Functional and microstructural plasticity following social and interoceptive mental training
- Max Planck Institute for Human Cognitive and Brain Sciences, Germany
- Technische Universität Dresden, Germany
- Inha University, Republic of Korea
- Institute for Basic Science, Republic of Korea
- University of Würzburg, Germany
- University of Freiburg, Germany
- McGill University, Canada
- 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
Fynn-Mathis Trautwein
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).
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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Functional and microstructural plasticity following social and interoceptive mental training
eLife 12:e85188.
https://doi.org/10.7554/eLife.85188
Further reading
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When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
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When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.
