Cargando…

Adolescent oligodendrogenesis and myelination restrict experience-dependent neuronal plasticity in adult visual cortex

BACKGROUND: Developmental myelination is a protracted process in the mammalian brain. One theory for why oligodendrocytes mature so slowly posits that myelination may stabilize neuronal circuits and temper neuronal plasticity as animals age. We tested this hypothesis in the visual cortex, which has...

Descripción completa

Detalles Bibliográficos
Autores principales: Xin, Wendy, Kaneko, Megumi, Roth, Richard H., Zhang, Albert, Nocera, Sonia, Ding, Jun B., Stryker, Michael P., Chan, Jonah R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10557765/
https://www.ncbi.nlm.nih.gov/pubmed/37808666
http://dx.doi.org/10.1101/2023.09.29.560231
_version_ 1785117147216740352
author Xin, Wendy
Kaneko, Megumi
Roth, Richard H.
Zhang, Albert
Nocera, Sonia
Ding, Jun B.
Stryker, Michael P.
Chan, Jonah R.
author_facet Xin, Wendy
Kaneko, Megumi
Roth, Richard H.
Zhang, Albert
Nocera, Sonia
Ding, Jun B.
Stryker, Michael P.
Chan, Jonah R.
author_sort Xin, Wendy
collection PubMed
description BACKGROUND: Developmental myelination is a protracted process in the mammalian brain. One theory for why oligodendrocytes mature so slowly posits that myelination may stabilize neuronal circuits and temper neuronal plasticity as animals age. We tested this hypothesis in the visual cortex, which has a well-defined critical period for experience-dependent neuronal plasticity. OBJECTIVES/METHODS: To prevent myelin progression, we conditionally deleted Myrf, a transcription factor necessary for oligodendrocyte maturation, from oligodendrocyte precursor cells (Myrf cKO) in adolescent mice. To induce experience-dependent plasticity, adult control and Myrf cKO mice were monocularly deprived by eyelid suture. Functional and structural neuronal plasticity in the visual cortex were assessed in vivo by intrinsic signal optical imaging and longitudinal two photon imaging of dendritic spines, respectively. RESULTS: During adolescence, visual experience modulated the rate of oligodendrocyte maturation in visual cortex. Myrf deletion from oligodendrocyte precursors during adolescence led to inhibition of oligodendrocyte maturation and myelination that persisted into adulthood. Following monocular deprivation, visual cortex activity in response to visual stimulation of the deprived eye remained stable in adult control mice, as expected for post-critical period animals. By contrast, visual cortex responses to the deprived eye decreased significantly following monocular deprivation in adult Myrf cKO mice, reminiscent of the plasticity observed in adolescent mice. Furthermore, visual cortex neurons in adult Myrf cKO mice had fewer dendritic spines and a higher level of spine turnover. Finally, monocular deprivation induced spatially coordinated spine size decreases in adult Myrf cKO, but not control, mice. CONCLUSIONS: These results demonstrate a critical role for oligodendrocytes in shaping the maturation and stabilization of cortical circuits and support the concept of myelin acting as a brake on neuronal plasticity during development.
format Online
Article
Text
id pubmed-10557765
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Cold Spring Harbor Laboratory
record_format MEDLINE/PubMed
spelling pubmed-105577652023-10-07 Adolescent oligodendrogenesis and myelination restrict experience-dependent neuronal plasticity in adult visual cortex Xin, Wendy Kaneko, Megumi Roth, Richard H. Zhang, Albert Nocera, Sonia Ding, Jun B. Stryker, Michael P. Chan, Jonah R. bioRxiv Article BACKGROUND: Developmental myelination is a protracted process in the mammalian brain. One theory for why oligodendrocytes mature so slowly posits that myelination may stabilize neuronal circuits and temper neuronal plasticity as animals age. We tested this hypothesis in the visual cortex, which has a well-defined critical period for experience-dependent neuronal plasticity. OBJECTIVES/METHODS: To prevent myelin progression, we conditionally deleted Myrf, a transcription factor necessary for oligodendrocyte maturation, from oligodendrocyte precursor cells (Myrf cKO) in adolescent mice. To induce experience-dependent plasticity, adult control and Myrf cKO mice were monocularly deprived by eyelid suture. Functional and structural neuronal plasticity in the visual cortex were assessed in vivo by intrinsic signal optical imaging and longitudinal two photon imaging of dendritic spines, respectively. RESULTS: During adolescence, visual experience modulated the rate of oligodendrocyte maturation in visual cortex. Myrf deletion from oligodendrocyte precursors during adolescence led to inhibition of oligodendrocyte maturation and myelination that persisted into adulthood. Following monocular deprivation, visual cortex activity in response to visual stimulation of the deprived eye remained stable in adult control mice, as expected for post-critical period animals. By contrast, visual cortex responses to the deprived eye decreased significantly following monocular deprivation in adult Myrf cKO mice, reminiscent of the plasticity observed in adolescent mice. Furthermore, visual cortex neurons in adult Myrf cKO mice had fewer dendritic spines and a higher level of spine turnover. Finally, monocular deprivation induced spatially coordinated spine size decreases in adult Myrf cKO, but not control, mice. CONCLUSIONS: These results demonstrate a critical role for oligodendrocytes in shaping the maturation and stabilization of cortical circuits and support the concept of myelin acting as a brake on neuronal plasticity during development. Cold Spring Harbor Laboratory 2023-09-30 /pmc/articles/PMC10557765/ /pubmed/37808666 http://dx.doi.org/10.1101/2023.09.29.560231 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Xin, Wendy
Kaneko, Megumi
Roth, Richard H.
Zhang, Albert
Nocera, Sonia
Ding, Jun B.
Stryker, Michael P.
Chan, Jonah R.
Adolescent oligodendrogenesis and myelination restrict experience-dependent neuronal plasticity in adult visual cortex
title Adolescent oligodendrogenesis and myelination restrict experience-dependent neuronal plasticity in adult visual cortex
title_full Adolescent oligodendrogenesis and myelination restrict experience-dependent neuronal plasticity in adult visual cortex
title_fullStr Adolescent oligodendrogenesis and myelination restrict experience-dependent neuronal plasticity in adult visual cortex
title_full_unstemmed Adolescent oligodendrogenesis and myelination restrict experience-dependent neuronal plasticity in adult visual cortex
title_short Adolescent oligodendrogenesis and myelination restrict experience-dependent neuronal plasticity in adult visual cortex
title_sort adolescent oligodendrogenesis and myelination restrict experience-dependent neuronal plasticity in adult visual cortex
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10557765/
https://www.ncbi.nlm.nih.gov/pubmed/37808666
http://dx.doi.org/10.1101/2023.09.29.560231
work_keys_str_mv AT xinwendy adolescentoligodendrogenesisandmyelinationrestrictexperiencedependentneuronalplasticityinadultvisualcortex
AT kanekomegumi adolescentoligodendrogenesisandmyelinationrestrictexperiencedependentneuronalplasticityinadultvisualcortex
AT rothrichardh adolescentoligodendrogenesisandmyelinationrestrictexperiencedependentneuronalplasticityinadultvisualcortex
AT zhangalbert adolescentoligodendrogenesisandmyelinationrestrictexperiencedependentneuronalplasticityinadultvisualcortex
AT nocerasonia adolescentoligodendrogenesisandmyelinationrestrictexperiencedependentneuronalplasticityinadultvisualcortex
AT dingjunb adolescentoligodendrogenesisandmyelinationrestrictexperiencedependentneuronalplasticityinadultvisualcortex
AT strykermichaelp adolescentoligodendrogenesisandmyelinationrestrictexperiencedependentneuronalplasticityinadultvisualcortex
AT chanjonahr adolescentoligodendrogenesisandmyelinationrestrictexperiencedependentneuronalplasticityinadultvisualcortex