Impact of mindfulness on the neural responses to emotional pictures in experienced and beginner meditators
Research highlights
► Mindfulness attenuated the subjective impact of emotional stimuli. ► Mindfulness was associated with amygdala deactivation during emotion processing for beginners. ► Mindfulness led to reduced prefrontal/cingulate activity for long-term meditators.
Introduction
Originating from ancient Eastern traditions (Nataraja, 2008), meditation is an increasingly prominent object of study within the fields of clinical psychology and behavioral neuroscience. Mindfulness is a form of meditation which has been operationally defined as “a kind of nonelaborative, nonjudgmental, present-centered awareness in which each thought, feeling, or sensation that arises in the attentional field is acknowledged and accepted as it is” (Bishop, 2004). The detached observation state which is adopted during mindfulness is thought to promote an objective and adaptive manner of responding to emotional triggers in contrast to a habitual pattern of emotional reactivation typically driven by past experiences, fears and preconceptions (Bishop, 2004). Consistent with this view, it has been demonstrated that mindfulness-based clinical interventions have beneficial outcomes on the treatment of affect-related psychopathology, including major depression (Bondolfi et al., 2010, Teasdale et al., 2000) and anxiety disorders (Goldin and Gross, 2010, Kabat-Zinn et al., 1992, Kim et al., 2009). However, there still remains much to uncover on the specific mechanisms as well as neural substrates through which this state of awareness influences emotional processes.
To date, a few studies have examined the effects of meditation on the processing of emotional stimuli. Focused-breathing typically practiced during mindfulness has been shown to promote emotional self-regulation by reducing reactivity to emotionally laden pictures (positive and negative) (Arch and Craske, 2006). Mindfulness meditation practiced following a sad mood induction was also shown to decrease dysphoric mood states (Broderick, 2005). Additionally, Brefczynski-Lewis et al. (2007) found a negative correlation between the number of hours of meditation training and right amygdala activation during concentration meditation in a group of experienced meditators while processing negative emotional sounds. In another study (Farb et al., 2010), the MBSR program led to reduced activation in regions associated with autobiographical memory and increased activity in the right insula (Farb et al., 2010). Finally, Lutz et al. (2008) investigated the effects of compassion meditation on the processing of emotional auditory stimuli. They found increased right insular activation for experienced meditators, relative to beginners, during a state of compassion meditation while listening to negative emotional sounds (compared to emotionally positive sounds). This brain region plays an important role in awareness of interoceptive states (Craig, 2004, Critchley et al., 2004). Compassion meditation also induced increased amygdalar activation while listening to emotional and neutral sounds for experienced meditators relative to beginners. It is noteworthy that since compassion meditation involves maintaining a non-referential state of compassion, different brain processes may be involved in mindfulness meditation during emotional processing as opposed to compassion meditation.
An increasing number of neuroimaging studies have investigated the neural substrates underlying emotional self-regulation strategies, such as cognitive distancing and reappraisal (Beauregard et al., 2001, Levesque et al., 2003, Ochsner et al., 2002, Ochsner et al., 2004). These strategies have commonly been associated with the recruitment of prefrontal cortical areas critically involved in executive control functions (e.g., lateral prefrontal cortex [LPFC], medial prefrontal cortex [MPFC], and anterior cingulate cortex [ACC]), and decreased activation in subcortical structures implicated in emotional processing (e.g., amygdala) (Beauregard et al., 2001, Levesque et al., 2003, Ochsner et al., 2002, Ochsner et al., 2004).
Convergent with neuroimaging studies of emotional self-regulation, there are some reports that meditative states are associated with increased activation in various prefrontal cortical areas. Such heightened prefrontal activation has been interpreted as reflecting increased recruitment of attentional resources during meditation (Newberg et al., 2001). Interestingly, mindfulness was shown to be associated with increased MPFC/LPFC activation and reduced amygdalar activation during affect labeling, which is commonly employed during meditation in order to identify emotional states (Creswell et al., 2007). In this study, Creswell et al. (2007) found that participants high in trait mindfulness also had negative correlations between areas of the PFC (MPFC and LPFC) and the right amygdala, but not those low in trait mindfulness. These findings are consistent with evidence that the MPFC, through its inhibitory downstream connections to the amygdala, is implicated in the extinction of conditioned fear as well as the dampening of negative affect (Amaral et al., 1992, Davidson, 1998). Similar results were also found in clinical populations. For example, Goldin and Gross (2010) reported that patients with social anxiety disorder (SAD) exhibited decreased right amygdalar activation after viewing phrases of negative self-beliefs, and increased activation in regions relevant to the control of attention (including regions of the parietal cortex) after having completed an 8-week mindfulness-based stress reduction program (MBSR). Goldin and Gross (2010) interpreted these results as indicating that mindfulness meditation helps to reduce avoidance-related behavior to threatening stimuli in SAD patients by enhancing the recruitment of brain regions involved in attentional control.
However, from a phenomenological perspective, it should be noted that controlled modulation and reappraisal differ to a large extent from mindfulness. Indeed, most emotional self-regulation strategies aim at altering emotional states, whereas mindfulness is based on accepting emotional states as they are (Kabat-Zinn, 1994). Consistent with this view, some neuroimaging studies suggest that long-term mindfulness meditation training can lead to decreased activation in prefrontal cortical areas, particularly the MPFC (Farb et al., 2007, Grant et al., 2011). In one of these studies, Farb et al. (2007) found that an experiential focus condition (monitoring the self in terms of present-moment circumstances) was associated with deactivations of the ventral and dorsal MPFC compared with a narrative self-focus task (monitoring the self in terms of self-descriptive traits). This effect was more pronounced and widespread in individuals having completed an 8-week MSBR program compared to a control group. A similar pattern of results has recently been reported in Zen meditators experiencing emotionally salient painful stimuli (Grant et al., 2011). In this study, when normally attending to painful stimulations, experienced meditators exhibited decreased activation in several brain regions involved in executive control and emotional appraisal, including the MPFC, LPFC, and amygdala compared to non-meditators. These decreased activations found in executive control areas have been proposed to reflect that meditation training is associated with a reduction in cognitive elaboration of aversive stimuli (Grant et al., 2011).
Clearly, however, methodological discrepancies in meditative and control tasks, as well as the different strategies or cognitive processes employed and the level or type of expertise in meditators may account for the inconsistencies in the literature. Nevertheless, the premise that meditation stabilizes emotion by not evaluating or appraising salient stimuli is in line with the prefrontal deactivations reported during mindfulness (Farb et al., 2007, Grant et al., 2011). Yet to date, little is known regarding the brain mechanisms through which mindfulness meditation modulates the processing of emotional stimuli.
In this context, a central goal of the present functional magnetic resonance imaging (fMRI) study was to investigate the neural mechanisms mediating the effect of this form of meditation on the processing of emotionally laden stimuli. Another major goal of this study was to examine the impact of the extent of mindfulness meditation experience on the brain mechanisms supporting the processing of emotional stimuli. Thus, a group of experienced meditators and a group of beginner meditators were scanned while they viewed negative, positive, or neutral pictures in a mindful state and a regular (non-mindful) state of awareness. They also rated stimuli on the emotional intensity they experienced when viewing the pictures. We hypothesized that the emotional stimuli viewed during mindfulness would be perceived as less emotionally intense than those viewed in a non-mindful state of awareness. Moreover, we hypothesized that mindfulness would lead to decreased activation in cerebral structures involved in emotional processing, such as the amygdala. Based on previous research (Brefczynski-Lewis et al., 2007), this was predicted to occur to a greater extent in experienced meditators relative to beginners. Finally, due to the lack of evaluative processes maintained during mindfulness meditation, we hypothesized that mindfulness would lead to reduced activation in prefrontal cortical areas, and that this would occur to a greater extent for the group of experienced meditators.
Section snippets
Participants
Before being selected for the study, potential participants underwent preliminary telephone screening and were not included if they had any current or previous psychiatric or neurological disorders, consumed any psychotropic drugs, or had any severe medical conditions. The group of experienced meditators consisted of 12 individuals with more than 1000 h of experience in Zen meditation (7 females, 5 males; 11 right-handed, 1 left-handed; 25–60 years of age, M = 46, SD = 11), and were recruited from
Self-report data
The ANOVA revealed a significant main effect of Valence (F(2, 18) = 122.39, p < .001, η2 = .87). Negative pictures (p < .0001, M = 2.08; SD = 0.65) and positive pictures (p < .001, M = 1.64; SD = 0.67) were rated as more emotionally intense than neutral pictures (M = 0.52; SD = 0.41). A significant main effect of Condition (F(1, 18) = 7.23, p < .05, η2 = .29) was also found. This effect was due to the fact that pictures viewed in the Mindful condition (M = 1.29; SD = 0.57) were rated as less emotionally intense than those
Discussion
The results of the present study can be summarized as follows. Behavioral response data revealed that mindfulness attenuated emotional intensity perceived from all valence categories of pictures across the entire sample of participants, whereas functional brain imaging data indicated that this attenuation was achieved via distinct neural mechanisms for each group. For experienced meditators relative to beginners, mindfulness induced deactivations of regions involved in the default mode network
Acknowledgments
This work was supported by a grant from National Sciences and Engineering Research Council of Canada (NSERC) to M.B. We thank the staff of the Unité de Neuroimagerie Fonctionnelle (UNF) of the Centre de recherche de l'Institut Universitaire de Gériatrie de Montréal (CRIUGM) for their technical assistance.
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