Can compassion be trained like a muscle? Active-controlled fMRI of compassion meditation.

by Neuroconscience

Among the cognitive training literature, meditation interventions are particularly unique in that they often emphasize emotional or affective processing at least as much as classical ‘top-down’ attentional control. From a clinical and societal perspective, the idea that we might be able to “train” our “emotion muscle” is an attractive one. Recently much has been made of the “empathy deficit” in the US, ranging from empirical studies suggesting a relationship between quality-of-care and declining caregiver empathy, to a recent push by President Obama to emphasize the deficit in numerous speeches.

While much of the training literature focuses on cognitive abilities like sustained attention and working memory, many investigating meditation training have begun to study the plasticity of affective function, myself included.  A recent study by Helen Weng and colleagues in Wisconsin investigated just this question, asking if compassion (“loving-kindness”) meditation can alter altruistic behavior and associated neural processing. Her study is one of the first of its kind, in that rather than merely comparing groups of advanced practitioners and controls, she utilized a fully-randomized active-controlled design to see if compassion responds to brief training in novices while controlling for important confounds.

As many readers should be aware, a chronic problem in training studies is a lack of properly controlled longitudinal design. At best, many rely on “passive” or “no-contact” controls who merely complete both measurements without receiving any training. Even in the best of circumstances “active” controls are often poorly matched to whatever is being emphasized and tested in the intervention of interest. While having both groups do “something” is better than a passive or no-control design, problems may still arise if the measure of interest is mismatched to the demand characteristics of the study.  Stated simply, if your condition of interest receives attention training and attention tests, and your control condition receives dieting instruction or relaxation, you can expect group differences to be confounded by an explicit “expectation to improve” in the interest group.

In this regard Weng et al present an almost perfect example of everything a training study should be. Both interventions were delivered via professionally made audio CDs (you can download them yourselves here!), with participants’ daily practice experiences being recorded online. The training materials were remarkably well matched for the tests of interest and extra care was taken to ensure that the primary measures were not presented in a biased way. The only thing they could have done further would be a single blind (making sure the experimenters didn’t know the group identity of each participant), but given the high level of difficulty in blinding these kinds of studies I don’t blame them for not undertaking such a manipulation. In all the study is extremely well-controlled for research in this area and I recommend it as a guideline for best practices in training research.

Specifically, Weng et al tested the impact of loving-kindness compassion meditation or emotion reappraisal training on an emotion regulation fMRI task and behavioral economic game measuring altruistic behavior. For the fMRI task, participants viewed emotional pictures (IAPS) depicting suffering or neutral scenarios and either practiced a compassion meditation or reappraisal strategy to regulate their emotional response, before and after training. After the follow-up scan, good-old fashion experimental deception was used to administer a dictator economics-game that was ostensibly not part of the primary study and involved real live players (both deceptions).

For those not familiar with the dictator game, the concept is essentially that a participant watches a “dictator” endowed with 100$ give “unfair” offers to a “victim” without any money. Weng et al took great care in contextualizing the test purely in economic terms, limiting demand confounds:

Participants were told that they were playing the game with live players over the Internet. Effects of demand characteristics on behavior were minimized by presenting the game as a unique study, describing it in purely economic terms, never instructing participants to use the training they received, removing the physical presence of players and experimenters during game play, and enforcing real monetary consequences for participants’ behavior.

This is particularly important, as without these simple manipulations it would be easy for stodgy reviewers like myself to worry about subtle biases influencing behavior on the task. Equally important is the content of the two training programs. If for example, Weng et al used a memory training or attention task as their active-control group, it would be difficult not to worry that behavioral differences were due to one group expecting a more emotional consequence of the study, and hence acting more altruistic. In the supplementary information, Weng et al describe the two training protocols in great detail:

Compassion

… Participants practiced compassion for targets by 1) contemplating and envisioning their suffering and then 2) wishing them freedom from that suffering. They first practiced compassion for a Loved One, such as a friend or family member. They imagined a time their loved one had suffered (e.g., illness, injury, relationship problem), and were instructed to pay attention to the emotions and sensations this evoked. They practiced wishing that the suffering were relieved and repeated the phrases, “May you be free from this suffering. May you have joy and happiness.” They also envisioned a golden light that extended from their heart to the loved one, which helped to ease his/her suffering. They were also instructed to pay attention to bodily sensations, particularly around the heart. They repeated this procedure for the Self, a Stranger, and a Difficult Person. The Stranger was someone encountered in daily life but not well known (e.g., a bus driver or someone on the street), and the Difficult Person was someone with whom there was conflict (e.g., coworker, significant other). Participants envisioned hypothetical situations of suffering for the stranger and difficult person (if needed) such as having an illness or experiencing a failure. At the end of the meditation, compassion was extended towards all beings. For each new meditation session, participants could choose to use either the same or different people for each target category (e.g., for the loved one category, use sister one day and use father the next day).

Reappraisal

… Participants were asked to recall a stressful experience from the past 2 years that remained upsetting to them, such as arguing with a significant other or receiving a lower-than- expected grade. They were instructed to vividly recall details of the experience (location, images, sounds). They wrote a brief description of the event, and chose one word to best describe the feeling experienced during the event (e.g., sad, angry, anxious). They rated the intensity of the feeling during the event, and the intensity of the current feeling on a scale (0 = No feeling at all, 100 = Most intense feeling in your life). They wrote down the thoughts they had during the event in detail. Then they were asked to reappraise the event (to think about it in a different, less upsetting way) using 3 different strategies, and to write down the new thoughts. The strategies included 1) thinking about the situation from another person’s perspective (e.g., friend, parent), 2) viewing it in a way where they would respond with very little emotion, and 3) imagining how they would view the situation if a year had passed, and they were doing very well. After practicing each strategy, they rated how reasonable each interpretation was (0 = Not at all reasonable, 100 = Completely reasonable), and how badly they felt after considering this view (0 = Not bad at all, 100 = Most intense ever). Day to day, participants were allowed to practice reappraisal with the same stressful event, or choose a different event. Participants logged the amount of minutes practiced after the session.

In my view the active control is extremely well designed for the fMRI and economic tasks, with both training methods explicitly focusing on the participant altering an emotional response to other individuals.  In tests of self-rated efficacy, both groups showed significant decreases in negative emotion, further confirming the active control. Interestingly when Weng et al compared self-ratings over time, only the compassion group showed significant reduction from the first half of training sessions to the last. I’m not sure if this constitutes a limitation, as Weng et al further report that on each individual training day the reappraisal group reported significant reductions, but that the reductions themselves did not differ significantly over time. They explain this as being likely due to the fact that the reappraisal group frequently changed emotional targets, whereas the compassion group had the same 3 targets throughout the training. Either way the important point is that both groups self-reported similar overall reductions in negative emotion during the course of the study, strongly supporting the active control.

Now what about the findings? As mentioned above, Weng et al tested participants before and after training on an fMRI emotion regulation task. After the training, all participants performed the “dictator game”, shown below. After rank-ordering the data, they found that the compassion group showed significantly greater redistribution:

The dictator task (left) and increased redistribution (right).

For the fMRI analysis, they analyzed BOLD responses to negative vs neutral images at both time points, subtracted the beta coefficients, and then entered these images into a second-level design matrix testing the group difference, with the rank-ordered redistribution scores as a covariate of interest. They then tested for areas showing group differences in the correlation of redistribution scores and changes of BOLD response to negative vs neutral images (pre vs post), across the whole brain and in several ROIs, while properly correcting for multiple comparisons. Essentially this analysis asks, where in the brain do task-related changes in BOLD correlate more or less with the redistribution score in one group or another. For the group x covariate interaction they found significant differences (increased BOLD-covariate correlation) in the right inferior parietal cortex (IPC), a region of the parietal attention network, shown on the left-hand panel:

Increased correlation between negative vs neutral imagery related BOLD and redistribution scores (left), connectivity with DLPFC (right).

They further extracted signal from the IPC cluster and entered it into a conjunction analysis, testing for areas showing significant correlation  with the IPC activity, and found a strong effect in right DLPFC (right panel). Finally they performed a psychophysiological interaction (PPI) analysis with the right DLPFC activity as the seed, to determine regions showing significant task-modulated connectivity with that DLPFC activity. The found increased emotion-modulated DLPFC connectivity to nucleus accumbens, a region involved in encoding positive rewards (below, right).

Screen shot 2013-05-23 at 3.21.15 PM

PPI shows increased emotion-modulated connectivity of nucleus accumbens and DLPFC.

Together these results implicate training-related BOLD activity increases to emotional stimuli in the parietal attention network and increased parietal connectivity with regions implicated in cognitive control and reward processing, in the observed altruistic behavior differences. The authors conclude that compassion training may alter emotional processing through a novel mechanism, where top-down central-executive circuits redirect emotional information to areas associated with positive reward, reflecting the role of compassion meditation in emphasizing increased positive emotion to the aversive states of others. A fitting and interesting conclusion, I think.

Overall, the study should receive high marks for its excellent design and appropriate statistical rigor. There is quite a bit of interesting material in the supplementary info, a strategy I dislike, but that is no fault of the authors considering the publishing journal (Psych Science). The question itself is extremely novel, in terms of previous active-controlled studies. To date only one previous active-controlled study investigated the role of compassion meditation on empathy-related neuroplasticity. However that study compared compassion meditation with a memory strategy course, which (in my opinion) exposes it to serious criticism regarding demand characteristic. The authors do reference that study, but only briefly to state that both studies support a role of compassion training in altering positive emotion- personally I would have appreciated a more thorough comparison, though I suppose I can go and to that myself if I feel so inclined :).

The study does have a few limitations worth mentioning. One thing that stood out to me was that the authors never report the results of the overall group mean contrast for negative vs neutral images. I would have liked to know if the regions showing increased correlation with redistribution actually showed higher overall mean activation increases during emotion regulation. However as the authors clearly had quite specific hypotheses, leading them to  restrict their alpha to 0.01 (due to testing 1 whole-brain contrast and 4 ROIs), I can see why they left this out. Given the strong results of the study, it would in retrospect perhaps have been more prudent to skip  the ROI analysis (which didn’t seem to find much) and instead focus on testing the whole brain results.  I can’t blame them however, as it is surprising not to see anything going on in insula or amygdala for this kind of training.  It is also a bit unclear to me why the DLPFC was used as the PPI seed as opposed to the primary IPC cluster, although I am somewhat unfamiliar with the conjunction-connectivity analysis used here. Finally, as the authors themselves point out, a major limitation of the study is that the redistribution measure was collected only at time two, preventing a comparison to baseline for this measure.

Given the methodological state of the topic (quite poor, generally speaking), I am willing to grant them these mostly minor caveats. Of course, without a baseline altruism measure it is difficult to make a strong conclusion about the causal impact of the meditation training on altruism behavior, but at least their neural data are shielded from this concern. So while we can’t exhaustively conclude that compassion can be trained, the results of this study certainly suggest it is possible and perhaps even likely, providing a great starting point for future research. One interesting thing for me was the difference in DLPFC. We also found task-related increases in dorsolateral prefrontal cortex following active-controlled meditation, although in the left hemisphere and for a very different kind of training and task. One other recent study of smoking cessation also reported alteration in DLPFC following mindfulness training, leading me to wonder if we’re seeing the emergence of empirical consensus for this region’s specific involvement in meditation training. Another interesting point for me was that affective regulation here seems to involve primarily top-down or attention related neural correlates,  suggesting that bottom-up processing (insula, amygdala) may be more resilient to brief training, something we also found in our study. I wonder if the group mean-contrasts would have been revealing here (i.e. if there were differences in bottom-up processing that don’t correlate with redistribution). All together a great study that raises the bar for training research in cognitive neuroscience!