Decoding subjective emotional arousal from eeg during an immersive virtual reality experience

  1. Simon M Hofmann  Is a corresponding author
  2. Felix Klotzsche  Is a corresponding author
  3. Alberto Mariola  Is a corresponding author
  4. Vadim Nikulin
  5. Arno Villringer
  6. Michael Gaebler  Is a corresponding author
  1. Max Planck Institute for Human Cognitive and Brain Sciences, Germany
  2. University of Sussex, United Kingdom

Abstract

Immersive virtual reality (VR) enables naturalistic neuroscientific studies while maintaining experimental control, but dynamic and interactive stimuli pose methodological challenges. We here probed the link between emotional arousal, a fundamental property of affective experience, and parieto-occipital alpha power under naturalistic stimulation: 37 young healthy adults completed an immersive VR experience, which included rollercoaster rides, while their EEG was recorded. They then continuously rated their subjective emotional arousal while viewing a replay of their experience. The association between emotional arousal and parieto-occipital alpha power was tested and confirmed by (1) decomposing the continuous EEG signal while maximizing the comodulation between alpha power and arousal ratings and by (2) decoding periods of high and low arousal with discriminative common spatial patterns and a Long Short-Term Memory recurrent neural network. We successfully combine EEG and a naturalistic immersive VR experience to extend previous findings on the neurophysiology of emotional arousal towards real-world neuroscience.

Data availability

We did not obtain participants' consent to release their individual data. Since our analyses focus on the single-subject level, we have only limited data which are sufficiently anonymized (e.g., summarized or averaged) to be publicly shared. Wherever possible, we provide "source data" to reproduce the manuscript's tables and figures (Figures 2, 4, 8 and 10). The scripts of all analyses are available at https://github.com/SHEscher/NeVRo

Article and author information

Author details

  1. Simon M Hofmann

    Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    For correspondence
    simon.hofmann@cbs.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0958-501X
  2. Felix Klotzsche

    Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    For correspondence
    klotzsche@cbs.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3985-2481
  3. Alberto Mariola

    Informatics, University of Sussex, Brighton, United Kingdom
    For correspondence
    a.mariola@sussex.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  4. Vadim Nikulin

    Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Arno Villringer

    Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Michael Gaebler

    Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    For correspondence
    gaebler@cbs.mpg.de
    Competing interests
    The authors declare that no competing interests exist.

Funding

Bundesministerium für Bildung und Forschung (13GW0206)

  • Felix Klotzsche
  • Michael Gaebler

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

Ethics

Human subjects: Participants signed informed consent before their participation, and the study was approved by the Ethics Committee of the Department of Psychology at the Humboldt-Universität zu Berlin (vote no. 2017-22).

Reviewing Editor

  1. Alexander Shackman, University of Maryland, United States

Publication history

  1. Preprint posted: October 25, 2020 (view preprint)
  2. Received: November 11, 2020
  3. Accepted: October 27, 2021
  4. Accepted Manuscript published: October 28, 2021 (version 1)
  5. Version of Record published: December 15, 2021 (version 2)

Copyright

© 2021, Hofmann 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

  • 2,604
    Page views
  • 467
    Downloads
  • 7
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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. Simon M Hofmann
  2. Felix Klotzsche
  3. Alberto Mariola
  4. Vadim Nikulin
  5. Arno Villringer
  6. Michael Gaebler
(2021)
Decoding subjective emotional arousal from eeg during an immersive virtual reality experience
eLife 10:e64812.
https://doi.org/10.7554/eLife.64812
  1. Further reading

Further reading

    1. Biochemistry and Chemical Biology
    2. Neuroscience
    Jinli Geng, Yingjun Tang ... Xiaodong Liu
    Research Article Updated

    Dynamic Ca2+ signals reflect acute changes in membrane excitability, and also mediate signaling cascades in chronic processes. In both cases, chronic Ca2+ imaging is often desired, but challenged by the cytotoxicity intrinsic to calmodulin (CaM)-based GCaMP, a series of genetically-encoded Ca2+ indicators that have been widely applied. Here, we demonstrate the performance of GCaMP-X in chronic Ca2+ imaging of cortical neurons, where GCaMP-X by design is to eliminate the unwanted interactions between the conventional GCaMP and endogenous (apo)CaM-binding proteins. By expressing in adult mice at high levels over an extended time frame, GCaMP-X showed less damage and improved performance in two-photon imaging of sensory (whisker-deflection) responses or spontaneous Ca2+ fluctuations, in comparison with GCaMP. Chronic Ca2+ imaging of one month or longer was conducted for cultured cortical neurons expressing GCaMP-X, unveiling that spontaneous/local Ca2+ transients progressively developed into autonomous/global Ca2+ oscillations. Along with the morphological indices of neurite length and soma size, the major metrics of oscillatory Ca2+, including rate, amplitude and synchrony were also examined. Dysregulations of both neuritogenesis and Ca2+ oscillations became discernible around 2–3 weeks after virus injection or drug induction to express GCaMP in newborn or mature neurons, which were exacerbated by stronger or prolonged expression of GCaMP. In contrast, neurons expressing GCaMP-X were significantly less damaged or perturbed, altogether highlighting the unique importance of oscillatory Ca2+ to neural development and neuronal health. In summary, GCaMP-X provides a viable solution for Ca2+ imaging applications involving long-time and/or high-level expression of Ca2+ probes.

    1. Neuroscience
    Maria Cecilia Martinez, Camila Lidia Zold ... Mariano Andrés Belluscio
    Research Article

    The automatic initiation of actions can be highly functional. But occasionally these actions cannot be withheld and are released at inappropriate times, impulsively. Striatal activity has been shown to participate in the timing of action sequence initiation and it has been linked to impulsivity. Using a self-initiated task, we trained adult male rats to withhold a rewarded action sequence until a waiting time interval has elapsed. By analyzing neuronal activity we show that the striatal response preceding the initiation of the learned sequence is strongly modulated by the time subjects wait before eliciting the sequence. Interestingly, the modulation is steeper in adolescent rats, which show a strong prevalence of impulsive responses compared to adults. We hypothesize this anticipatory striatal activity reflects the animals’ subjective reward expectation, based on the elapsed waiting time, while the steeper waiting modulation in adolescence reflects age-related differences in temporal discounting, internal urgency states, or explore–exploit balance.