IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42293-4.html
   My bibliography  Save this article

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

Author

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42293-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-42293-4?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Maria Wilhelm & Yaroslav Sych & Aleksejs Fomins & José Luis Alatorre Warren & Christopher Lewis & Laia Serratosa Capdevila & Roman Boehringer & Elizabeth A. Amadei & Benjamin Grewe & Eoin C. O’Connor , 2023. "Striatum-projecting prefrontal cortex neurons support working memory maintenance," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Chang Hoon Cho & Ilana Vasilisa Deyneko & Dylann Cordova-Martinez & Juan Vazquez & Anne S. Maguire & Jenny R. Diaz & Abigail U. Carbonell & Jaafar O. Tindi & Min-Hui Cui & Roman Fleysher & Sophie Molh, 2023. "ANKS1B encoded AIDA-1 regulates social behaviors by controlling oligodendrocyte function," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    3. Hannah Muysers & Hung-Ling Chen & Johannes Hahn & Shani Folschweiller & Torfi Sigurdsson & Jonas-Frederic Sauer & Marlene Bartos, 2024. "A persistent prefrontal reference frame across time and task rules," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Huee Ru Chong & Yadollah Ranjbar-Slamloo & Malcolm Zheng Hao Ho & Xuan Ouyang & Tsukasa Kamigaki, 2023. "Functional alterations of the prefrontal circuit underlying cognitive aging in mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Irina Pochinok & Tristan M. Stöber & Jochen Triesch & Mattia Chini & Ileana L. Hanganu-Opatz, 2024. "A developmental increase of inhibition promotes the emergence of hippocampal ripples," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Yoav Printz & Pritish Patil & Mathias Mahn & Asaf Benjamin & Anna Litvin & Rivka Levy & Max Bringmann & Ofer Yizhar, 2023. "Determinants of functional synaptic connectivity among amygdala-projecting prefrontal cortical neurons in male mice," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    7. Yann Vanrobaeys & Utsav Mukherjee & Lucy Langmack & Stacy E. Beyer & Ethan Bahl & Li-Chun Lin & Jacob J. Michaelson & Ted Abel & Snehajyoti Chatterjee, 2023. "Mapping the spatial transcriptomic signature of the hippocampus during memory consolidation," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Golia Shafiei & Ben D. Fulcher & Bradley Voytek & Theodore D. Satterthwaite & Sylvain Baillet & Bratislav Misic, 2023. "Neurophysiological signatures of cortical micro-architecture," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    9. Xhoela Bame & Robert A. Hill, 2024. "Mitochondrial network reorganization and transient expansion during oligodendrocyte generation," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    10. Frederic Fiore & Khaleel Alhalaseh & Ram R. Dereddi & Felipe Bodaleo Torres & Ilknur Çoban & Ali Harb & Amit Agarwal, 2023. "Norepinephrine regulates calcium signals and fate of oligodendrocyte precursor cells in the mouse cerebral cortex," Nature Communications, Nature, vol. 14(1), pages 1-25, December.
    11. Li-Pao Fang & Na Zhao & Laura C. Caudal & Hsin-Fang Chang & Renping Zhao & Ching-Hsin Lin & Nadine Hainz & Carola Meier & Bernhard Bettler & Wenhui Huang & Anja Scheller & Frank Kirchhoff & Xianshu Ba, 2022. "Impaired bidirectional communication between interneurons and oligodendrocyte precursor cells affects social cognitive behavior," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    12. M. Angeles Rabadan & Estanislao Daniel De La Cruz & Sneha B. Rao & Yannan Chen & Cheng Gong & Gregg Crabtree & Bin Xu & Sander Markx & Joseph A. Gogos & Rafael Yuste & Raju Tomer, 2022. "An in vitro model of neuronal ensembles," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    13. Steven Schepanski & Mattia Chini & Veronika Sternemann & Christopher Urbschat & Kristin Thiele & Ting Sun & Yu Zhao & Mareike Poburski & Anna Woestemeier & Marie-Theres Thieme & Dimitra E. Zazara & Ma, 2022. "Pregnancy-induced maternal microchimerism shapes neurodevelopment and behavior in mice," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    14. Brian P. Rummell & Solmaz Bikas & Susanne S. Babl & Joseph A. Gogos & Torfi Sigurdsson, 2023. "Altered corollary discharge signaling in the auditory cortex of a mouse model of schizophrenia predisposition," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42293-4. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.