Enhanced amygdala–cortical functional connectivity in meditators

Highlights

• Functional connectivity in meditation experts during emotion processing was studied.

• Enhanced neural connectivity in meditators during affective processing.

• The enhanced neural connectivity may relate to the mental training of meditation.

• Amygdala involves in meditation-related affective neuroplasticity.

Abstract

Previous studies have demonstrated that meditation is associated with neuroplastic changes in the brain regions including amygdala, anterior cingulate cortex (ACC), and temporal–parietal junction. Extended from these previous works, this study examined the functional connectivity of the amygdala in meditation experts during affective processing and observed that these experts had significantly stronger left amygdala (LA) connectivity with the dorsal ACC (dACC), premotor, and primary somatosensory cortices (PSC) while viewing affectively positive stimuli when compared to the novices. The current findings have implications for further understanding of affective neuroplastic changes associated with meditation in the amygdala.

Introduction

Loving-kindness meditation is a mental practice of the cultivation of unconditionally positive feelings toward the self and others [1]. Meditation practitioners usually commence their practice in forms that train attention or mindfulness and then move on to other forms of practice such as loving-kindness meditation. The initial attention practice is thought to be complementary to the subsequent compassion practice, which in turn provides a calm and peaceful state for one to enter an attentive state. The practice of meditation is associated with a reduction in anxiety and negative affect [2], [3], [4].

Lutz et al. [5] observed that practice of compassion meditation is associated with a significantly higher level of neural activity in the amygdala, right temporo–parietal junction, and right posterior superior temporal sulcus. Lee et al. [6] have demonstrated that experts of loving-kindness meditation showed significant activity in the ventral anterior cingulate cortex (ACC) and inferior frontal gyrus while viewing happy pictures and that in the caudate and middle frontal gyrus while viewing sad pictures. These regions are important for identifying the emotional value of stimuli, generation of affective states, and regulation of emotional responses [7].

Amygdala is a prime neural correlate of the limbic system essential for emotion processing [8]. Altered amygdala activity toward emotional stimuli has been consistently observed in patients with depression, anxiety, bipolar disorder, or post-traumatic stress disorder [9]. Stein et al. [10] reported that the amygdala is functionally connected with an extended cortical–subcortical network consisting of the anterior and posterior cingulate, insular, prefrontal, and parahippocampal cortices during the perception of angry and fearful faces. Specifically, the amygdala is strongly inhibited by the supragenual ACC when processing fearful/angry stimuli. Such inhibition of the amygdala is important for the down-regulation of the fear response [11]. Failure to engage the pregenual ACC to down-regulate the amygdalar response relates to difficulty in resolving emotional conflict in patients with generalized anxiety disorder [12]. Activity of the amygdala is also strongly inhibited by the activity of the posterior cingulate when processing fearful/angry stimuli [10].

A recent study which found that eight weeks of compassion training increased the activity of the right amygdala (RA) in response to negative images at trend-level in a group of meditation novices, and such increase correlates with a decrease in depression scores [13]. Change of functional synchrony of the amygdala with other brain regions during affective processing after long-term meditation practice remains unanswered. Taken together, because of the importance of the neural synchrony between the amygdala and its connected regions in emotion processing and initial evidence of meditation-related affective plasticity in the amygdala, this study explored, for the first time, the impact of long-term meditation practice on the amygdalar functional connectivity during emotion processing. A passive viewing paradigm was employed to probe the basic process of emotion perception in the absence of other cognitive demands. The hypothesis that meditation experts would exhibit a different pattern of amygdalar connectivity in regions involved in affective and reward processing such as the nucleus accumbens, ACC, and OFC compared to novices during emotion processing was verified in this study.