IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48008-7.html
   My bibliography  Save this article

De novo motor learning creates structure in neural activity that shapes adaptation

Author

Listed:
  • Joanna C. Chang

    (Imperial College London)

  • Matthew G. Perich

    (Faculté de Médecine, Université de Montréal
    Québec Artificial Intelligence Institute)

  • Lee E. Miller

    (Northwestern University and Shirley Ryan Ability Lab)

  • Juan A. Gallego

    (Imperial College London)

  • Claudia Clopath

    (Imperial College London)

Abstract

Animals can quickly adapt learned movements to external perturbations, and their existing motor repertoire likely influences their ease of adaptation. Long-term learning causes lasting changes in neural connectivity, which shapes the activity patterns that can be produced during adaptation. Here, we examined how a neural population’s existing activity patterns, acquired through de novo learning, affect subsequent adaptation by modeling motor cortical neural population dynamics with recurrent neural networks. We trained networks on different motor repertoires comprising varying numbers of movements, which they acquired following various learning experiences. Networks with multiple movements had more constrained and robust dynamics, which were associated with more defined neural ‘structure’—organization in the available population activity patterns. This structure facilitated adaptation, but only when the changes imposed by the perturbation were congruent with the organization of the inputs and the structure in neural activity acquired during de novo learning. These results highlight trade-offs in skill acquisition and demonstrate how different learning experiences can shape the geometrical properties of neural population activity and subsequent adaptation.

Suggested Citation

  • Joanna C. Chang & Matthew G. Perich & Lee E. Miller & Juan A. Gallego & Claudia Clopath, 2024. "De novo motor learning creates structure in neural activity that shapes adaptation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48008-7
    DOI: 10.1038/s41467-024-48008-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48008-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-48008-7?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. 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.
    2. Juan A. Gallego & Matthew G. Perich & Stephanie N. Naufel & Christian Ethier & Sara A. Solla & Lee E. Miller, 2018. "Cortical population activity within a preserved neural manifold underlies multiple motor behaviors," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    3. Gamaleldin F. Elsayed & Antonio H. Lara & Matthew T. Kaufman & Mark M. Churchland & John P. Cunningham, 2016. "Reorganization between preparatory and movement population responses in motor cortex," Nature Communications, Nature, vol. 7(1), pages 1-15, December.
    4. 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.
    5. James B. Heald & Máté Lengyel & Daniel M. Wolpert, 2021. "Contextual inference underlies the learning of sensorimotor repertoires," Nature, Nature, vol. 600(7889), pages 489-493, December.
    6. Min Fu & Xinzhu Yu & Ju Lu & Yi Zuo, 2012. "Repetitive motor learning induces coordinated formation of clustered dendritic spines in vivo," Nature, Nature, vol. 483(7387), pages 92-95, March.
    7. Edward H. Nieh & Manuel Schottdorf & Nicolas W. Freeman & Ryan J. Low & Sam Lewallen & Sue Ann Koay & Lucas Pinto & Jeffrey L. Gauthier & Carlos D. Brody & David W. Tank, 2021. "Geometry of abstract learned knowledge in the hippocampus," Nature, Nature, vol. 595(7865), pages 80-84, July.
    8. Richard J. Gardner & Erik Hermansen & Marius Pachitariu & Yoram Burak & Nils A. Baas & Benjamin A. Dunn & May-Britt Moser & Edvard I. Moser, 2022. "Toroidal topology of population activity in grid cells," Nature, Nature, vol. 602(7895), pages 123-128, February.
    9. Mostafa Safaie & Joanna C. Chang & Junchol Park & Lee E. Miller & Joshua T. Dudman & Matthew G. Perich & Juan A. Gallego, 2023. "Preserved neural dynamics across animals performing similar behaviour," Nature, Nature, vol. 623(7988), pages 765-771, November.
    10. Xulu Sun & Daniel J. O’Shea & Matthew D. Golub & Eric M. Trautmann & Saurabh Vyas & Stephen I. Ryu & Krishna V. Shenoy, 2022. "Cortical preparatory activity indexes learned motor memories," Nature, Nature, vol. 602(7896), pages 274-279, February.
    11. Michael Okun & Nicholas A. Steinmetz & Lee Cossell & M. Florencia Iacaruso & Ho Ko & Péter Barthó & Tirin Moore & Sonja B. Hofer & Thomas D. Mrsic-Flogel & Matteo Carandini & Kenneth D. Harris, 2015. "Diverse coupling of neurons to populations in sensory cortex," Nature, Nature, vol. 521(7553), pages 511-515, May.
    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. Eric A. Kirk & Keenan T. Hope & Samuel J. Sober & Britton A. Sauerbrei, 2024. "An output-null signature of inertial load in motor cortex," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. Tanner C Dixon & Christina M Merrick & Joni D Wallis & Richard B Ivry & Jose M Carmena, 2021. "Hybrid dedicated and distributed coding in PMd/M1 provides separation and interaction of bilateral arm signals," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-35, November.
    3. Kisho Ogasa & Atsushi Yokoi & Gouki Okazawa & Morimichi Nishigaki & Masaya Hirashima & Nobuhiro Hagura, 2024. "Decision uncertainty as a context for motor memory," Nature Human Behaviour, Nature, vol. 8(9), pages 1738-1751, September.
    4. Wei-Long Zheng & Zhongxuan Wu & Ali Hummos & Guangyu Robert Yang & Michael M. Halassa, 2024. "Rapid context inference in a thalamocortical model using recurrent neural networks," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Jan Weber & Anne-Kristin Solbakk & Alejandro O. Blenkmann & Anais Llorens & Ingrid Funderud & Sabine Leske & Pål Gunnar Larsson & Jugoslav Ivanovic & Robert T. Knight & Tor Endestad & Randolph F. Helf, 2024. "Ramping dynamics and theta oscillations reflect dissociable signatures during rule-guided human behavior," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    6. Pierre O. Boucher & Tian Wang & Laura Carceroni & Gary Kane & Krishna V. Shenoy & Chandramouli Chandrasekaran, 2023. "Initial conditions combine with sensory evidence to induce decision-related dynamics in premotor cortex," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    7. 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.
    8. P. Dylan Rich & Stephan Yves Thiberge & Benjamin B. Scott & Caiying Guo & D. Gowanlock R. Tervo & Carlos D. Brody & Alla Y. Karpova & Nathaniel D. Daw & David W. Tank, 2024. "Magnetic voluntary head-fixation in transgenic rats enables lifespan imaging of hippocampal neurons," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    9. 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.
    10. Nir Even-Chen & Blue Sheffer & Saurabh Vyas & Stephen I Ryu & Krishna V Shenoy, 2019. "Structure and variability of delay activity in premotor cortex," PLOS Computational Biology, Public Library of Science, vol. 15(2), pages 1-17, February.
    11. Javier G. Orlandi & Mohammad Abdolrahmani & Ryo Aoki & Dmitry R. Lyamzin & Andrea Benucci, 2023. "Distributed context-dependent choice information in mouse posterior cortex," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    12. Zhiwei Xu & Erez Geron & Luis M. Pérez-Cuesta & Yang Bai & Wen-Biao Gan, 2023. "Generalized extinction of fear memory depends on co-allocation of synaptic plasticity in dendrites," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    13. 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.
    14. Joao Barbosa & Rémi Proville & Chris C. Rodgers & Michael R. DeWeese & Srdjan Ostojic & Yves Boubenec, 2023. "Early selection of task-relevant features through population gating," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    15. Jan Humplik & Gašper Tkačik, 2017. "Probabilistic models for neural populations that naturally capture global coupling and criticality," PLOS Computational Biology, Public Library of Science, vol. 13(9), pages 1-26, September.
    16. Michael Fauth & Florentin Wörgötter & Christian Tetzlaff, 2015. "The Formation of Multi-synaptic Connections by the Interaction of Synaptic and Structural Plasticity and Their Functional Consequences," PLOS Computational Biology, Public Library of Science, vol. 11(1), pages 1-29, January.
    17. Giovanni Diana & Thomas T J Sainsbury & Martin P Meyer, 2019. "Bayesian inference of neuronal assemblies," PLOS Computational Biology, Public Library of Science, vol. 15(10), pages 1-31, October.
    18. Davide Spalla & Alessandro Treves & Charlotte N. Boccara, 2022. "Angular and linear speed cells in the parahippocampal circuits," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    19. Sravani Kondapavulur & Stefan M. Lemke & David Darevsky & Ling Guo & Preeya Khanna & Karunesh Ganguly, 2022. "Transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    20. Yann Zerlaut & Alain Destexhe, 2017. "Heterogeneous firing responses predict diverse couplings to presynaptic activity in mice layer V pyramidal neurons," PLOS Computational Biology, Public Library of Science, vol. 13(4), pages 1-27, April.

    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_s41467-024-48008-7. 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.