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Homeostatic coordination and up-regulation of neural activity by activity-dependent myelination

Abstract

Activity-dependent myelination (ADM) is a fundamental dimension of brain plasticity through which myelin changes as a function of neural activity. Mediated by structural changes in glia, ADM notably regulates axonal conduction velocity. Yet, it remains unclear how neural activity impacts myelination to orchestrate the timing of neural signalling, and how ADM shapes neural activity. We developed a model of spiking neurons enhanced with neuron–oligodendrocyte feedback and examined the relationship between ADM and neural activity. We found that ADM implements a homeostatic gain control mechanism that enhances neural firing rates and correlations through the temporal coordination of action potentials as axon lengths increase. Stimuli engage ADM plasticity to trigger bidirectional and reversible changes in conduction delays, as may occur during learning. Furthermore, ADM was found to enhance information transmission under various types of time-varying stimuli. These results highlight the role of ADM in shaping neural activity and communication.

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Fig. 1: ADM plasticity model.
Fig. 2: Effect of ADM on neural activity.
Fig. 3: Up-regulation of neural activity through changes in network geometry.
Fig. 4: Bidirectional control of axonal CVs and delays by stimuli.
Fig. 5: Enhanced information transmission.

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Data availability

Source data for Figs. 15 are available with this manuscript, via ref. 57 and publicly available on GitHub at https://github.com/Jeremie-Lefebvre/Talidou-et-al.-Nat-Comp-Sci-2022.

Code availability

Source codes for all results reported in this study are available with this manuscript via ref. 57 and publicly available on GitHub at https://github.com/Jeremie-Lefebvre/Talidou-et-al.-Nat-Comp-Sci-2022.

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Acknowledgements

We thank the National Research Council of Canada (NSERC grant RGPIN-2017-06662, J.L.) as well as the Canadian Institute of Health Research (CIHR grant NO PJT-156164, P.W.F., D.M. and J.L.) for funding.

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J.L. designed the study. J.L. and A.T. performed the mathematical derivations and simulations. J.L., A.T., P.W.F. and D.M. wrote the manuscript.

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Correspondence to Afroditi Talidou.

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Nature Computational Science thanks Maurice Chacron, Thomas R. Knösche and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Handling editor: Ananya Rastogi, in collaboration with the Nature Computational Science team.

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Talidou, A., Frankland, P.W., Mabbott, D. et al. Homeostatic coordination and up-regulation of neural activity by activity-dependent myelination. Nat Comput Sci 2, 665–676 (2022). https://doi.org/10.1038/s43588-022-00315-z

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