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Cortical preparatory activity indexes learned motor memories

Author

Listed:
  • Xulu Sun

    (Stanford University
    Stanford University)

  • Daniel J. O’Shea

    (Stanford University
    Stanford University)

  • Matthew D. Golub

    (Stanford University
    Stanford University)

  • Eric M. Trautmann

    (Stanford University
    Stanford University)

  • Saurabh Vyas

    (Stanford University
    Stanford University)

  • Stephen I. Ryu

    (Stanford University
    Palo Alto Medical Foundation
    Stanford University)

  • Krishna V. Shenoy

    (Stanford University
    Stanford University
    Stanford University
    Stanford University)

Abstract

The brain’s remarkable ability to learn and execute various motor behaviours harnesses the capacity of neural populations to generate a variety of activity patterns. Here we explore systematic changes in preparatory activity in motor cortex that accompany motor learning. We trained rhesus monkeys to learn an arm-reaching task1 in a curl force field that elicited new muscle forces for some, but not all, movement directions2,3. We found that in a neural subspace predictive of hand forces, changes in preparatory activity tracked the learned behavioural modifications and reassociated4 existing activity patterns with updated movements. Along a neural population dimension orthogonal to the force-predictive subspace, we discovered that preparatory activity shifted uniformly for all movement directions, including those unaltered by learning. During a washout period when the curl field was removed, preparatory activity gradually reverted in the force-predictive subspace, but the uniform shift persisted. These persistent preparatory activity patterns may retain a motor memory of the learned field5,6 and support accelerated relearning of the same curl field. When a set of distinct curl fields was learned in sequence, we observed a corresponding set of field-specific uniform shifts which separated the associated motor memories in the neural state space7–9. The precise geometry of these uniform shifts in preparatory activity could serve to index motor memories, facilitating the acquisition, retention and retrieval of a broad motor repertoire.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:nature:v:602:y:2022:i:7896:d:10.1038_s41586-021-04329-x
    DOI: 10.1038/s41586-021-04329-x
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    Cited by:

    1. 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.
    2. 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.
    3. 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.

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