Chapter 6 - Short-term mindful breath awareness training improves inhibitory control and response monitoring

https://doi.org/10.1016/bs.pbr.2018.10.019Get rights and content

Abstract

Mindfulness meditation is thought to lead to positive changes in cognitive and affective functioning. However, the mechanisms underlying these changes are not well understood. One reason for this is that so far only very few studies considered the effects of specific meditation practices. We thus investigated the effects of engaging in one specific form of mindfulness meditation for a brief time period on behavioral and neural indicators of inhibitory control and metacognition. Performance on the Go/No-Go task and concurrent neural activity (EEG) was assessed before and after participants engaged in 3 weeks of mindful breath awareness meditation. Compared to a waitlist control group, meditation training enhanced the N2 event-related potential in No-Go trials and the error-related negativity (ERN) after error responses. As these two components reflect conflict and response monitoring, respectively, our results support the notion that mindfulness meditation improves metacognitive processes. The changes in the ERN were correlated with the accumulated amount of meditation time, highlighting the importance of meditation practice. Furthermore, meditation improved a behavioral marker of impulsive responding, indicating the relevance of mindfulness-based approaches for supporting health-related behaviors that are associated with deficits in impulsive control, such as substance abuse or over-eating. This study demonstrated that investigating one particular meditation practice rather than complex mindfulness-based interventions can contribute to a deeper understanding of mindfulness meditation mechanisms.

Introduction

Mindfulness meditation, the mental practice of trying to maintain non-judgmental moment-to-moment awareness of arising thoughts, feelings, and sensations within a controlled setting, is thought to lead to a range of positive changes in cognitive and affective functioning. Here we ask whether regularly engaging in simple, brief mindfulness meditation exercises for only a few weeks can lead to improvements in metacognitive functions. In particular, we are probing inhibitory control and response monitoring as key indicators of metacognition.

Within the last 20 years the popularity of mindfulness meditation and mindfulness-based interventions (MBIs), which integrate meditation practices into more comprehensive programs, has grown immensely (Van Dam et al., 2018). These developments are accompanied by claims regarding the effectiveness of MBIs and by citing mechanisms that are responsible for these reported positive changes. However, at this point in time it is fair to say that evidence for the effectiveness of MBIs is still somewhat limited (Gotink et al., 2015; Goyal et al., 2014) and that the field is held back by a relatively limited understanding of the underlying psychological mechanisms, compounded by a lack of focus on the specific exercises that constitute these MBIs (Dorjee, 2016; Malinowski, 2017). As emphasized by Gotink et al. (2015), because well-established MBIs such as Mindfulness-based Stress Reduction (MBSR; Kabat-Zinn, 1990), Mindfulness-based Cognitive Therapy (MBCT; Segal et al., 2012), or Mindfulness-based Relapse Prevention (MBRP; Bowen et al., 2014; Witkiewitz et al., 2013) include multiple components such as psycho-education, yoga exercises, and group discussions, the results from such studies do not provide conclusive evidence whether meditation practice is the main active ingredient. In other words, standard research paradigms that use any of these complex MBIs as an active meditation condition are not suited for singling out the effects of specific meditation practices.

To address this gap in understanding, this study focuses on investigating the meditation exercise most commonly used in MBIs, mindful breath awareness practice (Kabat-Zinn, 1990; Niemiec, 2013; Segal et al., 2012). This meditation is also of interest because individuals are likely to encounter it—or a slight variation of it—early on when starting to engage with Buddhist meditation practices (e.g., Hanh, 2016; Nydahl, 2008; Shamar Rinpoche, 2013; Wangchug Dorje, 2009). Although it is a simple practice, it captures the key features of mindfulness meditation, namely the attentional focus on an object (in this case the breath), combined with the non-judging, accepting moment-to-moment awareness of concurrently arising experiences (Dahl et al., 2015; Lutz et al., 2008; Malinowski, 2013, Malinowski, 2017).

Thus, by solely focusing on this meditation we are isolating the smallest common denominator of many forms of mindfulness-related meditations that incorporate these key features. The resulting understanding of the precise effects and mechanisms of action of each exercise used within MBIs will in the future make it possible to tailor interventions more precisely to the requirements of different target groups.

A lot has been written about the challenges of defining mindfulness, mindfulness meditation, and mindfulness-based programs (Chiesa, 2013; Chiesa and Malinowski, 2011; Dorjee, 2010, Dorjee, 2016; Malinowski, 2008, Malinowski, 2017; Nilsson and Kazemi, 2016; Van Dam et al., 2018). To avoid the well-documented ambiguity and associated confusion resulting from using mindfulness as an umbrella term, we follow current suggestions (Van Dam et al., 2018) and explicitly identify the mental state targeted by the meditation and describe the instructions used to achieve that state. We focus on one specific, well-defined mindfulness meditation exercise, which we call mindful breath awareness training, or M-BAT. Doing so, we build on previous work from our lab, which investigated exactly the same meditation practice (Malinowski, 2013; Malinowski et al., 2017; Moore et al., 2012), and connect to a range of further M-BAT studies that are forthcoming.

Often, M-BAT goes under the label of “mindful breathing,” “mindful breathing exercise” (or practice, training, meditation), or something similar. Some of these labels can lead to misunderstandings, as “breathing exercise” suggests that a specific way of breathing is exercised, and would be key to the meditation training. However, this is not at all the case. On the contrary, in M-BAT the breath, or more precisely the various sensations associated with breathing, is taken as object of meditative awareness, combined with the explicit instruction not to manipulate or change the breath, nor to evaluate these sensations. Rather, the meditator is encouraged to let all arising experiences (such as thoughts, images, sensations, sounds) pass, neither “pushing them away” or ignoring them nor engaging with them.

It is important to distinguish this approach from meditation exercises where controlling and/or manipulating the breath is a key component, as, for example, pranayama practices (Sengupta, 2012), which may have distinct effects on neural functioning (Melnychuk et al., 2018). Similarly, M-BAT needs to be distinguished from pure focused attention (FA) meditation (Lutz et al., 2008) that exclusively targets the development of a narrow attentional focus, where all other experiences are excluded from awareness.

Such exclusive FA meditation is typically contrasted with open monitoring (OM) meditation (Lutz et al., 2008). Whereas FA meditations would aim to develop sustained attention, OM would train the open awareness of a broad range of experiences. M-BAT constitutes a combination of both, with a stronger emphasis on FA in meditation novices who only recently started engaging with meditation, as was the case in this study (Malinowski, 2013). By including aspects of FA and OM, M-BAT incorporates the key components of mindfulness meditation that the field appears to broadly agree upon, namely attention and awareness, qualified by an open, curious, accepting, and non-judging attitude (Bishop et al., 2004; Chiesa, 2013; Dorjee, 2016; Malinowski, 2008).

In keeping with these accounts, mindfulness meditation is expected to improve cognitive control processes and metacognitive awareness (Chiesa and Serretti, 2010; Dorjee, 2016; Jo et al., 2017; Malinowski, 2013; Tang et al., 2015). In terms of psychological processes this relates to the ability to self-regulate behavioral responses (Hofmann et al., 2012) and to establish introspective metacognition, in particular the awareness and knowledge of bodily sensations, of mental phenomena, and of behavior (Dahl et al., 2015; Dorjee, 2016).

During M-BAT the practitioner needs to detect and inhibit habitual mental tendencies of mind wandering in order to maintain the present-centered experience of the breath. Thus, training and refining metacognitive skills are a central component of mindfulness practices and of M-BAT in particular (Malinowski, 2013). Several studies seem to support this notion, indicating that mindfulness meditation improves the efficiency of cognitive control processes and appears to result in changes of associated brain structures (for reviews, see Chiesa et al., 2011; Tang et al., 2015). However, much of this evidence needs to be considered preliminary and/or indirect, because the research either employed cross-sectional designs or investigated complex, multi-component MBIs, leaving unanswered whether the observed changes are specific to meditation practice.

Using variations of the classical Go/No-Go task a few studies investigated how meditation and/or mindfulness are related to metacognitive processes, particularly response inhibition and related monitoring processes (Falkenstein, 2006). The task requires participants to respond to a frequent stimulus (Go), while inhibiting the response to another, infrequent (No-Go) stimulus. Several EEG studies have identified two main event-related potentials (ERPs) elicited by the Go/No-Go task (Bokura et al., 2001; Donkers and Van Boxtel, 2004; Kiefer et al., 1998), which are indicative of specific aspects of metacognitive processing. The N2 ERP is characterized as a negative deflection, typically peaking between 200 and 400 ms after stimulus onset, and has been related to conflict monitoring (Donkers and Van Boxtel, 2004; Nieuwenhuis et al., 2003). The P3 ERP is a subsequent positive deflection with a maximum that peaks between 300 and 600 ms after stimulus onset and has been linked to response inhibition processes (Bokura et al., 2001; Smith et al., 2008). Both ERPs are usually more pronounced for No-Go than for Go stimuli, indicating their involvement in inhibition and response monitoring. Thus, these two ERP components are thought to reflect cognitive processes that are engaged and practiced in M-BAT. As index of conflict monitoring, the N2 relates to the aspect of monitoring mental activity that conflicts with the meditation instruction. In M-BAT this corresponds to the task of keeping the focus on breath-related sensations. The P3, on the other hand, is more directly linked to the aspect of interrupting or inhibiting off-task activity, in particular mind wandering.

Up to now, only a few studies used the Go/No-Go paradigm to investigate inhibitory control and monitoring processes associated with meditation and mindfulness. Schoenberg et al. (2014) reported that participating in an 8-week MBCT intervention lead to enhanced P3 amplitudes to No-Go stimuli in ADHD patients, reflecting improved response inhibition. Similarly, Smart et al. (2016) found an increase in the No-Go P3 amplitude in older participants with subjective cognitive decline, after 8 weeks of an MBSR program that was adapted for this target group. Andreu et al. (2018) used a specifically adapted “smoking Go/No-Go task” to investigate inhibitory control in cigarette smokers after they had been exposed to smoking cues. The No-Go P3 amplitude was lower in participants who had listened to a single 15-min mindfulness instruction that contained key features of MBRP than in participants who were asked to cope in their own way with the urge to smoke. This P3 effect seems to be in the opposite direction to those reported by Schoenberg et al. (2014) and Smart et al. (2016). However, as the Go/No-Go task was only administered after the mindfulness/coping inductions pre-existing group differences cannot be ruled out. Furthermore, it is doubtful whether a single mindfulness induction can yield information about the effects of regular meditation practice.

To sum up, evidence regarding the effects of mindfulness meditation on inhibitory control and related monitoring processes as measured with the Go/No-Go task, is currently limited.

A frequently used and particularly fruitful way of assessing metacognitive awareness of one's own behavioral performance is the error-related negativity (ERN). It is a negative, response-locked ERP component with a fronto-central maximum, peaking in the first 100 ms after an incorrect behavioral response is made. It is virtually absent in trials with accurate responses and is considered to index monitoring processes during response selection (Hajcak et al., 2005; Nieuwenhuis et al., 2003; Steinhauser and Yeung, 2010).

Currently, the evidence whether mindfulness meditation or any other form of meditation influences the ERN is limited. Teper and Inzlicht (2013) were the first to report an enhanced ERN amplitude, in conjunction with fewer errors, in meditators compared to non-meditators. These results are corroborated by comparable results from a similar study by Andreu et al. (2017) who used a more thoroughly matched control group. Eichel and Stahl (2017) provided evidence that presumably meditation-naïve participants (history of meditation engagement is not stated) who reported higher levels of mindfulness had a relatively enhanced ERN amplitude for detected response errors (compared to undetected errors), indicating more error awareness of the more mindful participants, while there were no clear cut differences in performance. However, because all three studies were cross-sectional, causal links between meditation/mindfulness and the ERN cannot be established.

Inconclusive evidence comes from two studies that investigated changes of the ERN amplitude in meditation-naïve participants as a result of listening to a single recorded mindfulness meditation instruction at one time point. Larson et al. (2013) found no difference in the ERN after such mindfulness induction, while Saunders et al. (2016) report an enhanced ERN but only for participants who were subjected to an emotion-focused rather than a thought-focused mindfulness induction. In any case, it remains doubtful to what extent a single session of following a recorded mindfulness induction bears similarity to regular engagement with meditation.

So far, the only study demonstrating a specific effect of mindfulness meditation on ERN comes from Fissler et al. (2017), who reported an increase of the ERN in chronically depressed patients after 2 weeks of regular engagement in mindfulness meditation. The previously blunted ERN amplitude increased in these depressed patients, while there was no change in patients who were instructed to rest for a similar amount of time. Smart and Segalowitz (2017) also reported an increase of the ERN amplitude in older participants who engaged in an MBSR program adapted for older adults. On the other hand, patients with ADHD who took part in MBCT did not demonstrate any ERN enhancement (Schoenberg et al., 2014). The complexity of MBSR and MBCT interventions used in the two latter studies occludes information about specific effects of mindfulness meditation.

In sum, although some data are available, evidence regarding the specific effects of mindfulness meditation on the ERN is limited, with the only direct positive evidence stemming from chronically depressed participants who “recovered” their blunted ERN to some extent. Whether such amplitude enhancements can be found in healthy participants is an open question and is addressed in the current study.

As this brief review demonstrated, despite the growing interest in the mechanisms of mindfulness meditation and the role of cognitive control and metacognition, evidence regarding the specific effects of mindfulness meditation on inhibitory control and performance monitoring is limited. Therefore, this study aims to assess the influence of one central mindfulness meditation practice, M-BAT, on neural processes of response inhibition and error detection. To this end, we conducted a randomized waitlist controlled study to evaluate the training-related changes on behavioral and electrophysiological markers of the Go/No-Go task.

We expected that, compared to the control group, engaging for 3 weeks in M-BAT would lead to (1) improved conflict monitoring, evidenced by enhanced N2 amplitudes, (2) improved response inhibition, reflected in larger P3 amplitudes, and (3) improved performance monitoring, indicated by larger ERN amplitudes after the training.

Section snippets

Participants

Forty-seven healthy adults (25 males; mean age 31.5 years) were recruited via a combination of online advertisements and from a psychology participant panel maintained at Liverpool John Moores University (LJMU). To be included in the study participants had to be meditation-naïve (i.e., no previous meditation experience), have normal or corrected-to-normal visual acuity, confirm they have no ongoing or recent mental health problems or neurological disorders (e.g., epilepsy) and confirm they are

Meditation time

Overall, the participants in the meditation group managed to engage with the requested meditation schedule, although the level of engagement varied. Based on the meditation logs, the mean total time dedicated to meditation throughout the 3-week program was 268.2 min (range: 99–408 min) divided into an average of 15.2 days of practice (range: 9–21 days). This equates to participants engaging in meditation five times per week for 16.6 min each time.

Mindfulness

To examine changes in self-reported mindfulness, we

Discussion

The aim of this study was to evaluate the influence of a 3-week period of regular mindful breath awareness meditation on inhibitory control processes and meta-awareness, assessed by the classical Go/No-Go task. Our results show that 3 weeks of engaging with M-BAT results in less impulsive responding, indicated by a significant decrease of the impulsivity index (ImpI) in the MG only. In terms of brain activity, meditation practice led to a relative increase of the centro-parietal N2 amplitude,

Acknowledgments

This research was supported by a BIAL Foundation grant (Research Bursary No. 30/08) to P.M. and a fellowship from the Spanish Ministry of Science and Innovation (BES-2009-017932) awarded to J.P.P. We would like to thank Geraldine Thomas from Mindflow for offering the meditation training to our participants.

References (84)

  • C.E. Lakey et al.

    Dispositional mindfulness as a predictor of the severity of gambling outcomes

    Pers. Individ. Dif.

    (2007)
  • P. Lattimore et al.

    A cross-sectional investigation of trait disinhibition and its association with mindfulness and impulsivity

    Appetite

    (2011)
  • P. Lattimore et al.

    ‘I can't accept that feeling’: relationships between interoceptive awareness, mindfulness and eating disorder symptoms in females with, and at-risk of an eating disorder

    Psychiatry Res.

    (2017)
  • A. Lutz et al.

    Attention regulation and monitoring in meditation

    Trends Cogn. Sci.

    (2008)
  • H. Nolan et al.

    FASTER: fully automated statistical thresholding for EEG artifact rejection

    J. Neurosci. Methods

    (2010)
  • M. Ruchsow et al.

    Error processing and impulsiveness in normals: evidence from event-related potentials

    Cogn. Brain Res.

    (2005)
  • K.L. Sanger et al.

    Mindfulness training with adolescents enhances metacognition and the inhibition of irrelevant stimuli: evidence from event-related brain potentials

    Trends Neurosci. Educ.

    (2016)
  • P.L. Schoenberg et al.

    Effects of mindfulness-based cognitive therapy on neurophysiological correlates of performance monitoring in adult attention-deficit/hyperactivity disorder

    Clin. Neurophysiol.

    (2014)
  • J.L. Smith et al.

    Movement-related potentials in the Go/NoGo task: the P3 reflects both cognitive and motor inhibition

    Clin. Neurophysiol.

    (2008)
  • N.T. Van Dam et al.

    Differential item function across meditators and non-meditators on the five facet mindfulness questionnaire

    Personal. Individ. Differ.

    (2009)
  • P.J. Whalen et al.

    The emotional counting Stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division

    Biol. Psychiatry

    (1998)
  • K. Witkiewitz et al.

    Mindfulness-based relapse prevention for substance craving

    Addict. Behav.

    (2013)
  • Y.-W. Yao et al.

    Combined reality therapy and mindfulness meditation decrease intertemporal decisional impulsivity in young adults with internet gaming disorder

    Comput. Hum. Behav.

    (2017)
  • C.I. Andreu et al.

    Behavioral and electrophysiological evidence of enhanced performance monitoring in meditators

    Mindfulness

    (2017)
  • C.I. Andreu et al.

    Effects of a brief mindfulness-meditation intervention on neural measures of response inhibition in cigarette smokers

    PLoS One

    (2018)
  • R.A. Baer et al.

    Using self-report assessment methods to explore facets of mindfulness

    Assessment

    (2006)
  • R.A. Baer et al.

    Construct validity of the five facet mindfulness questionnaire in meditating and nonmeditating samples

    Assessment

    (2008)
  • A.J. Bell et al.

    An information-maximization approach to blind separation and blind deconvolution

    Neural Comput.

    (1995)
  • Y. Benjamini et al.

    Controlling the false discovery rate: a practical and powerful approach to multiple testing

    J. R. Stat. Soc. B. Methodol.

    (1995)
  • C. Bergomi et al.

    The assessment of mindfulness with self-report measures: existing scales and open issues

    Mindfulness

    (2012)
  • S.R. Bishop et al.

    Mindfulness: a proposed operational definition

    Clin. Psychol. Sci. Pract.

    (2004)
  • S. Bowen et al.

    Relative efficacy of mindfulness-based relapse prevention, standard relapse prevention, and treatment as usual for substance use disorders: a randomized clinical trial

    JAMA Psychiatry

    (2014)
  • A. Chiesa

    The difficulty of defining mindfulness: current thought and critical issues

    Mindfulness

    (2013)
  • A. Chiesa et al.

    Mindfulness based interventions: are they all the same?

    J. Clin. Psychol.

    (2011)
  • A. Chiesa et al.

    A systematic review of neurobiological and clinical features of mindfulness meditations

    Psychol. Med.

    (2010)
  • D. Dorjee

    Kinds and dimensions of mindfulness: why it is important to distinguish them

    Mindfulness

    (2010)
  • D. Dorjee

    Defining contemplative science: the metacognitive self-regulatory capacity of the mind, context of meditation practice and modes of existential awareness

    Front. Psychol.

    (2016)
  • K. Eichel et al.

    The role of mindfulness and emotional stability in error detection

    Mindfulness

    (2017)
  • M. Fissler et al.

    Brief training in mindfulness may normalize a blunted error-related negativity in chronically depressed patients

    Cogn. Affect. Behav. Neurosci.

    (2017)
  • R.A. Gotink et al.

    Standardised mindfulness-based interventions in healthcare: an overview of systematic reviews and meta-analyses of RCTs

    PLoS One

    (2015)
  • M. Goyal et al.

    Meditation programs for psychological stress and well-being: a systematic review and meta-analysis

    JAMA Intern. Med.

    (2014)
  • P. Grossman

    Defining mindfulness by how poorly I think I pay attention during everyday awareness and other intractable problems for psychology's (re)invention of mindfulness: comment on Brown et al. (2011)

    Psychol. Assess.

    (2011)
  • Cited by (34)

    • Comparative effectiveness of mindfulness and mindful eating programmes among low-income overweight women in primary health care: A randomised controlled pragmatic study with psychological, biochemical, and anthropometric outcomes

      2022, Appetite
      Citation Excerpt :

      PHC is generally the first point of contact for patients, offering care that can address 80%–90% of a person's health needs during that person's lifetime. However, weight issues require an expanded comprehension of aetiology, pathophysiology, and forms of treatment; this presents an excellent opportunity for the impact evaluation and implementation of mindfulness-based interventions (MBIs) (Caldwell, Baime, & Wolever, 2015; Czepczor-Bernat, Brytek-Matera, Gramaglia, & Zeppegno, 2020; Kabat-Zinn, 2003; Pozuelos, Mead, Rueda, & Malinowski, 2019; Rogers, Ferrari, Mosely, Lang, & Brennan, 2017; Warren, Smith, & Ashwell, 2017). The therapeutic approach to obesity has focused on a biological and reductionist model of human functioning; other approaches are derived from it that are more prescriptive and restrictive (Most & Redman, 2020).

    • Event-related potential (ERP) measures of error processing as biomarkers of externalizing disorders: A narrative review

      2021, International Journal of Psychophysiology
      Citation Excerpt :

      Last, meditation techniques are another promising avenue to improve cognitive control. Researchers are currently exploring its effects in healthy volunteers (Andreu et al., 2019; Lin et al., 2019; Pozuelos et al., 2019; Quaglia et al., 2019; Saunders et al., 2016; Slagter et al., 2011; Teper et al., 2013) and it seems too early to speculate about the effectiveness in general and for externalizing disorders in particular. At the moment there are no proven interventions that could indicate that error processing could be improved in patients with externalizing disorders, but cognitive training, particularly like the study of Schoenberg et al. (2014), brain stimulation, and meditation techniques are certainly worth exploring, as they can address cognitive control elements shown in studies with healthy samples.

    • Development and recovery time of mental fatigue and its impact on motor function

      2021, Biological Psychology
      Citation Excerpt :

      These power values were then averaged across epochs for each frequency band. Segments containing significant muscle movements, eye movements and/or eye blinks, indicated by a z-value of >4 in the EEG (Fz, Cz, P3, Pz, P4, Oz) or EOG channels were discarded and replaced by cubic interpolation between segments (Nolan, Whelan, & Reilly, 2010; Pozuelos, Mead, Rueda, & Malinowski, 2019). Visual inspection of the data was used to check for flat lines.

    View all citing articles on Scopus
    View full text