Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Goldstein, Evan Z., Pertsovskaya, Vera, Forbes, Thomas A., Dupree, Jeffrey L., Gallo, Vittorio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
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
_version_ 1783689933525876736
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
work_keys_str_mv AT goldsteinevanz prolongedenvironmentalenrichmentpromotesdevelopmentalmyelination
AT pertsovskayavera prolongedenvironmentalenrichmentpromotesdevelopmentalmyelination
AT forbesthomasa prolongedenvironmentalenrichmentpromotesdevelopmentalmyelination
AT dupreejeffreyl prolongedenvironmentalenrichmentpromotesdevelopmentalmyelination
AT gallovittorio prolongedenvironmentalenrichmentpromotesdevelopmentalmyelination