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Different neural correlates of facing pain with mindfulness: Contributions of strategy and skill. Comment on "Facing the experience of pain: A neuropsychological perspective" by Fabbro and Crescentini
... In regard to this latter aspect, in his commentary Gard [5] has elegantly reviewed the brain signatures of superior pain modulation through mindfulness meditation and, more importantly, has highlighted as such signatures differ depending on the strategy and skill applied by meditators when facing painful stimuli. Thus, it seems that only advanced meditators are able to "simply" process the sensory quality of the painful experience while refraining from excessive cognitive/emotional elaboration (non-judging/non-reactive attitude). ...
... Accordingly, pain modulation with this strategy in expert meditators occurs through an increased activation in pain related brain regions, such as the insula and the anterior cingulate cortex, and decreased activation in cognitive control/evaluative brain areas such as the lateral prefrontal cortex [10,27,28]. Of great interest and worth to be taken into consideration in future studies on pain modulation and mindfulness, Gard [5] has noticed that activation in pain related regions during pain processing also depends on skill learning, namely on how one is proficient in applying a strategy. Thus, increased effort and brain activation are required at the beginning of skill learning relative to what happens at higher levels of proficiency. ...
... Thus, increased effort and brain activation are required at the beginning of skill learning relative to what happens at higher levels of proficiency. Overall, recent researches investigating the neurofunctional mechanisms of pain modulation through mindfulness, as summarized by Gard [5], contribute to a point that we raised in our original target review [7], namely that stand mindfully in the face of pain is a difficult task that requires a long and constant meditation practice. However, despite the challenges that this task requires, the studies also suggest that the effort can be fully justified. ...
... The neural mechanisms underlying these benefits are now becoming clearer: reductions in pain intensity are often associated with increased activation of SLN hubs (i.e., ACC, anterior insula), reflecting changes in saliency processing and attentional monitoring of painful somatosensory cues. Across a variety of experimental paradigms, similar results were also found for pain processing and anxiety in naïve and experienced meditators, with increases in SLN regions relating to reductions in pain anticipation and unpleasantness and improved anxiety relief (Gard, 2014;Lutz et al., 2013;Zeidan & Vago, 2016). Intriguingly, the shift from DMN-to SLN-oriented processing during mindfulness of painful stimulation elevates activity of sensory regions involved in processing pain. ...
Mindfulness training (MT) represents a family of contemplative practices aimed at promoting well-being. Despite growing evidence for the clinical efficacy of MT interventions across a range of mental health disorders, mechanistic theories of MT remain difficult to validate through self-report techniques alone. Neuroimaging investigations of MT complement self-report approaches by characterizing changes in information processing associated with MT. Such approaches may be used to analyze mindfulness at three levels: as a transient state, as the product of longitudinal MT, and as trait-like differences in the tendency to be mindful. This chapter synthesizes neuroimaging research at all three of these levels to propose a neural network model of mindfulness, relating MT to the interactions between three commonly characterized brain networks. Current contemplative neuroscience studies converge around findings that MT often involves a reconfiguration of mental habits supported by the default mode network (DMN), most commonly increasing DMN connectivity to both sensory representation areas and the brain’s central executive network (CEN). This DMN’s “dorsal shift” to the CEN from more ventral, affectively laden connections to the brain’s salience network (SLN) may reflect an increased ability to reflect upon events without lapsing into habitual ways of judging or responding. Together, this pattern of increased sensory access to the prefrontal cortex, coupled with a dorsal shift in prefrontal connectivity to regions associated with cognitive control, is suggestive of an emerging neurophenotype of capacity to access and sustain mindful states.KeywordsMindfulnessDefault mode network (DMN)Central executive network (CEN)Salience network (SLN)Mindfulness-based stress reduction (MBSR)Mindfulness-based cognitive therapy (MBCT)Dispositional or trait mindfulnessMindful Attention Awareness ScaleFive Facet Mindfulness Scale (FFMQ)DecenteringPainRewardEnhanced sensory processingEmotion regulation/emotion processingResting-state imagingAttention regulationSelf-regulation
The subjective experience of one's environment is constructed by interactions among sensory, cognitive, and affective processes. For centuries, meditation has been thought to influence such processes by enabling a nonevaluative representation of sensory events. To better understand how meditation influences the sensory experience, we used arterial spin labeling functional magnetic resonance imaging to assess the neural mechanisms by which mindfulness meditation influences pain in healthy human participants. After 4 d of mindfulness meditation training, meditating in the presence of noxious stimulation significantly reduced pain unpleasantness by 57% and pain intensity ratings by 40% when compared to rest. A two-factor repeated-measures ANOVA was used to identify interactions between meditation and pain-related brain activation. Meditation reduced pain-related activation of the contralateral primary somato-sensory cortex. Multiple regression analysis was used to identify brain regions associated with individual differences in the magnitude of meditation-related pain reductions. Meditation-induced reductions in pain intensity ratings were associated with increased activity in the anterior cingulate cortex and anterior insula, areas involved in the cognitive regulation of nociceptive processing. Reductions in pain unpleasantness ratings were associated with orbitofrontal cortex activation, an area implicated in reframing the contextual evaluation of sensory events. Moreover, reductions in pain unpleasantness also were associated with thalamic deactivation, which may reflect a limbic gating mechanism involved in modifying interactions between afferent input and executive-order brain areas. Together, these data indicate that meditation engages multiple brain mechanisms that alter the construction of the subjectively available pain experience from afferent information.
Objectives:
Mindfulness-based pain management programs (MBPMs) aim to improve mental and physical health in individuals with chronic pain. In this study, we investigated whether improvement in mental health might require (1) reduction in the sensory pain experience and brain correlates of that experience, and/or (2) improved perceptions of the controllability of pain and corresponding brain activity related to cognitive control and emotional regulation.
Methods:
Twenty-eight patients with chronic pain were assessed and randomized into an intervention group (who attended an 8-wk MBPM) or a control group (treatment-as-usual), before being reassessed after 8 weeks. Outcome measures included clinical pain, perceived control over pain, mental and physical health, and mindfulness. Neural activity was measured during the anticipation and experience of acute experimental pain, using electroencephalography with source reconstruction.
Results:
Improvements were found in the MBPM group relative to the control group in mental health, which related to greater perceived control of pain, but not to reductions in clinical or experimental pain ratings. Anticipatory and pain-evoked event-related potentials to acute experimental pain were decreased, but sources of these event-related potentials were estimated to be in regions that modulate emotional responses rather than pain intensity. Mental health and perceived control outcomes correlated with reduced anticipatory deactivations of dorsolateral prefrontal and somatosensory cortices.
Discussion:
Increased activity in cognitive control regions of the brain during pain anticipation related to improved mental health and perceived control over pain, but not to decreased pain experience. Greater perceived control may therefore result from improved regulation of the emotional response to pain.
The cognitive modulation of pain is influenced by a number of factors ranging from attention, beliefs, conditioning, expectations, mood, and the regulation of emotional responses to noxious sensory events. Recently, mindfulness meditation has been found attenuate pain through some of these mechanisms including enhanced cognitive and emotional control, as well as altering the contextual evaluation of sensory events. This review discusses the brain mechanisms involved in mindfulness meditation-related pain relief across different meditative techniques, expertise and training levels, experimental procedures, and neuroimaging methodologies. Converging lines of neuroimaging evidence reveal that mindfulness meditation-related pain relief is associated with unique appraisal cognitive processes depending on expertise level and meditation tradition. Moreover, it is postulated that mindfulness meditation-related pain relief may share a common final pathway with other cognitive techniques in the modulation of pain.
Pain can be modulated by several cognitive techniques, typically involving increased cognitive control and decreased sensory
processing. Recently, it has been demonstrated that pain can also be attenuated by mindfulness. Here, we investigate the underlying
brain mechanisms by which the state of mindfulness reduces pain. Mindfulness practitioners and controls received unpleasant
electric stimuli in the functional magnetic resonance imaging scanner during a mindfulness and a control condition. Mindfulness
practitioners, but not controls, were able to reduce pain unpleasantness by 22% and anticipatory anxiety by 29% during a mindful
state. In the brain, this reduction was associated with decreased activation in the lateral prefrontal cortex and increased
activation in the right posterior insula during stimulation and increased rostral anterior cingulate cortex activation during
the anticipation of pain. These findings reveal a unique mechanism of pain modulation, comprising increased sensory processing
and decreased cognitive control, and are in sharp contrast to established pain modulation mechanisms.
The subjective experience of one's environment is constructed by interactions among sensory, cognitive, and affective processes. For centuries, meditation has been thought to influence such processes by enabling a nonevaluative representation of sensory events. To better understand how meditation influences the sensory experience, we used arterial spin labeling functional magnetic resonance imaging to assess the neural mechanisms by which mindfulness meditation influences pain in healthy human participants. After 4 d of mindfulness meditation training, meditating in the presence of noxious stimulation significantly reduced pain unpleasantness by 57% and pain intensity ratings by 40% when compared to rest. A two-factor repeated-measures ANOVA was used to identify interactions between meditation and pain-related brain activation. Meditation reduced pain-related activation of the contralateral primary somatosensory cortex. Multiple regression analysis was used to identify brain regions associated with individual differences in the magnitude of meditation-related pain reductions. Meditation-induced reductions in pain intensity ratings were associated with increased activity in the anterior cingulate cortex and anterior insula, areas involved in the cognitive regulation of nociceptive processing. Reductions in pain unpleasantness ratings were associated with orbitofrontal cortex activation, an area implicated in reframing the contextual evaluation of sensory events. Moreover, reductions in pain unpleasantness also were associated with thalamic deactivation, which may reflect a limbic gating mechanism involved in modifying interactions between afferent input and executive-order brain areas. Together, these data indicate that meditation engages multiple brain mechanisms that alter the construction of the subjectively available pain experience from afferent information.
How similar are the experiences of social rejection and physical pain? Extant research suggests that a network of brain regions that support the affective but not the sensory components of physical pain underlie both experiences. Here we demonstrate that when rejection is powerfully elicited--by having people who recently experienced an unwanted break-up view a photograph of their ex-partner as they think about being rejected--areas that support the sensory components of physical pain (secondary somatosensory cortex; dorsal posterior insula) become active. We demonstrate the overlap between social rejection and physical pain in these areas by comparing both conditions in the same individuals using functional MRI. We further demonstrate the specificity of the secondary somatosensory cortex and dorsal posterior insula activity to physical pain by comparing activated locations in our study with a database of over 500 published studies. Activation in these regions was highly diagnostic of physical pain, with positive predictive values up to 88%. These results give new meaning to the idea that rejection "hurts." They demonstrate that rejection and physical pain are similar not only in that they are both distressing--they share a common somatosensory representation as well.
Pain is a conscious experience, crucial for survival. To investigate the neural basis of pain perception in humans, a large number of investigators apply noxious stimuli to the body of volunteers while sampling brain activity using different functional neuroimaging techniques. These responses have been shown to originate from an extensive network of brain regions, which has been christened the Pain Matrix and is often considered to represent a unique cerebral signature for pain perception. As a consequence, the Pain Matrix is often used to understand the neural mechanisms of pain in health and disease. Because the interpretation of a great number of experimental studies relies on the assumption that the brain responses elicited by nociceptive stimuli reflect the activity of a cortical network that is at least partially specific for pain, it appears crucial to ascertain whether this notion is supported by unequivocal experimental evidence. Here, we will review the original concept of the "Neuromatrix" as it was initially proposed by Melzack and its subsequent transformation into a pain-specific matrix. Through a critical discussion of the evidence in favor and against this concept of pain specificity, we show that the fraction of the neuronal activity measured using currently available macroscopic functional neuroimaging techniques (e.g., EEG, MEG, fMRI, PET) in response to transient nociceptive stimulation is likely to be largely unspecific for nociception.
Our ability to have an experience of another's pain is characteristic of empathy. Using functional imaging, we assessed brain
activity while volunteers experienced a painful stimulus and compared it to that elicited when they observed a signal indicating
that their loved one—present in the same room—was receiving a similar pain stimulus. Bilateral anterior insula (AI), rostral
anterior cingulate cortex (ACC), brainstem, and cerebellum were activated when subjects received pain and also by a signal
that a loved one experienced pain. AIand ACC activation correlated with individual empathy scores. Activity in the posterior
insula/secondary somatosensory cortex, the sensorimotor cortex (SI/MI), and the caudal ACC was specific to receiving pain.
Thus, a neural response in AIand rostral ACC, activated in common for “self” and “other” conditions, suggests that the neural
substrate for empathic experience does not involve the entire “pain matrix.” We conclude that only that part of the pain network
associated with its affective qualities, but not its sensory qualities, mediates empathy.
Language acquisition is one of the most fundamental human traits, and it is obviously the brain that undergoes the developmental changes. During the years of language acquisition, the brain not only stores linguistic information but also adapts to the grammatical regularities of language. Recent advances in functional neuroimaging have substantially contributed to systems-level analyses of brain development. In this Viewpoint, I review the current understanding of how the "final state" of language acquisition is represented in the mature brain and summarize new findings on cortical plasticity for second language acquisition, focusing particularly on the function of the grammar center.
Since the first demonstrations that mindfulness-based therapies could have a positive influence on chronic pain patients, numerous studies have been conducted with healthy individuals in an attempt to understand meditative analgesia. This review focuses explicitly on experimental pain studies of meditation and attempts to draw preliminary conclusions based on the work completed in this new field over the past 6 years. Dividing meditative practices into the broad categories of focused attention (FA) and open monitoring (OM) techniques allowed several patterns to emerge. The majority of evidence for FA practices suggests they are not particularly effective in reducing pain. OM, on the other hand, seems to influence both sensory and affective pain ratings depending on the tradition or on whether the practitioners were meditating. The neural pattern underlying pain modulation during OM suggests meditators actively focus on the noxious stimulation while inhibiting other mental processes, consistent with descriptions of mindfulness. A preliminary model is presented for explaining the influence of mindfulness practice on pain. Finally, the potential analgesic effect of the currently unexplored technique of compassion meditation is discussed.
The beneficial clinical effects of mindfulness practices are receiving increasing support from empirical studies. However, the functional neural mechanisms underlying these benefits have not been thoroughly investigated. Some authors suggest that mindfulness should be described as a 'top-down' emotion regulation strategy, while others suggest that mindfulness should be described as a 'bottom-up' emotion regulation strategy. Current discrepancies might derive from the many different descriptions and applications of mindfulness. The present review aims to discuss current descriptions of mindfulness and the relationship existing between mindfulness practice and most commonly investigated emotion regulation strategies. Recent results from functional neuro-imaging studies investigating mindfulness training within the context of emotion regulation are presented. We suggest that mindfulness training is associated with 'top-down' emotion regulation in short-term practitioners and with 'bottom-up' emotion regulation in long-term practitioners. Limitations of current evidence and suggestions for future research on this topic are discussed.
Interventions based on Cognitive Behavioral Therapy (CBT) are widely used to treat chronic pain, but the brain mechanisms responsible for these treatment effects are poorly understood. The aim of this study was to validate the relevance of the cortical control theory in response to an exposure-based form of CBT, Acceptance and Commitment Therapy, in patients with chronic pain. Forty-three female patients diagnosed with fibromyalgia syndrome were enrolled in a randomized, 12-week, waiting-list controlled clinical trial (CBT n=25; controls n=18). CBT was administered in groups of six patients during 12 weekly sessions. Functional magnetic resonance imaging (fMRI) during pressure-evoked pain was assessed before and after treatment or the 12-week period. Self-report questionnaires of depression and anxiety were administered pre- and posttreatment as well as 3 months following end of treatment. Patients treated with CBT reported larger improvement of fibromyalgia on the Patient Global Impression of Change measure, and improved depression and anxiety symptoms, compared to the waiting-list controls. However, there were no effects on clinical pain or pain sensitivity measures. An analysis of fMRI scans revealed that CBT led to increased activations in the ventrolateral prefrontal/lateral orbitofrontal cortex; regions associated with executive cognitive control. We suggest that CBT changes the brain's processing of pain through an altered cerebral loop between pain signals, emotions, and cognitions; leading to increased access to executive regions for reappraisal of pain. Our data thereby support our hypothesis about the activation of a cortical control mechanism in response to CBT treatment in chronic pain.
Acceptance-based interventions such as mindfulness-based stress reduction program and acceptance and commitment therapy are alternative therapies for cognitive behavioral therapy for treating chronic pain patients. To assess the effects of acceptance-based interventions on patients with chronic pain, we conducted a systematic review and meta-analysis of controlled and noncontrolled studies reporting effects on mental and physical health of pain patients. All studies were rated for quality. Primary outcome measures were pain intensity and depression. Secondary outcomes were anxiety, physical wellbeing, and quality of life. Twenty-two studies (9 randomized controlled studies, 5 clinical controlled studies [without randomization] and 8 noncontrolled studies) were included, totaling 1235 patients with chronic pain. An effect size on pain of 0.37 was found for the controlled studies. The effect on depression was 0.32. The quality of the studies was not found to moderate the effects of acceptance-based interventions. The results suggest that at present mindfulness-based stress reduction program and acceptance and commitment therapy are not superior to cognitive behavioral therapy but can be good alternatives. More high-quality studies are needed. It is recommended to focus on therapies that integrate mindfulness and behavioral therapy. Acceptance-based therapies have small to medium effects on physical and mental health in chronic pain patients. These effects are comparable to those of cognitive behavioral therapy.
Concepts originating from ancient Eastern texts are now being explored scientifically, leading to new insights into mind/brain function. Meditative practice, often viewed as an emotion regulation strategy, has been associated with pain reduction, low pain sensitivity, chronic pain improvement, and thickness of pain-related cortices. Zen meditation is unlike previously studied emotion regulation techniques; more akin to 'no appraisal' than 'reappraisal'. This implies the cognitive evaluation of pain may be involved in the pain-related effects observed in meditators. Using functional magnetic resonance imaging and a thermal pain paradigm we show that practitioners of Zen, compared to controls, reduce activity in executive, evaluative and emotion areas during pain (prefrontal cortex, amygdala, hippocampus). Meditators with the most experience showed the largest activation reductions. Simultaneously, meditators more robustly activated primary pain processing regions (anterior cingulate cortex, thalamus, insula). Importantly, the lower pain sensitivity in meditators was strongly predicted by reductions in functional connectivity between executive and pain-related cortices. Results suggest a functional decoupling of the cognitive-evaluative and sensory-discriminative dimensions of pain, possibly allowing practitioners to view painful stimuli more neutrally. The activation pattern is remarkably consistent with the mindset described in Zen and the notion of mindfulness. Our findings contrast and challenge current concepts of pain and emotion regulation and cognitive control; commonly thought to manifest through increased activation of frontal executive areas. We suggest it is possible to self-regulate in a more 'passive' manner, by reducing higher-order evaluative processes, as demonstrated here by the disengagement of anterior brain systems in meditators.
This experiment used functional Magnetic Resonance Imaging to examine the relation between individual differences in cognitive skill and the amount of cortical activation engendered by two strategies (linguistic vs. visual-spatial) in a sentence-picture verification task. The verbal strategy produced more activation in language-related cortical regions (e.g., Broca's area), whereas the visual-spatial strategy produced more activation in regions that have been implicated in visual-spatial reasoning (e.g., parietal cortex). These relations were also modulated by individual differences in cognitive skill: Individuals with better verbal skills (as measured by the reading span test) had less activation in Broca's area when they used the verbal strategy. Similarly, individuals with better visual-spatial skills (as measured by the Vandenberg, 1971, mental rotation test) had less activation in the left parietal cortex when they used the visual-spatial strategy. These results indicate that language and visual-spatial processing are supported by partially separable networks of cortical regions and suggests one basis for strategy selection: the minimization of cognitive workload.
The perception of pain due to an acute injury or in clinical pain states undergoes substantial processing at supraspinal levels. Supraspinal, brain mechanisms are increasingly recognized as playing a major role in the representation and modulation of pain experience. These neural mechanisms may then contribute to interindividual variations and disabilities associated with chronic pain conditions.
To systematically review the literature regarding how activity in diverse brain regions creates and modulates the experience of acute and chronic pain states, emphasizing the contribution of various imaging techniques to emerging concepts.
MEDLINE and PRE-MEDLINE searches were performed to identify all English-language articles that examine human brain activity during pain, using hemodynamic (PET, fMRI), neuroelectrical (EEG, MEG) and neurochemical methods (MRS, receptor binding and neurotransmitter modulation), from January 1, 1988 to March 1, 2003. Additional studies were identified through bibliographies.
Studies were selected based on consensus across all four authors. The criteria included well-designed experimental procedures, as well as landmark studies that have significantly advanced the field.
Sixty-eight hemodynamic studies of experimental pain in normal subjects, 30 in clinical pain conditions, and 30 using neuroelectrical methods met selection criteria and were used in a meta-analysis. Another 24 articles were identified where brain neurochemistry of pain was examined. Technical issues that may explain differences between studies across laboratories are expounded. The evidence for and the respective incidences of brain areas constituting the brain network for acute pain are presented. The main components of this network are: primary and secondary somatosensory, insular, anterior cingulate, and prefrontal cortices (S1, S2, IC, ACC, PFC) and thalamus (Th). Evidence for somatotopic organization, based on 10 studies, and psychological modulation, based on 20 studies, is discussed, as well as the temporal sequence of the afferent volley to the cortex, based on neuroelectrical studies. A meta-analysis highlights important methodological differences in identifying the brain network underlying acute pain perception. It also shows that the brain network for acute pain perception in normal subjects is at least partially distinct from that seen in chronic clinical pain conditions and that chronic pain engages brain regions critical for cognitive/emotional assessments, implying that this component of pain may be a distinctive feature between chronic and acute pain. The neurochemical studies highlight the role of opiate and catecholamine transmitters and receptors in pain states, and in the modulation of pain with environmental and genetic influences.
The nociceptive system is now recognized as a sensory system in its own right, from primary afferents to multiple brain areas. Pain experience is strongly modulated by interactions of ascending and descending pathways. Understanding these modulatory mechanisms in health and in disease is critical for developing fully effective therapies for the treatment of clinical pain conditions.
Meditation refers to a family of mental training practices that are designed to familiarize the practitioner with specific types of mental processes. One of the most basic forms of meditation is concentration meditation, in which sustained attention is focused on an object such as a small visual stimulus or the breath. In age-matched participants, using functional MRI, we found that activation in a network of brain regions typically involved in sustained attention showed an inverted u-shaped curve in which expert meditators (EMs) with an average of 19,000 h of practice had more activation than novices, but EMs with an average of 44,000 h had less activation. In response to distracter sounds used to probe the meditation, EMs vs. novices had less brain activation in regions related to discursive thoughts and emotions and more activation in regions related to response inhibition and attention. Correlation with hours of practice suggests possible plasticity in these mechanisms.
• attention
• frontal
• parietal
• response inhibition
Meditation can be conceptualized as a family of complex emotional and attentional regulatory training regimes developed for various ends, including the cultivation of well-being and emotional balance. Among these various practices, there are two styles that are commonly studied. One style, focused attention meditation, entails the voluntary focusing of attention on a chosen object. The other style, open monitoring meditation, involves nonreactive monitoring of the content of experience from moment to moment. The potential regulatory functions of these practices on attention and emotion processes could have a long-term impact on the brain and behavior.
The perception of pain is sensitive to various mental processes such as the feelings and beliefs that someone has about pain. It is therefore not exclusively driven by the noxious input. Attentional modulation involving the descending pain modulatory system has been examined extensively in neuroimaging studies. However, the investigation of neural mechanisms underlying more complex cognitive modulation is an emerging field in pain research. Recent findings indicate an engagement of the ventrolateral prefrontal cortex during more complex modulation, leading to a change or reappraisal of the emotional significance of pain. Taking placebo-induced analgesia as an example, we discuss the contribution of attention, expectation and reappraisal as three basic mechanisms that are important for the cognitive modulation of pain.
Human brain mechanisms of pain perception and regulation in health and disease
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