The neuroscience of meditation: classification, phenomenology, correlates, and mechanisms

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The neuroscience of meditation: classification, phenomenology, correlates, and mechanisms Tracy Brandmeyera,b,c,*, Arnaud Delormeb,c,d,e, Helan
e Wahbehd,f a

Osher Center for Integrative Medicine, School of Medicine, University of California, San Francisco, CA, United States b Centre de Recherche Cerveau et Cognition (CerCo), Universit
e Paul Sabatier, Toulouse, France c CNRS, UMR 5549, Toulouse, France d Institute of Noetic Sciences (IONS), Petaluma, CA, United States e Swartz Center for Computational Neuroscience, Institute of Neural Computation (INC), University of California, San Diego, CA, United States f Oregon Health & Science University, Portland, OR, United States *Corresponding author: Tel.: +1-415-514-8139, e-mail address: [email protected]

Abstract Rising from its contemplative and spiritual traditions, the science of meditation has seen huge growth over the last 30 years. This chapter reviews the classifications, phenomenology, neural correlates, and mechanisms of meditation. Meditation classification types are still varied and largely subjective. Broader models to describe meditation practice along multidimensional parameters may improve classification in the future. Phenomenological studies are few but growing, highlighting the subjective experience and correlations to neurophysiology. Oscillatory EEG studies are not conclusive likely due to the heterogeneous nature of the meditation styles and practitioners being assessed. Neuroimaging studies find common patterns during meditation and in long-term meditators reflecting the basic similarities of meditation in general; however, mostly the patterns differ across unique meditation traditions. Research on the mechanisms of meditation, specifically attention and emotion regulation is also discussed. There is a growing body of evidence demonstrating positive benefits from meditation in some clinical populations especially for stress reduction, anxiety, depression, and pain improvement, although future research would benefit by addressing the remaining methodological and conceptual issues. Meditation research continues to grow allowing us to understand greater nuances of how meditation works and its effects.

Progress in Brain Research, ISSN 0079-6123, https://doi.org/10.1016/bs.pbr.2018.10.020 © 2019 Elsevier B.V. All rights reserved.

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Keywords Meditation, Neuroscience, Phenomenology

1 Introduction In the 1990s biologist, philosopher, and neuroscientist Francisco Varela proposed neurophenomenological methodologies as a path toward addressing the hard problems of studying consciousness (Chalmers, 1995; Varela, 1996). Due to the efforts of pioneers such as Varela, whose work was largely influenced by philosopher and founder of the school of phenomenology Edmund Husserl, we have seen a concerted effort to reintegrate first-person experiential accounts into behavioral and neuroscientific methodologies over the last several decades. The scientific investigation of meditation and contemplative traditions, which specifically leverage these individual accounts of direct experience to study state related changes in brain and physiological activity, has now gained the attention of researchers from broad number of academic disciplines, ranging from neuroscience, psychology and medicine, to researchers interested in identifying the neural correlates of consciousness (NCC; Rees et al., 2002). While most contemplative traditions are comprised of spiritual practices that aim to bring the practitioner closer to self-actualization, transcendence, or enlightenment, from a neuroscientific and clinical perspective meditation is usually considered as a set of diverse and specific methods of distinct attentional training in order to bring mental activity under improved insight into one’s own mental activity (Cahn and Polich, 2009). Through the observation of ongoing mental and physical experience, this training is thought to improve the mechanisms underlying self-regulation (H€olzel et al., 2011b; Kabat-Zinn et al., 1985; Lutz et al., 2008; Shapiro et al., 2006; Tang et al., 2007; Vago and David, 2012) and can manifest as changes in mental states or as longer lasting traits (Cahn and Polich, 2006). Now known as contemplative neuroscience, this young but rapidly growing multidisciplinary field investigates the underlying neural mechanisms of ancient contemplative meditation traditions and practices, alongside their clinical, psychological, and neurological manifestations. While advancements in this field are in part due to improvements in neuroimaging methods, they are also due to the variety of medical practices incorporating meditation into therapeutic protocols. Some of the most notable research findings suggest that the mental activity involved in meditation practices can facilitate neuroplasticity and connectivity in regions in the brain specifically related to emotion and attention regulation (H€olzel et al., 2011a; Lazar et al., 2005; Lutz et al., 2004; Shapiro et al., 2006; Vago and David, 2012). A significant number of fundamental neuroscience research findings suggest that consciousness reflects a series of perceptually cyclical and discrete neural processes (Baumgarten et al., 2015; VanRullen, 2016). However, our direct perception is that of a continuous and unified experience. According to William James, if we truly want to scientifically study consciousness, we must rigorously observe our personal

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experience of consciousness by means of introspection like Galileo, Planck, Einstein, and Darwin whose discoveries were rooted in rigorous, exhaustive, and precise “observation” of the phenomenon they studied (James, 1890). For scholars such as Alan Wallace, in order for a science of consciousness to exist, it can only progress after the establishment of the necessary means and refined instruments that can measure and observe consciousness with rigor and precision. Wallace argues that the only principal instrument humanity has ever possessed for directly observing the mind or consciousness is the mind itself. Thus, the mind itself is the instrument in need of refining through the practice of meditation. When attention is not trained, it is habitually prone to mind wandering, agitation, and dullness. Thus, if the mind is to be used as the instrument for exploring and experimenting with consciousness, these perhaps less desirable cognitive states can be replaced with greater attentional stability and vividness (Wallace and Shapiro, 2006). Indian and Hindu contemplative practitioners developed the initial methods for obtaining deeper levels of insight into the nature of the mind and consciousness by cultivating highly focused, stable and sustained attention, or “Samadhi” (Wallace, 2014). The Buddhist tradition later went on to refine and develop rigorous methods for stabilizing attention by using them in new and novel ways (Wallace, 1999). Contemplative neuroscience and the broader study of contemplative practices not only offers insight into the scientific, phenomenological and philosophical understanding of the nature of consciousness, but they also shed light on the highly plastic neural circuitry underlying attention, emotion, sensory perception and selfawareness. In the medical and clinical community, mindfulness (which is a spiritual or psychological faculty that forms an essential part of Buddhist meditation practice) is defined as the “awareness that arises through paying attention, on purpose, in the present moment, non-judgmentally” (Kabat-Zinn, 1982, 1990) The first Mindfulness-based intervention was initially developed by Dr. John Kabat-Zinn for a group of chronically ill patients who were unresponsive to traditional medical treatments. Having developed an 8-week protocol based on the fundamental teachings of Buddhist mindfulness and then secularized for western behavioral and clinical contexts, mindfulness practices are now practiced by hundreds of thousands of people and have been integrated into an enormous number of public, clinical and psychotherapeutic programs (Baer, 2003; Grossman et al., 2004; Kabat-Zinn, 2003; Kabat-Zinn et al., 1998). Mindfulness-based interventions have been widely implemented throughout various clinical contexts. The strongest positive effects are evident for brain structure and function, immune responses, mental health, chronic pain, and sleep. Numerous psychoneuroimmunology measures have also been evaluated for mindfulness meditation demonstrating improvements in immune and endocrine markers (Pascoe et al., 2017). For example, one meta-analysis of 4 randomized controlled trials of 190 participants found that mindfulness meditation leads to increased telomerase activity in peripheral blood mononuclear cells (Schutte and Malouff, 2014) demonstrating that meditation (or the associated mental activity) can influence the immune system. Many (but not all) studies of mindfulness meditation for mental health

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conditions or symptoms have shown some degree of positive benefit. Mindfulness meditation for psychiatric disorders was superior to various control conditions immediately post-intervention and also at long-term follow-up (Goldberg et al., 2017). Anxiety and depression symptoms have also been shown to improve after participating in mindfulness-based interventions (Goyal et al., 2014; Hofmann et al., 2010; Khoury et al., 2013, 2015; Roemer et al., 2008; Salters-Pedneault et al., 2008), in addition to new evidence suggesting improvements in post-traumatic stress disorder related symptoms (Colgan et al., 2016, 2017; Kearney et al., 2013; Wahbeh et al., 2016). Chronic pain can also be improved from mindfulness meditation (Bawa et al., 2015; Grossman et al., 2007; Hilton et al., 2017; Wells et al., 2017), with strong evidence for its role in reducing the perceived pain intensity of primary headache (Gu et al., 2018). Finally, multiple studies have shown some improvements in sleep quality and insomnia (Gong et al., 2016; Neuendorf et al., 2015). Research investigating contemplative practices began to surface in the broader mainstream neuroscientific community in the late 1990’s, and now almost a quarter of a century later, research on the effects of meditation research publications have increased dramatically (from 30 papers published in 1975 to 428 published in 2017 in PubMed). This is in large part due to advancements in neuroimaging methodologies, in addition to advancements in contemplative neuroscience that come from our rapidly evolving understanding of neuroplasticity; our brains are continuously changing in response to the environment, past experiences, and various forms of training. A large body of literature also suggests that there is an ongoing bidirectional communication between the mind, brain, and body, implying that psychological well-being is directly related to the physical health of both the body and brain (Kiecolt-Glaser et al., 2002). While the exact mechanisms are not yet fully understood, research consistently demonstrates the downstream effects that occur in the body as brain circuits are transformed (Vitetta et al., 2005). With this brief introduction of the history of contemplative neuroscience, this chapter aims to give an overview of phenomenology, classification, and neural correlates of various meditation traditions. The meditation traditions included are not exhaustive but we have made an attempt to include all major types of meditation. We will first address the classification of various meditation techniques. We will then examine the structural, functional, and oscillatory correlates of meditation (i.e., MRI, fMRI, EEG) in addition to providing an overview of the current research highlighting the primary mechanisms by which contemplative practices are thought to affect well-being, namely attention and emotion regulation.

2 Deconstructing mindfulness The Buddhist term Paliterm sati translates into English as mindfulness. The term Mindfulness can be defined differently in contemporary contexts, as compared to traditional Buddhist contexts which offer multiple and sometimes incompatible conceptions of mindfulness (Dunne, 2015; Sharf, 2014). With the rise of modern

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mindfulness-based interventions, the meaning of mindfulness has been extensively debated. The term sati means “to remember” or “remember the dharma” whereby the true nature of phenomena can be seen (Sharf, 2014). According to Kabat-Zinn, mindfulness is an “awareness that arises through paying attention, on purpose, in the present moment, non-judgmentally...it’s about knowing what is on your mind” (Kabat-Zinn, 1990). However, Kabat-Zinn (2011) has acknowledged that mindfulness represents a far broader scope of concepts and practices than the specific definition he provided back in the 1990s while developing Mindfulness-Based Stress Reduction (MBSR) implies (Van Dam et al., 2018). Furthermore, this definition is one of convenience facilitating the expression of these ideas and constructs in an accessible manner to individuals coming from Western cultures (Kabat-Zinn, 2011; Van Dam et al., 2018). Mindfulness in the context of the broader scientific research community generally refers to a self-regulated attentional state focused on present moment experiences, emphasizing curiosity, openness, and acceptance (Dahl et al., 2015). While several core features are considered to be fundamental in meditative practice, much debate remains over various western translations, applications and constructs of mindfulness when compared to the more traditional Buddhist frameworks (Dahl et al., 2015). Mindfulness, most notably understood in secular applications of mindfulness, is a cognitive act of the practice of focusing attention on the body, breath, and content of any thought (Wahbeh et al., 2016) and observing one’s own cognitive and affective processes. Examples of secular programs that include mindfulness are Mindfulness-Based Stress Reduction (Kabat-Zinn, 1982), MindfulnessBased Cognitive Therapy (Segal et al., 2002), and Mindfulness-Based Relapse Prevention (Bowen et al., 2014). However, mindfulness according to Buddhist philosophical dialogues may be structured conceptually as either “bearing in mind” or non-discursive “mere nondistraction” and is an integrated exercise incorporating a number of cognitive and bodily skills that involve ethically oriented behavior and actions (Thompson, 2017). In Thompson (2017) he posits that mindfulness is by no means an ethically neutral method for reducing stress and improving concentration, but rather that it is a method that can be learned for increasing wholesome mental states and behaviors, while decreasing unwholesome ones. Lutz et al. proposed a multidimensional phenomenological matrix rather than one definition for mindfulness that includes metaawareness, object orientation, and dereification along with the qualifiers of aperture (i.e., focused or diffuse focus), clarity, stability, and effort, and then attempted to classify common meditation practices according to the matrix (Lutz et al., 2015). Given the current confusion and rightful debate around the semantics surrounding “mindfulness,” as suggested by Van Dam et al. (2018) it is critical that scientists, practitioners, instructors, and the public news media avoid relying on overly broad and “umbrella rubric of ‘mindfulness’” and engage in explicating more differentiated and explicit descriptions of the mental states and specific meditation techniques and interventions that are under investigation. The phenomenological matrix proposed by Lutz is one step toward greater differentiation of meditation practices.

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3 Classifying meditation techniques Focused attention meditation (FA) practices are thought to cultivate enhanced concentration and single pointed focus on a given object in addition to the development of meta-awareness (Dahl et al., 2015; Lutz et al., 2008). Our focus of attention naturally fluctuates between various sources of information even when we intend to focus on a single object. Concentrative, object-based meditation techniques such as FA meditation can further be conceptualized as mental training to cultivate the faculty of absorption (Ott, 2003). Absorption reflects a person’s ability to fully engage his or her attention in an experience (Wenk-Sormaz, 2005), and can be seen as an accumulation of focused attention or attentional control (Grant et al., 2013). It is associated with openness to new emotional and cognitive experiences (Tellegen and Atkinson, 1974), leading to an increased ability to concentrate especially on inward experience (Pekala et al., 1985). Whenever the mind wanders or attention is drawn to another object, the meditator is supposed to redirect attention to the original target object. FA meditation is especially interesting because the cultivation of monitoring skills is necessary for many of the meditation types (Lutz et al., 2008) and particularly important for better monitoring of mind-wandering dynamics (Hasenkamp et al., 2012). The attentional and monitoring faculties cultivated in FA are related to dissociable systems in the brain involved in conflict monitoring, selective and sustained attention (Manna et al., 2010). Examples of focus-attention meditation are Zazen (zen) meditation (the concentration element), mantra meditation, yantra and candle gazing, and breath meditations, where the practitioner keeps their attention focused on their breath moving in and out of their body. Mantra meditation practices generally focus on the recitation of a mantra, which is traditionally a word or phrase assigned to them by their meditation teacher. Mantras are often derived from Sanskrit root words and syllables, whose resonance is thought to induce stability of the mind without the need for an overly intense focus (Acharya, 2003). Practitioner chosen mantras in Western studies have also been used (Bormann et al., 2014). In the Himalayan Yoga meditation tradition, meditators mentally repeated their Mantra (spoken aloud or silently in one’s head) with or without awareness of the breath and when deeper levels of meditation or stillness are obtained, mantra repetitions gradually cease (Braboszcz and Delorme, 2011; Brandmeyer and Delorme, 2016). While mantra meditation is often categorized as a style of focused meditation, Travis suggests that the repetition of a sound, word, or sentence renders mantra meditation unique in that there is voluntary linguistic, verbal-motor production, rather than naturally arising body sensations (like the breath) or external physical objects (such as a point in space upon which the gaze is focused) (Travis, 2014). Accumulating research suggests that the neural correlates of mantra meditation differ from other related forms of focused attention practice perhaps as a result of subvocalization or other unique characteristics to imagining a word or phrase (e.g., Davanger et al., 2010; Fox et al., 2016; Lazar et al., 2000; Shimomura et al., 2008; Tomasino et al., 2013). However, further research is needed to clarify this distinction.

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Open monitoring meditation (OM) is a meditation where monitoring skills are transformed to a state of reflexive awareness with a broad scope of attention without focusing on one specific object (Lutz et al., 2008, 2015). Open monitoring meditation also focuses on the cultivation of meta-awareness, but they do not involve selecting a specific object to orient one’s attention to. Meta-awareness or metacognition refers to the increased awareness of the ongoing physical and self-referential processes (Flavell, 1979). In these meditation practices, meditators attempt to expand their attentional scope to incorporate the flow of perceptions, thoughts, emotional content, and/or subjective awareness (Dahl et al., 2015; Lutz et al., 2008; Manna et al., 2010). Vipassana meditation is an example of open monitoring meditation, as well as the Shikantaza (just sitting) in the Soto Zen School and introspective elements of Zazen meditation. Non-dual meditation practices revolve around the concept of nonduality, which refers to the “non-dual, or non-two” understanding of reality. These practices include “object-oriented insight,” “subject-oriented insight,” and “non-dual-oriented insight” forms of meditation (Dahl et al., 2015; Josipovic, 2013) which have their origins in the Vedic, Hindu, Buddhist, and Tibetan Buddhist traditions. These practices are thought to reduce one’s sense of attachment or control removing the separation between the observer and the observed in order to achieve experiential insight into the true nature consciousness and to connect with a more unified reality underlying our daily experiences (Josipovic, 2013, 2014). Loving kindness and compassion meditation (LKM) practices primarily involve the generation and cultivation of compassion, traditionally using various mental imagery techniques, and is thought to shift self-referential cognitive, behavioral and affective patterns, toward tendencies and thoughts that involve the well-being of others (Dahl et al., 2015; Kang et al., 2014). Whereas concentration and attentional forms of meditation emphasize the ongoing monitoring of mental content and placement of attention, constructive compassion meditation-based practices aim at directly manipulating the content of thoughts and emotions (Dahl et al., 2015; Salzberg, 2011). Non-dual traditions express that love and compassion are innate aspects of one’s being and are already present within the practitioner (Josipovic, 2016). Automatic self-transcendence meditation or transcendental meditation practices are said to allow the individual to transcend through a process of appreciating mantras at finer levels. The mantra becomes increasingly secondary inexperience, ultimately disappearing and allowing self-awareness to become the primary consciousness (Travis, 2014; Travis and Shear, 2010; Yogi and Tompkins, 1966). While some may argue this classification is the same as mantra or focused awareness, Travis and Parim have argued that it is a distinct category than mantra or focused attention meditation (Travis and Parim, 2017). Yogi describes transcending as turning one’s attention inwards toward subtler levels of thought, until the mind transcends the experience of the subtlest state and becomes completely still, at rest, yet fully awake and called this transcended state “pure consciousness” or “transcendence” (Yogi and Tompkins, 1966). In this description of transcendence, there is no customary content of experience such as thoughts, feelings or perceptions, but instead a self-referral consciousness. Self-referral consciousness is conscious of itself alone, where by the mind is identified with the greater creative intelligence (Travis and Parim, 2017; Travis and Shear, 2010).

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4 Phenomenology What is the subjective qualitative experience of people who meditate and does this experience differ by person and between traditions? Phenomenology in a broad sense can be understood as a discipline that characterizes phenomenal invariants of the lived first-person experiences of attention, emotion, action, memory, perception, mental imagery, empathy, self-consciousness, contemplative states, dreaming, and so forth (Lutz and Thompson, 2003). There is an accumulating body of literature and research pertaining to the phenomenological experience of meditation (e.g., Louchakova-Schwartz, 2013). In addition, there are an increasing number of cognitive scientists who acknowledge the necessity of systematic methods for collecting detailed introspective phenomenological reports when studying states of awareness, such as those during meditation, as well the for scientists interested in identifying a brain basis of consciousness (Dehaene and Naccache, 2001; Jack and Roepstorff, 2002; Jack and Shallice, 2001; Lutz et al., 2002). Meditation practices are known to facilitate “altered states of consciousness” which include phenomenological characteristics such as a joint alteration in the sense of time, space, and body representation (Berkovich-Ohana et al., 2013). Pioneer meditation teacher Jack Kornfield conducted study of meditators during a 3-month Vipassana retreat where he questioned the practitioners about “unusual” experiences yielded reports uncommon in the research literature, including strong negative emotions, involuntary movements, anomalous somatic sensations, and out-of-body experiences (Kornfield, 1979). Along these lines, research by Berkovich-Ohana and Glicksohn (2017) found that meditators score higher on a Mystical Scale than comparable controls, and found some support for their hypothesis that advanced practitioners would display reductions on both positive and negative affect (Berkovich-Ohana and Glicksohn, 2017). Przyrembel and colleagues investigated differences in phenomenological experiences across meditation styles through the implementation of psycholinguistic analysis, quantitative ratings and qualitative explorations. They found that breath meditations were described with the most body-related vocabulary, notably of sensations in nose and abdomen. Observing-thought meditation contained cognition-related vocabulary, with sensations focused in the head and face. Furthermore, loving kind meditations contained vocabulary related to socio-affective processes, with physical sensations concentrated around the heart, and with the feeling of warmth (Przyrembel and Singer, 2018). In a study which used a novel interpretative phenomenological analysis to study the experiences of participants taking part in secularized intervention that adheres to a more traditional Buddhist approach called meditation awareness training (MAT) found that participants with issues of stress and low mood reported significant improvements in psychological well-being (Shonin et al., 2014). In line with these findings, a study by Kok and Singer found that loving-kindness meditation led to the most significant increase in feelings of warmth and positive thoughts about others, whereas observing-thought meditation led to the greatest increase in metacognitive awareness (Kok and Singer, 2017).

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These findings suggest that specific meditation practices are characterized by distinct phenomenological experiences, and this holds important implications for the application of meditative practices in specific populations within the context of clinical and behavioral interventions. There is a large body of findings highlighting the positive physical and mental health effects of meditation, one study asked active meditators to “recount their involvement with meditation,” and received both positive and negative reports. Meditators reported “exacerbation of psychological problems,” including anxiety and depression, “troubling experiences of self,” and “reality being challenged,” which included out-of-body experiences and in one case resulted in patient hospitalization for psychosis (Lomas et al., 2014). In another study, meditator interviews asked questions about the cognitive, perceptual, affective, somatic, sense of self, and social aspects of meditation and found different interpretations of and responses to the similar phenomenological experiences. The responses ranged in valence from very positive to very negative, and the associated level of distress and functional impairment from minimal and transient, to severe and enduring (Lindahl et al., 2017). Additionally, they reported findings suggesting that across clinical, experimental, and qualitative research on meditation, the degree to which adverse meditation experiences are reported is directly proportional to how specifically they are queried (Lindahl et al., 2017). While the integration of such first-person data into the experimental protocols of cognitive neuroscience still faces a number of epistemological and methodological challenges, identifying a broader range of experiences associated with meditation is necessary. Factors that contribute to the presence and management of experiences reported as challenging, difficult, distressing or functionally impairing will help to advance our understanding of various contemplative practices, and provide valuable resources for teachers, practitioners and scientists. Researchers asking for subjective reports of participants mental states and experiences on a moment to moment basis may help prevent retrospective biasing of responses in self-report measures conducted after the experience of interest. Additionally, repeated measure designs may help identify patterns in phenomenological experiences (Bengtsson, 2016; Kok and Singer, 2017).

5 Structural and functional correlates of meditation practices Basic sciences research has identified some of the neurological and physiological correlates of meditation practices leading to an improved understanding of the mechanisms by which emotional, cognitive and psychosocial factors can influence well-being and health-related outcomes. Scientific interest in the neurophysiological bases of meditation has in large part come from our understanding of neuroplasticity and various forms of experience-induced changes that occur in the brain (Lutz et al., 2007). Contemplative Science research has shown that through the active

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and intentional shaping of our brains (neuroplasticity), we can promote and cultivate well-being. The regular practice of meditation is associated with relatively reduced activity in the default mode network an important network of the brain implicated in attention and emotion regulation specifically self-related thinking and mindwandering when compared to rest and active task conditions (Garrison et al., 2015) as well increased cortical thickness in areas such as the prefrontal cortices and insula (Fox et al., 2014, 2016; H€olzel et al., 2011a; Lazar et al., 2005). Lazar and colleagues were the first to show that the prefrontal cortex and right anterior insula, regions associated with attention, interception and sensory processing were thicker in experienced meditation participants than in matched controls. They also found that the between-group differences in prefrontal cortical thickness were most pronounced in older participants suggesting that meditation may slow age-related cortical thinning, and that the thickness of these two specific areas also correlated with meditation experience. Lazar and her colleagues provided some of the first structural evidence for experience-dependent cortical plasticity associated with meditation practice (Lazar et al., 2005). Kang et al. conducted a whole-brain cortical thickness analysis based on magnetic resonance imaging, and diffusion tensor imaging to quantify white matter integrity in the brains of 46 experienced meditators compared with 46 matched meditation-naı¨ve volunteers. They found significantly increased cortical thickness in the anterior regions of the brain, located in frontal and temporal areas, including the medial prefrontal cortex, superior frontal cortex, temporal pole and the middle and inferior temporal cortices in meditators as compared to controls. They additionally found that meditators had both higher fractional anisotropy values and greater cortical thickness in the region adjacent to the medial prefrontal cortex, suggesting structural changes in both gray and white matter (Kang et al., 2012). These findings demonstrate that meditation can indeed induce neuroplasticity and in the Lazar study’s case in a very short amount of time as the mindfulness intervention was only 8 weeks long. These results are robust and have been reproduced (H€ olzel et al., 2011a). Results from study of epigenetics and functional genomics have elucidated some of the processes involved in the mind-body connection and how these can influence health outcomes. For example, recent findings have shown that short-term exposure to stress, diet and physical exercise can cause changes that are detectable in human peripheral tissues (Kaliman et al., 2011; Pham and Lee, 2012). In a study by Buchanan and colleagues, elevated cortisol levels were found in individuals who scored high on empathy measures after observing stressful experiences in others, whereas observing stressful experiences in others while generating compassion was linked to reductions in cortisol levels (Buchanan et al., 2012; Cosley et al., 2010). These findings suggest that emotional qualities such as compassion and empathy can directly interact with the peripheral nervous system. Kaliman and colleagues explored the impact of intensive mindfulness meditation for a day in experienced meditation practitioners on the expression of circadian, chromatin modulatory and inflammatory genes in peripheral blood mononuclear cells (PBMCs) and found a reduced expression of histone deacetylase genes (genes which play an important role in the regulation of gene expression) and a decreased expression of pro-inflammatory genes

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in meditators compared with controls. They suggest that the regulation of these genes and inflammatory pathways may represent some of the mechanisms underlying the therapeutic potential of mindfulness-based interventions (Chaix et al., 2017; Kaliman et al., 2014; Muehsam et al., 2017). Research investigating the effects of compassion training has found links between the duration of compassion training in years and inflammatory biomarkers, with an increased duration of compassion training leading to decreased levels of C-reactive protein and interleukin 6, both of which are biomarkers used to predict vascular risk (Pace et al., 2013). Jacobs and colleagues investigated the effects of a 3-month meditation retreat on changes in telomerase activity, which is considered to be a reliable predictor of long-term cellular viability (Epel et al., 2004; Jacobs et al., 2011). Increases in perceived control and decreases in negative affect (which are central features targeted by the meditation practice) were correlated with increases in telomerase activity, telomere length and immune cell longevity (Jacobs et al., 2011). These findings suggest that through various meditation practices we can change the way our minds and bodies react to stressful events in the environment, and that these changes directly impact our peripheral biology. Consistent with this hypothesis, awareness of visceral and internal psychological states, including heart rate and respiration is often referred to as interoception and has been consistently linked to activity in the insula (Craig and Craig, 2009; Critchley et al., 2004) in addition to metacognitive awareness (Fleming and Dolan, 2012) and emotional self-awareness (Craig, 2004). Multiple neuroimaging studies have evaluated changes in the brain during meditation in the short-term and long-term changes from meditation. Meta-analyses have synthesized the many studies conducted to date. When comparing meditators during meditation versus non-meditation, we find that brain areas focused on selfregulation, focused problem-solving, adaptive behavior, interoception, monitoring body states, reorienting attention, and processing self-relevant information (Boccia et al., 2015). Researchers found similar functional changes over the long-term with brain areas affecting self-referential processes, perspective-taking, cognitive distancing, sustained attention, memory formation, and high-level perception— especially in perceiving complex and ambiguous visual stimuli being more active in meditators versus non-meditators (Boccia et al., 2015). Another systematic review of 21 neuroimaging studies (n ¼  300 meditators; Fox et al., 2014) found eight brain regions consistently altered in meditators: meta-awareness (frontopolar cortex/BA 10); exteroceptive and interoceptive body awareness (sensory cortices and insula), memory consolidation and reconsolidation (hippocampus), self and emotion regulation (anterior and mid cingulate; orbitofrontal cortex), and intraand interhemispheric communication (superior longitudinal fasciculus; corpus callosum) (Fox et al., 2014). In a follow-up study a few years later, Fox et al. evaluated 78 studies (n ¼ 527; Fox et al., 2016) and found similar functional brain areas being activated during meditation: interoception, empathy, complex mental tasks, working memory, mental imagery, conceptual reasoning, regulation of attention and emotion, monitoring performance, meta-awareness, and meta-cognitive capacity. Interestingly, they then separated their results by meditation tradition.

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All meditation types had activations in the insula (interoception, empathy, metacognition), pre/supplementary motor cortices (complex mental tasks, working memory, attentional control, mental imagery, conceptual reasoning), dorsal anterior cingulate cortex (regulation of attention and emotion, as well as monitor performance), and the frontopolar cortex (meta-awareness and meta-cognitive capacity). These areas align with the goals of these meditations and the subjective experiences as well. Focused attention meditations have shown activations in brain areas for cognitive control that require monitoring performance, voluntary regulation of attention and behavior, consistent with largely effortful, sustained attention with a range of regulation demands and deactivations in mind-wandering, episodic memory retrieval, simulation of future events, and conceptual semantic processing. Mantra Recitation has shown activations in brain areas of the motor control network, including Broca’s area, premotor and supplementary motor cortices, putamen within the basal ganglia, and consistent with internally generating and staying focused on a phrase within one’s mind (or recited out loud) and decreased processing of external sensory inputs (somatosensory) and the primary auditory cortex. Open Monitoring meditation has activations in brain areas for voluntary regulation of thought and action, interoceptive processing (insula), cognitive control (coordinating, monitoring attention to both internal and external channels of information) and deactivations in sensory gating (right thalamus) and no blocking of sensory information. Loving-Kindness Compassion meditations show activations in brain areas of somatosensory processing, creating a unified sense of the body, empathy and theory of mind (mentalizing), perceptions of pain and no deactivations. This comparative analysis highlights that while meditation in general shares common characteristics, individual meditation traditions have commonalities but are also marked with unique characteristics that affect the practitioner in different ways (Fox et al., 2016).

6 Oscillatory correlates of meditation While EEG has been a key methodology in the neuroscientific study meditation, no clear consensus has emerged pertaining the generalizable effects of meditation on EEG activity. This is likely due to the phenomenological differences associated with differences in meditation practices and suggests that various meditative states (those that involve focus on an object and those that are objectless), as well as meditation traits, may be associated with very different specific oscillatory signatures (Cahn and Polich, 2006). A number of reports have suggested that increased theta (4–8 Hz) may be a specific state effect of long-term meditation practice (Aftanas and Golocheikine, 2001, 2002; Anand et al., 1961; Banquet, 1973; Brandmeyer and Delorme, 2016; Corby et al., 1978; Elson et al., 1977; Fenwick et al., 1977; Pagano and Warrenburg, 1983; Travis et al., 2002). A majority of EEG studies report both state and trait bidirectional changes of power of lower frequencies bands, such as theta and alpha; however studies directly assessing the EEG correlates of different practices

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are limited (Braboszcz et al., 2017; Cahn and Polich, 2006). Some studies of yogic meditative practice found increases in alpha and theta to be associated with proficiency in meditative technique (Aftanas and Golocheikine, 2001; Corby et al., 1978; Elson et al., 1977; Kasamatsu and Hirai, 1966) and early investigations with Zen meditation indicate frontal theta increases to be characteristic of only the more advanced practitioners (Kasamatsu and Hirai, 1966). While increased frontal midline theta has been observed during focused attention meditations (Aftanas and Golocheikine, 2002; Brandmeyer and Delorme, 2016; Hebert and Lehmann, 1977; Kubota et al., 2001), similar frontal midline activations occur throughout nonmeditation-related studies of sustained attention and memory (Cavanagh and Frank, 2014; Lisman and Jensen, 2013; Scheeringa et al., 2009). In the early 1970s, some of the first biofeedback studies discovered that global increases in alpha activity seem to correlate with reductions in anxiety, and increased feelings of calm and positive affect (Brown, 1970; Hardt and Kamiya, 1978; Kamiya, 1969). Following the discovery that alpha rhythm modulation is correlated with sensory filtering during body-sensation focused attention, Kerr et al. found that subjects trained in mindfulness showed enhanced top-down modulation of a localized alpha rhythm in somatosensory cortices. Increased intra- and interhemispheric alpha–theta range coherence has also been observed during meditation (Aftanas and Golocheikine, 2001, 2002; Anand et al., 1961; Banquet, 1973; Farrow and Hebert, 1982; Gaylord et al., 1989; Hebert and Tan, 2004; Kerr et al., 2013; Pagano and Warrenburg, 1983; Travis and Wallace, 1999), while similar effects were found in long-term meditators at rest or while engaged in cognitive tasks (Dillbeck and Vesely, 1986; Hebert and Tan, 2004; Orme-Johnson and Haynes, 1981). In a study using magnetoencephalography (MEG) recording of the somatosensory finger representation, Kerr et al. found that experienced meditators showed an enhanced alpha power modulation in response to a cue, potentially reflecting an enhanced filtering of inputs to primary sensory cortex. They also found that experienced meditators demonstrated modified alpha rhythm properties and an increase in non-localized tonic alpha power when compared to controls (Kerr et al., 2011). These findings can most likely be attributed to the emphasis on somatic attention training in mindfulness meditation techniques in which individuals train to develop metacognition, a process in which one directs their attention, moment-bymoment, to an overall somatosensory awareness of physical sensations, feelings and thoughts (Cahn and Polich, 2006; Farb et al., 2012). Whitmarsh et al. investigated participants metacognitive ability to report on their attentional focus and found that contralateral somatosensory alpha depression correlated with higher reported attentional focus on either their left or right hand, respectively (Whitmarsh et al., 2014). Baird et al. found that a 2-week meditation program leads to significantly enhanced metacognitive ability for memory, but not for perceptual decisions, suggesting that while meditation training can enhance certain elements of introspective acuity, such improvements may not translate equally to all cognitive domains (Baird et al., 2014). Enhanced body awareness was also found to be associated with greater subjective

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emotional experience and awareness of the heart during exposure to emotionally provocative stimuli in Vipassana meditators, when compared to expert dancers, and controls (Sze et al., 2010). Given that top-down attentional modulations of cortical excitability have been repeatedly shown to result in better discrimination and performance accuracy, the aforementioned findings provide support for both the enhancement of metacognitive accuracy via the direct monitoring of current mental states resulting from long-term meditation practice, and for potential changes in the supporting neural structures underlying sustained attention processes. Along with changes in low frequency bands, recent research findings point to the presence of higher frequency gamma activation (>30 Hz) specifically associated with both meditation state and trait effects across various meditation practices (Berkovich-Ohana et al., 2012; Braboszcz et al., 2017; Cahn and Polich, 2009; Ferrarelli et al., 2013; Lutz and Thompson, 2003). Accumulating research suggests that the EEG gamma frequency has been associated with a wide array of cognitive functions, and has been proposed as a potential neural correlate of consciousness (NCC; Gaillard et al., 2009; Varela, 2001) corresponding with interesting findings of a direct link between increases in gamma power and increases in the BOLD signal (Conner et al., 2011; Logothetis et al., 2001). While the findings surrounding gamma remain controversial due to potential role of eye (Yuval-Greenberg and Deouell, 2009), temporal, facial, and scalp muscle contamination in high frequency EEG activity (Buzsa´ki and Wang, 2012; Shackman et al., 2009), prominent neuroscientists have proposed that gamma activity facilitates the neural mechanisms underlying attention (Landau et al., 2007; Tallon-Baudry et al., 2004), long-range neuronal communication (Fries, 2005; Salinas and Sejnowski, 2001), and visual representation (Jokisch and Jensen, 2007; Lachaux et al., 2005). Braboszc and colleagues compared practitioners of three different meditation traditions (Vipassana, Himalayan Yoga and Isha Shoonya) with a control group during a meditative and instructed mind-wandering block and found that all meditators showed higher parieto-occipital 60–110 Hz gamma amplitude than control subjects as a trait effect observed during meditation and when considering meditation and instructed mind-wandering periods together. Moreover, this gamma power was positively correlated with participants meditation experience. Additionally, they controlled for the potential contamination of muscle artifact and studied artifact activity in different experimental conditions using independent component analysis (Braboszcz et al., 2017; Delorme and Makeig, 2004; Delorme et al., 2007). Cahn et al. found that the cross-experimental session occipital gamma power was significantly larger in meditators with more than 10 years of daily practice, and that the meditation-related gamma power increase was similarly the strongest in such advanced practitioners (Cahn et al., 2010). These findings suggest that long-term Vipassana meditation contributes to increased parieto-occipital gamma power related to long-term meditational expertise and enhanced sensory awareness. In a separate study, long-term Tibetan Nyingmapa and Kagyupa Buddhist practitioners were able to self-induce sustained high-amplitude gamma-band (25–42 Hz) oscillations and phase-synchrony, most notably over the lateral frontoparietal electrodes

ARTICLE IN PRESS 7 Mechanisms underlying meditation and attention regulation

during a period of meditation (Lutz et al., 2004). Hauswald et al. found that scores on a mindfulness scale in Zen meditation practitioners correlate with gamma power during meditation at frequencies above 100 Hz. Additional research has shown that during states referred to as fruition, a known stage within the Mahasi School of Theravada Buddhism in which meditation practitioners experience a culmination of contemplation-induced stages of consciousness, global long-range gamma (25–45 Hz) synchronization was found, when compared to the EEG recorded during the meditation not in fruition states. The authors suggest that long-range global gamma synchronization may facilitate the underlying mechanism for the deconditioning of habitual mental patterns, which may serve as the underpinning for the neural correlate of what some Buddhist traditions refer to as enlightenment or liberation (Berkovich-Ohana, 2017; Hauswald et al., 2015). In a study by Lutz et al. long-distance phase-synchronized gamma-band oscillations were observed when meditators practiced a non-referential form of compassion meditation when compared to a control group. The authors emphasize in their article that according to the first-person accounts of “objectless meditation,” the methods and states that occur during this meditation differ radically from those of concentration meditation, lacking specific objects and with the focus on the cultivation of a particular state of being. Given the large amplitude of the gamma oscillations in Lutz et al., the authors conclude that the size and scale of the oscillating neural population reflected the activity of widely distributed neural assemblies that were synchronized with a high temporal precision (Lutz et al., 2004). While this interpretation would require that the oscillations posses the same phase, phase coherence was not specifically explored in the study. Differences between the control and the meditation populations during the resting state before meditation were also observed, suggesting that the differences between neural activity during formal seated meditation practice and everyday life is reduced in advanced practitioners and that the resting state of the brain may be altered by long-term meditative practice. Similarly, increased gamma activity across parieto-occipital electrodes during periods of NREM sleep is positively correlated with the length of lifetime meditation practice (Ferrarelli et al., 2013).

7 Mechanisms underlying meditation and attention regulation One of the key findings from contemplative neuroscience research relates to its mediating role on neural mechanisms underlying top-down feedback mechanisms involved in attention regulation and sensory perception. According to the neurocognitive model developed by Posner and Petersen (1990), attention can be divided into three different anatomically and functionally distinct networks that implement the functions of alerting (which refer to the anticipatory preparation for an incoming stimulus), orienting (the directing of attention to a specific stimulus), and conflict monitoring and executive attention (resolving conflict between competing neural activity) (Posner and Petersen, 1990; Posner et al., 2007). Additional distinctions

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between different forms of attention refer to combinations of these three components (Posner and Petersen, 1990). For example, sustained attention refers to the sense of vigilance during long continued tasks and may involve both tonic alerting and orienting, whereas selective attention may involve either orienting (when a stimulus is present) or executive function (when stored information is involved; Desimone and Duncan, 1995). A study by Slagter and colleagues demonstrated that 3 months of focused meditation training resulted in a smaller attentional blink and reduced brain-resource allocation to the first target (T1), demonstrated by a significantly smaller T1-elicited P3b, a neural index of resource allocation after training (Slagter et al., 2007). Subjects with the largest decrease in cognitive resource allocation to T1 showed the largest reduction in the measured attentional-blink size, suggesting that the ability to accurately identify T2 depends upon the efficient deployment of cognitive resources to T1. They hypothesized that increases in phase-locking were induced via mental training and the subjects enhanced capacity to sustain task-related attentional focus, while reducing the tendency to engage in task-unrelated thoughts. These findings suggest that through meditation practices one can improve cognitive capacity, potentially via the self-regulation of lower level elements of neurogenesis (Vago and David, 2012), and demonstrate that mental training can result in increased control over the distribution of limited brain resources (Slagter et al., 2007). A considerable number of studies have associated the practice of mindfulness meditation practices with improvements in attention (Brefczynski-Lewis et al., 2007; Chan and Woollacott, 2007; Jha et al., 2007; Lutz et al., 2009; MacLean et al., 2010; Moore and Malinowski, 2009; Slagter et al., 2007; Valentine and Sweet, 1999; van den Hurk et al., 2010). For instance, in the studies by Moore and Malinowski (2009) and Chan and Woollacott (2007), reduced effects of distracting and conflicting information were found in the Stroop task. van den Hurk et al. (2010) found that mindfulness meditators showed reduced interference by distracting flankers during performance on the attention network test. These findings provide support for the notion that one of the cognitive mechanisms engaged during long term meditation practice may involve the flexible orienting of attention and subsequently, a reduction in the time needed to shift attention from one location to another (Hodgins and Adair, 2010; Jha et al., 2007; van den Hurk et al., 2010). Another study compared open monitoring meditation (OM), focused attention meditation (FA) and a relaxation group on performance on an emotional variant of the Attention Network Test (ANT) and found that OM and FA practice improved executive attention, with no change observed in the relaxation control group. Together, these findings suggest that mindfulness meditation targets the broader neural mechanisms and circuitry underlying the executive attention network, and provides a viable explanation for the benefits that have been observed in individuals with mood and anxiety disorders (Ainsworth et al., 2013). A number of structural and functional MRI studies on meditation training have investigated the neuroplasticity in brain regions supporting attention regulation. The anterior cingulate cortex (ACC) is an area in the brain that has been most consistently

ARTICLE IN PRESS 8 Mechanisms underlying meditation and emotion regulation

linked to the effects of mindfulness training on attention (H€olzel et al., 2007; Tang et al., 2010, 2012, 2013, 2015). However, other regions including the insula, temporo-parietal junction, fronto-limbic network, and other structures associated with the default mode network have been consistently identified with extensive meditation practice (Fox et al., 2012). The ACC and the fronto-insular cortex are thought to enable executive attention and control (Veen and Carter, 2002) by detecting the presence of conflicts emerging from incompatible streams of information processing, thus facilitating cognitive processing through long-range connections to other brain areas. These mechanisms may work synergistically by establishing a process of enhanced meta-awareness and self-regulation following long-term meditation practice (Fox et al., 2012; Tang et al., 2015).

8 Mechanisms underlying meditation and emotion regulation Well-being is a complex phenomenon related to a variety of factors, including cultural differences, socioeconomic status, health, the quality of interpersonal relations, and specific psychological processes (Dinero et al., 2008). Clinical research suggests that an ability to distance oneself and observe the ongoing internal train of thoughts plays a vital role in psychological well-being (Farb et al., 2007). Within the domain of cognitive psychology, latent conceptions of self underlie to a great extent our thoughts and emotions and directly impact brain functioning (Hoffman et al., 2012). One of the proposed primary mechanisms by which contemplative practices affect well-being is by targeting and altering maladaptive self-referential patterns of thought (Dahl et al., 2015). Additional research investigating the neural mechanisms underlying the regulation of emotion which have been directly linked to brain regions associated with cognitive control, including the dorsomedial, dorsolateral, and ventrolateral prefrontal cortex, as well as the posterior parietal cortex, provides support for this concept (Ochsner and Gross, 2004, 2005). Meditation and mindfulness may mediate emotion regulation by strengthening prefrontal cognitive control mechanisms via improved top-down regulation of the amygdala. Diminished activations in the amygdala in response to emotional stimuli have been observed in meditation practitioners (Tang et al., 2015). Another study examining the amygdala response to emotional pictures in long-term and short-term meditators found that amygdala reactivity was reduced when viewing emotional pictures, and that the connection between the amygdala and ventromedial pre-frontal cortex was strengthened (Kral et al., 2018). Furthermore, a longitudinal study found that the reduced right amygdala activity may be carried over from meditation into non-meditative states (Leung et al., 2018). Weng and colleagues (2013) found that participants who were trained in compassion-based meditation showed increased connectivity in response to emotionally provocative images between the dorsolateral prefrontal cortex, a region commonly linked to cognitive functions, such as reappraisal, and the nucleus accumbens, considered to be a key hub in the reward network associated with positive affect (Weng et al., 2013).

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Key factors involved in emotion regulation include reappraisal, exposure, extinction and reconsolidation (H€ olzel et al., 2011a), while additional findings suggest that mindfulness practice leads to increases in positive reappraisal. Research findings suggest that mindfulness practices facilitate “positive reappraisal,” with reappraisal functioning as an adaptive process through which stressful events are reconstructed as beneficial, meaningful, or benign (Hanley and Garland, 2014). There are notable similarities in the brain regions being influenced by mindfulness meditation and those involved in mediating fear extinction, namely the hippocampus, amygdala, medial PFC, and the ventromedial PFC (Goldin and Gross, 2010; H€olzel et al., 2007; Lazar et al., 2000; Lou et al., 1999; Luders et al., 2009; Newberg et al., 2001). During mindfulness meditation, one allows themselves be affected by the experience, while refraining from engaging in internal reactivity toward it, while cultivating acceptance to bodily and affective responses. This is supported by findings which suggest that meditation practice may help to facilitate enhanced awareness and reduced reactivity to the content of our ongoing internal dialogue (Hart, 1987; H€ olzel et al., 2011b). As an example, Wahbeh et al. conducted a mindfulness meditation study with combat veterans with posttraumatic stress disorder. The mindfulness meditation recipients showed no significant reductions in their posttraumatic stress disorder symptoms when compared with the active control group. However, they did find that mindfulness meditation recipients demonstrated a significant change in their relationship to their symptoms (i.e., their meta-awareness and selfregulation) such that they were not as easily triggered by events perceived as adverse (i.e., emotion regulation; Hart, 1987; H€olzel et al., 2011a,b; Wahbeh et al., 2016).

9 Future perspectives One of the major factors and potential confounds pertaining to research studying the neuroscientific and physiological effects of short- and long-term meditation practice remains the self-selection bias. Therefore, longitudinal studies that implement the random selection of individuals who engage in the meditative practice would be useful in delineating the complex interplay between initial baseline effects, state effects, and long-term training trait effects (Braboszcz et al., 2017). Additionally, there is a significant likelihood that individuals who choose to engage in meditation practice share common features, such as personality and lifestyle dispositions. These features hold the potential to significantly influence aspects of cognitive development, such as the long-term effects of living in monasteries on highly restrictive diets, along with meditation practitioners being more likely to have vegetarian or plant-based diets. They are also likely to have significant differences from a non-monastic individual in terms factors such as physical exercise, and sleep patterns (Britton et al., 2014) which may directly influence brain structure and functions (Fox et al., 2016). The use of randomized, longitudinal designs with active control groups would allow to control for the potentially confounding effects of nonmeditation-specific qualities of the lifestyle associated with contemplative practices.

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It is especially important for researchers involved in both fundamental and clinical research studies to remain cautious regarding the degree to which respective research findings are translational and generalizable to clinical practice (Goyal et al., 2014; Van Dam et al., 2018). The translation of laboratory findings into future clinical practice must also depend on the replicability and potential practical relevance of a given finding. Another component that has not been well-studied is the evaluation of meditation efficacy or competence. Is there a way to evaluate how well someone is meditating beyond their lifetime practice hours or daily practice time? Some efforts have been made to develop EEG, respiration, and ERP models by which to assess meditation competence (Ahani et al., 2014; Atchley et al., 2016). And last, the secular definitions of “mindfulness” are still in need of further clarification. Nuanced terminology and clear and detailed neurophenomenological methodologies for studying to the various distinct mental and physical states and traits of contemplative practice will help to advance the key transnational aspects of the field.

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Further reading Davidson, R.J., Lutz, A., 2008. Buddha’s brain: neuroplasticity and meditation [in the spotlight]. IEEE Signal Process. Mag. 25, 174–176.

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