Elsevier

Brain and Cognition

Volume 135, October 2019, 103585
Brain and Cognition

Breath-focused mindfulness alters early and late components during emotion regulation

https://doi.org/10.1016/j.bandc.2019.103585Get rights and content

Highlights

  • Breath-focused mindfulness reduced P1, N2, and LPP amplitudes for emotional pictures.

  • P1 amplitudes for emotional minus neutral pictures correlated positively with focus attention.

  • N2 amplitudes for emotional minus neutral pictures correlated positively with mindful trait.

  • Breath-focused mindfulness works through a top-down emotion regulation strategy.

Abstract

Breath-focused mindfulness (BFM), which induces changes in brain structure and function, is applied in the clinical treatment of mental disorders as a method to regulate one’s emotions. However, whether BFM works through a top-down emotional regulation strategy to alter brain dynamics and its relationship with individual differences in trait mindfulness are unclear. Event-related potentials (ERPs) of 20 healthy BFM-naïve undergraduates were recorded when they conducted BFM/viewing tasks while viewing affective pictures. Participants completed the Attentional Control Scale (ACS) and the Mindful Attention Awareness Scale (MAAS). The results indicated that under the viewing condition, positive and negative pictures elicited greater P1, N2, and late positive potential (LPP) amplitudes than did neutral pictures. However, BFM attenuated P1, N2, and LPP amplitudes for positive and negative pictures but not for neutral pictures. P1 amplitudes for emotional minus neutral pictures correlated with individual differences in focus attention measured by the ACS, while N2 amplitudes for emotional minus neutral pictures correlated with individual differences in trait mindfulness measured by the MAAS. These observations suggest that, consistent with the dual-process model, BFM is an effective emotion regulation strategy and might activate the dorsal top-down prefrontal system to alter early and late neural dynamics of affective processing.

Introduction

Breath-focused mindfulness (BFM), a type of mindful meditation, is central to mindfulness-based interventions and is widely applied in the clinical treatment of mental disorders (e.g., social anxiety disorder; Goldin & Gross, 2010) as a skill to foster emotion regulation (Grossman, Niemann, Schmidt, & Walach, 2004). Using cross-section design, Arch and Craske (2006) reported that a 15-min BFM induction in a normal, primarily undergraduate population decreased the intensity and negativity of emotional responses to affectively valenced picture slides and increased willingness to remain in contact with aversive picture slides. Following a BFM intervention program comprised of two weekly 1-h group sessions during a five-week period, female undergraduate students with high worry scores reported better emotional meta-cognition and showed improved indices of somatic and autonomic regulation (Delgado et al., 2010). After a brief BFM intervention (4 days), Zeidan, Gordon, Merchant, and Goolkasian (2010) assessed mood, verbal fluency, visual coding, and working memory of undergraduate students who had no prior meditation experience. They found that brief BFM training also significantly improved visuospatial processing, working memory, and executive functioning. Briefly, many mental and physiological benefits have been discovered after a BFM task (Chiesa and Serretti, 2010, Kabat-Zinn, 2018, Witkiewitz et al., 2019). However, the neural mechanism behind BFM during instant affective processing is still not thoroughly understood.

Within the field of emotional regulation, the dual-process model proposes that top-down emotion regulation refers to explicit, voluntary, and conscious attention and cognitive control processes (e.g., detachment) including dorsal brain regions such as the dorsolateral prefrontal cortex (PFC) in the frontoparietal network (Braunstein et al., 2017, Gyurak et al., 2011, Raschle et al., 2019). In contrast, bottom-up emotional regulation refers to implicit, nonconscious, and automatic processes including ventral regions such as the ventromedial PFC (Grecucci et al., 2015, Taylor et al., 2018). However, there is no consensus as to whether mindful practice (including BFM) as an attentive nonjudgmental focus on experiences in the here and now (Kabat-Zinn, 1990) (e.g., focus on the sensations of breathing) belongs to a top-down or bottom-up strategy (Guendelman, Medeiros, & Rampes, 2017). Some authors have argued that the salutary effect of mindfulness on attentional control and emotional regulation occurs through increased top-down modulation of limbic systems by the prefrontal cortex (PFC) (Herwig et al., 2018, Lutz et al., 2016, Prakash et al., 2014). For example, mindful mediation (e.g., focusing attention on present-moment experience) increases PFC integration while subjects view aversive pictures following a two-week mindful practice (Doll et al., 2016). In contrast, others posit that mindfulness might exert a unique emotional regulation strategy mainly through the privileged engagement of the bottom-up systems (Farb, Anderson, & Segal, 2012). Consistent with this view, mindful mediation activates the insula and amygdala in the default mode network (Goldin and Gross, 2010, Farrés et al., 2019). Particularly, Sevinc et al. (2019) reported that mindfulness training is associated with differential engagement of the right supramarginal gyrus as well as hippocampal-cortical reorganization and that it enhances hippocampal connectivity to the primary sensory cortex during retrieval of extinguished stimuli. Thus, functional magnetic resonance image (fMRI) research with high spatial resolution has revealed that different top-down or bottom-up brain systems might be involved in different components of mindful meditation. However, assuming that BFM is a dynamic process, fMRI research cannot reveal changes in the temporal processing of BFM.

Event-related potentials (ERPs) with high temporal resolution can capture rapid neural responses. For example, the P1 amplitude is significantly attenuated during both generation of inner speech and performance of visual imagery involving inward attention compared with external tasks (Villena-González, López, & Rodríguez, 2016). In particular, Villena-González et al. (2017) studied the effects of shifting attention to the heart using a cue-target detection paradigm and found that directing attention to the heart (i.e., inward attention) significantly reduced the visual P1/N1 amplitude evoked by the attentional probe. Other studies have assessed how mindfulness training influences ERPs. For example, after mindfulness-based cognitive therapy (MBCT) practice comprising eight weekly two-hour sessions, the mindfulness task in which depressive patients were instructed to focus on their breath, as taught in MBCT, increased late contingent negative variation response to an auditory test stimulus (Bostanov, Keune, Kotchoubey, & Hautzinger, 2012). Following 8-week mindfulness-based pain management programs, the intervention group had reduced anticipation-evoked potential during late anticipation and pain-evoked P2 to acute experimental pain compared with the control group (Brown & Jones, 2013). Eddy, Brunyé, Tower-Richardi, Mahoney, and Taylor (2015) found that after participants completed a brief mindfulness induction (15 min) and then passively viewed images for approximately 15 min, only those participants who reported feeling more decentered exhibited reduced P3 responses to negative versus neutral images. Moreover, P3 amplitudes elicited by target tones were attenuated during the breath counting task in comparison to the tones task (Atchley et al., 2016). Contingent negative variation and P3 are modulated after mindful movement training (Lasaponara, Glicksohn, Mauro, & Ben-Soussan, 2018). Attentional benefits of mindfulness in healthy older adults were accompanied by reductions in frontal N2 and P3 latency (Isbel, 2019). Until now, it has been unclear how BFM alters ERP components in the face of simultaneous emotional stimulation.

A number of ERP studies on affective processing have determined three early and late components which are modulated by affective pictures in different attentional stages (for a review, see Olofsson et al., 2008, Keil, 2013). P1, originating in the extrastriate visual cortex, peaks approximately 80–150 ms poststimulus. (Di Russo et al., 2005). P1 is sensitive to attention allocation (Smith, Cacioppo, Larsen, & Chartran, 2003) and is enhanced by emotional compared to neutral stimuli (Holmes, Kragh, Tipper, & Green, 2009). The negative wave, N2, peaks 200–350 ms poststimulus, is found primarily over anterior scalp sites, and appears to be related to the attention-monitoring process originating from dorsomedial PFC (Dickter and Bartholow, 2010, Folstein and Van Petten, 2008). Additionally, late positive potential (LPP) is a positive component with a central-parietal scalp distribution that begins within 400–500 ms after stimulus onset (Weinberg, Hilgard, Bartholow, & Hajcak, 2012). Positive and negative pictures induce larger LPP amplitudes than neutral pictures (Hajcak, Dunning, & Foti, 2009), indicating that the LPP reflects an increase in attention to visual emotional stimuli (Schupp, Flaisch, Stockburger, & Junghofer, 2006). Using these components, the first aim of our study was to investigate the time course of BFM in response to emotional stimulation.

Research has shown that BFM exhibits experience-dependent functional plasticity. The second aim of this study was to examine the relationship between individual differences in trait mindfulness and BFM-related ERP components. Following the hypothesis from Chiesa, Serretti, and Jakobsen (2013), mindfulness training is associated with top-down emotion regulation in short-term practitioners and with bottom-up emotional regulation in long-term practitioners. For example, short-term BFM training increased activation in frontal areas involved in sustaining and monitoring the focus of attention such as the orbitofrontal cortex (OFC) or dorsolateral PFC (Froeliger et al., 2017, Percik et al., 2018, Tomasino and Fabbro, 2016, Zeidan et al., 2011), while longer meditation experience was associated with lower responses in the thalamus and insula (Bachmann et al., 2018, Grant et al., 2010, Lee et al., 2017). ERP research has also indicated that LPP amplitudes in control subjects with no experience in meditation significantly increased in response to negative pictures compared to long-term meditators (Sobolewski, Holt, Kublik, & Wróbel, 2011). Specially, the increased amygdala-PFC connectivity during a BFM task is associated with individual difference in trait mindfulness measured by the Mindful Attention Awareness Scale (MAAS) (Doll et al., 2016). Resting-state fMRI found that individuals with high trait mindfulness had greater within-network connectivity in the default mode network and salience network (Lim, Teng, Patanaik, Tandi, & Massar, 2018); more mindful youth showed a state-specific reduction in connectivity between salience/emotion and central executive networks (Marusak et al., 2018). Those high in dispositional mindfulness (even without formal mindfulness training) appear to be able to regulate emotions by top-down attenuation of early sensory experience (Wheeler, Arnkoff, & Glass, 2017). Thus, individual differences in trait mindfulness might correlate with BFM-related ERP components.

The present study investigated how momentary BFM modulates visual ERP components of affective pictures and the association with individual differences in trait mindfulness. According to the hypothesis of intrinsic relevance that emotional stimuli are preferentially processed (Olofsson et al., 2008, Schupp et al., 2006), we predicted that in the viewing condition, affective images would evoke more notable P1, N2, and LPP amplitudes than neutral pictures. In the first aim, based on the dual-process model, the hypothesis that short term mindfulness is involved in top-down emotion regulation (Chiesa et al., 2013, Doll et al., 2016), and that affective processing was under the control of BFM from the start of presenting pictures in this study, we expected that as an explicit emotion regulation, the BFM task performed by participants with naïve mindfulness would decrease P1, N2, and LPP amplitudes to affective images relative to viewing during different attentional processing stages. Moreover, with regard to the second aim, we predicted that in the BFM condition but not in the viewing condition, P1 amplitudes reflecting early attention allocation would be related with individual differences in attention control because BFM induces a sustained attention to respiration sensation in the present moment (Bishop et al., 2004), while N2 amplitudes reflecting attention monitoring would be associated with individual differences in trait mindfulness because BFM exhibits experience-dependent plasticity by engaging in top-down cognitive change (Wheeler et al., 2017).

Section snippets

Participants

This study recruited 20 Han Chinese undergraduate students (nine men and 11 women; M = 18.89, SD = 0.71) through advertisements on campus from Shanghai Normal University in China. All participants reported being right-handed and declared normal or corrected-to-normal vision. They had no prior history of or current unstable medical illness, head injury, or neurological illness. They all reported that they were not acquainted with mindful meditation and had little mindful meditation experience.

Manipulation check

Considering the participants were naïve to the BFM task and only had three minutes to familiarize with BFM, participants were requested to complete a postexperiment questionnaire at to determine whether participants followed the instructions to perform the BFM task. The results indicated that all participants strictly performed the BFM task according to the instructions (M = 6.24, SD = 0.32).

Arousal intensity

A two-way repeated measures ANOVA detected a significant main effect of valence on arousal intensity [F

Discussion

The present study investigated how BFM modulates the time course of affective pictures and links with individual differences in trait mindfulness. The results from the postexperiment questionnaire demonstrated that all participants strictly completed the BFM task during the viewing of affective pictures. As predicted, we observed affective modulation effects with increases in the ERP amplitude following the presentation of affective pictures relative to neutral pictures. During the BFM task,

Acknowledgement

This study was funded by the National Natural Science Foundation of China (31470997 and 81171289).

Declaration of Competing Interest

None of the authors have potential conflicts of interest to be disclosed.

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