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Remodeling of pre-existing myelinated axons and oligodendrocyte differentiation is stimulated by environmental enrichment in the young adult brain

View ORCID ProfileMadeline Nicholson, Rhiannon J Wood, Jessica L Fletcher, David G Gonsalvez, Anthony J Hannan, Simon S Murray, Junhua Xiao
doi: https://doi.org/10.1101/2020.01.21.914572
Madeline Nicholson
1Neurotrophin and Myelin Laboratory, Department of Anatomy and Neuroscience, School of Biomedical Sciences, Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Parkville, Victoria, 3010, Australia
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  • ORCID record for Madeline Nicholson
Rhiannon J Wood
1Neurotrophin and Myelin Laboratory, Department of Anatomy and Neuroscience, School of Biomedical Sciences, Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Parkville, Victoria, 3010, Australia
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Jessica L Fletcher
1Neurotrophin and Myelin Laboratory, Department of Anatomy and Neuroscience, School of Biomedical Sciences, Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Parkville, Victoria, 3010, Australia
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David G Gonsalvez
1Neurotrophin and Myelin Laboratory, Department of Anatomy and Neuroscience, School of Biomedical Sciences, Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Parkville, Victoria, 3010, Australia
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Anthony J Hannan
2Florey Institute of Neuroscience and Mental Health, The University of Melbourne, Parkville, Victoria, 3010, Australia
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Simon S Murray
1Neurotrophin and Myelin Laboratory, Department of Anatomy and Neuroscience, School of Biomedical Sciences, Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Parkville, Victoria, 3010, Australia
2Florey Institute of Neuroscience and Mental Health, The University of Melbourne, Parkville, Victoria, 3010, Australia
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Junhua Xiao
1Neurotrophin and Myelin Laboratory, Department of Anatomy and Neuroscience, School of Biomedical Sciences, Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Parkville, Victoria, 3010, Australia
2Florey Institute of Neuroscience and Mental Health, The University of Melbourne, Parkville, Victoria, 3010, Australia
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  • For correspondence: xiaoj@unimelb.edu.au
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Abstract

Oligodendrocyte production and central nervous system (CNS) myelination is a protracted process, extending into adulthood. While stimulation of neuronal circuits has been shown to enhance oligodendrocyte production and myelination during development, the extent to which physiological stimuli induces activity-dependent plasticity within oligodendrocytes and myelin is unclear, particularly in the adult CNS. Here, we find that using environmental enrichment (EE) to physiologically stimulate neuronal activity for 6-weeks during young adulthood in C57Bl/6 mice results in an enlargement of callosal axon diameters, with a corresponding increase in thickness of pre-existing myelin sheaths. Additionally, EE uniformly promotes the direct differentiation of pre-existing oligodendroglia in both corpus callosum and somatosensory cortex, while differentially impeding OPC homeostasis in these regions. Furthermore, results of this study indicate that physiologically relevant stimulation in young adulthood exerts little influence upon the de novo generation of new myelin sheaths on previously unmyelinated segments and does not enhance OPC proliferation. Rather in this context, activity-dependent plasticity involves the coincident structural remodeling of axons and pre-existing myelin sheaths and increases the direct differentiation of pre-existing oligodendroglia, implying constraints on maximal de novo production in the adult CNS. Together, our findings of myelinated axon remodeling and increased pre-existing oligodendroglial differentiation constitute a previously undescribed form of adaptive myelination that likely contributes to neuronal circuit maturation and the maintenance of optimum cognitive function in the young adult CNS.

Main points

  • Environmental enrichment induces the plasticity of myelinated axons, resulting in axon caliber enlargement and increased thickness of pre-existing myelin sheaths

  • Environmental enrichment increases the direct differentiation of pre-existing oligodendroglia

  • Environmental enrichment alters OPC homeostasis

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Conflict of interest statement The authors declare no conflicting financial or other interests.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted April 21, 2020.
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Remodeling of pre-existing myelinated axons and oligodendrocyte differentiation is stimulated by environmental enrichment in the young adult brain
Madeline Nicholson, Rhiannon J Wood, Jessica L Fletcher, David G Gonsalvez, Anthony J Hannan, Simon S Murray, Junhua Xiao
bioRxiv 2020.01.21.914572; doi: https://doi.org/10.1101/2020.01.21.914572
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Remodeling of pre-existing myelinated axons and oligodendrocyte differentiation is stimulated by environmental enrichment in the young adult brain
Madeline Nicholson, Rhiannon J Wood, Jessica L Fletcher, David G Gonsalvez, Anthony J Hannan, Simon S Murray, Junhua Xiao
bioRxiv 2020.01.21.914572; doi: https://doi.org/10.1101/2020.01.21.914572

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