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Rapid volumetric brain changes after acute psychosocial stress

View ORCID ProfileMarie Uhlig, Janis D. Reinelt, Mark E. Lauckner, View ORCID ProfileDeniz Kumral, View ORCID ProfileH. Lina Schaare, Toralf Mildner, Anahit Babayan, Harald E. Möller, Veronika Engert, Arno Villringer, Michael Gaebler
doi: https://doi.org/10.1101/2021.12.01.470604
Marie Uhlig
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
2International Max Planck Research School NeuroCom, Leipzig, Germany
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  • For correspondence: muhlig@cbs.mpg.de
Janis D. Reinelt
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
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Mark E. Lauckner
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
3Independent Research Group “Adaptive Memory”, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
11Medical Faculty of Leipzig University, Leipzig, Germany
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Deniz Kumral
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
4Institute of Psychology, Neuropsychology, University of Freiburg, Freiburg im Breisgau, Germany
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H. Lina Schaare
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
5Otto Hahn Group “Cognitive Neurogenetics”, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
6Institute of Neuroscience and Medicine (INM-7: Brain and Behaviour), Research Centre Jülich, Germany
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Toralf Mildner
7NMR Methods & Development Group, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
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Anahit Babayan
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
8MindBrainBody Institute at the Berlin School of Mind and Brain, Faculty of Philosophy, Humboldt-Universität zu Berlin, Berlin, German
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Harald E. Möller
7NMR Methods & Development Group, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
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Veronika Engert
9Institute of Psychosocial Medicine, Psychotherapy and Psychooncology, Jena University Hospital, Friedrich-Schiller University, Jena, Germany
10Independent Research Group “Social Stress and Family Health”, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
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Arno Villringer
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
8MindBrainBody Institute at the Berlin School of Mind and Brain, Faculty of Philosophy, Humboldt-Universität zu Berlin, Berlin, German
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Michael Gaebler
1Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
8MindBrainBody Institute at the Berlin School of Mind and Brain, Faculty of Philosophy, Humboldt-Universität zu Berlin, Berlin, German
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Abstract

Stress is an important trigger for brain plasticity: Acute stress can rapidly affect brain activity and functional connectivity, and chronic or pathological stress has been associated with structural brain changes. Measures of structural magnetic resonance imaging (MRI) can be modified by short-term motor learning or visual stimulation, suggesting that they also capture rapid brain changes. Here, we investigated volumetric brain changes (together with changes in T1 relaxation rate and cerebral blood flow) after acute stress in humans as well as their relation to psychophysiological stress measures.

Sixty-seven healthy men (25.8±2.7 years) completed a standardized psychosocial laboratory stressor (Trier Social Stress Test) or a control version while blood, saliva, heart rate, and psychometrics were sampled. Structural MRI (T1 mapping / MP2RAGE sequence) at 3T was acquired 45 min before and 90 min after intervention onset. Grey matter volume (GMV) changes were analysed using voxel-based morphometry. Associations with endocrine, autonomic, and subjective stress measures were tested with linear models.

We found significant group-by-time interactions in several brain clusters including anterior/mid-cingulate cortices and bilateral insula: GMV was increased in the stress group relative to the control group, in which several clusters showed a GMV decrease. We found a significant group-by-time interaction for cerebral blood flow, and a main effect of time for T1 values (longitudinal relaxation time). In addition, GMV changes were significantly associated with state anxiety and heart rate variability changes.

Such rapid GMV changes assessed with VBM may be induced by local tissue adaptations to changes in energy demand following neural activity. Our findings suggest that endogenous brain changes are counteracted by acute psychosocial stress, which emphasizes the importance of considering homeodynamic processes and generally highlights the influence of stress on the brain.

Highlights

  • We investigated rapid brain changes using MRI in a stress and a control group

  • VBM-derived GMV showed a significant group-by-time interaction in several clusters

  • Main pattern: GMV in the stress group increased relative to the control group, in which GMV decreased

  • GMV changes across groups were associated with state anxiety and heart rate variability

  • Neither cerebral blood flow, nor T1 values fully account for the VBM results

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Introduction and Discussion were updated for clarity, Flow Charts of the Study design and sample sizes per analysis were added to the supplement (S1 and S3), supplementary analyses were added including 1) analysis of T1 changes at different GM thresholds, 2) whole-brain VBM-analysis with 6mm smoothing kernel, 3) Analysis of GMV changes in a thalamus-cluster, which previously showed stress-induced eigenvector centrality changes in this sample, 4) results section titles were given summarising headings.

  • https://gitlab.gwdg.de/necos/vbm.git

  • https://osf.io/vjyan/

  • https://www.neurovault.org/collections/SFQXOIUB/

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted November 04, 2022.
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Rapid volumetric brain changes after acute psychosocial stress
Marie Uhlig, Janis D. Reinelt, Mark E. Lauckner, Deniz Kumral, H. Lina Schaare, Toralf Mildner, Anahit Babayan, Harald E. Möller, Veronika Engert, Arno Villringer, Michael Gaebler
bioRxiv 2021.12.01.470604; doi: https://doi.org/10.1101/2021.12.01.470604
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Rapid volumetric brain changes after acute psychosocial stress
Marie Uhlig, Janis D. Reinelt, Mark E. Lauckner, Deniz Kumral, H. Lina Schaare, Toralf Mildner, Anahit Babayan, Harald E. Möller, Veronika Engert, Arno Villringer, Michael Gaebler
bioRxiv 2021.12.01.470604; doi: https://doi.org/10.1101/2021.12.01.470604

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