IDEAS home Printed from https://ideas.repec.org/a/plo/pcbi00/1009338.html
   My bibliography  Save this article

An approximate stochastic optimal control framework to simulate nonlinear neuro-musculoskeletal models in the presence of noise

Author

Listed:
  • Tom Van Wouwe
  • Lena H Ting
  • Friedl De Groote

Abstract

Optimal control simulations have shown that both musculoskeletal dynamics and physiological noise are important determinants of movement. However, due to the limited efficiency of available computational tools, deterministic simulations of movement focus on accurately modelling the musculoskeletal system while neglecting physiological noise, and stochastic simulations account for noise while simplifying the dynamics. We took advantage of recent approaches where stochastic optimal control problems are approximated using deterministic optimal control problems, which can be solved efficiently using direct collocation. We were thus able to extend predictions of stochastic optimal control as a theory of motor coordination to include muscle coordination and movement patterns emerging from non-linear musculoskeletal dynamics. In stochastic optimal control simulations of human standing balance, we demonstrated that the inclusion of muscle dynamics can predict muscle co-contraction as minimal effort strategy that complements sensorimotor feedback control in the presence of sensory noise. In simulations of reaching, we demonstrated that nonlinear multi-segment musculoskeletal dynamics enables complex perturbed and unperturbed reach trajectories under a variety of task conditions to be predicted. In both behaviors, we demonstrated how interactions between task constraint, sensory noise, and the intrinsic properties of muscle influence optimal muscle coordination patterns, including muscle co-contraction, and the resulting movement trajectories. Our approach enables a true minimum effort solution to be identified as task constraints, such as movement accuracy, can be explicitly imposed, rather than being approximated using penalty terms in the cost function. Our approximate stochastic optimal control framework predicts complex features, not captured by previous simulation approaches, providing a generalizable and valuable tool to study how musculoskeletal dynamics and physiological noise may alter neural control of movement in both healthy and pathological movements.Author summary: Model-based simulations have advanced our insight in how movement is controlled, but computational limitations have prevented us from simultaneously considering the effects of nonlinear musculoskeletal dynamics and noise on neural control on movement strategies. Here we present a novel simulation framework that addresses this methodological gap and demonstrate its potential to predict features of motor control that have not been predicted previously. Our framework enables neural control mechanisms to be simulated and the optimal control strategy in the presence of noise to be computed. We demonstrate for the first time that muscle co-contraction–a motor strategy thought to be energetically costly–can help to reduce the effort required to stabilize standing postural control, even when feedback is present. We also demonstrate that multi-segmental models of the arm actuated by muscle can predict complex reach and perturbed reach trajectories that were not explained by simplified models. The ability to predict muscle activation patterns and kinematics of joints extends the theory of optimal control to variables that can be used to directly explain muscle and joint coordination. Our computational approach is broadly applicable and may be extendable to other normal and impaired movements, as well as aid in the design of assistive devices.

Suggested Citation

  • Tom Van Wouwe & Lena H Ting & Friedl De Groote, 2022. "An approximate stochastic optimal control framework to simulate nonlinear neuro-musculoskeletal models in the presence of noise," PLOS Computational Biology, Public Library of Science, vol. 18(6), pages 1-30, June.
  • Handle: RePEc:plo:pcbi00:1009338
    DOI: 10.1371/journal.pcbi.1009338
    as

    Download full text from publisher

    File URL: https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1009338
    Download Restriction: no

    File URL: https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1009338&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pcbi.1009338?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. repec:plo:pcbi00:1006993 is not listed on IDEAS
    2. Christopher M. Harris & Daniel M. Wolpert, 1998. "Signal-dependent noise determines motor planning," Nature, Nature, vol. 394(6695), pages 780-784, August.
    3. Etienne Burdet & Rieko Osu & David W. Franklin & Theodore E. Milner & Mitsuo Kawato, 2001. "The central nervous system stabilizes unstable dynamics by learning optimal impedance," Nature, Nature, vol. 414(6862), pages 446-449, 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. Ashesh Vasalya & Gowrishankar Ganesh & Abderrahmane Kheddar, 2018. "More than just co-workers: Presence of humanoid robot co-worker influences human performance," PLOS ONE, Public Library of Science, vol. 13(11), pages 1-19, November.
    2. Bastien Berret & Frédéric Jean, 2020. "Stochastic optimal open-loop control as a theory of force and impedance planning via muscle co-contraction," PLOS Computational Biology, Public Library of Science, vol. 16(2), pages 1-28, February.
    3. Bastien Berret & Adrien Conessa & Nicolas Schweighofer & Etienne Burdet, 2021. "Stochastic optimal feedforward-feedback control determines timing and variability of arm movements with or without vision," PLOS Computational Biology, Public Library of Science, vol. 17(6), pages 1-24, June.
    4. repec:plo:pone00:0099087 is not listed on IDEAS
    5. Abdelhamid Kadiallah & David W Franklin & Etienne Burdet, 2012. "Generalization in Adaptation to Stable and Unstable Dynamics," PLOS ONE, Public Library of Science, vol. 7(10), pages 1-11, October.
    6. Shogo Yonekura & Yasuo Kuniyoshi, 2017. "Bodily motion fluctuation improves reaching success rate in a neurophysical agent via geometric-stochastic resonance," PLOS ONE, Public Library of Science, vol. 12(12), pages 1-16, December.
    7. Shih-Wei Wu & Maria F Dal Martello & Laurence T Maloney, 2009. "Sub-Optimal Allocation of Time in Sequential Movements," PLOS ONE, Public Library of Science, vol. 4(12), pages 1-13, December.
    8. Max Berniker & Megan K O’Brien & Konrad P Kording & Alaa A Ahmed, 2013. "An Examination of the Generalizability of Motor Costs," PLOS ONE, Public Library of Science, vol. 8(1), pages 1-11, January.
    9. repec:plo:pone00:0125464 is not listed on IDEAS
    10. Ian S Howard & David W Franklin, 2015. "Neural Tuning Functions Underlie Both Generalization and Interference," PLOS ONE, Public Library of Science, vol. 10(6), pages 1-21, June.
    11. Lionel Rigoux & Emmanuel Guigon, 2012. "A Model of Reward- and Effort-Based Optimal Decision Making and Motor Control," PLOS Computational Biology, Public Library of Science, vol. 8(10), pages 1-13, October.
    12. Yanhao Ren & Qiang Luo & Wenlian Lu, 2023. "Synchronization Analysis of Linearly Coupled Systems with Signal-Dependent Noises," Mathematics, MDPI, vol. 11(10), pages 1-15, May.
    13. Jack Brookes & Faisal Mushtaq & Earle Jamieson & Aaron J Fath & Geoffrey Bingham & Peter Culmer & Richard M Wilkie & Mark Mon-Williams, 2020. "Exploring disturbance as a force for good in motor learning," PLOS ONE, Public Library of Science, vol. 15(5), pages 1-21, May.
    14. Christopher J Hasson & Zhaoran Zhang & Masaki O Abe & Dagmar Sternad, 2016. "Neuromotor Noise Is Malleable by Amplifying Perceived Errors," PLOS Computational Biology, Public Library of Science, vol. 12(8), pages 1-28, August.
    15. Seth W. Egger & Stephen G. Lisberger, 2022. "Neural structure of a sensory decoder for motor control," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    16. repec:plo:pcbi00:1002843 is not listed on IDEAS
    17. repec:plo:pone00:0013601 is not listed on IDEAS
    18. Josh Merel & Donald M Pianto & John P Cunningham & Liam Paninski, 2015. "Encoder-Decoder Optimization for Brain-Computer Interfaces," PLOS Computational Biology, Public Library of Science, vol. 11(6), pages 1-25, June.
    19. Nidhi Seethapathi & Barrett C. Clark & Manoj Srinivasan, 2024. "Exploration-based learning of a stabilizing controller predicts locomotor adaptation," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    20. repec:plo:pcbi00:1002634 is not listed on IDEAS
    21. Maxime Teremetz & Isabelle Amado & Narjes Bendjemaa & Marie-Odile Krebs & Pavel G Lindberg & Marc A Maier, 2014. "Deficient Grip Force Control in Schizophrenia: Behavioral and Modeling Evidence for Altered Motor Inhibition and Motor Noise," PLOS ONE, Public Library of Science, vol. 9(11), pages 1-11, November.
    22. Frederic Danion & Raoul M Bongers & Reinoud J Bootsma, 2014. "The Trade-Off between Spatial and Temporal Variabilities in Reciprocal Upper-Limb Aiming Movements of Different Durations," PLOS ONE, Public Library of Science, vol. 9(5), pages 1-10, May.
    23. repec:plo:pone00:0226596 is not listed on IDEAS
    24. Julian J Tramper & Bart van den Broek & Wim Wiegerinck & Hilbert J Kappen & Stan Gielen, 2012. "Time-Integrated Position Error Accounts for Sensorimotor Behavior in Time-Constrained Tasks," PLOS ONE, Public Library of Science, vol. 7(3), pages 1-10, March.
    25. Konrad P Körding & Izumi Fukunaga & Ian S Howard & James N Ingram & Daniel M Wolpert, 2004. "A Neuroeconomics Approach to Inferring Utility Functions in Sensorimotor Control," PLOS Biology, Public Library of Science, vol. 2(10), pages 1-1, September.
    26. Pierre Morel & Philipp Ulbrich & Alexander Gail, 2017. "What makes a reach movement effortful? Physical effort discounting supports common minimization principles in decision making and motor control," PLOS Biology, Public Library of Science, vol. 15(6), pages 1-23, June.

    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:plo:pcbi00:1009338. 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: ploscompbiol (email available below). General contact details of provider: https://journals.plos.org/ploscompbiol/ .

    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.