Review
A systematic review of the neurophysiology of mindfulness on EEG oscillations

https://doi.org/10.1016/j.neubiorev.2015.09.018Get rights and content

Highlights

  • We conducted a systematic review of EEG studies of mindfulness meditation.

  • We examined power differentials between mindfulness and a control state.

  • Mindfulness was associated with enhanced alpha and theta power.

  • No consistent patterns were observed in terms of beta, delta and gamma.

  • Elevated alpha and theta may signify a state of relaxed alertness.

Abstract

Mindfulness meditation has been purported to be a beneficial practice for wellbeing. It would therefore be expected that the neurophysiology of mindfulness would reflect this impact on wellbeing. However, investigations of the effects of mindfulness have generated mixed reports of increases, decreases, as well as no differences in EEG oscillations in comparison with a resting state and a variety of tasks. We have performed a systematic review of EEG studies of mindfulness meditation in order to determine any common effects and to identify factors which may impact on the effects. Databases were reviewed from 1966 to August 2015. Eligibility criteria included empirical quantitative analyses of mindfulness meditation practice and EEG measurements acquired in relation to practice. A total of 56 papers met the eligibility criteria and were included in the systematic review, consisting of a total 1715 subjects: 1358 healthy individuals and 357 individuals with psychiatric diagnoses. Studies were principally examined for power outcomes in each bandwidth, in particular the power differentials between mindfulness and a control state, as well as outcomes relating to hemispheric asymmetry and event-related potentials. The systematic review revealed that mindfulness was most commonly associated with enhanced alpha and theta power as compared to an eyes closed resting state, although such outcomes were not uniformly reported. No consistent patterns were observed with respect to beta, delta and gamma bandwidths. In summary, mindfulness is associated with increased alpha and theta power in both healthy individuals and in patient groups. This co-presence of elevated alpha and theta may signify a state of relaxed alertness which is conducive to mental health.

Introduction

Meditation refers to a diverse range of mental activities which share a common focus on the regulation of attention and awareness (Cahn and Polich, 2006) in order to improve voluntary control of mental processes, which is purported to foster general wellbeing (Walsh and Shapiro, 2006). Most world cultures have developed their own forms of meditation; for example, Christianity has a long tradition of contemplative prayer (Egan, 1978). Much of the recent scientific interest in meditation has centred on mindfulness meditation, a practice that is believed to have originated with Buddhism around the fifth century B.C., although its roots may stretch back further to the third millennium B.C. in Hindu culture (Cousins, 1996).

The most common forms of meditation may be conceptualized as involving either focused attention or an open-monitoring process (Lutz et al., 2008). Focused attention practices can be operationalized into their respective attention networks (Posner and Petersen, 1990, Mirsky et al., 1991): sustained attention (e.g. towards a target, such as the breath), executive attention (e.g. preventing one's focus from ‘wandering’), attention switching (e.g. disengaging from distractions), selective attention and attention re-orienting (e.g. redirecting focus back to the breath), and working memory (Lutz et al., 2008, Vago and Silbersweig, 2012). Open-monitoring refers to a broader receptive awareness, a capacity to detect events within an unrestricted awareness without a specific focus (Raffone and Srinivasan, 2010), which can include a process of ‘meta-awareness’ (i.e. awareness of awareness, in which practitioners are able to reflect on the process of consciousness itself).

Mindfulness has been described as the awareness that arises through purposeful, nonjudgmental attentiveness to present moment experience (Kabat-Zinn, 2003). While mindfulness has been commonly viewed as an example of open-monitoring, it has been proposed to involve an admixture of focused attention and open-monitoring (Lutz et al., 2008, Vago and Silbersweig, 2012) as most mindfulness practices begin with a period of focused attention on a target, such as the breath, in order to focus awareness, followed by the more receptive state of open-monitoring (Cahn and Polich, 2006). In Vago and Silbersweig's model (2012), the practice of mindfulness leads to three overarching self-related capacities: meta self-awareness, self-regulation, and self-transcendence. These are subserved by numerous cognitive subcomponents, including motivation (which is crucial in terms of people practicing meditation in the first place), attention regulation (via the development of attention modalities), and de-centring (an ability, defined below, that arises from enhanced attention regulation, and which facilitates self-awareness and transcendence). It is further proposed that these three overarching capacities modulate ‘self-specifying and narrative self-networks’ through an integrative fronto-parietal control network.

Mindfulness has been applied as a clinical intervention based on the notion that it is a method for training attention and awareness. By developing the ability to observe one's thoughts and feelings, practitioners learn how to perceive them as temporary, objective events in the mind as opposed to reflections of the self that are necessarily true, which has been termed as the ability to “decentre” (Fresco et al., 2007). As a clinical intervention, it involves a process of engaging with negative experiences, such as pain or dysphoric emotions, with more dispassion and less reactivity (Shapiro et al., 2005). Mindfulness was initially applied as an intervention for chronic pain with Kabat-Zinn's (1982) Mindfulness-Based Stress Reduction (MBSR) program. The MBSR program has since been applied in the treatment for number of conditions, including cancer (Ledesma and Kumano, 2009) and migraine (Schmidt et al., 2010), and adapted as a treatment to prevent relapse in depression (Mindfulness-Based Cognitive Therapy; Segal et al., 2002) and for the treatment of substance abuse (Mindfulness-Based Relapse Prevention; Bowen et al., 2014, Mindfulness-Oriented Recovery Enhancement; Garland et al., 2014).

The effectiveness of mindfulness has been assessed by measures such as for depression and quality of life (Hofmann et al., 2010). As mindfulness may be considered to be a method of attention training and emotion regulation, we would expect that the corresponding neurophysiological states should be observable. Electroencephalography (EEG) is a non-invasive technique that analyses spatiotemporal aspects of underlying brain activity, providing a measure of the large-scale synchronization of neural networks (Cacioppo et al., 2007). Patterns of EEG activity for particular meditative states have been investigated. A commonly reported feature of meditation has been theta and alpha event-related synchronization (Fell et al., 2010), which are regarded as markers of internally-directed attention processing (Shaw, 1996). Such synchronization has been observed across different meditation practices, including mindfulness, as well as practices such as transcendental meditation, which involves focused attention upon an internally-voiced mantra. However, different types of meditation practice have been associated with unique frequency patterns, reflecting the form of attention (Dunn et al., 1999). For example, mindfulness has been associated with increased alpha power, while focused attention has been associated with increased gamma activity, and idiosyncratic meditation with decreased alpha and beta (Hinterberger et al., 2014).

Additionally, event-related potentials (ERPs) provide a measure of a large number of time-locked experimental trials, enabling the analysis of sensory, perceptual, and cognitive processing (Light et al., 2010). Such studies involve the precision analysis of populations of neuronal transients directly manifested via a stimulus/event, which is frequently a stimulus connected to an attention-based task (e.g. listening to an auditory signal) (Schoenberg and Speckens, 2014). The high temporal resolution of this approach, involving millisecond precision, allows the investigation of early information processing stages and subsequent transitions to higher-level cognitive operations. ERP studies have been used to corroborate the idea of mindfulness as a system of attention training. For example, van Leeuwen et al. (2012) examined the impact of mindfulness practice on hierarchical stimulus processing and attentional selection, focusing on differences in early components of the evoked visual response (e.g. P1 and N1 components) in meditators versus matched controls. Meditators exhibited faster attentional disengagement from a dominant global presentation in order to focus in on specific stimuli, suggesting that meditation enhances speed of attention allocation and relocation, thus increasing the depth of information processing.

In the present review, we have focused on mindfulness meditation. We have examined factors which appear to impact upon EEG measures, including the experience of the meditator (being a novice or relative expert), as experience has been reported to accentuate amplitude differences between meditation and the resting state (Hinterberger et al., 2014), although the converse has also been observed (Cahn et al., 2010). An additional factor includes the location of the brain activity. For example, increased alpha during mindfulness has been localized to frontal regions (Takahashi et al., 2005) but has also been observed in posterior regions (Lagopoulos et al., 2009, Cahn et al., 2010). Furthermore, EEG analysis of meditation may be affected by whether the control task is a resting state or a cognitive task, as increased theta amplitude during meditation has been observed in comparison to a resting state baseline, but was comparable in amplitude to an executive attention task, with these patterns further modulated by the experience of the meditator (Lomas et al., 2014).

We sought to perform a systematic review of patterns of electrophysiological activity associated with mindfulness in order to examine its impact on neurophysiology, as assessed by EEG bandwidth activation and other measures, including hemispheric asymmetry or event-related potentials, and the functional significance of these activities. If mindfulness is expected to impact on functioning attentional networks as well as open-monitoring, then we would expect to observe distinct neural features associated with its practice. We also expected that the experience of the meditator, type of control task, and location of the EEG oscillation would moderate the impact of mindfulness on neurophysiology.

Section snippets

Methods

The literature search was conducted using the MEDLINE and Scopus electronic databases with the criteria: “EEG” (AND) “mindfulness OR meditation”, in all fields in MEDLINE, and limited to article title, abstract, and keywords in Scopus, with the dates from 1966 to 1st August 2015. Regarding the participants, interventions, comparisons, outcomes and study design (PICOS) characteristics, the key criteria were, interventions: mindfulness meditation or functional equivalent; participants: adults;

Search results

Following removal of duplicate citations, 284 potentially relevant papers were identified. From the abstract review, 120 papers were excluded. From the full text reviews of 164 papers, 108 papers were excluded. Thus, a total of 56 papers were included in the systematic analysis. Ten of these papers were identified as reporting on overlapping samples: (Berkovich-Ohana et al., 2012, Berkovich-Ohana et al., 2013); (Cahn et al., 2010, Cahn et al., 2013); (Slagter et al., 2007, Slagter et al., 2009

Discussion

The main finding to emerge from the systematic review is an increase in alpha power associated with mindfulness relative to a resting state. Additional effects have been reported in the other oscillation bandwidths, including a majority trend towards increased theta power during meditation compared to a resting state. The patterns of increased alpha and theta amplitude associated with meditation were observed in both experienced and novice meditators. Clinical studies of mindfulness-based

References (105)

  • M. Grunwald et al.

    Power of theta waves in the EEG of human subjects increases during recall of haptic information

    Neurosci. Lett.

    (1999)
  • T. Harmony et al.

    EEG delta activity: an indicator of attention to internal processing during performance of mental tasks

    Int. J. Psychophysiol.

    (1996)
  • A. Hauswald et al.

    What it means to be Zen: marked modulations of local and interareal synchronization during open monitoring meditation

    Neuroimage

    (2015)
  • Z. Josipovic

    Duality and nonduality in meditation research

    Consciousness Cogn.

    (2010)
  • J. Kabat-Zinn

    An outpatient program in behavioral medicine for chronic pain patients based on the practice of mindfulness meditation: theoretical considerations and preliminary results

    Gen. Hosp. Psychiatry

    (1982)
  • C.E. Kerr et al.

    Effects of mindfulness meditation training on anticipatory alpha modulation in primary somatosensory cortex

    Brain Res. Bull.

    (2011)
  • P.M. Keune et al.

    Mindfulness-based cognitive therapy (MBCT), cognitive style, and the temporal dynamics of frontal EEG alpha asymmetry in recurrently depressed patients

    Biol. Psychol.

    (2011)
  • P.M. Keune et al.

    Approaching dysphoric mood: state-effects of mindfulness meditation on frontal brain asymmetry

    Biol. Psychol.

    (2013)
  • Y. Kubota et al.

    Frontal midline theta rhythm is correlated with cardiac autonomic activities during the performance of an attention demanding meditation procedure

    Cogn. Brain Res.

    (2001)
  • D. Lehmann et al.

    Reduced functional connectivity between cortical sources in five meditation traditions detected with lagged coherence using EEG tomography

    Neuroimage

    (2012)
  • A. Lutz et al.

    Attention regulation and monitoring in meditation

    Trends Cogn. Sci.

    (2008)
  • A.B. Newberg et al.

    The neural basis of the complex mental task of meditation: neurotransmitter and neurochemical considerations

    Med. Hypotheses

    (2003)
  • J. Onton et al.

    Frontal midline EEG dynamics during working memory

    Neuroimage

    (2005)
  • G. Pfurtscheller et al.

    Event-related synchronization (ERS) in the alpha band – an electrophysiological correlate of cortical idling: a review

    Int. J. Psychophysiol.

    (1996)
  • M.I. Posner et al.

    Attentional networks

    Trends Neurosci.

    (1994)
  • S. Schmidt et al.

    Mindfulness-based stress reduction is an effective intervention for patients suffering from migraine – results from a controlled trial

    Eur. J. Integr. Med.

    (2010)
  • P.L.A. 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.C. Shaw

    Intention as a component of the alpha-rhythm response to mental activity

    Int. J. Psychophysiol.

    (1996)
  • A. Sobolewski et al.

    Impact of meditation on emotional processing – a visual ERP study

    Neurosci. Res.

    (2011)
  • B. Stinson et al.

    A novel EEG for alpha brain state training, neurobiofeedback and behavior change

    Complement. Ther. Clin. Pract.

    (2013)
  • T. Takahashi et al.

    Changes in EEG and autonomic nervous activity during meditation and their association with personality traits

    Int. J. Psychophysiol.

    (2005)
  • C. Tallon-Baudry et al.

    Oscillatory gamma activity in humans and its role in object representation

    Trends Cogn. Sci.

    (1999)
  • A. Ahani et al.

    Quantitative change of EEG and respiration signals during mindfulness meditation

    J. Neuroeng. Rehabil.

    (2014)
  • I. Amihai et al.

    Arousal vs. relaxation: a comparison of the neurophysiological and cognitive correlates of Vajrayana and Theravada meditative practices

    PLoS One

    (2014)
  • H. Arita

    Anterior prefrontal cortex and serotonergic system activation during Zen meditation practice induces negative mood improvement and increased alpha band in EEG

    Rinsho Shinkeigaku (Clin. Neurol.)

    (2012)
  • T. Barnhofer et al.

    State effects of two forms of meditation on prefrontal EEG asymmetry in previously depressed individuals

    Mindfulness

    (2010)
  • T. Barnhofer et al.

    Effects of meditation on frontal alpha-asymmetry in previously suicidal individuals

    Neuroreport

    (2007)
  • D.E. Becker et al.

    Physiological responses to clicks during Zen, Yoga, and TM meditation

    Psychophysiology

    (1981)
  • A. Berkovich-Ohana et al.

    Studying the default mode and its mindfulness-induced changes using EEG functional connectivity

    Soc. Cogn. Affect. Neurosci.

    (2013)
  • 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)
  • C.A. Brown et al.

    Psychobiological correlates of improved mental health in patients with musculoskeletal pain after a mindfulness-based pain management program

    Clin. J. Pain

    (2013)
  • W.B. Britton et al.

    Awakening is not a metaphor: the effects of Buddhist meditation practices on basic wakefulness

    Ann. N.Y. Acad. Sci.

    (2014)
  • R.L. Buckner et al.

    The brain's default network

    Ann. N.Y. Acad. Sci.

    (2008)
  • J.T. Cacioppo et al.

    Handbook of Psychophysiology

    (2007)
  • B.R. Cahn et al.

    Occipital gamma activation during Vipassana meditation

    Cogn. Process.

    (2010)
  • B.R. Cahn et al.

    Event-related delta, theta, alpha and gamma correlates to auditory oddball processing during Vipassana meditation

    Soc. Cogn. Affect. Neurosci.

    (2013)
  • B.R. Cahn et al.

    Meditation states and traits: EEG, ERP, and neuroimaging studies

    Psychol. Bull.

    (2006)
  • J.L. Cantero et al.

    Sleep-dependent {theta} oscillations in the human hippocampus and neocortex

    J. Neurosci.

    (2003)
  • A.S. Chan et al.

    Electroencephalographic (EEG) measurements of mindfulness-based triarchic body-pathway relaxation technique: a pilot study

    Appl. Psychophysiol. Biofeedback

    (2008)
  • N.R. Cooper et al.

    Investigating evoked and induced electroencephalogram activity in task-related alpha power increases during an internally directed attention task

    Neuroreport

    (2006)
  • Cited by (0)

    View full text