The Buddha s Extra Scoop: Neural Correlates of Mindfulness and Clinical Sport Psychology

Journal of Clinical Sport Psychology, 2008, 2, 216-241 2008 Human Kinetics, Inc. The Buddha s Extra Scoop: Neural Correlates of Mindfulness and Clinical Sport Psychology Donald R. Marks La Salle University Recent studies using neuroimaging technologies offer evidence that ancient beliefs about the benefits (e.g., enhanced attention, increased distress tolerance) associated with mindfulness practice and other forms of meditation may be supported by identifiable neuroanatomical changes in the brain. Although it is too early to make probative statements regarding exactly how and why contemplative practices affect the structure and activity of the brain, sport psychologists may want to consider the potential implications of the findings that have begun to emerge from this neural correlates research. The goal of this article is to (a) review the findings from the principal studies of contemplative practice that have employed measures of neuronal activity (e.g., fmri, EEG) and (b) examine the potential relevance of these studies to the treatment of psychological disorders among athletes and the enhancement of athletic performance. Keywords: meditation, contemplative science, performance, athletes, neuroimaging Over the centuries, meditation practitioners have often wondered whether the Buddha s prominent ushnisha the symbolic protuberance atop his head, often represented as a topknot contained an extra scoop of gray matter (Austin, 1998). Only access to additional cognitive processing power, they reasoned, could explain the sheer insight, patience, good humor, and affection that they found in Buddhist texts and practices. Like many folk beliefs, this one may contain an important kernel of truth. Recent research has discovered that, in addition to reducing pain perception and relieving psychological distress, mindfulness and related meditation practices contribute to increased tissue volume in specific areas of the brain (Lazar et al., 2000; Pagnoni & Cekic, 2007). In addition, mindfulness meditation has also been associated with enhanced activation in brain regions involved in attention, perception, memory, and empathy, suggesting that it may, in fact, contribute to higher levels of psychosocial functioning. Western athletes, coaches, and sport psychologists have had an ambivalent relationship with mindfulness and other forms of meditation since the awakening of Donald R. Marks is with the Department of Psychology at La Salle University in Philadelphia. E-mail: marksd1@lasalle.edu. 216

Neural Correlates of Mindfulness 217 interest in Zen Buddhism and other Eastern practices in the 1950s. While there may be few archers and probably few professional golfers who have never heard of Eugene Herrigel s Zen and the Art of Archery (1953), the percentage of those who have read the book and used its techniques is undoubtedly much smaller. Indeed, the tendency in the West to parody Zen or other mystical approaches ( be the ball ) often precedes attempts to overcome an obstacle or reach a new training plateau through brute force and control. Phil Jackson s (Jackson & Delehanty, 1995) cultivation of mindful awareness over mindless aggression remains the exception rather than the rule. Yet a mounting body of evidence from studies using electroencephalography (EEG) and, more recently, neuroimaging technologies such as functional magnetic resonance imaging (fmri), indicates that mindfulness meditation and other forms of contemplative practice offer more than just a better mindset. They have surprising, and potentially profound, effects on neural functioning, including the electrical activity patterns of the brain, and on neuroanatomy, including the activity (and even the relative size) of specific brain regions. In fact, studies of neural activity during contemplative practice reveal evidence that ancient beliefs regarding the beneficial effects of meditation (e.g., strengthening attention, increasing distress tolerance, fostering empathy) are supported by identifiable changes in the cortical areas associated with these functions. To date, research regarding neural correlates of meditation has examined (a) a range of contemplative practices, including Zen, vipassana, Tibetan, and Vedic meditation techniques as well as the Christian practice of centering prayer (see Cahn & Polich, 2006); (b) differences between novice and experienced meditators; (c) differences between individuals with high and low levels of dispositional mindfulness as measured by self-report; and (d) differences between individuals who undergo brief mindfulness training in the course of medical interventions or psychological treatment and those who do not. There have been, it should be noted, no randomized controlled trials of mindfulness that have used neural correlates as an outcome measure. Moreover, it is still too early in the process of evaluating neural correlates to make probative statements regarding how and why contemplative practices affect the structure and activity of the brain in the manner that they do. Yet sport psychologists and other professionals involved in athletes physical and mental training may want consider the potential implications of these findings. The goal of this paper is twofold: (a) to review the most influential studies of contemplative practice that have assessed outcomes through measurement of specific neurological correlates and (b) to examine the potential relevance of these studies to clinical sport psychology, including the insight they provide into the enhancement of athletic performance, treatment of psychological disorders among athletes, and other issues across the multilevel classification system for sport psychology (MCS-SP; Gardner & Moore, 2004b, 2006). What Is Being Studied? Although most mindfulness tasks appear quite simple (e.g., attending to one s breathing, focusing the attention on a single object), the psychological and physiological processes that underlie these functions are quite complex (see Newberg & Iverson, 2003). Before evaluating the fmri and EEG data regarding mindfulness and related forms of contemplative practice, it is useful to look carefully at the

218 Marks phenomena under study, including both the nature of the contemplative tasks these studies use and the theoretical framework in which neural correlates or activity occurring in specific neuroanatomical regions during performance of a given set of processes are understood. Mindfulness and Related Contemplative Practices Building upon Goleman s (1988) initial efforts to categorize the various types of meditative experience, reviews of contemplative practices and interventions (Cahn & Polich, 2006; Dunn, Hartigan, & Miklaus, 1999) have attempted to make distinctions between concentration and mindfulness practices. Concentration practices are said to include those designed to focus the attention on a single stimulus or group of stimuli, such as the breath or the sounds one can hear in the room at the moment. Transcendental meditation and forms of Kundalini yoga, which involve efforts to maintain attention on a specific mantra, could also serve as examples of concentration practices. Mindfulness practices, by contrast, are designed to cultivate an undifferentiated, receptive form of attention one that involves awareness of all stimuli within a curious, if diffuse, state of mind. Yet even the authors who have proposed this recognize that concentration and mindfulness or, put another way, the narrow and dispersed focusing of attention each involve degrees of both concentrated attention and receptivity to new information. In fact, such efforts to distinguish between concentration and mindfulness practices are likely to prove unproductive. It should be noted also, as Rosch (2007) observed, that mindfulness and related practices may be inherently heterogeneous in nature, involving multiple tasks and systems. Moreover, they are typically conducted within the context of larger intervention packages and frameworks, making it difficult to isolate and ascribe unique effects to a particular aspect of a mindfulness practice. An alternative way to think about the contemplative practices that neuroscience research has examined would be to employ a broader, more encompassing definition that comprises both their concentrative and receptive aspects. Kabat-Zinn s (1994) description of mindfulness as a form of contemplation that involves paying attention in a particular way: on purpose, nonjudgmentally, and in the present moment (p. 4) offers a useful starting point. Though it is not an operational definition, it effectively applies to a range of contemplative techniques and emphasizes the functional domains of awareness and acceptance. In keeping with Kabat-Zinn s approach, Bishop and colleagues (2004) have presented a two-component model of mindfulness practice, which includes (a) the self-regulation of attention so that it is maintained on immediate experience, thereby allowing for increased recognition of mental events in the present moment and (b) the adoption of a particular orientation toward one s experiences in the present moment, an orientation that is characterized by curiosity, openness, and acceptance (p. 232). Dimidjian and Linehan (2002) also offer a similar framework for understanding mindfulness, contending that it consists of a what and a how dimension. The what dimension includes three components: (a) observing what one experiences, (b) describing the experience, and (c) participating fully in the experience. The how dimension, which also features three elements, pertains to the manner in which the what dimension is carried out: (a) nonjudgmentally with acceptance, (b) in the present moment, and (c) effectively.

Neural Correlates of Mindfulness 219 Drawing upon these and other attempts to operationalize mindfulness and related practices, numerous self-report measures have been developed to assess the degree to which individuals believe they engage in these behaviors (Block- Lerner, Salters-Pedneault, & Tull, 2005). Baer and colleagues (2006) conducted a factor analytical study of several of these measures and five facets of trait or dispositional mindfulness emerged: (a) observing, (b) describing, (c) accepting without judging, (d) acting with awareness, and (e) nonreactivity. These five facets, though challenging to operationalize in adequate ways for study, capture several of the elements to which Kabat-Zinn s more impressionistic definition points. They also underscore the inadequacy of efforts to distinguish between concentration and mindfulness-oriented contemplative practices. Clearly, mindfulness and related contemplative practices require concentration of attention, which is necessary for observation, description, and acting with awareness as well as receptivity, which is a prerequisite for accepting without judging and nonreactivity. One can concentrate on a narrow object of focus while minimizing reactivity to distractions or one can open receptively to awareness while minimizing reactivity to individual phenomena. In either case, heightened attentional efficiency is a potential result. As Gardner and Moore (2004a, 2006, 2007) have observed, mindfulness practice promotes greater awareness of internal experiences and defusion of one s thoughts, emotions, and bodily sensations as realities to which one must respond (2007, p. 34). In other words, it is a training of the attention that enables attuned awareness to one s internal and external context, while strengthening one s ability to observe without responding. Indeed, as Bishop et al. (2004) have explained, it is possible to define the practice of mindfulness in purely attentional terms. In this model, mindfulness involves (a) sustained attention the maintenance of awareness on present-moment experience, whether that be broadly or narrowly defined; (b) attention switching bringing the attention back to the present moment when it wanders; (c) inhibition of elaborative processing suspension of rumination on thoughts or feelings regarding events outside the present moment; and (d) nondirected attention use of curiosity and openness to enhance awareness of present experience, unfiltered by assumptions or expectations. In sum, mindfulness and practices that are closely related to it (e.g., Zen meditation, vipassana practice, Transcendental Meditation, centering prayer, etc.) are believed to involve heightened attention to one s experiences, including private events such as thoughts and emotions, as well as the inhibition of persistent attending to particular cognitions or emotions. Moreover, as a result of this attentional training, it is possible for the contemplative practitioner to develop enhanced self-regulation skills. Because contextual stimuli are perceived more readily and more accurately, reactions to them can be made deliberately rather than impulsively. In addition, the same processes of attentional deployment can be applied to internal experience, including cognitions and emotions, as to external phenomena. In this way, the practitioner can adopt an open, nonreactive approach that allows experience and processing of thoughts and emotions without necessitating an immediate response. Neural Correlates Research Until recently, what has been most intriguing about mindfulness research is the variety of applications its proponents have identified. Mindfulness-based stress

220 Marks reduction (MBSR) alone has been studied as a treatment for many types of problems, from psoriasis (Kabat-Zinn et al., 1998) to the terrors of medical school (Shapiro, Schwartz, & Bonner, 1998). Mindfulness practices also have, for some time, been a component part of important cognitive-behavioral therapies, including DBT (Linehan, 1993) and acceptance and commitment therapy (ACT; Hayes, Strosahl, & Wilson, 1999). Thanks to new imaging technologies, however, researchers have begun to make even more fascinating discoveries regarding underlying physiological changes that may account for these wide-ranging treatment effects. The fundamental phenomenon at work in mindfulness practice, recent findings suggest, is neuroplasticity the ability of the brain to change its own functional and physical anatomy in response to repeated task demands. Richard Davidson (2002), a leading figure in neural correlates research, has argued that neuroplasticity permits the training of characteristics (e.g., reactivity, empathy), which psychologists have long considered fixed aspects of personality. The potential implications for human performance are profound: Neural correlates data indicate significant enhancements in areas that facilitate attentional control, emotion-regulation, and the perception of others actions and intentions skills that allow for effective athletic training and make peak performance possible. The notion that neuroanatomical substrates give rise to mental phenomena, including emotional experience, thought, and perception, is nearly as old as Western science itself though it emerged powerfully in the 19th century among such diverse figures as Franz Joseph Gall, Pierre Flourens, and Theodor Meynert (Clarke, Aminoff, & Dewhurst, 1996). The actual study of the neural correlates of consciousness, however, has emerged only recently as biomedical technology permitted electrical stimulation of the brains of living animals and later noninvasive technologies such as EEG and fmri enabled observation of brain activity in response to specific tasks. Pioneering researchers in the 1950 and 1960s, such as Vernon Mountcastle who discovered and elaborated the columnar organization of the cerebral cortex through a series of animal studies and David Hubel and Torsten Wiesel who described the neurophysiology of the visual system, provided proof that the neurological basis of human activity could be observed and explained (Koch, 2004; Metzinger, 2000). The goal of neural correlates research historically has been to map, as precisely as possible, the relationship between thinking or other aspects of consciousness and specific neuronal circuits. Throughout the 1990s, Davidson and other researchers at the University of Wisconsin have been applying the precepts and procedures of neural correlates research to the study of emotions and emotion regulation, examining in particular the relationship between mental training techniques involved in contemplative practice and responses to emotional experience (Harrington, 2008). Using EEG and fmri scanning technologies and working with a variety of participants ranging from recently suicidal outpatients to Tibetan Buddhist monks with more than 40,000 hours of meditation experience, Davidson and researchers at other institutions have discovered important, visible ways in which contemplative practices change the brain. Although the neuroplasticity of the brain during childhood and adolescence has been well-documented, these neural correlates researchers have demonstrated that it continues into adulthood. In addition, they discovered that mental training in the form of meditation can promote neuroplasticity in specific brain regions and that practitioners with adequate training begin to experience trait-like differences in

Neural Correlates of Mindfulness 221 their ability to regulate emotion and function in the face of stress-inducing stimuli (Davidson, 2002). These contemplative adepts, Davidson has argued, are mental athletes, capable of modifying their own cognitive and affective responding in enduring ways through consistent practice. In addition, these mental and emotional results of mental training are reflected in changes to neural circuitry that are both substantive and lasting. In short, Davidson and his colleagues have discovered, as Begley (2007) writes, one can sculpt the brain s emotional circuitry as powerfully as one can sculpt one s pectoral muscles (p. 231). The actual brain regions shown to be activated during meditation and after prolonged periods of meditation practice enhanced are numerous and widespread. One of the first studies to use fmri technology as a window into the neural correlates of meditation was conducted by Lazar and colleagues (2000) at Massachusetts General Hospital in Boston. It involved practitioners of a mantra-based Kundalini meditation, and the images obtained revealed activation in the following areas: (a) frontal and parietal cortex, which are areas associated with attention and perception; (b) the pregenual anterior cingulate, amygdala, midbrain, hypothalamus, which are areas relating to emotional experience as well as autonomic awareness and control; (c) the putamen, which is part of the basal ganglia associated with inhibition and maintenance of attention; and (d) the hippocampus, which is implicated in learning and formation of memories. Subsequent studies of contemplative practice have revealed similar patterns of activation, involving these brain regions or regions closely associated with them. Meditation practices involving compassion or loving kindness also have implicated the areas that Lazar and colleagues found, as well as additional brain regions, including the temporoparietal junction and posterior superior temporal sulcus (Lutz, Brefczynski-Lewis, Johnstone, & Davidson, 2008). In the Thick of It Researchers studying the phenomenon of neuroplasticity have shown in numerous studies using fmri scans that particular behaviors, including juggling (Draganski et al., 2004), playing music (Gaser & Schlaug, 2003), and language learning (Mechelli et al., 2004), correlate with increases in cortical thickness in specific brain areas. These findings are believed to be a result of the brain s ability to undergo structural changes necessary to support increased functional demands. The increases in cortical volume associated with these changes are not, however, well understood. They could result from the growth of new connections between existing neurons, which is known as arborization, from increases in glial cell volume or from enhanced vascularization (Lazar et al., 2005). To date, two studies have assessed cortical volume associated with contemplative practices, and both have yielded significant findings. In the first, Lazar and colleagues (2005) compared 20 participants who had extensive training in Buddhist insight meditation to 15 novice controls who were matched to experts on sex, age, race, and amount of educational experience. The experienced meditators had an average of 9.1 years of practice experience, and they practiced an average of 6 hr per week. They also had attended at least one week-long meditation retreat that involved 10 hr of meditation per day. The controls had no prior meditation or yoga experience. Specific cortical regions that were found to be thicker in

222 Marks the experienced meditators than in the novice controls included (a) the insula; (b) Brodmann areas near the right middle and superior frontal sulci (prefrontal cortex); (c) the somatosensory cortex, particularly a small region in the fundus of the central sulcus; (d) the auditory cortex in the left superior temporal gyrus; and (e) the inferior occipitotemporal visual cortex. Interestingly, results revealed that the thickness of certain cortical areas did not show expected age-related declines in the experienced meditator groups. In the second study, Pagnoni and Cekic (2007) compared gray matter volume of 13 Zen meditators with three or more years of experience to 13 age- and educationmatched novice controls who had never practiced meditation. Again, control subjects displayed significant age-related declines in cortical volume, but meditators did not. It should be noted that in both studies, the mean cortical thickness did not differ between the experienced meditators and controls. That is, the differences in cortical thickness that were found between the groups were located in specific areas and these differences were not sufficient in terms of overall cortical volume to yield a significant difference in average cortical thickness between the groups. The Lazar et al. (2005) and Pagnoni and Cekic (2007) studies differ, however, in regard to which brain regions displayed the greatest change in expected cortical thinning. In the Pagnoni and Cekic (2007) study, the greatest difference in age-related decline occurred in the putamen, a dopaminergic structure associated with motor control, learning, and cognitive flexibility. Age-related thinning commonly occurs in the putamen, but it was not found among experienced meditators. The putamen has been implicated in both attention deficit-hyperactivity disorder (ADHD) and in loss of dopaminergic activity in senescence. In fact, age-related reduction in cortical volume in the putamen may be a primary contributor to diminished attentional capacity and decline in executive functioning in older adults. In the Lazar et al. study (2005), the area displaying the greatest evidence of cortical thickening was the inferior occipitotemporal visual cortex or fusiform gyrus an area implicated in a variety of forms of recognition, including recognition of faces and words. This area was also correlated with a decrease in respiration rate that veteran meditators experienced while practicing, and both cortical increase and respiration rate decline were correlated with total hours of formal practice experience. Other research has found that relaxation during meditation may facilitate the cortical plasticity associated with learning (Gottselig et al., 2004), and it may be that the lower respiration rate achieved by long-time practitioners could contribute to their increased cortical thickness. This increase in thickness, as both Lazar et al. (2005) and Pagnoni and Cekic (2007) have argued, could offset normal age-related decrements. In addition, it could result in the maintenance of functioning in the affected areas, perhaps preventing age-related declines in attention, perception, and other capabilities. Attentional Expertise: The Inverted U? One recent study by Brefczynski-Lewis and colleagues (2007), which attempted to identify the neuroanatomical effects associated with achieving sustained, focused attention on an external object, found important functional differences in attention between expert meditators and novices. This study compared 12 expert meditators,

Neural Correlates of Mindfulness 223 who had 10,000 54,000 hr of meditation practice, to 12 age-matched novices with no prior meditation experience. In addition, to control for motivation of the meditators, the study also made use of a third group of 10 novice meditators who were offered a monetary incentive if they could rank among the best activators of brain regions associated with attention. All participants alternated between attending to a small dot on a computer screen and a resting state with no object of concentration. Distracting external stimuli, including sounds with positive, neutral, and negative associations taken from the International Affective Digitized Sounds (IADS) database, were presented during both the meditation and resting state. Brain function for all participants was recorded using functional magnetic resonance imaging (fmri) technology. Alternate blocks of approximately 3 min of meditation time and 1 1/2 min of resting time were monitored. Pupillary dilation also was monitored to assess participants autonomic arousal to distracting sounds. Results revealed that during meditation, both the experienced and novice meditators activated large overlapping networks of attention-related brain regions: ventral prefrontal cortex, frontal parietal, lateral occipital, insula, thalamic nuclei, basal ganglia, and cerebellum (Brefczynski-Lewis et al., 2007). During the resting phase, the novice meditators also showed bilateral activation of anterior temporal lobe areas, though the experienced meditators did not. The experienced meditators also showed greater activation than nonincentivized novices in several regions, including (a) the frontal parietal and temporal regions, (b) the parahippocampal regions, (c) the posterior occipital cortex, and (d) the cerebellum. Surprisingly, however, there were no significant differences in activation of these areas between the experienced meditators and the incentivized novices, suggesting that motivation to succeed in the meditation task affected the participants neural activity. Experienced meditators did, however, sustain attention longer than either of the novice meditator groups, suggesting that the skills involved in attention-focus were not simply a matter of effort. In fact, a key finding in the study was that experienced meditators with the highest number of total hours (37,000 52,000) showed less activation in areas associated with concentration than experienced meditators with fewer total hours (10,000 24,000). This inverted U pattern suggests a pattern of meditation development in which earlier stages require the most effort while later stages require much less a finding consistent with the verbal reports of meditation practitioners and with data from other forms of behavioral learning (e.g., athletic activity). In other words, even the task of sustaining mindful focused attention can be automated so that it is no longer effortful to attain and maintain a state of enhanced awareness. One reason that required effort may decrease with meditation experience is that they perceive phenomena and achieve expected (or higher) states of autonomic arousal with less unnecessary cortical activation or noise. Slagter and colleagues (2007) found that meditators with 3 months of experience were able to allocate attentional resources more efficiently than those without the training. Using a task in which two visual stimuli are presented in quick succession (approximately 500 ms apart), these researchers demonstrated that meditators were less susceptible to the attentional blink phenomenon in which the second stimulus is missed because cognitive resources are dedicated to perception of the first stimulus. Unlike nonmeditator controls, the meditators appeared to expend fewer resources

224 Marks on perception of the first visual target, allowing sufficient resources for perception of the second target. Slagter and colleagues theorize that the resting mode activity of the meditators was essentially quieter than that of the controls, allowing them to perceive one stimulus while having additional cognitive capacity remaining for the perception of another. Efficient use of limited resources helps explain the neural correlates revealed in the study by Brefczynski and colleagues (2007). In that study, experienced meditators demonstrated less activity overall in the so-called default-mode network the pattern of activity across the posterior cingulate gyrus, precuneus, medial frontal gyrus, and anterior cingulate that constitutes the brain s resting state. In addition, in response to potentially distracting sounds, experienced meditators show less reactivity in affective regions (i.e., amygdala, posterior cingulate) than do incentivized novice meditators. Yet experienced meditators also display greater pupillary dilation responses to emotional sounds and greater activation in the anterior insula (a key emotion-processing structure) and ventral attention network (i.e., ventral prefrontal cortex, intraparietal lobule) than novice meditators. Brefczynski-Lewis and colleagues hypothesize that this improved sensitivity is a result of more effective monitoring of concentration and internal arousal on the part of the experienced meditators. In addition, they contend that expert meditators may engage in less verbal and emotional processing than novices thanks to increased activation in the basal ganglia (specifically, the subthalamic nuclei), which play a role in the inhibition of habitual physical and mental processes. At the highest levels of meditative expertise, the authors suggest, concentration may require less cognitive activation to remain on task, and as a result, other tasks may be performed with fewer resource demands. Expert meditators could, therefore, respond accurately to potentially distracting sounds, allowing more efficient autonomic responding (greater pupillary dilation), without expending additional effort to sustain focused attention. In a similar study, Hölzel and colleagues (2007) employed a vipassana meditation task to compare responses of expert and novice meditators. Rather than concentrating the attention on an external point, the vipassana practice required meditators to focus on their own breath, specifically the sensations evoked in the area below the nostrils and above the upper lip (p. 17). Hölzel et al. compared 15 expert vipassana meditators with 7.9 years average experience to an age- and gender-matched sample of 15 novice meditators. The conditions alternated between 1 min of mindful breathing and 30 s of performing a mental arithmetic task. Results of this study showed activation in many of the same areas that Brefczynski-Lewis and colleagues (2007) identified, but they also suggest potentially important differences in activation levels, which may pertain to the nature of the mediation task. Specifically, the authors found that mindful breathing gave rise to activation in the following areas: (a) rostral anterior cingulate cortex, (b) medial prefrontal cortex, (c) postcentral gyri to rolandic operculum (area over the insula), (d) parahippocampal region, and (e) the cerebellum. Allowing for variation according to participants and tasks, these areas are essentially similar regions to those identified by Brefczynski-Lewis et al. (2007). What Hölzel and colleagues (2007) did not find, however, was the inverted-u pattern of anterior cingulate cortex activation that characterized the expert meditators in the Brefczynski-Lewis study. Instead, these authors found that rostral anterior

Neural Correlates of Mindfulness 225 cingulate cortex activation increased linearly with the degree of meditation experience. They also found linear increases in activation of the dorsal medial prefrontal cortex among the more experienced meditators. Both of these areas are associated with emotion processing, and the authors contend that their increased activation during this task indicates that experienced meditators engage in more active processing of emotion. Moreover, both the experienced and novice meditators in this study displayed similar levels of activation in the dorsal anterior cingulate cortex during completion of the mental arithmetic task, suggesting significance for the differential activation in the rostral anterior cingulate. The dorsal anterior cingulate cortex, in contrast to the rostral anterior cingulate cortex, has been associated with cognitive problem solving, specifically error detection (Posner & DiGirolamo, 1998; Taylor et al., 2006). It is difficult to draw conclusions regarding the absence of the inverted-u pattern in this case. On one hand, it may be that Hölzel and colleagues employed expert meditators with less cumulative experience than those employed by Brefczynski-Lewis and colleagues. On the other, it may be that divergent activation patterns result according to the nature of the meditation task (e.g., focusing on one s own breathing as opposed to an external object of attention). The study by Slagter and colleagues, however, suggests that increased mental efficiency, which may explain the inverted-u phenomenon, could develop after only three months of practice. Additional research comparing various meditation tasks and strategies will be needed to address such questions. Neural Correlates of Dispositional Mindfulness Researchers in clinical psychology have made numerous efforts to measure mindfulness via self-report questionnaires. The majority of these measures, including, among others, the Five Facet Mindfulness Questionnaire (Baer, Smith, Hopkins, Krietemeyer, & Toney, 2006), the Cognitive and Affective Mindfulness Scale (Feldman, Hayes, Kumar, & Greeson, 2003) and the Mindful Attention Awareness Scale (MAAS; Brown & Ryan, 2003) are designed to assess dispositional or trait mindfulness, as opposed to mindful states achieved through meditation. Yet it has been difficult to know precisely how this construct relates to an individual s capacity to engage in mindfulness practices (Block-Lerner et al., 2005). A study by Creswell, Way, Eisenberger, and Lieberman (2007) provides the only examination to date of the neural correlates associated with dispositional mindfulness, and the findings suggest that individuals endorsing high levels of dispositional mindfulness may share neuroanatomical features relating to contemplative practice. Creswell and colleagues (2007) assessed dispositional mindfulness of 27 participants using the MAAS. They then performed fmri scans while participants either labeled the emotion displayed in a photograph of a person s face (experimental condition) or ascribed a gender-appropriate name to a photograph of a person s face (control condition). Higher scores on the dispositional mindfulness measure were associated with widespread prefrontal cortex activation and attenuated amygdala responding during labeling of affect. High mindfulness participants also displayed an inverse relationship between activation of the prefrontal cortex and activation of the right amygdala, while low mindfulness participants did not show these effects. These findings, it should be noted, appear consistent with the goal of mindfulness, which involves treating emotional state as object of attention

226 Marks (thereby promoting detachment). Specifically, Creswell and colleagues found that dispositional mindfulness correlated with increased activity in three principal areas: (a) the medial prefrontal cortex, (b) the right ventrolateral prefrontal cortex, and (c) the ventromedial prefrontal cortex. These findings are consistent with the areas of activation identified by Hölzel and colleagues (2007), which also associated increased mindfulness experience with heightened activation in brain areas related to emotion processing. Compassion Meditation and Social Circuits Enhanced functioning in emotion processing and emotion regulation centers particularly the ability to experience an emotional response to others without loss of attentional control may be a key benefit of contemplative practice. Recognizing that the Buddhist practice of mindfulness meditation typically occurs within the context of cultivating compassion, Lutz, Brefczynski-Lewis, Johnstone, and Davidson (2008) have examined brain function during a compassion, or lovingkindness, meditation. This form of meditation practice is believed to enhance the sense of joy experienced when perceiving the pleasure of others and the sense of compassion experienced when observing the suffering of others. It may also, as the neural correlates research suggests, promote enhanced awareness of the actions and intentions of others. Loving-kindness meditation does not use an external object of attention, but instead focuses on allowing pure compassion or unrestricted readiness and availability to help living beings to pervade the mind (Lutz, Greischar, Rawlings, Ricard, & Davidson, 2004, p. 16369.) The specific instructions given to meditators for this task, which were developed by Matthieu Ricard, an interpreter for the Dalai Lama and a Western monk trained in the Tibetan Nyingma and Kagyu traditions, were as follows: During the training session, the subject will think about someone he cares about, such as his parents, sibling or beloved, and will let his mind be invaded by a feeling of altruistic love (wishing well-being) or of compassion (wishing freedom from suffering) toward these persons. After some training the subject will generate such feeling toward all beings and without thinking specifically about someone. While in the scanner, the subject will try to generate this state of loving kindness and compassion. (Lutz et al., 2008, p. 8) For purposes of the study, these instructions were provided to 15 expert meditators (those with 10,000 or more hours of meditation experience) and to 15 age- and gender-matched novice meditators with little meditation experience. Novices practiced the compassion meditation one hour per day for one week before completing the scans. During the scans, participants alternated between periods of meditation (3 min) and neutral rest (1.5 min). For the neutral resting period, meditators were encouraged to maintain an emotional state that was neither pleasant nor unpleasant, while also allowing themselves to remain relaxed. While participants were scanned, 2-s auditory sounds taken from the IADS database were presented at random across the meditation and resting periods (Lutz et al., 2008). The sounds included those categorized as positive (e.g., a laughing baby), neutral (e.g., restaurant crowd noise), and negative (e.g., cries of distressed

Neural Correlates of Mindfulness 227 woman). The sounds were presented every 6 10 s after the first 40 s of the meditative periods and after 15 s of the resting periods. For comparison purposes, null trials (silent events) were also randomly presented between the auditory stimuli. Participants were instructed to maintain their current practice, whether it was the compassion meditation or neutral resting task, during the presentation of the sounds. They were also asked to keep their eyes open and their gaze directed toward a fixation point displayed on a blank screen. Pupillary dilation was measured before and after presentation of sounds as an assessment of autonomic arousal, and participants were asked to report on the quality of their meditative state, ranking its intensity on a scale of 1 (lowest intensity) to 9 (highest intensity). Lutz et al. (2008) found that the areas activated during compassion meditation included the attention centers of the ventral prefrontal cortex, as well as anterior insula and anterior cingulate cortex, areas which have been associated with empathic responding in several previous studies (de Vignemont & Singer, 2006; Ruby & Decety, 2004; Singer et al., 2004). Activity in the insular cortex was associated with participants perception of the quality of their meditative state, with greater activation corresponding to higher participant ratings. Insula activation was also correlated with the expertise of the meditator with accomplished practitioners displaying higher levels of activation. Insula activation was related to the valence of emotional sounds experienced during compassion meditation. All participants exhibited stronger activation in the anterior insula and anterior cingulate cortex in response to all emotional sounds, and activation was significantly greater during compassion meditation than when at rest. Accomplished meditators displayed greater change in activation from rest to meditation in the presence of both negative and positive emotion sounds than did novice meditators. Good meditation intensity also moderated change from rest to meditation in insular activity when hearing negative and positive emotion sounds. According to Lutz and colleagues (2008), the pattern of responding to emotion sounds suggests that cultivating the intent to be compassionate can enhance empathic reactions to social stimuli. As expected, the autonomic arousal of meditators, measured by pupillary diameter, was greater in response to negative emotion sounds than in response to positive or neutral sounds. This arousal level was increased during compassion meditation for both groups, but the increase was greater for experienced meditators. The increase in pupil diameter also correlated with increased anterior insula activation. In addition, experts also showed increased activation in the amygdala and the right posterior superior temporal sulcus (psts) in response to all sounds, indicating greater detection of the emotional sounds and an enhanced response to emotional human vocalizations during meditation. Interestingly, experts also displayed a pattern of reduced activation in the right temporoparietal junction (TPJ) when responding to negative emotion sounds in the resting task but increased activation in this area when exposed to negative emotion sounds during the compassion meditation. Overall, the accomplished practitioners demonstrated strong right-sided activation bias in the TPJ between meditation and rest, while novices showed virtually no activation difference between meditation and rest in response to the emotional sounds. The TPJ has been associated with the ability to distinguish between self and other, as well as the development of theory of mind, including the ability to postulate what another person might be thinking or feeling (Samson, Apperly, Chiavarino, & Humphreys, 2004). It is also part of a

228 Marks larger system of social circuitry that also involves the STS and the orbitofrontal cortex. This area, as Johnson and colleagues (2005) have found, appears to be related to processing of a variety of social information, including both visual and auditory cues about the intentions of others. Lutz and colleagues (2004) also conducted an EEG study that involved a compassion meditation similar to that used in fmri scans. This study, which compared 8 long-term (10,000 50,000 hr) practitioners to 10 student volunteers without prior meditation experience, revealed that accomplished meditators were able to sustain high-frequency gamma-band (25 42 Hz) activity during and following meditation while novice controls were not. In addition, for the accomplished practitioners, gamma-band activity extended over most scalp electrodes indicating long-distance gamma synchrony a phenomenon that has been associated with the coordination or binding of distributed neural activity, including internal and external cues as well as information about self and other (Basar-Eroglu, Struber, Schurmann, Stadler, & Basar, 1996; Lee, Williams, Breakspear, & Gordon, 2003) in ways that give rise to consciousness (Melloni et al., 2007; Posner, DiGirolamo, & Fernandez-Duque, 1997). Moreover, Lutz and colleagues claim that the gamma-band recordings of expert practitioners in this study were the highest ever reported in the EEG literature involving nonpathological subjects. EEG Studies of Mindfulness-Based Interventions While studies that involve expert meditators yield fascinating information regarding peak states of consciousness and potential insight into basic brain activity, they have revealed little about the neural effects of short-term meditation training. Given that most mindfulness-based clinical interventions involve relatively brief courses of meditation instruction typically 8 weeks it is important to understand the neural correlates associated with such short-term training. Although fmri studies of these interventions are still lacking, two recent EEG studies focused on the neural effects of participating in MBSR and mindfulness-based cognitive therapy (MBCT) for depression. EEG, which monitors electrical activity of the brain, offers little in the way of spatial resolution provided by fmri, yet it does possess two advantages that contribute to its continued use: (a) it records brain activity as it happens in real time, whereas fmri does not provide precise time resolution, and (b) it is less cost and resource intensive than fmri. Davidson and colleagues (2003) used EEG to measure baseline brain activity and response to positive and negative emotion inductions among 48 adults without prior meditation experience. Participants were randomly assigned to either an 8-week MBSR course or a wait-list control group, and EEG readings were taken before, immediately after, and 4 months after the experimental group completed the MBSR course. The MBSR protocol consists of 8 weekly group meetings lasting approximately 2 1/2 3 hr, as well as a 7-hr silent retreat held during week 6. In addition, participants are instructed to practice meditation at home for 1 hr per day, 6 days per week, using recordings of guided meditations. Davidson and colleagues found no differences in EEG performance between the MBSR and wait list control groups. At 8 weeks, however, the MBSR group showed higher left-side activation, particularly in alpha waves (8 12 Hz), than controls at both prefrontal and central

Neural Correlates of Mindfulness 229 electrode locations. This asymmetry was maintained at 4 months postintervention. In addition, the MBSR group showed greater left-side activation in response to both positive and negative emotion inductions than did wait-list controls. Left-side alpha asymmetry has been associated with reduced reactivity and increased positive mood states (Tomarken, Davidson, & Henriques, 1990; Wheeler, Davidson, & Tomarken, 1993), although these findings have not been consistently replicated (Gotlib, Ranganath, & Rosenfeld, 1998). In a study that sheds light on the utility of mindfulness interventions for psychological distress, Barnhofer and colleagues (2007) examined EEG (alphaasymmetry) in 34 previously suicidal individuals who were assigned at random to either an MBCT condition or a treatment as usual condition (i.e., relapse prevention group). MBCT is an 8-week program based on MBSR, which consists of 8 weekly meetings for 2 1/2 3 hr, a 7-hr silent retreat held during week 6, and 1 hr of daily practice 6 days a week using guided mediations. Resting EEG assessments were completed immediately before the start of the course and immediately after the completion of the 8-week training. At baseline, the groups did not differ significantly on EEG, though the MBCT group had higher mean scores on the Beck Depression Inventory and a higher number of previous depressive episodes than the treatment as usual group. After the 8 weeks, the treatment as usual group, who received individual treatment under the direction of a physician, showed mood deterioration along with increased right-side prefrontal activation and left-side hypoactivation alpha asymmetry patterns associated with depressive mood states (Davidson, 1993). By contrast, the MBCT group showed stable patterns of leftand right-side prefrontal activation. One notable confound in this study, however, concerns the percentage of participants in each group that received antidepressant medication during the 8-week intervention: Fully 70% of those in the MBCT condition were receiving antidepressants compared with only 50% of those in the treatment as usual group. Relevance for Clinical Sport Psychologists Mindfulness meditation and related practices have been associated with numerous benefits for mental and physical health, ranging from reductions in depressive symptoms to improvements in immune functioning. Yet the fundamental mechanisms of action of these practices remain only dimly understood. Examining the neural correlates of mindfulness tasks through the use of fmri and other neuroimaging technologies presents an opportunity to understand, at least in part, how the effects of mindfulness are produced. It also sheds light on the workings of attentional and emotion processing systems. Such knowledge may ultimately yield clinically useful insights regarding the neuroanatomical structures and processes implicated in psychiatric disorders such as depression, anxiety, and attention deficit-hyperactivity disorder (ADHD), all of which could prove valuable to clinical sport psychologists. Using Gardner and Moore s (2004b) MCS-SP framework for classifying the issues sport psychologists typically face, one can identify important implications of this research for interventions at each of the framework s four classification levels, including (a) performance development, (b) performance dysfunction, (c) performance impairment, and (d) performance termination.

230 Marks Performance Development According to Gardner and Moore (2004b, 2006), performance development issues can be classified as belonging to one of two subtypes: (a) PD-I, which includes cases in which mental skills training is deemed helpful to ongoing development of physical athletic skills and (b) PD-II, which includes cases in which the athlete has already acquired significant physical skills, but mental skills training is needed for optimal levels of performance. Neural correlates research provides data of relevance for performance enhancement interventions at both PD-I and PD-II. First of all, enhanced attentional control and the ability to experience autonomic arousal in ways that interfere in only minimal ways with the maintenance of attentional tasks are likely to prove invaluable skills in athletic performance situations. Mental skills training in sport psychology has typically focused on goal-setting, imagery, positive self-talk, and arousal regulation via precompetition behavioral routines. All of these approaches, in one manner or another, involve efforts to control affective responses so that the athlete can concentrate more efficiently on athletic performance. Yet none have demonstrated that they can effect trait-like, enduring changes to the athlete s pattern of emotional responding and certainly none have shown evidence of direct modification of neural circuitry. Clinicians choosing to employ mindfulness-based interventions, by contrast, have at their disposal empirical evidence of neuroanatomical changes that contemplative practices can yield. Having this empirically informed rationale for the effects of an intervention is likely to render it more compelling to both the clinician and the athlete alike. Moreover, mindfulness-based interventions offer two benefits that other performance enhancement strategies do not: (a) they do not involve discussion of the sport or performance, making them generalizable to other dimensions of the athlete s experience, and (b) they offer tangible benefits in the form of improved mood (Teasdale et al., 2002), heightened immune functioning (Davidson et al., 2003), and enhanced alertness, orienting, and with prolonged practice, conflict monitoring (Jha, Krompinger, & Baime, 2007). One way to think about the benefits that mindfulness or related meditation practices could afford individuals who are developing their athletic skills is as mental efficiency training. Through the repeated exercise of attentional control in contemplative practice, the developing athlete automates a process of detecting and directing the attention to a desired stimulus without neglecting other relevant data from the senses or from within the body (e.g., autonomic arousal). As Brefczynski-Lewis and colleagues (2007) discovered in their comparison of highly experienced expert meditators to novices and less experienced experts, this automation process eventually may allow for more efficient allocation of cognitive resources, whereby attentional focus and emotional responding occur at heightened levels with relatively lower levels of activation overall. EEG findings involving elite athletes appear to support this automation and efficiency hypothesis. For example, in an EEG-based study of elite golfers, Crews and Landers (1993) discovered decreased left-side cortical activity and increased right-side activity associated with putting performance. Alpha-wave activity in left temporal regions, which are typically associated with verbal activity, dropped precipitously as the putting task approached. One way of interpreting this data is that linguistic functioning decreases during performance as kinesthetic procedural memory increases in importance.