IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43257-4.html
   My bibliography  Save this article

Internal states as a source of subject-dependent movement variability are represented by large-scale brain networks

Author

Listed:
  • Macauley Smith Breault

    (Massachusetts Institute of Technology
    Johns Hopkins University)

  • Pierre Sacré

    (University of Liège)

  • Zachary B. Fitzgerald

    (Northwestern University)

  • John T. Gale

    (DIXI Neurolab, Inc.)

  • Kathleen E. Cullen

    (Johns Hopkins University)

  • Jorge A. González-Martínez

    (University of Pittsburgh)

  • Sridevi V. Sarma

    (Johns Hopkins University)

Abstract

Humans’ ability to adapt and learn relies on reflecting on past performance. These experiences form latent representations called internal states that induce movement variability that improves how we interact with our environment. Our study uncovered temporal dynamics and neural substrates of two states from ten subjects implanted with intracranial depth electrodes while they performed a goal-directed motor task with physical perturbations. We identified two internal states using state-space models: one tracking past errors and the other past perturbations. These states influenced reaction times and speed errors, revealing how subjects strategize from trial history. Using local field potentials from over 100 brain regions, we found large-scale brain networks such as the dorsal attention and default mode network modulate visuospatial attention based on recent performance and environmental feedback. Notably, these networks were more prominent in higher-performing subjects, emphasizing their role in improving motor performance by regulating movement variability through internal states.

Suggested Citation

  • Macauley Smith Breault & Pierre Sacré & Zachary B. Fitzgerald & John T. Gale & Kathleen E. Cullen & Jorge A. González-Martínez & Sridevi V. Sarma, 2023. "Internal states as a source of subject-dependent movement variability are represented by large-scale brain networks," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43257-4
    DOI: 10.1038/s41467-023-43257-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43257-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-43257-4?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. Anthony Randal McIntosh & Natasa Kovacevic & Roxane J Itier, 2008. "Increased Brain Signal Variability Accompanies Lower Behavioral Variability in Development," PLOS Computational Biology, Public Library of Science, vol. 4(7), pages 1-9, July.
    2. Eun Jung Hwang & Jeffrey E. Dahlen & Madan Mukundan & Takaki Komiyama, 2017. "History-based action selection bias in posterior parietal cortex," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    3. Howard Muchen Hsu & Zai-Fu Yao & Kai Hwang & Shulan Hsieh, 2020. "Between-module functional connectivity of the salient ventral attention network and dorsal attention network is associated with motor inhibition," PLOS ONE, Public Library of Science, vol. 15(12), pages 1-15, December.
    4. Megan T. deBettencourt & Paul A. Keene & Edward Awh & Edward K. Vogel, 2019. "Real-time triggering reveals concurrent lapses of attention and working memory," Nature Human Behaviour, Nature, vol. 3(8), pages 808-816, August.
    5. Nikos K. Logothetis, 2008. "What we can do and what we cannot do with fMRI," Nature, Nature, vol. 453(7197), pages 869-878, June.
    6. Aaron Kucyi & Amy Daitch & Omri Raccah & Baotian Zhao & Chao Zhang & Michael Esterman & Michael Zeineh & Casey H. Halpern & Kai Zhang & Jianguo Zhang & Josef Parvizi, 2020. "Electrophysiological dynamics of antagonistic brain networks reflect attentional fluctuations," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    7. Christopher M. Harris & Daniel M. Wolpert, 1998. "Signal-dependent noise determines motor planning," Nature, Nature, vol. 394(6695), pages 780-784, August.
    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. Luis M. Franco & Michael J. Goard, 2024. "Differential stability of task variable representations in retrosplenial cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. 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.
    3. 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.
    4. Ankita Sengupta & Sanjna Banerjee & Suhas Ganesh & Shrey Grover & Devarajan Sridharan, 2024. "The right posterior parietal cortex mediates spatial reorienting of attentional choice bias," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    5. 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.
    6. Jessie M H Szostakiwskyj & Stephanie E Willatt & Filomeno Cortese & Andrea B Protzner, 2017. "The modulation of EEG variability between internally- and externally-driven cognitive states varies with maturation and task performance," PLOS ONE, Public Library of Science, vol. 12(7), pages 1-27, July.
    7. 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.
    8. repec:hum:wpaper:sfb649dp2014-036 is not listed on IDEAS
    9. 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.
    10. Alejandro Morán & Miguel C Soriano, 2018. "Improving the quality of a collective signal in a consumer EEG headset," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-21, May.
    11. 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.
    12. Adam S. Tuzolele Mbuku, 2024. "Evolution of the concept of Homo Economicus in light of advances in Neuroeconomics: towards a more realistic model of economic decision-making [Evolution du concept de l'Homo Economicus à la lumièr," Post-Print hal-04564775, HAL.
    13. 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.
    14. Mazen El-Baba & Daniel J Lewis & Zhuo Fang & Adrian M Owen & Stuart M Fogel & J Bruce Morton, 2019. "Functional connectivity dynamics slow with descent from wakefulness to sleep," PLOS ONE, Public Library of Science, vol. 14(12), pages 1-13, December.
    15. 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.
    16. 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.
    17. 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.
    18. 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.
    19. Pérez-Centeno, Victor, 2018. "Brain-driven entrepreneurship research: Expanded review and research agenda towards entrepreneurial enhancement," Working Papers 02/18, Institut für Mittelstandsforschung (IfM) Bonn.
    20. 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.
    21. Wei Zhang & Sasha Reschechtko & Barry Hahn & Cynthia Benson & Elias Youssef, 2019. "Force-stabilizing synergies can be retained by coordinating sensory-blocked and sensory-intact digits," PLOS ONE, Public Library of Science, vol. 14(12), pages 1-17, 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_s41467-023-43257-4. 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.