Introduction

Meditative practices have generated much interest in the scientific community, in particular with regards to how meditation affects brain function (Lutz et al., 2007; Austin, 2009; Slagter et al., 2011). While meditative states are interesting to study per se, perhaps more intriguing is the possibility that meditation training leads to enduring changes in brain function, even outside meditation sessions (Slagter et al., 2011).

Contemplative practices purportedly lead to increased well-being (e.g., Dalai Lama and Cutler, 1998), a claim supported by subjective reports of participants in mindfulness-based interventions (reviewed in Grossman et al., 2004; Chambers et al., 2009; Rubia, 2009). It has been proposed that these beneficial effects of meditation training may be due to improvements in attentional skills, which are themselves associated with better emotion regulation skills (Chambers et al., 2009; Wadlinger and Isaacowitz, 2011). Accumulating evidence suggests that meditation training yields improved emotional regulation, both in clinical and non-clinical populations. In non-clinical populations mindfulness-based interventions have been associated with lowered intensity and frequency of negative affect (Brown and Ryan, 2003; Chambers et al., 2008), reduced anxiety (Shapiro et al., 1998), more adaptive responding to stress (Davidson et al., 2003), decreased ego-defensive responsivity under threat (Brown et al., 2008), decreases in difficulties regulating emotions (Robins et al., 2012), reduced emotional interference from unpleasant stimuli (Ortner et al., 2007), and less prolonged physiological reactivity to emotional stimuli, in the form of decreased autonomic arousal (skin conductance response) (Ortner et al., 2007).

The interactions between attention and emotion regulation are complex, and likely involve several interrelated brain networks. One brain region that is centrally involved in emotional processing and the interactions between attention and emotion is the amygdala (Davis and Whalen, 2001; Phelps, 2006; Pessoa, 2008). The amygdala facilitates attention toward emotionally significant, or relevant, stimuli (Whalen, 1998; Sander et al., 2003; Vuilleumier, 2005; Whalen and Phelps, 2009). It is involved with attending to and encoding emotional stimuli, learning about the emotional significance of potentially ambiguous stimuli, distinguishing threat from safety, and appraising and responding to emotionally significant events—including stimuli of both positive and negative valence (Baxter and Murray, 2002; Phan et al., 2002; Sander et al., 2003; Zald, 2003; Haas and Canli, 2008; Sergerie et al., 2008; reviewed in Whalen and Phelps, 2009). Interestingly, Schaefer et al. (2002) found that amygdala activation could be voluntarily increased when subjects were asked to “maintain” the emotional response to negative-valence stimuli, and the amount of amygdala activation increase was correlated with subjects’ self-reported dispositional levels of negative affect. Conversely, decreased amygdala activation was observed during the application of emotional regulation strategies such as cognitive distancing and reappraisal (Beauregard et al., 2001; Ochsner et al., 2002, 2004; Lévesque et al., 2003).

While it is well-known that amygdala function is impaired in a number of disorders including depression, anxiety, and post-traumatic stress disorder, amygdala activation also differs across healthy individuals according to their personality traits (Davidson, 1998; Davidson and Irwin, 1999; Lapate et al., 2012). Individuals differ in how they attend to, process, and remember emotional stimuli. Individual differences in personality traits can be traced to a brain attentional network driven primarily by amygdala reactivity during the encoding of emotional stimuli (Haas and Canli, 2008). For example, Fischer et al. (2001) found that amygdala activation while viewing fear-eliciting stimuli was correlated with dispositional pessimism. Canli and colleagues found that amygdala response to positive and negative-valence stimuli was correlated with the personality traits of extraversion and neuroticism (Canli et al., 2001, 2002).

Individuals also vary in their propensity to engage in spontaneous emotion regulation strategies, such as reappraisal or suppression. Spontaneous reappraisal tendencies have been associated with lower levels of negative affect, greater interpersonal functioning, and greater psychological and physical well-being, and the opposite was found for spontaneous tendencies for emotional suppression (Gross and John, 2003). Individual differences in self-reported reappraisal tendencies were associated with decreased amygdala activity during the processing of negative emotional facial expressions (Drabant et al., 2009), pointing again at a crucial role of the amygdala in trait-like emotion regulation skills.

Given the association between amygdala activation and trait emotion regulation and attention, and given the hypothesis that meditation training may contribute to the development of such traits (Slagter et al., 2011), the question naturally arises as to whether amygdala activation may be modified by meditation training. Previous studies indicate that this might be the case. Several neuroimaging studies have implicated the amygdala in the effects of meditation training on the brain. In participants without prior meditation experience, mindfulness meditation training was associated with lower amygdala response to emotional stimuli when the subject entered a meditative state of mindful-attention, both in patients with social anxiety disorder (Goldin and Gross, 2010) and in healthy subjects (Taylor et al., 2011). Similar results have been reported in highly experienced meditation practitioners (Brefczynski-Lewis et al., 2007; but see Taylor et al., 2011). While the above studies investigated meditative states, it has also been proposed that meditation training may induce learning that is not stimulus- or task-specific, but process-specific, and thereby may result in enduring changes in mental function (Lutz et al., 2007, 2008b). These changes should correspond to changes in the brain that outlast the functional changes measured during meditation, and would be more indicative of a change in trait. Some support for this hypothesis can be found in structural differences in the brain which have been reported in relation to meditation training, both cross-sectionally in comparing experienced meditators with matched, meditation-naïve controls (Lazar et al., 2005; Pagnoni and Cekic, 2007; Luders et al., 2009, 2011; Grant et al., 2010), and longitudinally as measured before and after a meditation-based intervention (Hölzel et al., 2010, 2011a; Tang et al., 2010). In addition, several recent cross-sectional studies found differences in functional connectivity in the “resting state” which indicated stronger coupling between brain regions implicated in self-monitoring, cognitive control, and attention in experienced meditators compared to subjects with less or no meditation experience (Brewer et al., 2011; Jang et al., 2011; Hasenkamp and Barsalou, 2012; Taylor et al., 2012). However, little is known on the longitudinal effects of meditation training on emotional reactivity when participants are in an ordinary, non-meditative state.

In the present study, based on the extensive literature implicating the amygdala in emotion regulation, we tested the hypothesis that the amygdala response to emotional stimuli, as measured with functional magnetic resonance imaging (fMRI), would longitudinally decrease after an 8-week training in mindful-attention meditation. We also investigated how the effect might differ in another type of meditation training that has received less scientific attention so far, namely compassion meditation. The rationale for choosing these two types of meditation training is explained below.

Attention training is considered the foundation of meditation practices, as emphasized in the traditional texts (reviewed in Lutz et al., 2007; Austin, 2009). Meditation training demonstrably improves attentional skills (Valentine and Sweet, 1999; Jha et al., 2007; Tang et al., 2007; Chambers et al., 2008; Lutz et al., 2009b; MacLean et al., 2010; van den Hurk et al., 2010; reviewed in Lutz et al., 2008b; Baijal et al., 2011; Wadlinger and Isaacowitz, 2011), and theoretical accounts emphasize the role of attention regulation as one of the core components of mindfulness meditation (Brown and Ryan, 2003; Lutz et al., 2008b; Carmody, 2009; Hölzel et al., 2011b). Substantial evidence exists that attentional skills are a critical component of the emotion regulatory process (reviewed in Wadlinger and Isaacowitz, 2011), and it has been suggested that meditative interventions may be one of the most effective attention-based training methods available to improve emotional regulation (Wadlinger and Isaacowitz, 2011).

In this study, we implemented an 8-week program of mindful-attention training, in which subjects practice meditative techniques for enhancing mindful awareness of one’s internal state and external environment (Wallace, 2006). This program has been used principally in the form of 3-month intensive retreats, as was the case in the Shamatha Project—a longitudinal study aimed at investigating a broad range of health-related outcomes and effects on basic physiology and brain function (MacLean et al., 2010; Jacobs et al., 2011; Sahdra et al., 2011; Saggar et al., 2012). The training includes two components of attention, which have been called focused attention (FA) and open monitoring (OM) (Lutz et al., 2008b), also known as concentrative attention and receptive attention, respectively (Brown, 1977; Valentine and Sweet, 1999; Jha et al., 2007; Austin, 2009). Three main meditative techniques are taught: mindfulness of breathing (i.e., cultivating awareness of one’s breathing), mindfulness of mental events (i.e., cultivating awareness of the contents of one’s mind, such as thoughts, emotions, etc.), and awareness of awareness (in which awareness itself becomes the focus of meditation).

In contrast to mindful-attention practices aimed at improving attentional skills, compassion meditation is a distinct form of contemplative practice aimed at cultivating higher levels of compassion. Compassion can be defined as the feeling that arises in witnessing another’s suffering and that motivates a subsequent desire to help (Goetz et al., 2010). In the Mahayana Buddhist tradition, compassion is considered the ultimate source of well-being and happiness (Davidson and Harrington, 2001). Buddhist-inspired practices for cultivating compassion for self and others have been proposed by a number of authors as accessible methods to help alleviate psychological problems and improve well-being (Salzberg, 1995; Gilbert, 2005; Makransky, 2007; Germer, 2009; Hofmann et al., 2011; Ozawa-de Silva and Dodson-Lavelle, 2011; Jazaieri et al., 2012; Wallmark et al., 2012). Emerging scientific evidence suggests that these interventions may be beneficial on multiple levels. A pilot study indicated that compassionate mind training could lead to significant reductions in depression, anxiety, self-criticism, and shame (Gilbert and Procter, 2006). Another study suggested that compassion meditation may offer health-related benefits such as reduced immune and behavioral response to psychosocial stress (Pace et al., 2009, 2010). In a pilot study of loving-kindness meditation, a practice related to compassion meditation, chronic low back pain patients showed significant improvements in pain and psychological distress (Carson et al., 2005). Remarkably, Hutcherson et al. (2008b) found that even only a few minutes of loving-kindness meditation could increase feelings of social connection and positivity toward novel individuals. A few hours of training over the course of several days increased positive affective experiences and elicited activity in brain regions previously associated with positive affect and social affiliation (Klimecki et al., 2012). In a larger field experiment, Fredrickson et al. (2008) found that loving-kindness meditation produced increases over a 2-month period in daily experiences of positive emotions, which promoted increases in a wide range of personal resources (e.g., increased mindfulness, purpose in life, social support, decreased illness symptoms), which, in turn, predicted increased life satisfaction and reduced depressive symptoms. In a recent randomized controlled trial, an intensive meditation/emotion regulation intervention that included multiple elements of compassion training yielded reduced trait negative affect, rumination, depression, and anxiety, increased trait positive affect and mindfulness, and improved recognition of subtle facial expressions of emotion (Kemeny et al., 2012). Taken together, these recent studies support the hypothesis that compassion meditation contributes to improved emotion regulation. However, a direct comparison of mindful-attention training and compassion meditation training has been lacking.

In this study, we investigated how 8 weeks of training in either mindful-attention meditation or compassion meditation affected amygdala responses to emotional stimuli. Since we were interested in putative changes in affective trait, study participants were not instructed to enter a meditative state, so that changes in brain activity would reflect uncontrived emotional responses without being influenced by a purposeful manipulation of brain state.

Materials and Methods

Study Participants

Study participants were a subset of the subjects enrolled in a parent study being conducted at Emory University in Atlanta, GA, called the Compassion and Attention Longitudinal Meditation (CALM) study. All procedures were approved by the Institutional Review Boards at Emory University and Boston University. Healthy, medication-free adults (25–55 year-old) with no prior meditation experience were recruited in the Atlanta metropolitan area. Study participants gave written informed consent with Emory University to participate in the parent study, and additionally with Boston University to participate in the brain imaging study reported here. Participants in the parent study were randomized to eight weeks of training in either Mindful Attention Training (MAT), or Cognitively-Based Compassion Training (CBCT), or an active control intervention consisting of a health discussion group (CTRL). All interventions are described below. Fifty-one subjects (31 females, 20 males; age 34.1 ± 7.7 years, mean ± standard deviation) volunteered to participate in the brain imaging study. They underwent the pre-intervention scan before their randomization to any of the three groups. Of those who completed baseline assessments, five subjects dropped out of the study, and 10 either fell asleep or showed excessive motion in the scanner in at least one of their two scanning sessions. The final subject population in the present brain imaging study was N = 12 (8 females, 4 males; age 34.3 ± 9.6 years, mean ± standard deviation) in the MAT group, N = 12 (9 females, 3 males; age 32.0 ± 5.4 years) in the CBCT group, and N = 12 (5 females, 7 males; age 36.0 ± 7.6 years) in the CTRL group.