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Different modulation of oscillatory common neural drives to ankle muscles during abrupt and gradual gait adaptations

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Abstract

Different neural contributions to motor learning might be involved when different error sizes of perturbation are introduced. Although the corticospinal drive contributes to abrupt gait adaptation processes, no studies have investigated whether cortical involvement during gait differs between perturbations applied abruptly and gradually. This study aimed to investigate the differences in oscillatory common neural drives to ankle muscles during gait between abrupt and gradual adaptations, using coherence analyses of paired surface electromyographic (EMG) recordings. Sixteen healthy young adults performed the treadmill gait with perturbation resisting forward movement of the swing leg for 10 min under two conditions: abrupt (a large perturbation from the beginning of the adaptation period) and gradual (a series of small perturbations that gradually increased). Swing phase duration and step length showed significantly greater asymmetry in the abrupt condition than in the gradual condition in the early adaptation period (p < 0.01), despite no significant differences in gait symmetries between the two conditions in the early post-adaptation period. EMG–EMG coherence calculated from the tibialis anterior muscle in the beta band (15–35 Hz) on the perturbed side was significantly higher in the early adaptation period in the abrupt condition (p < 0.05), but not in the gradual condition. There were significant relationships between changes in temporal gait symmetry and EMG–EMG coherence during the different adaptation periods between the two conditions (p < 0.05). The abrupt large perturbation seems to require a cortical involvement, whereas a gradual adaptation with small gait asymmetry requires no modulation of cortical involvement.

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Data availability

The data in this study will be made available upon reasonable request to the corresponding author.

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Acknowledgements

We would like to thank Editage (http://www.editage.jp) for English language editing.

Funding

This study was partially supported by Grants-in-Aid for Research Activity Start-up (17H06770) and Early-Career Scientists (19K19866 and 21K17455) from the Japan Society for the Promotion of Science.

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Authors and Affiliations

  1. Department of Physical Therapy, Niigata University of Health and Welfare, 1398, Shimami‑cho, Kita‑ku, Niigata, 950‑3198, Japan

    Ryosuke Kitatani

  2. Institute for Human Movement and Medical Sciences, Niigata University of Health and Welfare, Niigata, Japan

    Ryosuke Kitatani

  3. Department of Physical Therapy, Human Health Sciences, Graduate School of Medicine, Kyoto University, Kyoto, Japan

    Ryosuke Kitatani, Ayaka Maeda, Jun Umehara & Shigehito Yamada

  4. Center for Information and Neural Networks, National Institute of Information and Communications Technology, Osaka, Japan

    Jun Umehara

  5. Japan Society for the Promotion of Science, Tokyo, Japan

    Jun Umehara

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  1. Ryosuke Kitatani
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  3. Jun Umehara
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  4. Shigehito Yamada
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Contributions

All authors have made significant contributions to this article. Specifically, RK, AM, JU, and SY contributed to the research design and manuscript writing, and RK, AM, and JU contributed to data collection and analysis. All authors approved the final version of the manuscript.

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Correspondence to Ryosuke Kitatani.

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All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards. This study procedure was approved by the ethics committee of Kyoto University Graduate School and Faculty of Medicine (Approval No. R1348).

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Informed consent was obtained from all individual participants included in this study.

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Communicated by Winston D. Byblow.

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Kitatani, R., Maeda, A., Umehara, J. et al. Different modulation of oscillatory common neural drives to ankle muscles during abrupt and gradual gait adaptations. Exp Brain Res 240, 871–886 (2022). https://doi.org/10.1007/s00221-021-06294-3

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