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.

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.

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.

Metrics

  • 1,637
    views
  • 387
    downloads
  • 9
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Evolutionary Biology
    2. Neuroscience
    Gregor Belušič
    Insight

    The first complete 3D reconstruction of the compound eye of a minute wasp species sheds light on the nuts and bolts of size reduction.

    1. Neuroscience
    Mathias Guayasamin, Lewis R Depaauw-Holt ... Ciaran Murphy-Royal
    Research Article

    Early-life stress can have lifelong consequences, enhancing stress susceptibility and resulting in behavioural and cognitive deficits. While the effects of early-life stress on neuronal function have been well-described, we still know very little about the contribution of non-neuronal brain cells. Investigating the complex interactions between distinct brain cell types is critical to fully understand how cellular changes manifest as behavioural deficits following early-life stress. Here, using male and female mice we report that early-life stress induces anxiety-like behaviour and fear generalisation in an amygdala-dependent learning and memory task. These behavioural changes were associated with impaired synaptic plasticity, increased neural excitability, and astrocyte hypofunction. Genetic perturbation of amygdala astrocyte function by either reducing astrocyte calcium activity or reducing astrocyte network function was sufficient to replicate cellular, synaptic, and fear memory generalisation associated with early-life stress. Our data reveal a role of astrocytes in tuning emotionally salient memory and provide mechanistic links between early-life stress, astrocyte hypofunction, and behavioural deficits.