IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-44979-9.html
   My bibliography  Save this article

Early excitatory-inhibitory cortical modifications following skill learning are associated with motor memory consolidation and plasticity overnight

Author

Listed:
  • Tamir Eisenstein

    (Weizmann Institute of Science)

  • Edna Furman-Haran

    (Weizmann Institute of Science)

  • Assaf Tal

    (Weizmann Institute of Science)

Abstract

Consolidation of motor memories is vital to offline enhancement of new motor skills and involves short and longer-term offline processes following learning. While emerging evidence link glutamate and GABA dynamics in the primary motor cortex (M1) to online motor skill practice, its relationship with offline consolidation processes in humans is unclear. Using two-day repeated measures of behavioral and multimodal neuroimaging data before and following motor sequence learning, we show that short-term glutamatergic and GABAergic responses in M1 within minutes after learning were associated with longer-term learning-induced functional, structural, and behavioral modifications overnight. Furthermore, Glutamatergic and GABAergic modifications were differentially associated with different facets of motor memory consolidation. Our results point to unique and distinct roles of Glutamate and GABA in motor memory consolidation processes in the human brain across timescales and mechanistic levels, tying short-term changes on the neurochemical level to overnight changes in macroscale structure, function, and behavior.

Suggested Citation

  • Tamir Eisenstein & Edna Furman-Haran & Assaf Tal, 2024. "Early excitatory-inhibitory cortical modifications following skill learning are associated with motor memory consolidation and plasticity overnight," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44979-9
    DOI: 10.1038/s41467-024-44979-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-44979-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-44979-9?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. Rubin, Mark, 2021. "When to adjust alpha during multiple testing: A consideration of disjunction, conjunction, and individual testing," MetaArXiv tj6pm, Center for Open Science.
    2. Tonghui Xu & Xinzhu Yu & Andrew J. Perlik & Willie F. Tobin & Jonathan A. Zweig & Kelly Tennant & Theresa Jones & Yi Zuo, 2009. "Rapid formation and selective stabilization of synapses for enduring motor memories," Nature, Nature, vol. 462(7275), pages 915-919, December.
    3. Matthew P. Walker & Tiffany Brakefield & J. Allan Hobson & Robert Stickgold, 2003. "Dissociable stages of human memory consolidation and reconsolidation," Nature, Nature, vol. 425(6958), pages 616-620, October.
    4. Jocelyn Breton & Edwin M. Robertson, 2017. "Dual enhancement mechanisms for overnight motor memory consolidation," Nature Human Behaviour, Nature, vol. 1(6), pages 1-7, June.
    5. Ji Won Bang & Kazuhisa Shibata & Sebastian M. Frank & Edward G. Walsh & Mark W. Greenlee & Takeo Watanabe & Yuka Sasaki, 2018. "Consolidation and reconsolidation share behavioural and neurochemical mechanisms," Nature Human Behaviour, Nature, vol. 2(7), pages 507-513, July.
    6. N. Toni & P.-A. Buchs & I. Nikonenko & C. R. Bron & D. Muller, 1999. "LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite," Nature, Nature, vol. 402(6760), pages 421-425, November.
    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. Sho K Sugawara & Satoshi Tanaka & Shuntaro Okazaki & Katsumi Watanabe & Norihiro Sadato, 2012. "Social Rewards Enhance Offline Improvements in Motor Skill," PLOS ONE, Public Library of Science, vol. 7(11), pages 1-6, November.
    2. Francesco Paolo Ulloa Severino & Oluwadamilola O. Lawal & Kristina Sakers & Shiyi Wang & Namsoo Kim & Alexander David Friedman & Sarah Anne Johnson & Chaichontat Sriworarat & Ryan H. Hughes & Scott H., 2023. "Training-induced circuit-specific excitatory synaptogenesis in mice is required for effort control," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    3. Denis Ertelt & Karsten Witt & Kathrin Reetz & Wolfgang Frank & Klaus Junghanns & Jutta Backhaus & Vera Tadic & Antonello Pellicano & Jan Born & Ferdinand Binkofski, 2012. "Skill Memory Escaping from Distraction by Sleep—Evidence from Dual-Task Performance," PLOS ONE, Public Library of Science, vol. 7(12), pages 1-9, December.
    4. Benedikt Lauber & Jesper Lundbye-Jensen & Martin Keller & Albert Gollhofer & Wolfgang Taube & Christian Leukel, 2013. "Cross-Limb Interference during Motor Learning," PLOS ONE, Public Library of Science, vol. 8(12), pages 1-8, December.
    5. Barbara Feulner & Matthew G. Perich & Raeed H. Chowdhury & Lee E. Miller & Juan A. Gallego & Claudia Clopath, 2022. "Small, correlated changes in synaptic connectivity may facilitate rapid motor learning," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. Devesh Mishra & Nicholas R Harrison & Carolina B Gonzales & Björn Schilström & Åsa Konradsson-Geuken, 2015. "Effects of Age and Acute Ethanol on Glutamatergic Neurotransmission in the Medial Prefrontal Cortex of Freely Moving Rats Using Enzyme-Based Microelectrode Amperometry," PLOS ONE, Public Library of Science, vol. 10(4), pages 1-15, April.
    7. Bhavin R Sheth & Davit Janvelyan & Murtuza Khan, 2008. "Practice Makes Imperfect: Restorative Effects of Sleep on Motor Learning," PLOS ONE, Public Library of Science, vol. 3(9), pages 1-9, September.
    8. Sander Greenland, 2023. "Divergence versus decision P‐values: A distinction worth making in theory and keeping in practice: Or, how divergence P‐values measure evidence even when decision P‐values do not," Scandinavian Journal of Statistics, Danish Society for Theoretical Statistics;Finnish Statistical Society;Norwegian Statistical Association;Swedish Statistical Association, vol. 50(1), pages 54-88, March.
    9. Scott R. Burlingham & Nicole F. Wong & Lindsay Peterkin & Lily Lubow & Carolina Dos Santos Passos & Orion Benner & Michael Ghebrial & Thomas P. Cast & Matthew A. Xu-Friedman & Thomas C. Südhof & Soham, 2022. "Induction of synapse formation by de novo neurotransmitter synthesis," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    10. Rany Abend & Avi Karni & Avi Sadeh & Nathan A Fox & Daniel S Pine & Yair Bar-Haim, 2013. "Learning to Attend to Threat Accelerates and Enhances Memory Consolidation," PLOS ONE, Public Library of Science, vol. 8(4), pages 1-9, April.
    11. Roberta Patalano, 2007. "Mind-dependence. The past in the grip of the present," Discussion Papers 1_2007, D.E.S. (Department of Economic Studies), University of Naples "Parthenope", Italy.
    12. Moritz Deger & Moritz Helias & Stefan Rotter & Markus Diesmann, 2012. "Spike-Timing Dependence of Structural Plasticity Explains Cooperative Synapse Formation in the Neocortex," PLOS Computational Biology, Public Library of Science, vol. 8(9), pages 1-13, September.
    13. Konuk, Faruk Anıl & Otterbring, Tobias, 2024. "The dark side of going green: Dark triad traits predict organic consumption through virtue signaling, status signaling, and praise from others," Journal of Retailing and Consumer Services, Elsevier, vol. 76(C).
    14. Ella Gabitov & Arnaud Boutin & Basile Pinsard & Nitzan Censor & Stuart M Fogel & Geneviève Albouy & Bradley R King & Julie Carrier & Leonardo G Cohen & Avi Karni & Julien Doyon, 2019. "Susceptibility of consolidated procedural memory to interference is independent of its active task-based retrieval," PLOS ONE, Public Library of Science, vol. 14(1), pages 1-19, January.
    15. Johannes Holz & Hannah Piosczyk & Nina Landmann & Bernd Feige & Kai Spiegelhalder & Dieter Riemann & Christoph Nissen & Ulrich Voderholzer, 2012. "The Timing of Learning before Night-Time Sleep Differentially Affects Declarative and Procedural Long-Term Memory Consolidation in Adolescents," PLOS ONE, Public Library of Science, vol. 7(7), pages 1-10, July.
    16. Eleni Mitsea & Athanasios Drigas & Charalabos Skianis, 2022. "ICTs and Speed Learning in Special Education: High-Consciousness Training Strategies for High-Capacity Learners through Metacognition Lens," Technium Social Sciences Journal, Technium Science, vol. 27(1), pages 230-252, January.
    17. Fang, Ximeng & Goette, Lorenz & Rockenbach, Bettina & Sutter, Matthias & Tiefenbeck, Verena & Schoeb, Samuel & Staake, Thorsten, 2023. "Complementarities in behavioral interventions: Evidence from a field experiment on resource conservation," Journal of Public Economics, Elsevier, vol. 228(C).
    18. Sanne Ten Oever & Alexander T. Sack & Carina R. Oehrn & Nikolai Axmacher, 2021. "An engram of intentionally forgotten information," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    19. Roberta Patalano, 2007. "Mind-Dependence. The Past in the Grip of the Present," Journal of Bioeconomics, Springer, vol. 9(2), pages 85-107, August.
    20. Martin Hruska & Rachel E. Cain & Matthew B. Dalva, 2022. "Nanoscale rules governing the organization of glutamate receptors in spine synapses are subunit specific," Nature Communications, Nature, vol. 13(1), pages 1-19, 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:15:y:2024:i:1:d:10.1038_s41467-024-44979-9. 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.