Spatially bivariate EEG-neurofeedback can manipulate interhemispheric inhibition

Abstract

Human behavior requires interregional crosstalk to employ the sensorimotor processes in the brain. Although external neuromodulation techniques have been used to manipulate interhemispheric sensorimotor activity, a central controversy concerns whether this activity can be volitionally controlled. Experimental tools lack the power to up- or down-regulate the state of the targeted hemisphere over a large dynamic range and, therefore, cannot evaluate the possible volitional control of the activity. We addressed this difficulty by using the recently developed method of spatially bivariate electroencephalography (EEG)-neurofeedback to systematically enable the participants to modulate their bilateral sensorimotor activities. Herein, we report that participants learn to up- and down-regulate the ipsilateral excitability to the imagined hand while maintaining constant the contralateral excitability; this modulates the magnitude of interhemispheric inhibition (IHI) assessed by the paired-pulse transcranial magnetic stimulation (TMS) paradigm. Further physiological analyses revealed that the manipulation capability of IHI magnitude reflected interhemispheric connectivity in EEG and TMS, which was accompanied by intrinsic bilateral cortical oscillatory activities. Our results show an interesting approach for neuromodulation, which might identify new treatment opportunities, for example, in patients suffering from a stroke.

Data availability

Source data used to generate the figures are publicly available via Dryad Digital Repository, accessible here:Hayashi, Masaaki (2021), Spatially bivariate EEG-neurofeedback can manipulate interhemispheric rebalancing of M1 excitability, Dryad, Dataset, https://doi.org/10.5061/dryad.hhmgqnkj3Scripts used for the neurofeedback experiment are available on GitHub (https://github.com/MasaakiHayashi/elife-neurofeedback-experiment).

The following data sets were generated

Article and author information

Author details

  1. Masaaki Hayashi

    Graduate School of Science and Technology, Keio University, Kanagawa, Japan
    Competing interests
    Masaaki Hayashi, is employed by Connect Inc..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7104-6765
  2. Kohei Okuyama

    Department of Rehabilitation Medicine, Keio University, Tokyo, Japan
    Competing interests
    No competing interests declared.
  3. Nobuaki Mizuguchi

    Research Organization of Science and Technology, Ritsumeikan University, Shiga, Japan
    Competing interests
    No competing interests declared.
  4. Ryotaro Hirose

    Graduate School of Science and Technology, Keio University, Kanagawa, Japan
    Competing interests
    No competing interests declared.
  5. Taisuke Okamoto

    Graduate School of Science and Technology, Keio University, Kanagawa, Japan
    Competing interests
    No competing interests declared.
  6. Michiyuki Kawakami

    Department of Rehabilitation Medicine, Keio University, Tokyo, Japan
    Competing interests
    No competing interests declared.
  7. Junichi Ushiba

    Faculty of Science and Technology, Keio University, Kanagawa, Japan
    For correspondence
    ushiba@bio.keio.ac.jp
    Competing interests
    Junichi Ushiba, is a founder and the Representative Director of the University Startup Company, Connect Inc. involved in the research, development, and sales of rehabilitation devices including brain-computer interfaces. He receives a salary from Connect Inc., and holds shares in Connect Inc. This company does not have any relationships with the device or setup used in the current study..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1161-983X

Funding

Ministry of Education, Culture, Sports, Science and Technology (Grant-in-Aid for Transformative Research Areas (A) (#20H05923))

  • Junichi Ushiba

Japan Agency for Medical Research and Development (Strategic International Brain Science Research Promotion Program (#JP20dm030702))

  • Junichi Ushiba

Ushioda Memorial Fund (The Keio University Doctorate Student Grant-in-Aid Program)

  • Masaaki Hayashi

Japan Science and Technology Agency (Moonshot R&D program (Grant Number JPMJMS2012))

  • Junichi Ushiba

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Nicole Wenderoth, ETH Zürich, Switzerland

Ethics

Human subjects: The experiments conformed to the Declaration of Helsinki and were performed in accordance with the current TMS safety guidelines of the International Federation of Clinical Neurophysiology (Rossi et al., 2009). The experimental procedure was approved by the Ethics Committee of the Faculty of Science and Technology, Keio University (no.: 31-89, 2020-38, and 2021-74). Written informed consent was obtained from participants prior to the experiments.

Version history

  1. Received: December 15, 2021
  2. Preprint posted: December 16, 2021 (view preprint)
  3. Accepted: July 6, 2022
  4. Accepted Manuscript published: July 7, 2022 (version 1)
  5. Version of Record published: July 20, 2022 (version 2)

Copyright

© 2022, Hayashi et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Masaaki Hayashi
  2. Kohei Okuyama
  3. Nobuaki Mizuguchi
  4. Ryotaro Hirose
  5. Taisuke Okamoto
  6. Michiyuki Kawakami
  7. Junichi Ushiba
(2022)
Spatially bivariate EEG-neurofeedback can manipulate interhemispheric inhibition
eLife 11:e76411.
https://doi.org/10.7554/eLife.76411

Share this article

https://doi.org/10.7554/eLife.76411

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