ReviewA systematic review of the neurophysiology of mindfulness on EEG oscillations
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
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