Ritter, P., Everling, S., & McIntosh, A. R. (2019) · Scientific Data · doi:10.1038/s41597-019-0129-z · Cited by 83 · see citing works
Petkoski, S., Palva, J. M., & Jirsa, V. (2018) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006160 · Cited by 82 · see citing works
Axonal Regulation of Central Nervous System Myelination: Structure and Function
Klingseisen, A., & Lyons, D. A. (2017) · The Neuroscientist · doi:10.1177/1073858417703030 · Cited by 77 · see citing works
Bells, S., Lefebvre, J., Prescott, S. A., Dockstader, C. L., Bouffet, É., Skocic, J., Laughlin, S., & Mabbott, D. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0560-17.2017 · Cited by 70 · see citing works
Self-citationNunez, P. L., & Srinivasan, R. (2013) · Brain Research · doi:10.1016/j.brainres.2013.10.036 · Cited by 62 · see citing works
White matter plasticity and maturation in human cognition
Bells, S., Lefebvre, J., Longoni, G., Narayanan, S., Arnold, D. L., Yeh, E. A., & Mabbott, D. (2019) · Glia · doi:10.1002/glia.23661 · Cited by 53 · see citing works
Self-citationRole of white-matter pathways in coordinating alpha oscillations in resting visual cortex
Hindriks, R., Woolrich, M. W., Luckhoo, H., Joensson, M., Mohseni, H., Kringelbach, M. L., & Deco, G. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.10.057 · Cited by 44 · see citing works
Bezgin, G., Solodkin, A., Bakker, R., Ritter, P., & McIntosh, A. R. (2017) · Human Brain Mapping · doi:10.1002/hbm.23506 · Cited by 29 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation
Fernández-Castañeda, A., Lu, P., Geraghty, A. C., Song, E., Lee, M.-H., Wood, J., O’Dea, M. R., Dutton, S., Shamardani, K., Nwangwu, K., et al. (2022) · Cell · doi:10.1016/j.cell.2022.06.008 · Cited by 521 · see citing works
- Authors
- Noori, R., Park, D., Griffiths, J. D., Bells, S., Frankland, P. W., Mabbott, D., & Lefebvre, J.
- Affiliations
- University Health Network (CA)
- Centre for Addiction and Mental Health (CA)
- Hospital for Sick Children (CA)
- University of Toronto (CA)
- Krembil Research Institute, University Health Network, Toronto, ON M5T 0S8, Canada;
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2020-06
- Volume
- 117
- Issue
- 24
- Pages
- 13227-13237
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC7306810
- OpenAlex
- W3029829036
- Cited by
- 137
- References
- 61
- Citations by year
- 2026: 17 · 2025: 20 · 2024: 16 · 2023: 28 · 2022: 28 · 2021: 22 · 2020: 6
- FWCI
- 11.29
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Gouvernement du Canada | National Research Council Canada (RGPIN-2017-06662)
- Gouvernement du Canada | Canadian Institutes of Health Research (PJT-156164)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Physical Sciences › Computer Science › Computer Networks and Communications › Nonlinear Dynamics and Pattern Formation
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Keywords
- activity-dependent myelination, white matter plasticity, oligodendrocytes, neural oscillations, phase synchronization, conduction velocity, large-scale brain networks, network resilience, network models
- MeSH terms
- Animals, Brain, Models, Neurological, Myelin Sheath, Nerve Net, Neural Conduction, Neuroglia, Neuronal Plasticity, Primates, Electroencephalography Phase Synchronization, Connectome, White Matter
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
