Elsevier

Neuropsychologia

Volume 116, Part A, 31 July 2018, Pages 26-33
Neuropsychologia

Structural changes in socio-affective networks: Multi-modal MRI findings in long-term meditation practitioners

https://doi.org/10.1016/j.neuropsychologia.2017.08.024Get rights and content

Highlights

  • Multimodal MRI in long-term meditators (LTMs) and meditation-naïve controls.

  • Cortical thickening in LTMs vs controls in fronto-insular regions.

  • Overlap with fMRI amplitude increases during loving-kindness meditation in LTMs.

  • Findings motivate longitudinal studies addressing training-related plasticity.

Abstract

Our goal was to assess the effects of long-term mental training in socio-affective skills on structural brain networks. We studied a group of long-term meditation practitioners (LTMs) who have focused on cultivating socio-affective skills using loving-kindness and compassion meditation for an average of 40k h, comparing these to meditation-naïve controls. To maximize homogeneity of prior practice, LTMs were included only if they had undergone extensive full-time meditation retreats in the same center. MRI-based cortical thickness analysis revealed increased thickness in the LTM cohort relative to meditation-native controls in fronto-insular cortices. To identify functional networks relevant for the generation of socio-affective states, structural imaging analysis were complemented by fMRI analysis in LTMs, showing amplitude increases during a loving-kindness meditation session relative to non-meditative rest in multiple prefrontal and insular regions bilaterally. Importantly, functional findings partially overlapped with regions of cortical thickness increases in the left ventrolateral prefrontal cortex and anterior insula, suggesting that these regions may play a central role in the generation of emotional states relevant for the meditative practice. Our multi-modal MRI approach revealed structural changes in LTMs who have cultivated loving-kindness and compassion for a significant period of their life in functional networks activated by these practices. These preliminary cross-sectional findings motivate future longitudinal work studying brain plasticity following the regular practice of skills aiming at enhancing human altruism and prosocial motivation.

Introduction

There has been a long-standing interest in the neurosciences to study brain plasticity (Huttenlocher, 2002, Kandel, 2012). Plasticity can occur across multiple time scales from short-term to long-term within functional networks, and at the level of structural networks. In humans, most previous studies addressing structural plasticity have focused on training and/or expertise effects on motor, sensory, or memory functions (Draganski et al., 2004, Taubert et al., 2011), but also skills like musicality (Bermudez et al., 2009). Conversely, except for work showing limbic network reorganization in the context of negative affect and fear conditioning (LeDoux, 2000, Phelps and LeDoux, 2005), only a few studies have addressed plasticity in networks mediating socio-affective skills, especially those that require the generation of positive affect, loving-kindness, and compassion.

Behavioral and autonomic research has suggested that cultivating qualities such as loving kindness and compassion are associated with increases in prosocial behavior (Leiberg et al., 2011), and vagal tone as a proxy of physical health (Kok et al., 2013). Furthermore, some studies have supported the application of these strategies in clinical populations, for example as a means to reduce stress, pain, and mood problems (Hofmann et al., 2011). Training of loving-kindness meditation involves the active generation of feelings of warmth, love, kindness, and prosocial motivation for others; confronted with the suffering of others, loving-kindness may furthermore become compassion, associated with a wish to alleviate the suffering (Salzberg, 1995, Singer and Klimecki, 2014). Using short-term longitudinal functional MRI studies, our group recently demonstrated short-term functional plasticity after the training of loving-kindness and compassion in meditation-naïve participants (Klimecki et al., 2013a, Klimecki et al., 2013b). Changes were observed in subcortical networks and fronto-limbic cortices, centred on prefrontal-cingulate as well as insula regions. On a behavioral level, training effects manifested in increased reports of positive affect, even when participants were exposed to distressing videos, and increased helping behavior (Leiberg et al., 2011). While providing initial evidence of subjectively and behaviorally relevant functional changes following the training of compassion and loving-kindness in a network typically associated with positive affect, affiliation, and reward (Grabenhorst and Rolls, 2011, Kringelbach and Berridge, 2009), the short duration of the training protocol and retest-interval did not allow us to robustly study the effects of compassion-related mental practices on brain structure.

In the absence of long-term and sufficiently powered longitudinal mental training studies that involve costly and state-of-the art neuroimaging (Valk et al., in press), cross-sectional assessments of mental training experts, specifically long-term meditation practitioners (LTMs), provides a useful framework to infer brain plasticity following frequent mental training (Ricard et al., 2014). A series of functional MRI studies have shown alterations in the activation of limbic networks, particularly insular regions, in experts relative to controls (Lutz et al., 2008, Lutz et al., 2009). Additional analyses of brain structure provide and relatively state-invariant measure of training effects that may not be affected by specific demand characteristics of a given task. Structural changes in LTMs have been reported previously, but generally in cohorts practicing attention and mindfulness (Fox et al., 2014); conversely, practitioners who have explicitly cultivated socio-affective capacities, such as compassion and loving-kindness, are less well studied and we thus do not know about the effects specifically associated to their long-term training expertise.

To study expertise effects related to long-term mental training in socio-affective skills on brain structure, we recruited LTMs from a school of Tibetan Buddhism that focuses on cultivating loving-kindness, altruism, and compassion. Included LTMs have formally practiced meditation more 40k h on average before our study. Moreover, and to furthermore increase the homogeneity in the form of meditative practice, LTMs were included only if they had participated in at least one extensive full-time meditation retreat in the same center by the same group of teachers. In addition to undergoing high-resolution structural MRI acquisitions that were analyzed with surface-based techniques assess between-cohort differences in cortical thickness, our LTMs underwent two counterbalanced functional MRI sessions that were each seven-minutes long. In one session, they were asked to perform a loving-kindness meditation; a counterbalanced non-meditative resting-state session served as control condition. Functional amplitude increases during loving-kindness relative to non-meditative rest were mapped onto cortical surfaces, to assess overlaps with regions of cortical thickness changes. We expected that our LTMs would show alterations in brain structure compared to age-matched controls in regions relevant to the generation of loving-kindness and socio-affective processing, which we hypothesized to likely be situated in prefrontal and insular cortical networks.

Section snippets

Subjects

Participants were tested between November 2011 and March 2013. We studied a cohort of 17 long-term meditators (LTM; 5 women; 45–62 years, mean ± SD age = 56 ± 5 years). All meditators were adepts of the Nyingma tradition of Tibetan Buddhism (one of the schools focussing on the cultivation of loving-kindness, altruism, and compassion). Participants were included only if they had previously participated in multiple intensive full-time meditation retreats (3 months to 3 years of retreat), which

Cortical thickness increases in LTMs: surface-based findings

Surface-based analysis revealed increased cortical thickness in LTMs compared to controls in a right prefrontal cluster encompassing fronto-polar cortex and left ventrolateral (cluster-wise pFWE < 0.029) as well as a trend in right fronto-insular cortices (cluster-wise pFWE = 0.069, Fig. 1, Supplementary Table 1). There were no significant cortical thickness decreases in LTMs. Inter-hemispheric asymmetry analysis (following the mapping of the thickness data to a hemisphere-symmetric surface

Discussion

The focus of the current work was to investigate structural brain changes in a unique cohort of long term meditators (LTMs), with extensive and homogenous experience in compassion and loving kindness meditation – a family of meditation techniques that has only received relatively little attention in the literature. Using structural MRI, the LTMs were compared with an age- and sex-matched meditation-naïve control group, allowing us to identify changes in gray matter thickness in the cortical

Acknowledgements

We would like to thank all LTMs and control participants involved in this study. We are grateful to the support staff of the social neuroscience department, particularly Dr. Sandra Zurborg, for her help with the study logistics and organization, Henrik Grunert for his technical assistance, Elisabeth Murzik for her help with data archiving, as well as Sylvie Neubert and Nicole Pampus for their help with scanning. We also thank Sofie Valk and Bram Cordemans for their help in assessing

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    Authors contributed equally to this work.

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