BOLD signal in insula is differentially related to cardiac function during compassion meditation in experts vs. novices

Abstract

The brain and the cardiovascular system influence each other during the processing of emotion. The study of the interactions of these systems during emotion regulation has been limited in human functional neuroimaging, despite its potential importance for physical health. We have previously reported that mental expertise in cultivation of compassion alters the activation of circuits linked with empathy and theory of mind in response to emotional stimuli. Guided by the finding that heart rate increases more during blocks of compassion meditation than neutral states, especially for experts, we examined the interaction between state (compassion vs. neutral) and group (novice, expert) on the relation between heart rate and BOLD signal during presentation of emotional sounds presented during each state. Our findings revealed that BOLD signal in the right middle insula showed a significant association with heart rate (HR) across state and group. This association was stronger in the left middle/posterior insula when experts were compared to novices. The positive coupling of HR and BOLD was higher within the compassion state than within the neutral state in the dorsal anterior cingulate cortex for both groups, underlining the role of this region in the modulation of bodily arousal states. This state effect was stronger for experts than novices in somatosensory cortices and the right inferior parietal lobule (group by state interaction). These data confirm that compassion enhances the emotional and somatosensory brain representations of others' emotions, and that this effect is modulated by expertise. Future studies are needed to further investigate the impact of compassion training on these circuits.

Figure 1. Compassion increases emotional cardiovascular arousal

Average HR significantly increased from neutral to compassion states for 10 experts (red) and 13 novices (blue) (main effect of State, see Table 1). During both states, emotional vocalizations were presented to the participants. Note that the practitioners showed significantly larger HR increase than the novices (State by Group interaction, see Table 1).

Figure 2. Expertise effect on HR/BOLD coupling parameter across states

A. Voxel-wise analysis comparing the coupling between HR and BOLD across states (compassion and neutral) between 10 experts (red) and 12 novices (blue) (z = 2, corrected, color code: orange, p < 0.05, yellow, p < 0.02) in insula (ins.). B. The cluster in the left insula shows an expertise-related effect consistent with our previous study (Lutz, 2008). The average HR/BOLD coupling in the left insula (Ins.) was larger for experts than novices (t-test, t(1,20) = 3.6, p < 0.005) and significantly positive for experts (t-test, t(1,9) = 3.9, p < 0.005). The coupling in this cluster shows additional emotion-specific effects: for both groups, there was no significant coupling within the neutral state (t-test, at least p>0.45 with each group), but, within the compassion state, the coupling was higher for experts than novices (t-test, t(1,20) = 3.8, p < 0.005) and was significantly positive only for the experts (t-test, t(1,9) = 4.0, p < 0.005). The HR/BOLD coupling represents the percent BOLD signal change per ratio of change in heart rate.

Figure 3. Compassion-specific neural correlates of HR

A. Voxel-wise analysis of the main effect of State (compassion vs. neutral) on the HR/BOLD coupling parameter in the dorsal ACC/premotor cortex (y = 22, corrected, color code: orange, p < 0.05, yellow, p < 0.02) 10 experts (red) and 12 novices (blue)). B. In this cluster the HR/BOLD coupling parameter was larger during the compassion state than the neutral state for 10 experts (red) and 12 novices (blue) (repeated ANOVA, main effect of state, F(1,20) = 8.1, p = 0.01). This finding suggests stronger cardiovascular autonomic control from the dorsal ACC during the compassion state than the neutral state.

Figure 4. Expertise effect on compassion-specific neural correlates of HR

A. Voxel-wise analysis of Group (experts vs. Novices) by State (compassion vs. neutral) interaction on the HR/BOLD coupling parameter in somatosensory and inferior parietal lobule (z = 52, corrected, color code: orange, p < 0.05, yellow, p < 0.02, 10 experts (red) and 12 novices (blue)). B. Compassion expertise affects the HR/BOLD coupling parameter, in particular in the inferior parietal lobule (IPL). In the cluster from A., the experts showed a larger HR/BOLD coupling parameter in compassion than neutral states and than the novices (repeated ANOVA, F(1,20) = 7.2, p < 0.05).