IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37981-0.html
   My bibliography  Save this article

Multidimensional cerebellar computations for flexible kinematic control of movements

Author

Listed:
  • Akshay Markanday

    (Eberhard Karls University Tübingen)

  • Sungho Hong

    (Okinawa Institute of Science and Technology)

  • Junya Inoue

    (Eberhard Karls University Tübingen)

  • Erik Schutter

    (Okinawa Institute of Science and Technology)

  • Peter Thier

    (Eberhard Karls University Tübingen)

Abstract

Both the environment and our body keep changing dynamically. Hence, ensuring movement precision requires adaptation to multiple demands occurring simultaneously. Here we show that the cerebellum performs the necessary multi-dimensional computations for the flexible control of different movement parameters depending on the prevailing context. This conclusion is based on the identification of a manifold-like activity in both mossy fibers (MFs, network input) and Purkinje cells (PCs, output), recorded from monkeys performing a saccade task. Unlike MFs, the PC manifolds developed selective representations of individual movement parameters. Error feedback-driven climbing fiber input modulated the PC manifolds to predict specific, error type-dependent changes in subsequent actions. Furthermore, a feed-forward network model that simulated MF-to-PC transformations revealed that amplification and restructuring of the lesser variability in the MF activity is a pivotal circuit mechanism. Therefore, the flexible control of movements by the cerebellum crucially depends on its capacity for multi-dimensional computations.

Suggested Citation

  • Akshay Markanday & Sungho Hong & Junya Inoue & Erik Schutter & Peter Thier, 2023. "Multidimensional cerebellar computations for flexible kinematic control of movements," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37981-0
    DOI: 10.1038/s41467-023-37981-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37981-0
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-37981-0?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. Peter Thier & Peter W. Dicke & Roman Haas & Shabtai Barash, 2000. "Encoding of movement time by populations of cerebellar Purkinje cells," Nature, Nature, vol. 405(6782), pages 72-76, May.
    2. 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.
    3. David J. Herzfeld & Yoshiko Kojima & Robijanto Soetedjo & Reza Shadmehr, 2015. "Encoding of action by the Purkinje cells of the cerebellum," Nature, Nature, vol. 526(7573), pages 439-442, October.
    4. 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.
    5. Jaeeon Lee & Bernardo L. Sabatini, 2021. "Striatal indirect pathway mediates exploration via collicular competition," Nature, Nature, vol. 599(7886), pages 645-649, November.
    6. Marta Jelitai & Paolo Puggioni & Taro Ishikawa & Arianna Rinaldi & Ian Duguid, 2016. "Dendritic excitation–inhibition balance shapes cerebellar output during motor behaviour," Nature Communications, Nature, vol. 7(1), pages 1-13, December.
    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. 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.
    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. Chris. I. De Zeeuw & Julius Koppen & George. G. Bregman & Marit Runge & Devika Narain, 2023. "Heterogeneous encoding of temporal stimuli in the cerebellar cortex," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    4. 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.
    5. François G. C. Blot & Joshua J. White & Amy van Hattem & Licia Scotti & Vaishnavi Balaji & Youri Adolfs & R. Jeroen Pasterkamp & Chris I. De Zeeuw & Martijn Schonewille, 2023. "Purkinje cell microzones mediate distinct kinematics of a single movement," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Shan Yu & Andreas Klaus & Hongdian Yang & Dietmar Plenz, 2014. "Scale-Invariant Neuronal Avalanche Dynamics and the Cut-Off in Size Distributions," PLOS ONE, Public Library of Science, vol. 9(6), pages 1-12, June.
    7. Adrian M Haith & David M Huberdeau & John W Krakauer, 2015. "Hedging Your Bets: Intermediate Movements as Optimal Behavior in the Context of an Incomplete Decision," PLOS Computational Biology, Public Library of Science, vol. 11(3), pages 1-21, March.
    8. 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.
    9. Hagai Lalazar & L F Abbott & Eilon Vaadia, 2016. "Tuning Curves for Arm Posture Control in Motor Cortex Are Consistent with Random Connectivity," PLOS Computational Biology, Public Library of Science, vol. 12(5), pages 1-27, May.
    10. Benjamin R Cowley & Matthew A Smith & Adam Kohn & Byron M Yu, 2016. "Stimulus-Driven Population Activity Patterns in Macaque Primary Visual Cortex," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-31, December.
    11. 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.
    12. Daigo Takeuchi & Dheeraj Roy & Shruti Muralidhar & Takashi Kawai & Andrea Bari & Chanel Lovett & Heather A. Sullivan & Ian R. Wickersham & Susumu Tonegawa, 2022. "Cingulate-motor circuits update rule representations for sequential choice decisions," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    13. David Kappel & Bernhard Nessler & Wolfgang Maass, 2014. "STDP Installs in Winner-Take-All Circuits an Online Approximation to Hidden Markov Model Learning," PLOS Computational Biology, Public Library of Science, vol. 10(3), pages 1-22, March.
    14. Simon Sponberg & Thomas L Daniel & Adrienne L Fairhall, 2015. "Dual Dimensionality Reduction Reveals Independent Encoding of Motor Features in a Muscle Synergy for Insect Flight Control," PLOS Computational Biology, Public Library of Science, vol. 11(4), pages 1-23, April.
    15. Julian Rossbroich & Daniel Trotter & John Beninger & Katalin Tóth & Richard Naud, 2021. "Linear-nonlinear cascades capture synaptic dynamics," PLOS Computational Biology, Public Library of Science, vol. 17(3), pages 1-27, March.
    16. Svenja Melbaum & Eleonora Russo & David Eriksson & Artur Schneider & Daniel Durstewitz & Thomas Brox & Ilka Diester, 2022. "Conserved structures of neural activity in sensorimotor cortex of freely moving rats allow cross-subject decoding," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    17. Yuangen Yao & Haiyou Deng & Chengzhang Ma & Ming Yi & Jun Ma, 2017. "Impact of Bounded Noise and Rewiring on the Formation and Instability of Spiral Waves in a Small-World Network of Hodgkin-Huxley Neurons," PLOS ONE, Public Library of Science, vol. 12(1), pages 1-13, January.
    18. Jorge Gámez & Germán Mendoza & Luis Prado & Abraham Betancourt & Hugo Merchant, 2019. "The amplitude in periodic neural state trajectories underlies the tempo of rhythmic tapping," PLOS Biology, Public Library of Science, vol. 17(4), pages 1-32, April.
    19. Maria N Ayala & Denise Y P Henriques, 2018. "Context-dependent concurrent adaptation to static and moving targets," PLOS ONE, Public Library of Science, vol. 13(2), pages 1-23, February.
    20. Maya Zhe Wang & Benjamin Y. Hayden & Sarah R. Heilbronner, 2022. "A structural and functional subdivision in central orbitofrontal cortex," Nature Communications, Nature, vol. 13(1), pages 1-12, December.

    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:14:y:2023:i:1:d:10.1038_s41467-023-37981-0. 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.