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...
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doaj-f076371601564d16ad414a390f14d56b2021-04-26T05:54:34ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2021-04-01910.3389/fcell.2021.665409665409Prolonged Environmental Enrichment Promotes Developmental MyelinationEvan Z. Goldstein0Vera Pertsovskaya1Thomas A. Forbes2Jeffrey L. Dupree3Vittorio Gallo4Center for Neuroscience Research, Children’s Research Institute, Children’s National Hospital, Washington, DC, United StatesSchool of Medicine and Health Sciences, The George Washington University, Washington, DC, United StatesCenter for Neuroscience Research, Children’s Research Institute, Children’s National Hospital, Washington, DC, United StatesDepartment of Anatomy and Neurobiology, Virginia Commonwealth University, Richmond, VA, United StatesCenter for Neuroscience Research, Children’s Research Institute, Children’s National Hospital, Washington, DC, United StatesPostnatal 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.https://www.frontiersin.org/articles/10.3389/fcell.2021.665409/fullenriched environmentoligodendrocytemyelinhypermyelinationgliadevelopment |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Evan Z. Goldstein Vera Pertsovskaya Thomas A. Forbes Jeffrey L. Dupree Vittorio Gallo |
spellingShingle |
Evan Z. Goldstein Vera Pertsovskaya Thomas A. Forbes Jeffrey L. Dupree Vittorio Gallo Prolonged Environmental Enrichment Promotes Developmental Myelination Frontiers in Cell and Developmental Biology enriched environment oligodendrocyte myelin hypermyelination glia development |
author_facet |
Evan Z. Goldstein Vera Pertsovskaya Thomas A. Forbes Jeffrey L. Dupree Vittorio Gallo |
author_sort |
Evan Z. Goldstein |
title |
Prolonged Environmental Enrichment Promotes Developmental Myelination |
title_short |
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_sort |
prolonged environmental enrichment promotes developmental myelination |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Cell and Developmental Biology |
issn |
2296-634X |
publishDate |
2021-04-01 |
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. |
topic |
enriched environment oligodendrocyte myelin hypermyelination glia development |
url |
https://www.frontiersin.org/articles/10.3389/fcell.2021.665409/full |
work_keys_str_mv |
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