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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
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    References listed on IDEAS

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    1. 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.
    2. 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.
    3. 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.
    4. Nikos K. Logothetis, 2008. "What we can do and what we cannot do with fMRI," Nature, Nature, vol. 453(7197), pages 869-878, June.
    5. 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.
    6. 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.
    7. Christopher M. Harris & Daniel M. Wolpert, 1998. "Signal-dependent noise determines motor planning," Nature, Nature, vol. 394(6695), pages 780-784, August.
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