Oligodendrocyte dynamics dictate cognitive performance outcomes of working memory training in mice
Abstract Previous work has shown that motor skill learning stimulates and requires generation of myelinating oligodendrocytes (OLs) from their precursor cells (OLPs) in the brains of adult mice. In the present study we ask whether OL production is also required for non-motor learning and cognition,...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-10-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-42293-4 |
| _version_ | 1797558496622804992 |
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| author | Takahiro Shimizu Stuart G. Nayar Matthew Swire Yi Jiang Matthew Grist Malte Kaller Cassandra Sampaio Baptista David M. Bannerman Heidi Johansen-Berg Katsutoshi Ogasawara Koujiro Tohyama Huiliang Li William D. Richardson |
| author_facet | Takahiro Shimizu Stuart G. Nayar Matthew Swire Yi Jiang Matthew Grist Malte Kaller Cassandra Sampaio Baptista David M. Bannerman Heidi Johansen-Berg Katsutoshi Ogasawara Koujiro Tohyama Huiliang Li William D. Richardson |
| author_sort | Takahiro Shimizu |
| collection | DOAJ |
| description | Abstract Previous work has shown that motor skill learning stimulates and requires generation of myelinating oligodendrocytes (OLs) from their precursor cells (OLPs) in the brains of adult mice. In the present study we ask whether OL production is also required for non-motor learning and cognition, using T-maze and radial-arm-maze tasks that tax spatial working memory. We find that maze training stimulates OLP proliferation and OL production in the medial prefrontal cortex (mPFC), anterior corpus callosum (genu), dorsal thalamus and hippocampal formation of adult male mice; myelin sheath formation is also stimulated in the genu. Genetic blockade of OL differentiation and neo-myelination in Myrf conditional-knockout mice strongly impairs training-induced improvements in maze performance. We find a strong positive correlation between the performance of individual wild type mice and the scale of OLP proliferation and OL generation during training, but not with the number or intensity of c-Fos+ neurons in their mPFC, underscoring the important role played by OL lineage cells in cognitive processing. |
| first_indexed | 2024-03-10T17:32:14Z |
| format | Article |
| id | doaj.art-0c5951f15afa4a27aeb235a513dc66e0 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-10T17:32:14Z |
| publishDate | 2023-10-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-0c5951f15afa4a27aeb235a513dc66e02023-11-20T09:58:19ZengNature PortfolioNature Communications2041-17232023-10-0114111910.1038/s41467-023-42293-4Oligodendrocyte dynamics dictate cognitive performance outcomes of working memory training in miceTakahiro Shimizu0Stuart G. Nayar1Matthew Swire2Yi Jiang3Matthew Grist4Malte Kaller5Cassandra Sampaio Baptista6David M. Bannerman7Heidi Johansen-Berg8Katsutoshi Ogasawara9Koujiro Tohyama10Huiliang Li11William D. Richardson12Wolfson Institute for Biomedical Research, University College LondonWolfson Institute for Biomedical Research, University College LondonWolfson Institute for Biomedical Research, University College LondonWolfson Institute for Biomedical Research, University College LondonWolfson Institute for Biomedical Research, University College LondonWellcome Centre for Integrative Neuroimaging, Department of Clinical Neurosciences, John Radcliffe Hospital, University of OxfordWellcome Centre for Integrative Neuroimaging, Department of Clinical Neurosciences, John Radcliffe Hospital, University of OxfordDepartment of Experimental Psychology, University of OxfordWellcome Centre for Integrative Neuroimaging, Department of Clinical Neurosciences, John Radcliffe Hospital, University of OxfordTechnical Support Center for Life Science Research, Iwate Medical UniversityDepartment of Physiology, Iwate Medical UniversityWolfson Institute for Biomedical Research, University College LondonWolfson Institute for Biomedical Research, University College LondonAbstract Previous work has shown that motor skill learning stimulates and requires generation of myelinating oligodendrocytes (OLs) from their precursor cells (OLPs) in the brains of adult mice. In the present study we ask whether OL production is also required for non-motor learning and cognition, using T-maze and radial-arm-maze tasks that tax spatial working memory. We find that maze training stimulates OLP proliferation and OL production in the medial prefrontal cortex (mPFC), anterior corpus callosum (genu), dorsal thalamus and hippocampal formation of adult male mice; myelin sheath formation is also stimulated in the genu. Genetic blockade of OL differentiation and neo-myelination in Myrf conditional-knockout mice strongly impairs training-induced improvements in maze performance. We find a strong positive correlation between the performance of individual wild type mice and the scale of OLP proliferation and OL generation during training, but not with the number or intensity of c-Fos+ neurons in their mPFC, underscoring the important role played by OL lineage cells in cognitive processing.https://doi.org/10.1038/s41467-023-42293-4 |
| spellingShingle | Takahiro Shimizu Stuart G. Nayar Matthew Swire Yi Jiang Matthew Grist Malte Kaller Cassandra Sampaio Baptista David M. Bannerman Heidi Johansen-Berg Katsutoshi Ogasawara Koujiro Tohyama Huiliang Li William D. Richardson Oligodendrocyte dynamics dictate cognitive performance outcomes of working memory training in mice Nature Communications |
| title | Oligodendrocyte dynamics dictate cognitive performance outcomes of working memory training in mice |
| title_full | Oligodendrocyte dynamics dictate cognitive performance outcomes of working memory training in mice |
| title_fullStr | Oligodendrocyte dynamics dictate cognitive performance outcomes of working memory training in mice |
| title_full_unstemmed | Oligodendrocyte dynamics dictate cognitive performance outcomes of working memory training in mice |
| title_short | Oligodendrocyte dynamics dictate cognitive performance outcomes of working memory training in mice |
| title_sort | oligodendrocyte dynamics dictate cognitive performance outcomes of working memory training in mice |
| url | https://doi.org/10.1038/s41467-023-42293-4 |
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