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Reach-dependent reorientation of rotational dynamics in motor cortex

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  • David A. Sabatini

    (The University of Chicago
    The University of Chicago)

  • Matthew T. Kaufman

    (The University of Chicago
    The University of Chicago)

Abstract

During reaching, neurons in motor cortex exhibit complex, time-varying activity patterns. Though single-neuron activity correlates with movement parameters, movement correlations explain neural activity only partially. Neural responses also reflect population-level dynamics thought to generate outputs. These dynamics have previously been described as “rotational,” such that activity orbits in neural state space. Here, we reanalyze reaching datasets from male Rhesus macaques and find two essential features that cannot be accounted for with standard dynamics models. First, the planes in which rotations occur differ for different reaches. Second, this variation in planes reflects the overall location of activity in neural state space. Our “location-dependent rotations” model fits nearly all motor cortex activity during reaching, and high-quality decoding of reach kinematics reveals a quasilinear relationship with spiking. Varying rotational planes allows motor cortex to produce richer outputs than possible under previous models. Finally, our model links representational and dynamical ideas: representation is present in the state space location, which dynamics then convert into time-varying command signals.

Suggested Citation

  • David A. Sabatini & Matthew T. Kaufman, 2024. "Reach-dependent reorientation of rotational dynamics in motor cortex," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51308-7
    DOI: 10.1038/s41467-024-51308-7
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    References listed on IDEAS

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    1. A. H. Lara & J. P. Cunningham & M. M. Churchland, 2018. "Different population dynamics in the supplementary motor area and motor cortex during reaching," Nature Communications, Nature, vol. 9(1), pages 1-16, December.
    2. Stefano Recanatesi & Matthew Farrell & Guillaume Lajoie & Sophie Deneve & Mattia Rigotti & Eric Shea-Brown, 2021. "Predictive learning as a network mechanism for extracting low-dimensional latent space representations," Nature Communications, Nature, vol. 12(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. Mark M. Churchland & John P. Cunningham & Matthew T. Kaufman & Justin D. Foster & Paul Nuyujukian & Stephen I. Ryu & Krishna V. Shenoy, 2012. "Neural population dynamics during reaching," Nature, Nature, vol. 487(7405), pages 51-56, July.
    5. Jonathan C. Kao & Paul Nuyujukian & Stephen I. Ryu & Mark M. Churchland & John P. Cunningham & Krishna V. Shenoy, 2015. "Single-trial dynamics of motor cortex and their applications to brain-machine interfaces," Nature Communications, Nature, vol. 6(1), pages 1-12, November.
    6. Jonathan A Michaels & Benjamin Dann & Hansjörg Scherberger, 2016. "Neural Population Dynamics during Reaching Are Better Explained by a Dynamical System than Representational Tuning," PLOS Computational Biology, Public Library of Science, vol. 12(11), pages 1-22, November.
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