Functional and microstructural plasticity following social and interoceptive mental training
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
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.
Reviewing Editor
- Camilla L. Nord, University of Cambridge, United Kingdom
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).
Version history
- Preprint posted: November 11, 2020 (view preprint)
- Received: November 25, 2022
- Accepted: July 1, 2023
- Accepted Manuscript published: July 7, 2023 (version 1)
- 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.
Metrics
-
- 1,346
- views
-
- 273
- downloads
-
- 10
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
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)
Further reading
-
- Neuroscience
Abnormal activity in the cerebellar nuclei can be used to predict motor symptoms and induce them experimentally, pointing to potential therapeutic strategies.
-
- Neuroscience
Daily experiences often involve the processing of multiple sequences, yet storing them challenges the limited capacity of working memory (WM). To achieve efficient memory storage, relational structures shared by sequences would be leveraged to reorganize and compress information. Here, participants memorized a sequence of items with different colors and spatial locations and later reproduced the full color and location sequences one after another. Crucially, we manipulated the consistency between location and color sequence trajectories. First, sequences with consistent trajectories demonstrate improved memory performance and a trajectory correlation between reproduced color and location sequences. Second, sequences with consistent trajectories show neural reactivation of common trajectories, and display spontaneous replay of color sequences when recalling locations. Finally, neural reactivation correlates with WM behavior. Our findings suggest that a shared common structure is leveraged for the storage of multiple sequences through compressed encoding and neural replay, together facilitating efficient information organization in WM.