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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Main Authors: Evan Z. Goldstein, Vera Pertsovskaya, Thomas A. Forbes, Jeffrey L. Dupree, Vittorio Gallo
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-04-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2021.665409/full
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spelling 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 AT evanzgoldstein prolongedenvironmentalenrichmentpromotesdevelopmentalmyelination
AT verapertsovskaya prolongedenvironmentalenrichmentpromotesdevelopmentalmyelination
AT thomasaforbes prolongedenvironmentalenrichmentpromotesdevelopmentalmyelination
AT jeffreyldupree prolongedenvironmentalenrichmentpromotesdevelopmentalmyelination
AT vittoriogallo prolongedenvironmentalenrichmentpromotesdevelopmentalmyelination
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