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. 2024 Aug 28:12:RP87634.
doi: 10.7554/eLife.87634.

Differential increase of hippocampal subfield volume after socio-affective mental training relates to reductions in diurnal cortisol

Sofie Louise Valk #  1   2   3 , Veronika Engert #  4   5 , Lara Puhlmann  5   6 , Roman Linz  5 , Benoit Caldairou  7 , Andrea Bernasconi  7 , Neda Bernasconi  7 , Boris C Bernhardt #  7 , Tania Singer #  8
Affiliations

Differential increase of hippocampal subfield volume after socio-affective mental training relates to reductions in diurnal cortisol

Sofie Louise Valk et al. Elife. .

Abstract

The hippocampus is a central modulator of the HPA-axis, impacting the regulation of stress on brain structure, function, and behavior. The current study assessed whether three different types of 3 months mental Training Modules geared towards nurturing (a) attention-based mindfulness, (b) socio-affective, or (c) socio-cognitive skills may impact hippocampal organization by reducing stress. We evaluated mental training-induced changes in hippocampal subfield volume and intrinsic functional connectivity, by combining longitudinal structural and resting-state fMRI connectivity analysis in 332 healthy adults. We related these changes to changes in diurnal and chronic cortisol levels. We observed increases in bilateral cornu ammonis volume (CA1-3) following the 3 months compassion-based module targeting socio-affective skills (Affect module), as compared to socio-cognitive skills (Perspective module) or a waitlist cohort with no training intervention. Structural changes were paralleled by relative increases in functional connectivity of CA1-3 when fostering socio-affective as compared to socio-cognitive skills. Furthermore, training-induced changes in CA1-3 structure and function consistently correlated with reductions in cortisol output. Notably, using a multivariate approach, we found that other subfields that did not show group-level changes also contributed to changes in cortisol levels. Overall, we provide a link between a socio-emotional behavioural intervention, changes in hippocampal subfield structure and function, and reductions in cortisol in healthy adults.

Keywords: cortisol; hippocampus; human; mental training; neuroscience; structure-function.

Plain language summary

Too much stress is harmful to the brain and overall health, as it can lead to chronically high levels of the stress hormone cortisol. The part of the brain that regulates memory and emotions, called the hippocampus, is especially sensitive to stress because it has a high number of receptors that bind to cortisol. This connection may explain why stress can lead to memory lapses or strong emotions. Studies have shown that mental training exercises, such as mindfulness and meditation, may change the structure of the brain and reduce stress. However, the results from these experiments have been mixed due to the variation in mental practices used by different programs. Here, Valk, Engert et al. set out to find how distinct types of mental training affect the brain, focusing on the hippocampus and cortisol levels. The team used various magnetic resonance imaging techniques to study the hippocampus of 322 healthy adult volunteers who had undergone three months of mental training. The relationship between mental training, hippocampus size, and stress levels was complex when studying the results of each individual. However, when the results were grouped together, it revealed that volunteers who underwent training to increase empathy and compassion experienced expansion in parts of their hippocampus. As these areas of the brain increased in size, these individuals experienced corresponding reductions in cortisol levels. But volunteers who underwent mental training focused on attention or developing perspective did not experience such increases. These findings suggest that mental training to increase empathy and compassion alters brain structure and lowers cortisol levels. Future studies may explain how this happens, which could lead to improved mental training programs for mitigating stress.

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Conflict of interest statement

SV, VE, LP, RL, BC, AB, NB, BB, TS No competing interests declared

Figures

Figure 1.
Figure 1.. Training induced plasticity of hippocampal subfield volume.
(A) Training modules; (B) Training design; (C) Subfield volumes in left and right hemispheres across individuals and timepoints; (D) Scatterplot of subfield volumes as a function of timepoints and training cohorts. Panels A and B are reproduced from Figure 1A, B of Valk et al., 2023a.
Figure 2.
Figure 2.. Training induced plasticity of CA1-3 functional connectivity.
(A) upper: CA1-3 functional connectivity at baseline, top 10% of regions representing the CA1-3 functional network; lower: scatter plot visualizing change within the CA1-3 network across timepoints and groups; networks and scatters of SUB and CA4/DG are available in the supplements; (B) Regional change within CA1-3 functional network Affect versus Perspective (FDRq <0.05); right: scatter plot visualizing mean change within the CA1-3, FDRq <0.05 regions across timepoints and groups.
Figure 3.
Figure 3.. Associations between changes in structure and function of hippocampal subfield volume and markers of stress change.
(A). Upper left: Correlation between hippocampal subfield volume change in Affect and CAR, slope, and AUC markers of stress change, Upper right: Correlation between hippocampal subfield intrinsic functional change in Affect and CAR, slope, and AUC markers of stress change, middle: Scatter plots visualize the correlation between volume change and cortisol marker change (below p<0.05), bottom: region level change within left CA1-3, FDRq <0.05. CA1-3 is the focus of this analysis based on our group-level findings and highlighted with boxes in A; (B). Upper: Overall impact of diurnal cortisol markers on hippocampal subfield volume and function over Presence, Affect and Perspective; Lower: Overall impact of hair cortisol markers on hippocampal subfield volume and function over Presence, Affect and Perspective.
Figure 4.
Figure 4.. Multivariate associations between changes in structure and function of hippocampal subfield volume and markers of stress change in Affect.
(A). Multivariate associations between bilateral CA1-3 volume and intrinsic function and stress markers. Left: Scatter of loadings, colored by Training Module; Right upper: individual correlations of stress markers; Right lower: individual correlation of subfields; (B). Multivariate associations between all subfields’ volume and intrinsic function and stress markers. Left: Scatter of loadings, colored by Training Module; Right upper: individual correlations of stress markers; Right lower: individual correlation of subfields.
See this image and copyright information in PMC

Update of

  • doi: 10.1101/2023.03.03.531039
  • doi: 10.7554/eLife.87634.1
  • doi: 10.7554/eLife.87634.2
  • doi: 10.7554/eLife.87634.3

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