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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One of the most fundamental laws of physics is the principle of least action. Motivated by its predictive power, we introduce a neuronal least-action principle for cortical processing of sensory streams to produce appropriate behavioral outputs in real time. The principle postulates that the voltage dynamics of cortical pyramidal neurons prospectively minimizes the local somato-dendritic mismatch error within individual neurons. For output neurons, the principle implies minimizing an instantaneous behavioral error. For deep network neurons, it implies the prospective firing to overcome integration delays and correct for possible output errors right in time. The neuron-specific errors are extracted in the apical dendrites of pyramidal neurons through a cortical microcircuit that tries to explain away the feedback from the periphery, and correct the trajectory on the fly. Any motor output is in a moving equilibrium with the sensory input and the motor feedback during the ongoing sensory-motor transform. Online synaptic plasticity reduces the somatodendritic mismatch error within each cortical neuron and performs gradient descent on the output cost at any moment in time. The neuronal least-action principle offers an axiomatic framework to derive local neuronal and synaptic laws for global real-time computation and learning in the brain.
