Functional and microstructural plasticity following social and interoceptive mental training

  1. Sofie Louise Valk  Is a corresponding author
  2. Philipp Kanske
  3. Bo-yong Park
  4. Seok-Jun Hong
  5. Anne Böckler
  6. Fynn-Mathis Trautwein
  7. Boris C Bernhardt  Is a corresponding author
  8. Tania Singer
  1. Max Planck Institute for Human Cognitive and Brain Sciences, Germany
  2. Technische Universität Dresden, Germany
  3. Inha University, Republic of Korea
  4. Institute for Basic Science, Republic of Korea
  5. University of Würzburg, Germany
  6. University of Freiburg, Germany
  7. McGill University, Canada
  8. Max Planck Society, Germany

Abstract

The human brain supports social cognitive functions, including Theory of Mind, empathy, and compassion, through its intrinsic hierarchical organization. However, it remains unclear how the learning and refinement of social skills shapes brain function and structure. We studied if different types of social mental training induce changes in cortical function and microstructure, investigating 332 healthy adults (197 women, 20-55 years) with repeated multimodal neuroimaging and behavioral testing. Our neuroimaging approach examined longitudinal changes in cortical functional gradients and myelin-sensitive T1 relaxometry, two complementary measures of cortical hierarchical organization. We observed marked changes in intrinsic cortical function and microstructure, which varied as a function of social training content. In particular, cortical function and microstructure changed as a result of attention-mindfulness and socio-cognitive training in regions functionally associated with attention and interoception, including insular and parietal cortices. Conversely, socio-affective and socio-cognitive training resulted in differential microstructural changes in regions classically implicated in interoceptive and emotional processing, including insular and orbitofrontal areas, but did not result in functional reorganization. Notably, longitudinal changes in cortical function and microstructure predicted behavioral change in attention, compassion and perspective-taking. Our work demonstrates functional and microstructural plasticity after the training of social-interoceptive functions, and illustrates the bidirectional relationship between brain organisation and human social skills.

Data availability

In line with EU data regulations (General Data Protection Regulation, GDPR), we regret that data cannot be shared publicly because we did not obtain explicit participant agreement for data-sharing with third parties. Our work is based on personal data (age, sex, and neuroimaging data) that could be matched to individuals. The data is therefore pseudonominized rather than anonymized and falls under the GDPR. Data are available upon request (contact via valk@cbs.mpg.de). Summary data and analysis scripts (Matlab and python) to reproduce primary analyses and figures are publicly available on GitHub (https://github.com/CNG-LAB/social_function_structure_change), and raw data-plots are provided for network-level analyses. To construct gradients, we used the brainspace package, available at brainspace.readthedocs.io. To construct intra-cortical myelin profiles code is available at micapipe.readthedocs.io. Meta-analytical functional MRI maps are downloaded from neurosynth.org and available on GitHub.

Article and author information

Author details

  1. Sofie Louise Valk

    Otto Hahn Group Cognitive Neurogenetics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    For correspondence
    valk@cbs.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2998-6849
  2. Philipp Kanske

    Technische Universität Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2027-8782
  3. Bo-yong Park

    Department of Data Science, Inha University, Incheon, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7096-337X
  4. Seok-Jun Hong

    Center for Neuroscience Imaging Research, Institute for Basic Science, Suwon, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1847-578X
  5. Anne Böckler

    Department of Psychology, University of Würzburg, Würzburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Fynn-Mathis Trautwein

    Department of Psychosomatic Medicine and Psychotherapy, University of Freiburg, Freiburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9928-0193
  7. Boris C Bernhardt

    Montreal Neurological Institute and Hospital, McGill University, Montreal, Canada
    For correspondence
    boris.bernhardt@mcgill.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9256-6041
  8. Tania Singer

    Social Neuroscience Lab, Max Planck Society, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.

Funding

European Research Council (205557)

  • Tania Singer

Natural Sciences and Engineering Research Council of Canada (Discovery-1304413)

  • Boris C Bernhardt

Canadian Institutes of Health Research (CIHR FDN-154298)

  • Boris C Bernhardt

Sick Kids Foundation (NI17-039)

  • Boris C Bernhardt

Azrieli Foundation (ACAR-TACC)

  • Boris C Bernhardt

Canada Research Chairs (Tier 2)

  • Boris C Bernhardt

Molson Foundation

  • Bo-yong Park

Fonds de recherche du Québec

  • Bo-yong Park

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

Ethics

Human subjects: All participants gave written informed consent and the study was approved by the Research Ethics Committees of the University of Leipzig (#376/12-ff) and Humboldt University in Berlin (#2013-02, 2013-29, 2014-10).

Reviewing Editor

  1. Camilla L. Nord, University of Cambridge, United Kingdom

Version history

  1. Preprint posted: November 11, 2020 (view preprint)
  2. Received: November 25, 2022
  3. Accepted: July 1, 2023
  4. Accepted Manuscript published: July 7, 2023 (version 1)
  5. Version of Record published: August 10, 2023 (version 2)

Copyright

© 2023, Valk 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. Sofie Louise Valk
  2. Philipp Kanske
  3. Bo-yong Park
  4. Seok-Jun Hong
  5. Anne Böckler
  6. Fynn-Mathis Trautwein
  7. Boris C Bernhardt
  8. Tania Singer
(2023)
Functional and microstructural plasticity following social and interoceptive mental training
eLife 12:e85188.
https://doi.org/10.7554/eLife.85188

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