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Prolonged Environmental Enrichment Promotes Developmental Myelination
Postnatal neurodevelopment is profoundly influenced by environmental experiences. Environmental enrichment is a commonly used experimental paradigm that has uncovered numerous examples of experience-dependent plasticity in health and disease. However, the role of environmental enrichment in normal d...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8107367/ https://www.ncbi.nlm.nih.gov/pubmed/33981706 http://dx.doi.org/10.3389/fcell.2021.665409 |
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author | Goldstein, Evan Z. Pertsovskaya, Vera Forbes, Thomas A. Dupree, Jeffrey L. Gallo, Vittorio |
author_facet | Goldstein, Evan Z. Pertsovskaya, Vera Forbes, Thomas A. Dupree, Jeffrey L. Gallo, Vittorio |
author_sort | Goldstein, Evan Z. |
collection | PubMed |
description | Postnatal neurodevelopment is profoundly influenced by environmental experiences. Environmental enrichment is a commonly used experimental paradigm that has uncovered numerous examples of experience-dependent plasticity in health and disease. However, the role of environmental enrichment in normal development, especially glial development, is largely unexplored. Oligodendrocytes, the myelin-forming glia in the central nervous system, provide metabolic support to axons and establish efficient saltatory conduction by producing myelin. Indeed, alterations in myelin are strongly correlated with sensory, cognitive, and motor function. The timing of developmental myelination is uniquely positioned to be influenced by environmental stimuli, as peak myelination occurs postnatally and continues into adulthood. To determine if developmental myelination is impacted by environmental experience, mice were housed in an enriched environment during peak myelination through early adulthood. Using translating ribosome affinity purification, oligodendrocyte-specific RNAs were isolated from subcortical white matter at various postnatal ages. RNA-sequencing revealed that differences in the oligodendrocyte translatome were predominantly evident after prolonged and continuous environmental enrichment. These translational changes corresponded with altered oligodendrocyte lineage cell dynamics and enhanced myelination. Furthermore, consistent with increased developmental myelination, enriched mice displayed enhanced motor coordination on a beam walking task. These findings indicate that protracted environmental stimulation is sufficient to modulate developmental myelination and to promote behavioral function. |
format | Online Article Text |
id | pubmed-8107367 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-81073672021-05-11 Prolonged Environmental Enrichment Promotes Developmental Myelination Goldstein, Evan Z. Pertsovskaya, Vera Forbes, Thomas A. Dupree, Jeffrey L. Gallo, Vittorio Front Cell Dev Biol Cell and Developmental Biology Postnatal neurodevelopment is profoundly influenced by environmental experiences. Environmental enrichment is a commonly used experimental paradigm that has uncovered numerous examples of experience-dependent plasticity in health and disease. However, the role of environmental enrichment in normal development, especially glial development, is largely unexplored. Oligodendrocytes, the myelin-forming glia in the central nervous system, provide metabolic support to axons and establish efficient saltatory conduction by producing myelin. Indeed, alterations in myelin are strongly correlated with sensory, cognitive, and motor function. The timing of developmental myelination is uniquely positioned to be influenced by environmental stimuli, as peak myelination occurs postnatally and continues into adulthood. To determine if developmental myelination is impacted by environmental experience, mice were housed in an enriched environment during peak myelination through early adulthood. Using translating ribosome affinity purification, oligodendrocyte-specific RNAs were isolated from subcortical white matter at various postnatal ages. RNA-sequencing revealed that differences in the oligodendrocyte translatome were predominantly evident after prolonged and continuous environmental enrichment. These translational changes corresponded with altered oligodendrocyte lineage cell dynamics and enhanced myelination. Furthermore, consistent with increased developmental myelination, enriched mice displayed enhanced motor coordination on a beam walking task. These findings indicate that protracted environmental stimulation is sufficient to modulate developmental myelination and to promote behavioral function. Frontiers Media S.A. 2021-04-26 /pmc/articles/PMC8107367/ /pubmed/33981706 http://dx.doi.org/10.3389/fcell.2021.665409 Text en Copyright © 2021 Goldstein, Pertsovskaya, Forbes, Dupree and Gallo. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Cell and Developmental Biology Goldstein, Evan Z. Pertsovskaya, Vera Forbes, Thomas A. Dupree, Jeffrey L. Gallo, Vittorio Prolonged Environmental Enrichment Promotes Developmental Myelination |
title | Prolonged Environmental Enrichment Promotes Developmental Myelination |
title_full | Prolonged Environmental Enrichment Promotes Developmental Myelination |
title_fullStr | Prolonged Environmental Enrichment Promotes Developmental Myelination |
title_full_unstemmed | Prolonged Environmental Enrichment Promotes Developmental Myelination |
title_short | Prolonged Environmental Enrichment Promotes Developmental Myelination |
title_sort | prolonged environmental enrichment promotes developmental myelination |
topic | Cell and Developmental Biology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8107367/ https://www.ncbi.nlm.nih.gov/pubmed/33981706 http://dx.doi.org/10.3389/fcell.2021.665409 |
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