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Oligodendrocyte dynamics dictate cognitive performance outcomes of working memory training in mice

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Listed:
  • Takahiro Shimizu

    (University College London)

  • Stuart G. Nayar

    (University College London)

  • Matthew Swire

    (University College London)

  • Yi Jiang

    (University College London)

  • Matthew Grist

    (University College London)

  • Malte Kaller

    (University of Oxford)

  • Cassandra Sampaio Baptista

    (University of Oxford
    University of Glasgow)

  • David M. Bannerman

    (University of Oxford)

  • Heidi Johansen-Berg

    (University of Oxford)

  • Katsutoshi Ogasawara

    (Iwate Medical University)

  • Koujiro Tohyama

    (Iwate Medical University)

  • Huiliang Li

    (University College London)

  • William D. Richardson

    (University College London)

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.

Suggested Citation

  • 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 To, 2023. "Oligodendrocyte dynamics dictate cognitive performance outcomes of working memory training in mice," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42293-4
    DOI: 10.1038/s41467-023-42293-4
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    References listed on IDEAS

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    1. Makoto Tamura & Timothy J. Spellman & Andrew M. Rosen & Joseph A. Gogos & Joshua A. Gordon, 2017. "Hippocampal-prefrontal theta-gamma coupling during performance of a spatial working memory task," Nature Communications, Nature, vol. 8(1), pages 1-9, December.
    2. Torfi Sigurdsson & Kimberly L. Stark & Maria Karayiorgou & Joseph A. Gogos & Joshua A. Gordon, 2010. "Impaired hippocampal–prefrontal synchrony in a genetic mouse model of schizophrenia," Nature, Nature, vol. 464(7289), pages 763-767, April.
    3. Dwight E. Bergles & J. David B. Roberts & Peter Somogyi & Craig E. Jahr, 2000. "Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus," Nature, Nature, vol. 405(6783), pages 187-191, May.
    4. Timothy Spellman & Mattia Rigotti & Susanne E. Ahmari & Stefano Fusi & Joseph A. Gogos & Joshua A. Gordon, 2015. "Hippocampal–prefrontal input supports spatial encoding in working memory," Nature, Nature, vol. 522(7556), pages 309-314, June.
    5. Stanislaw Mitew & Ilan Gobius & Laura R. Fenlon & Stuart J. McDougall & David Hawkes & Yao Lulu Xing & Helena Bujalka & Andrew L. Gundlach & Linda J. Richards & Trevor J. Kilpatrick & Tobias D. Merson, 2018. "Pharmacogenetic stimulation of neuronal activity increases myelination in an axon-specific manner," Nature Communications, Nature, vol. 9(1), pages 1-16, December.
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