Regulation of the neural circuitry of emotion by compassion meditation: effects of meditative expertise

Abstract

Recent brain imaging studies using functional magnetic resonance imaging (fMRI) have implicated insula and anterior cingulate cortices in the empathic response to another's pain. However, virtually nothing is known about the impact of the voluntary generation of compassion on this network. To investigate these questions we assessed brain activity using fMRI while novice and expert meditation practitioners generated a loving-kindness-compassion meditation state. To probe affective reactivity, we presented emotional and neutral sounds during the meditation and comparison periods. Our main hypothesis was that the concern for others cultivated during this form of meditation enhances affective processing, in particular in response to sounds of distress, and that this response to emotional sounds is modulated by the degree of meditation training. The presentation of the emotional sounds was associated with increased pupil diameter and activation of limbic regions (insula and cingulate cortices) during meditation (versus rest). During meditation, activation in insula was greater during presentation of negative sounds than positive or neutral sounds in expert than it was in novice meditators. The strength of activation in insula was also associated with self-reported intensity of the meditation for both groups. These results support the role of the limbic circuitry in emotion sharing. The comparison between meditation vs. rest states between experts and novices also showed increased activation in amygdala, right temporo-parietal junction (TPJ), and right posterior superior temporal sulcus (pSTS) in response to all sounds, suggesting, greater detection of the emotional sounds, and enhanced mentation in response to emotional human vocalizations for experts than novices during meditation. Together these data indicate that the mental expertise to cultivate positive emotion alters the activation of circuitries previously linked to empathy and theory of mind in response to emotional stimuli.

Figure 1. State by Group by valence Interaction: A.

(AI) and (Ins.) stand for anterior insula and insula, respectively (z = 12 and z = 19, 15 experts and 15 novices, color codes: orange, p<5.10ˆ-2, yellow, p<2.10ˆ-2). B, C. Impulse response from rest to compassion in response to emotional sounds in AI (B) and Ins. (C). D–E. Responses in AI (D) and Ins. (E) during poor and good blocks of compassion, as verbally reported, for 12 experts (red) and 10 novices (blue).

Figure 2. Meditation modulates right insula response to emotional sounds:

A. Voxel-wise analysis of the Group by State by Valence (negative versus positive sounds) interaction in insula (Ins.) (z = 2, corrected, colors code: orange, p<5.10ˆ-2, yellow, p<2.10ˆ-2, 15 experts (red) and 15 novices (blue)). B. Average response in Ins. from rest to compassion for experts (red) and novices (blue) for negative and positive sounds. C–D. Voxel-wise analysis of BOLD response to emotional sounds during during poor vs. good blocks of compassion, as verbally reported. C. Main effect for verbal report in insula (Ins.) (z = 13, corrected, colors: orange, p<10ˆ-3, yellow, p<5.10ˆ-4, 12 experts and 10 novices). D. Average response in (Ins.) for experts (red) and novices (blue).

Figure 3. State by Group Interaction: A.

(Amyg.) stands for amygdala (y = −5, color codes: orange, p<2.10ˆ-3, yellow, p<5.10ˆ-4). B. Impulse response in (Amyg.) for 15 experts (red) and for 15 novices (blue) during rest (dashed line) and compassion (full line). C–D. Same as A–B in TPJ; y = −61. E. Side by state effect and side by state by group effect in TPJ on the average impulse response between meditation and rest; experts are in red, novices in blue.

Figure 4. Directionality of the brain activation.

Areas showing a negative ( dark blue, p<0.01, blue, p<0.005) or positive (orange, p<0.01, yellow, p<0.005) impulse response on average across 10 seconds in responses to all emotional sounds for the 15 novices and 15 experts at z = 31 compared to baseline (figs. A–D) and z = 13 (figs. E–H) (voxel-by-voxel paired t test compared to 0, corrected at p<0.01).