Author


Copyright © 2021 Christoph Spiessens

An investigation into the potential neural and cognitive mechanisms of loving-kindness meditation (LKM) is presented in this article. A selection of peer-reviewed articles based on studies applying various methodologies was reviewed to establish the evolution and contribution of research to the theory of LKM in mindfulness-based programmes (MBPs). The essay concludes with inferred relevance of LKM neuroscience research for suicide prevention in veterans.

Although a global issue, there is an estimated average of 28 veteran suicide deaths daily in the United States alone (Department of Veteran Affairs, 2019). Suicide risk is linked to post-traumatic stress disorder (PTSD) which drives self-criticism, rumination, depression, anxiety, self-harm and interpersonal difficulties (Krupnick et al., 2008; Werner et al., 2019). Encouragingly, among veterans, self-compassion can reduce PTSD symptoms, trauma-related guilt and worrying (Dahm et al., 2015; Hiraoka et al., 2015). In addition, self-compassion can foster proactive coping, which makes it easier to assess anxiety-provoking situations (Neff, 2003), therefore reducing impulsivity (Mantzios, 2014). Although these observations are based on cross-sectional studies using self-report measures and sample groups may not be typical for the overall specialised veteran population, compassion and its protective role in times of distress is remarkable.

Loving-kindness meditation practice aims to help participants of MBPs including Mindfulness-Based Stress Reduction (MBSR) cultivate positive affect toward oneself and others (Fredrickson et al., 2017). In addition to the development of greater levels of self-compassion and compassionate love (Weibel et al., 2017), benefits resulting from LKM practice include a decrease in rumination and improvements in interpersonal relations (Shonin et al., 2015). Further skillsets and cognitive mechanisms developed during LKM include attention training (Fredrickson et al., 2017), emotion regulation (Leung et al., 2013), cognitive reappraisal and perspective taking (Dahl et al., 2015).

LKM is introduced during the all-day silent retreat towards the end of the 8-week MBSR programme (Kabat-Zinn, 2013). Indeed, the literature mentions the importance of first establishing enhanced presence and concentration to help generate increases in self-compassion before cultivating compassion towards others (Hofmann et al., 2011). However, various loving-kindness studies demonstrate short-term effectiveness of single-session practice on the emotions of first-time practitioners. In a recent study on the effect of loving-kindness practice on entrepreneurial fear of failure, Engel et al. (2019) observed that entrepreneurs generated self-compassion after listening to a guided LKM recording for just a few minutes. This outcome is similar to the results of a study by Hutcherson and colleagues (2008) which revealed that just seven minutes of LKM exercise sufficed for participants of a randomised control trial (RCT) to direct feelings of love to a neutral stranger (Hutcherson et al., 2008).

Initially, little empirical research was conducted on LKM (Wallace & Shapiro, 2006), but in the last decade and a half, LKM has become a widely researched meditation practice (Mantzios et al., 2021). Although an abundance of empirical results is available, limited LKM-specific studies using electroencephalogram (EEG) and functional magnetic resonance imaging (fMRI) have been conducted (Kim et al., 2020).

Behavioural and psychological research overwhelmingly supports the use and effectiveness of LKM (Mantzios et al., 2021), and theory has been validated by pioneering neuroscience studies (Mascaro et al., 2015). For example, the perception-action model of empathy (state activated in observer is same as in person being observed) (Preston & de Waal, 2002) is consistent with data from fMRI studies revealing neural networks involved with empathy, including the anterior insula, rostral anterior cingulate, brainstem and cerebellum (Lutz et al., 2008). Gray matter volume increase in the right angular gyrus in the brains of 25 expert LKM practitioners compared with novices confirmed the specific involvement of the right angular gyrus during this meditation practice for the first time, verifying its role in cognitive empathy theory (Leung et al., 2013). In the same study, an increase in gray matter volume was also recorded for the parahippocampal gyri in experienced loving-kindness practitioners. Along with the right angular gyrus these regions are associated with regulation of anxiety, mood and empathic response, further demonstrating the benefits of LKM (Leung et al., 2013).

What becomes apparent is that in the academic literature, the constructs of loving-kindness, compassion and empathy often overlap and are used interchangeably, which is acknowledged in the field (Gilbert et al., 2019; Shonin et al., 2015). For example, a pioneering 2008 cross-sectional fMRI study by Lutz et al. assessed brain activity during “loving-kindness-compassion.” The researchers specifically refer to this as, “a state of compassion, short for compassion and loving-kindness meditation state” (Lutz et al., 2008, p.1).

Derived from Buddhism, loving-kindness (Pāli mettā), along with compassion, equanimity and empathic joy, constitute the Four Sublime States, cultivated by “Four Immeasurables Meditations” (Zeng et al., 2017). Treatment programmes often combine compassion-based interventions and loving-kindness, and the common denominator is the establishment of a kindly stance towards self and others (Graser & Stangier, 2018). Separately, compassion focuses on reducing suffering (Gilbert, 2010), whereas loving-kindness expresses the desire for wellbeing and happiness for self and others (Salzberg, 1995).

Given the apparent lack of standardisation in scientific research and MBPs in terms of terminology and meditation instructions, questions arise: Do LKM and Compassion Meditation (CM), for example, affect different emotions and does that equate to differentiated cognitive mechanisms and neural activity? When Sirotina and Shchebetenko (2020) sought to identify the distinct features of LKM and CM by observing the differential effects between both practices in an RCT with university students (= 201), they found that other-focused positive emotions and positive affect generally increased for both LKM and CM, but LKM effect sizes were consistently larger than CM. This led to the conclusion that two theoretically different practices are involved (Sirotina & Shchebetenko, 2020). However, studies on LKM and CM appear to demonstrate the involvement of similar neural networks. The findings of a compassion study by Klimecki and colleagues (2014) were similar to previous cross-sectional studies which focused on compassion (Klimecki et al., 2013; Klimecki et al., 2014) and to the aforementioned loving-kindness-compassion study by Lutz and colleagues (2008) which recruited the help from meditation specialist Dr. Matthieu Ricard for meditation instructions. Overall, subjects’ brain activity involved during LKM/CM studies is observed in regions including the insula, amygdala, right temporo-parietal junction (TPJ) as well as regions linked to executive function including the dorsolateral prefrontal cortex (dlPFC) and anterior cingulate cortex (ACC) (Klimecki et al., 2013; Lutz et al., 2008; Weng et al., 2013).

Whereas focused-attention meditation (FAM) is the most-widely researched form of meditation, the neural basis of LKM was, initially, less examined by neuroscientific research (Lee et al., 2012). The first study to directly compare FAM and LKM neural activity during affective and cognitive fMRI tasks, therefore filling a research gap, was carried out by Lee and colleagues (2012). Their aim was to investigate distinct and overlapping neural correlates of both meditation types. During this cross-sectional study, 22 male expert meditators (11 FAM/11 LKM) and 22 male novice meditators (11 FAM/11 LKM), all Chinese, performed continued performance tests (CPT) (the cognitive task) and emotion-processing tasks (EPT) (the affective task) in a meditation and baseline state. During the CPT, participants were instructed to watch numbers zero to nine displayed on a screen and press a button once when they saw the number zero appear. During the EPT, participants viewed affective human and nonhuman pictures and then rated the valance and arousal of every happy and sad picture. It was hypothesised that there would be a distinction in blood-oxygen-level-dependent (BOLD) signal (a neural activity measure) for different states and groups between FAM and LKM during the CPT and the EPT. The researchers predicted that brain activity in attention- and emotion-related regions would be stronger in FAM experts during meditation versus baseline, and with stronger effects than in novices. All novices received FAM or LKM meditation instructions (written by one of the researchers and similar to the guidance from Dr. Ricard) to practice one hour per day for seven consecutive days. All participants carried out the continued performance and emotion-processing tasks during a FAM or LKM meditation state and also at baseline.

The results helped advance the neuroscientific research on meditation: No neuronal overlap was found between the state-by-group interactions during any of the fMRI tasks. All significant differences between meditation and baseline states and between experts and novices were different for both meditation types. Looking at LKM specifically during CPT, the researchers did not find any significant neural activity on state-by-group interaction, which suggests that LKM expertise does not affect change in regions related to attention.

As for affective processing, when participants viewed happy faces, increased left ventral ACC activity during meditation compared to baseline for experts and also versus novices was observed. Inferior frontal gyrus (IFG) activity was greater for experts only during the meditation state. Experts also showed greater BOLD activation in the right precuneus when they were meditating. The left ventral ACC plays an important role in the assessment of emotional value of stimuli, which generates related affective states, and the right IFG plays a role in regulation of emotional responses (Phillips et al., 2003). Cavanna and Trimble (2006) proposed that a network establishes between the precuneus and the right prefrontal cortex through the ACC linked to self-referential processing and episodic memory retrieval. Therefore, cultivating love and kindness may enable LKM experts to share others’ positive emotions by feeling the happiness of others as their own and wanting that happiness to continue for others (Phillips et al., 2003). Because LKM practice is linked to neural activity in these regions involved with emotion processing, this may influence emotion regulation and corresponding positive emotion generation (Lee et al., 2012).

When presented with sad images during meditation, LKM experts had increased BOLD responses in their middle frontal gyrus (MFG) and left caudate compared to novices. Activity in the caudate is linked with processing positive and aversive affect, and the left caudate is linked with the arousal level of emotion (Carretie et al., 2009). Voluntary emotion regulation is linked with dlPFC activity in the framework of appraisal theory (Phillips et al., 2003). The researchers observed that in LKM experts, activity in the left caudate and MFG and the arousal level of sad pictures were negatively correlated and therefore suggest that loving-kindness meditation could be associated with increased emotional reactivity combined with more deliberate emotion regulation.

In addition to the pioneering study aim, a particular strength was the rigorous fMRI data analysis of the behavioural and neuroimaging results. For example, trials of happy and sad faces were separated because different neural networks could be involved when processing happy and sad emotions (Lee et al., 2005). Furthermore, in order to reveal common brain regions unique for the experts’ meditation state and discernible interactions between state and group when meditating, conjunction and exclusive masking analyses were performed, supporting the researchers’ assertion that there is no shared neural mechanism between FAM and LKM. However, these findings come with limitations: Since all subjects were Chinese men, generalisation of the findings to female populations and other ethnicities is limited. Moreover, FAM and LKM may not have a common neural mechanism for attention and emotion processing during these specific CPT and EPT tasks but might do so during other tasks. Finally, this study does not provide conclusive information on the neural mechanisms during LKM without a task.

Garrison et al. (2014) aimed to improve on existing studies by investigating the neural substrate of LKM as follows: A large sample size of 20 expert meditators from the Theravada tradition and 26 novices, no concurrent tasks during the fMRI scans (participants completed a task but not whilst meditating) and the use of intrinsic connectivity distribution (ICD) of functional connectivity, allowing the researchers to detect between-group region differences in intrinsic connectivity. ICD is a voxel-to-voxel connectivity measure, enabling the creation of parametric maps for subjects, with every voxel signifying the correlation of a voxel to the rest of the brain. For this, the researchers drew upon their prior study region of interest, the posterior cingulate cortex/precuneus (PCC/PCu), enabling them to establish which connections are different between groups during LKM with this brain region using seed-based connectivity analysis.

This earlier study (Brewer et al., 2011) aimed to investigate common neural pathways across different meditation types (loving-kindness, choiceless awareness and concentration) and revealed reduced BOLD signal during LKM in 12 experts relative to 13 meditation-naïve controls in the PCC/PCu, inferior temporal gyrus going into hippocampal formations, inferior parietal lobule, uncus and amygdala. A relative reduction in BOLD response in the PCC/PCu is a significant finding because this area is considered a hub of the default mode network (DMN), linked to mind wandering and self-related thought processes (Northoff et al., 2006). Upon conducting further functional connectivity analysis, the researchers found that experienced meditators also showed a stronger connection between the PCC, dorsal ACC and dlPFC at baseline and also during meditation — brain regions linked through previous studies with self-monitoring and cognitive control (Brewer et al., 2011).

For the present study, fMRI sessions ran as follows: 90-second active baseline session during which participants had to decide if words displayed described them and appeared in upper case letters or not, followed by a 180-second meditation. As for the whole brain contrast map, a remarkable BOLD signal difference during the LKM practice between both groups was apparent: In all regions, there was less BOLD signal for expert meditators relative to novices. Functional connectivity with the PCC/PCu in experts was significantly different relative to novices. Experts showed more robust connectivity between the PCC/PCu and left IFG, right cerebellum, and the middle frontal gyrus and insula. Novices showed increased connectivity between PCC/PCu and related cortical midline structures, often linked with self-referential thinking (Ives-Deliperi et al., 2011), including their ACC, medial prefrontal cortex and bilateral parahippocampus/hippocampus. In general, reduced BOLD response and intrinsic connectivity when practicing LKM was observed in experts relative to the novice controls, particularly in the PCC/PCu.

This study also provides insights into distinctions in cognitive strategy between experts and novices during LKM, revealing the associated brain areas. For example: Given that LKM is considered a present-centered and non-self-referential practice, novices are likely to find this challenging and thus engage brain activity linked to mind wandering and self-referential processing such as the DMN. This makes sense when we appreciate that novices are instructed to “imagine catching up with a friend you have not seen in a long time and pay attention to this heartfelt feeling in your chest.” Initially, it will be hard for novices to simply rest in that feeling. Also, in empathy and social cognition, the left TPJ plays an important role in processing information about others with regard to social importance (Saxe & Wexler, 2005). More activation in this area could suggest increased mentalising compared with experts. The right TPJ has been linked with empathy and theory of mind (Saxe & Wexler, 2005) and more ICD versus experts may again indicate more self-referential processing or mentalising. Inner speech may also play a role: The left IFG is associated with inner speech (McGuire et al., 1996) and given that novices are likely to rely more on their inner speech during LKM (“May you be happy”) compared with experts who are more in a state of loving-kindness, this could reflect in the IFG group differences. Likewise, given that the hippocampus is associated with memory (Bird & Burgess, 2008), the instruction “Think of a time when…” could explain increased activation between PCC/PCu and hippocampus in novices since they would rely more on memory processes.

This study contributes to the research by assessing the neural substrate of LKM without a concurrent task for a large sample group using multiple neuroimaging analysis methods. Meditation instructions were provided by eminent mettā teacher Joseph Goldstein so we can assume that traditional Theravadin practice applied. Despite these strengths, the following limitations should be considered: Although there were nine women in the expert group and 11 women in the novices group, no results by gender breakdown are provided and thus potential differences are not known. All participants were white non-Hispanic, which again limits relevance of the findings for other ethnicities. Although the researchers compared brain changes during a state of meditation against the brain at baseline to identify which brain changes were specific to LKM, the choice behind the task at baseline is not made clear, although the instruction is likely to create a baseline condition which includes self-referential processing. One can also question if there is a qualitative difference in LKM between novices and experts. Is the expression of loving-kindness inferior when the self is recruited? It is also worth considering how these findings relate to compassionate behaviour outside a testing environment. Does it increase over time as a result of practicing LKM? This is a cross-sectional study and therefore changes in neural substrates and related behavioural changes across meditation training are not tracked (an opportunity for future studies). Finally, pre-existing differences may be present in experts versus novices given their strong interest in meditation. Specifically, this could imply state-dependent differences based on long-term meditation experience and not just generated by LKM.

Possible underlying cognitive mechanisms of LKM which can contribute to the generation of compassion -and therefore relevant to suicide prevention in veterans- will now be considered. Based on neuroscientific findings, cognitive reappraisal, perspective-taking and self-perspective-related positive changes are proposed by Dahl and colleagues (2015), whereas Engen and Singer (2016) assert that positive affect and prosocial motivation constitute the principal mechanisms active during LKM. Although there is no consensus on which of these suggested mechanisms applies more -again an opportunity for further studies- neuroscientific and clinical data suggest that all of these mechanisms are associated with the practice of meditations in the family of constructive meditations (Graser & Stangier, 2018). These are practices that can cultivate cognitive and affective patterns that promote wellbeing and healthy interpersonal dynamics (Dahl et al., 2015).

Looking at the cognitive mechanism of perspective-taking, including changing the perspective on the self by recognising thoughts and emotion as temporary events, this might be facilitated through decentering or disidentification (Graser & Stangier, 2018). Ives-Deliperi et al. (2011) used fMRI to explore decentering in a cross-sectional study with ten experienced meditators. After a 2-minute focused attention task to juxtapose the meditation state, participants practiced 12 minutes of open awareness meditation (observing without judging/identifying). This was a small sample without a control group, yet the study yielded remarkable information on the mechanisms of mindfulness and brain regions involved. Significant signal decreases were observed in participants in meditation state, particularly in the right medial prefrontal cortex, left ventral ACC, bilateral anterior insula and PCu. As previously mentioned, these are midline cortical structures linked with self-referential thinking and mind wandering. Interestingly, a considerable BOLD response increase was observed in the right PCC, associated with autobiographical memory recall (Ryan et al., 2001). It was assumed that this signal increase is associated with inhibition in this area in favour of maintaining focus on the present moment, based on previous research findings (Ritter & Villringen, 2002). These study findings support the proposition that a process of disidentification is one way mindfulness enables positive outcomes.

A remarkable study that combines researching the mechanism of decentering and the cultivation of prosocial affective qualities was conducted by Trautwein and colleagues (2016). Social neuroscience suggests that self and other are interconnected and that human intersubjectivity is based on an overlap of self and other representations (Decety & Sommerville, 2003). Intersubjective skills can be enhanced by meditation training (Mascaro et al., 2015) and LKM in particular could foster social connectedness (Hutcherson et al., 2008), compassion (Klimecki et al., 2013) and empathy (Mascaro et al., 2013). The researchers set out to explore if LKM promotes prosocial affect development by rebalancing self/other-associated processing through increased self/other representations overlap, similar to the construct of LKM promoting the cultivation of loving-kindness for self and then extending that feeling toward others (Salzberg, 1995).

For this cross-sectional EEG study with 11 long-term meditators and 11 novices, the researchers recorded event-related potentials (ERP) produced when subjects viewed pictures of their own face and faces of close others, and then compared these to measure P300 amplitudes. In previous studies, the P300 ERP has consistently been associated with preferential processing of self-related stimuli (e.g., autobiographical information) compared to control stimuli that are not self-related (Gray et al., 2004). Choosing the P300 to gauge self-other integration was based on the assumption that if an individual’s self-representation is less self-isolated and integrated into a social context (one feels connected to the wider world), they should elicit similar cognitive processing when self- and other-related stimuli are presented to them. It was hypothesised that a reduction in self- and other-related P300 amplitude differences would be observed, given the assumption that LKM practice cultivates prosocial mental qualities. Indeed, the researchers found that P300 amplitude differences were smaller in the LKM group relative to novices and that those differences were strongly negatively correlated with the extent of individual meditation practice.

Although the control group was gender matched, another limitation further to the small sample size should be considered: The influence of other meditation practice in long-term meditators on these results. All long-term meditators also practice mindfulness meditation which, as previously discussed, reduces self-referential processing, therefore part of the effects of the LKM in this study could be influenced by mindfulness meditation. This study provides preliminary insight into how social qualities such as compassion can be cultivated by reducing distinctions between self and others with the solitary practice of LKM, but further longitudinal studies could investigate common and LKM-specific influences.

Since the role of decentering may be important in improving mental health (Bernstein et al., 2015) and self-compassion can be particularly helpful for suicide prevention among veterans (Bryan et al., 2015), offering LKM practice in mental wellbeing initiatives for veterans could be beneficial, as demonstrated by previous research. Kearney et al. (2014) conducted a longitudinal LKM trial with 42 veterans suffering with PTSD. The researchers obtained PTSD, depression, mindfulness and self-compassion measures at baseline, at the end of a 12-week LKM course, and three months later. There were medium to large effect sizes for mindfulness and self-compassion increases, and reduced PTSD symptoms and a decrease in depression were attributed to the cultivation of enhanced self-compassion. However, this was not an RCT, changes could be related to effects different from LKM (e.g., belonging to a group) and many of the veterans received additional mental health support.

In conclusion, loving-kindness meditation has become a widely researched meditation practice with increased reports on associated mental health benefits. Although there is an abundance of empirical LKM research, significantly fewer controlled fMRI and EEG studies are available. These can, however, contribute to a converging evidence base, combining self-report methods with neuroscientific measures across dispositional, cross-sectional and longitudinal studies. This could be instrumental in the development of LKM-based interventions for veterans and other populations vulnerable to suicidality, enabling researchers to make strong and well-supported conclusions, gain a better understanding of localisation and activation of associated brain regions and establish clarity in contentious matters, including contradictory findings and null reports.

Despite some limitations, key studies presented in this essay helped advance the field of neuroscientific mindfulness research, improving on previous LKM/compassion studies by closing methodological gaps and revealing opportunities for further research. To confirm the promising contribution of loving-kindness meditation to MBPs, further neuroscience studies would benefit from improved methodological rigor. This could include larger-scale, mixed-gender longitudinal studies with multiple ethnicities and active control groups, study replication to determine whether the findings of an original LKM study can be reproduced, as well as standardisation of loving-kindness/compassion/empathy definitions and practices within consistent experimental frameworks to drive consensus about associated cognitive mechanisms and neural substrates. Specific to the development of LKM interventions for veterans, studies could also consider subjects’ vulnerability related to army service length and varying degrees of trauma exposure to allow for further generalisation of findings, thus supporting the development of evidence-based interventions that can help prevent veteran suicides globally.

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