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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
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    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
    11. 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.
    Full references (including those not matched with items on IDEAS)

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