ISSUE #003 - Jul 11, 2018
Allostasis, Plasticity, and Integration: The Neuroscience of Mindfulness
“Mental activities, such as purposely paying attention to the present moment, actually stimulate the brain to become active in specific ways that then promote the growth of integrative regions. These neuroplastic changes…help us see the link between mindful awareness and the creation of well-being.” —Daniel Siegel, The Mindful Brain
The growing role of mindfulness in psychiatry dates to the beginnings of meditation research. As soon as Benson and Kabat-Zinn evolved the first evidence-based paradigms for the clinical use of meditation–the relaxation response (Beary & Benson, 1974) and mindfulness-based stress reduction (MBSR) (Kabat-Zinn, 1982)–they began studying the application of these methods in mental health. The results of the first pilot studies in anxiety (Benson et al., 1978) were promising enough to encourage the development of clinical paradigms tailored for mental health. Early paradigms used mindfulness in treatment-resistant conditions like borderline personality (Linehan et al., 1991) and recurrent depression (Teasdale et al., 1995). As studies of Linehan’s dialectical behavior therapy (DBT) and Teasdale’s mindfulness-based cognitive therapy (MBCT) showed reductions in self-injurious behavior and depression-relapse, mindfulness was applied to other conditions, and interest in it as an adjunct in mental health grew (Baer, 2003).
Meanwhile, our understanding of the neural mechanisms of mindfulness grew exponentially. In my first review (Loizzo, 2000), I proposed that meditation shares a common mechanism with psychotherapy, combining two elements: the reduction of stress, and the enrichment of learning. The most common conditions we treat in psychiatry have been linked to “wear and tear” on the brain, caused by overexposure to stress hormones and inflammatory cytokines. In contrast to the adaptive responses to normal challenges called “allostasis,” the syndrome of “wear and tear” caused by chronic stress and trauma has been described as “allostatic load/overload.” Meanwhile, others reported a seemingly contradictory finding: under persistent positive stimulation, the brain underwent tissue growth, repair, and regeneration. This “use it or loose it” process we now know as neuroplasticity not only counterbalanced the wear and tear of stress, but was linked to findings that learning and neurogenesis were enhanced in “enriched environments” (Rosensweig & Bennet, 1996)
The implications of neuroplasticity did not escape the attention of pioneers like Kandel, who made it the basis for a new paradigm in psychiatry (Kandel, 1998). Yet the paradigm he proposed would not be complete without another line of research. Twenty years after the stress response was described, Benson introduced the idea of the relaxation response as its complement (Beary & Benson, 1974). Given the binary structure of the autonomic nervous system (ANS), and the role of sympathetic activation in stress, meditation was said to elicit the relaxation response, by increasing parasympathetic activation. Research on MBSR distinguished mindfulness as “a discipline of attention” from the relaxation response (Goleman & Schwartz, 1976). In contrast to relaxation alone, the effects of mindfulness were attributed to a hybrid mechanism like the one I proposed: the calming function of meditation improving allostasis by reducing the stress-response; and its attentional function enriching learning by stimulating use-dependent plasticity (Davidson, 2000).
Further studies supported the mechanistic role of neuroplasticity, linking mindfulness with EEG patterns and structural changes consistent with increased activation, myelination and neurogenesis (Lazar et al., 2000, 2005). One key study showed that Tibetan-trained experts were able to consciously induce EEG findings indicative of increased learning and plasticity—unprecedented trains of gamma activity and synchrony—at will (Lutz et al., 2004). More recent studies confirmed the link between meditation and neurogenesis (Luders et al., 2009; Holzel et al., 2011a) and also linked meditation to brain connectivity (Jang et al. 2010; Guard et al., 2014). Today meditation is seen as a missing link in conscious self-regulation, connecting mental training on the one hand, to the electrochemical processes of neuronal firing, epigenetic regulation of gene-transcription, and new neural connectivity on the other.
While such studies have clarified how mindfulness enriches learning, a related set of findings have revealed the other side of its mechanism and effects: conscious ANS regulation. Decades of studies of conscious breath practices have all shown some modulation of the ANS (Harinath et al., 2004). Recently, our understanding of such shifts has been expanded by new work on the ANS (Porges, 2011). Porges explains how the myelinated “smart vagus” that evolved in mammals not only supports voluntary breathing but also helps modulate primitive vagal and sympathetic reflexes to support expanded use of higher cortical capacities for social engagement.
Another general model views meditation as an integrative practice. When attention and relaxation combine, they help shift the dissociative, reactive mode of neural processing that prevails under stress, trauma and insecure attachment to the integrative, responsive style of processing that emerges under conditions of social safety, positive stimulation, and secure attachment (Siegel, 2012). Integrative models and mindfulness converge in research on the most recently evolved brain region: the prefrontal cortex (PFC). An inventory of prefrontal functions reads like a wish list of human development: selective attention and working memory; planning and execution; emotional regulation; empathy and morality; problem-solving; and body-awareness. Given its intimate links with other brain regions–neocortical, limbic, subcortical, midbrain, and brainstem—the PFC is seen as the “conductor” of the neural symphony, and seat of conscious brain integration. Not surprisingly, it also plays the central role in current meditation research, as we see from Vago’s model of mindfulness as enhancing an integrative network based in the PFC, fostering self-awareness, self-regulation, and self-transcendence (Vago et al., 2014).
Mindfulness and Psychotherapy: Vertical and Lateral Integration
For decades, researchers have reflected on the similarities between mindfulness and free-association. Apart from the surface resemblance between Freud’s “evenly hovering attention” and descriptions of mindfulness as “unbiased awareness,” these reflections raise two deeper mechanistic questions (Loizzo, 2000). What level of consciousness do mindfulness and free-association occupy along the spectrum from normal wakefulness to sleep or trance? And which mode of consciousness do they engage on the bimodal spectrum from abstract-analytic to embodied-sensorimotor.
EEG studies of common meditation techniques like TM and mindfulness show a pattern of gradually increasing neocortical alpha amplitude and coherence (Fenwick, 1987), suggesting an initial phase of deepening introspection and calm comparable to drowsiness (Cahn & Polich, 2006). However, meditators routinely stop the progression that normally leads to somnolence, and instead of generating slow theta or delta waves typical of stage 1 sleep show a rise of high frequency theta activity, consistent with increased attentiveness (Gruzelier, 2009). A similar pattern of wakeful relaxation is thought to be cultivated by free association, which Freud conceived as “waking state hypnosis” (Delmonte, 1995).
The question of where mindfulness falls on the spectrum of states of consciousness relates to the theme of vertical integration. While some dissociation between levels and states of consciousness is the default condition of the human mind-brain, it would appear that with the right methods and repeated practice, they can be reorganized into an integrated system. In fact, the level of consciousness at which insight and attention can be maintained is not fixed, but varies with the type of practice and the level of expertise. This is evident not just from studies that show self-regulation of deeper structures with expertise (Lutz et al., 2008; Luders et al., 2013), but also from studies of virtuosos who show markers of waking state consciousness in the dream and deep sleep states (Mason et al., 1997), and of aroused consciousness in hypometabolic states resembling hibernation, estivation, and the diving state of aquatic mammals
(Heller et al,, 1987).
Given the increasing evidence of lateral specialization among the cerebral hemispheres, as well as among key subcortical structures like the insula, cingulate, hippocampus, and amygdala, our second question is how meditation and psychotherapy alter hemispheric lateralization. Since Roger Sperry’s studies of epileptics with surgically bisected hemispheres, evidence has mounted that the verbal-expressive left hemisphere preferentially supports analytic processing, optimistic thinking, positive affect, and approach behaviors, while the sensorimotor-receptive right supports synthetic processing, worst-case thinking, aversive affect, and avoidance. This is consistent with findings that vagal activation generally dominates left hemisphere processing while sympathetic activation tends to dominate on the right (Shannahoff-Khalsa, 2007). So the mix of moderate relaxation with heightened attention common to both meditation and psychotherapy suggests they may share a mechanism of altering hemispheric laterality (Loizzo, 2009). This mechanism has been supported by numerous findings, and explained in two ways.
Delmonte suggested that a shift toward balanced dominance reduces the default dissociation between the hemispheres, offering verbal consciousness greater access to normally suppressed emotion and repressed trauma (Delmonte, 1995). This is consistent with findings that meditation increases the size of the corpus callosum (Luders et al., 2012); increases cortical integration (Guard et al., 2014); increases the activity and size of the right anterior cingulate cortex and the right insula (Lazar et al., 2005); decreases the activation and size of the right amygdala (Holzel et al., 2010); and increases activation in implicit learning structures like the caudate and putamen (Tang et al., 2009).
Davidson offers a complementary explanation, based on the left lateral shift in prefrontal activity in mindfulness (Davidson et al, 2003). He attributes the enhanced emotional regulation in mindfulness to greater involvement of the left hemisphere. This is consistent with the clinical evidence that mindfulness helps prevent depression relapse by enhancing metacognition (Teasdale et al., 1995), as well as with findings of increased attentional flexibility and resilience in meditators (Guard et al., 2014). It also overlaps with recent clinical models of common psychopathology–anxiety, depression, trauma, attention deficit, impulse control, and addictive disorders–as a syndrome of hypofrontality: a dysregulation of limbic reactivity and subcortical impulsivity based on developmental deficits or disuse of “top-down” prefrontal regulatory centers and pathways (Menon, 2011).
Both these explanations have validity, and reflect complementary mechanisms. Increased access to normally suppressed, dissociated, or repressed material opens the way to deeper insight, corrective experience, and transformation. Higher faculties of metacognitive insight, narrative reframing, and emotional regulation are equally necessary to constructively re-process the newly accessed material. This second general mechanism shared by meditation and psychotherapy clearly relates to the theme of lateral integration. As in vertical integration, it appears that the human mind and brain has a greater capacity for lateral integration than we thought, especially given rigorous methods and practice (Luders et al., 2012).
Mindful Body and Self-Awareness: Integrating the Neocortex Of the five basic forms of mindfulness practice, the simplest—body mindfulness—begins by using breath as a focal point to reconnect conscious attention to the body. This practice offers an accessible, reproducible methodology for building attention and cultivating self-awareness. Since all mindfulness practice exercises awareness, it is no surprise that it has been found to heighten attention and expand working memory, increasing activation and grey matter in executive regions like the dorsolateral and anterior PFC (Lazar et al., 2005; Luders et al., 2009). Mindfulness has been shown to increase not just attention but metacognitive functions like attentional flexibility, fluid intelligence (Jha et al., 2007), resilience, global network efficiency, and network integration (Gard et al., 2014). Consistent with this expansion of metacognitive awareness, mindfulness has also been shown to enhance emotional regulation (Creswell et al., 2007), by greater activation of the orbitofrontal region of the PFC (Holzel at al., 2011b).
Yet this does not come at the cost of a dissociation from sensitivity. In fact, mindfulness enhances bodily self-awareness, increasing the activation and size of the (right) insula, a deep neocortical region that serves as an interoceptive map or link to bodily sensations (Farb et al., 2012), and increasing the activation and size of the right thalamus (Luders et al., 2009). Likewise, mindfulness and related practices have been found to enhance perceptual sensitivity, introspective accuracy (Fox et al., 2012), and the discrimination of emotions (MacLean et al., 2010).
Among the findings linking mindfulness with neocortical self-awareness, the most intriguing relate to the impact of mindfulness on the offline processing of the default mode network (DMN). The DMN maintains the internally generated loop of self-referential narrative and self-world imagery that fills the void when mind and brain are idling between tasks. This network functions differently in meditators than non-meditators, with the former showing less self-referential activity not just within practice sessions but also in everyday life (Brewer et al., 2014). Yet mindfulness practice does not lead to a detached self-awareness stuck in a pure, internal present. It opens self-awareness outward to the world, growing mirror regions and DMN regions that support facial recognition, the self-other empathy system, and cerebellar regions involved in planning and executing intentional action (Holzel et al., 2011b). These findings suggest that mindfulness increases self-awareness and neocortical integration by de-automatizing self-constructive processing, and bringing metacognitive awareness and flexibility to default habits of identity, social recognition, and intentionality. The evidence that mindfulness practice helps expand the capacity of the neocortex for integrated social engagement is also consistent with Porges’ model of ANS modulation.
Therapeutically, basic mindfulness is not just a key element in mindfulness-based cognitive therapy (MBCT), but works like free-association to support dynamic psychotherapy, fostering the emergence of observing ego and insight as alternatives to self-limiting ego defenses. This neocortical mechanism may help explain why it strengthens recovery from depression and why it has been taken up as a helpful adjunct in psychodynamic practice.
Mindful Sensitivity, Kindness, and Self-Regulation: Integrating the Limbic System
The second basic form of mindfulness practice–mindful sensitivity–focuses on the raw feelings of pleasure, pain, and neutrality that color all experiences of body, mind, and world, and trigger subliminal reactivity to positive, negative, and neutral stimulation. This key practice trains the mind to anticipate and prevent sensory reactivity based on past conditioning. It also dovetails with the mindfulness-based practice of loving-kindness, which trains the mind to prevent reactive emotions like fear, rage, and shame, by anticipating and transforming them into proactive emotions like kindness, tolerance, and acceptance.
This level of practice relates to Vago’s second rubric: self-regulation. The relevance of self-regulation to mindfulness stems from the vulnerability of the neocortex to dysregulation, based on the default self-protective structure of the human brain. The neocortex maintains its default social engagement mode—lead by the PFC—only under conditions of perceived safety. Once the brain detects potential harm, it typically shifts into stress-protective mode, under the influence of the amygdala. This shift not only triggers the general stress-response, with its sympathetic and HPAA components, but disables the top-down regulation of the PFC and “hijacks” the neocortex. In this mode, the brain falls into a functional syndrome of hypofrontality. The damage done is compounded when the stresses are chronic, and we end up in states of allostatic overload like depression, chronic fatigue syndrome, learned helplessness, or PTSD.
Mindfulness has been shown to decrease levels of anxiety and perceived stress, a finding correlated with decreased activation and gray matter in the right amygdala (Goldin et al., 2011). One mechanism for this enhanced self-regulation of bottom-up stress-reactivity is increased activation of the anterior cingulate cortex (ACC) by regions of the PFC known to moderate fear and stress perception (Posner at al., 2007), since the ACC is the hub for top-down control of the limbic system by cognitive-emotional integration. Along with heightened attention, Tang found a practice of mind/body self-regulation similar to mindfulness increased ACC activation as well as heart rate variability (HRV), a measure of smart vagal activation (Tang et al., 2009).
Another mechanism of self-regulation in mindful sensitivity reflects the increasing emotional context provided by the hippocampus. If the amygdala is the brain’s emotional alarm bell, the hippocampus serves as its emotional moderator or damper. Given its function to form and retain explicit memories, the hippocampus maps present data points onto an inner universe of spatiotemporal, social emotional and narrative perspective. The reference setting of the hippocampus helps contextualize raw sensory input processed in the amygdala, reframing worst-case fears in light of a broader range of personal and interpersonal experience.
The second main practice for self-regulation of the emotional brain is loving kindness or compassion practice. While research on kindness practice is more recent, the last decade has seen a number of key findings that clarify its effectiveness and mechanisms. Barbara Fredrickson found that simple loving-kindness meditation—exercising and gradually expanding positive emotions towards self and others in a mindful state—enhanced a range of positive emotions, expanded well-being, and enriched social resources and relationships (Fredrickson et al., 2008). More recent studies have shed light on the mechanisms of compassion training. The normal brain typically responds to seeing distressed faces with activation of the frontopariental mirror neuron system and middle ACC, which triggers conditioned disgust activation in the anterior insula and fear reactivity in the amygdala. After brief mindful compassion training, novices’ brains showed less connectivity of the PFC with the AI and amydgala, more activation of PFC regulatory regions (dlPFC, mOFC) and the superior ACC intentional hub (Klimecki et al., 2012), and also showed significant activation of mesolimbic reward system structures (Weng et al., 2013). These effects of kindness-compassion practice reflect a self-regulatory shift in limbic functioning from a bottom-upsocial emotional stress-reactive mode to a top-down mode of positive affective self-regulation and proactive social engagement.
Clinically, the first intervention integrating mindful sensitivity and kindness practices was Linehan’s DBT (Linehan et al., 1991). More recently, the study of inwardly directed kindness practice as “self-compassion” was proposed as integral to the effects of interventions like MBSR and MBCT, suggesting the broad therapeutic potential of self-regulatory forms of mindfulness practice (Neff, 2003; Kuyken et al., 2010). A second generation of interventions has developed around Tibetan methods, formulated as cognitive behavioral compassion training (CBCT) (Desbordes et al., 2012) and compassion cultivation training (CCT) (Klimecki et al., 2014). The most developed of these has been the compassion-focused therapy formulated by Paul Gilbert based on MBCT (Gilbert, 2014). Initial studies show that it has real promise in a range of mental and physical health applications including depression, anxiety, psychosis, and smoking cessation (Leaviss & Uttley, 2015). Finally, the practice of mindful sensitivity and kindness has been artfully woven into object relational approaches to psychotherapy by psychoanalysts Mark Epstein (Epstein, 1995) and Jeffrey Rubin (Rubin, 1996).
Mindful Awareness, Mindful Insight, and Self-Transcendence: Integrating the Core Brain
This last set of practices—mindful awareness and experience—is the least known. In mindful awareness, attention is focused on the primary process of mind, traditionally taken to mean the raw data of sense intuitions or mental impressions prior to any association with verbal concepts, symbolic images, or emotional memories. The benefits of such “upstream” access to preprocessed mind-body states has obvious relevance to the correction of conditioned associations involved in bottom-up reactivity to stress and trauma. The complement to this practice is mindful insight. Based on direct access to preprocessed input via mindful awareness, this practice brings unbiased awareness to the way that input is processed by conditioned associations to memory images, emotional responses, and verbal narratives. It allows a metacognitive assessment and correction of the mentality with which the input is processed, including correcting perceptual distortions, reactive emotions, and/or traumatic narratives. This set of practices presents a depth-psychological insight practice meant to support self-transcendence through the deconstruction and reconstruction of personality (Dahl et al., 2015).
The first potential mechanism for the practice of mindful awareness comes from findings that mindfulness increases activation and grey matter in core brain regions critical to sense perception and implicit learning: the caudate, putamen, and thalamus (Tang et al., 2012; Pickut et al., 2013). A second mechanism involves modulation of primary regulatory structures and processes within the pontine brainstem. A recent study shed light on the possible mechanism of the much discussed impact of mindfulness practice on well-being; increases in well-being from mindfulness were correlated with increases in gray matter concentration the dorsal pons (Singleton et al., 2014). The correlation appears to support the mechanistic link between the well-being generated by mindfulness and the pontine nuclei of the mood and arousal modulating neuro-transmitters serotonin, norepinephrine, and acetylcholine. This mechanism is supported by the findings of a prior study on the closely related practice of Zazen, that greater prefrontal activation and increased serotonin are correlated with the improved mood in novice practitioners (Yu et al., 2011).
While the Singleton study offers a plausible mechanism of how mindful awareness and insight could support the affective component of self-transcendence, it is likely that the cognitive component involves alterations in the medullary brainstem, where the two vagal complexes intersect with the main centers of cardiorespiratory regulation and regenerative states. Early studies found that bare awareness practices linked with advanced breath control could elicit profoundly hypometabolic states akin to lucid hibernation (Heller et al., 1987), supporting paradoxically high levels of cortical arousal (Benson et al., 1990). Recent studies have replicated these findings (Amihai & Koshevnikov, 2014), and linked them to increased gray matter density in the medulla oblongata (Verstergaard-Poulsen et al., 2009). This is consistent with Porges’ theory that full integration of the brainstem social engagement system is supported by smart vagal modulation of primitive vagal freeze reactivity.
Conclusion: Mindfulness and the Future of Neuropsychiatry
In this review, I have brought together converging breakthroughs in neuroscience and physiology, including key elements of the emerging paradigm for psychiatry in the twenty-first century: allostasis, neural plasticity, social neuroscience, affective neuroscience, and polyvagal theory. The ways in which different forms of mindfulness help moderate traumatic stress reactivity and support social engagement at all levels of the nervous system further illumines the therapeutic benefits of mindful brain integration, rekindling the original promise of psychoanalysis to help bring unconscious structures and processes into the light of higher consciousness.
For clinicians, the single most remarkable and significant conclusion of this review is that mindfulness practices seem to share not only many of their beneficial effects but also their primary brain mechanisms with psychotherapy. This, in addition to the rising tide of neural research on these practices and the promising findings of mindfulness interventions in many conditions, makes a strong case for all mental health professionals to take an interest in the growing field of contemplative psychotherapy.
Key points for further study and reflection:
1) Basic mindfulness practice expands the size and capacity of the prefrontal and insular cortex, increasing self-awareness, attention, flexibility, interoception, and emotional regulation.
2) Mindful sensitivity and loving kindness practice expand the size of the ACC and hippocampus, enhancing self-regulation of social emotions, responses, and rewards, while reducing right amygdala size and “bottom-up” traumatic stress-reactivity.
3) Mindful awareness and insight promote the transcendence of aversive conditioning and default HPAA-autonomic stress-reactivity, by accessing and modulating subcortical and brainstem structures involved in implicit learning, internal reward, neuroendocrine rhythms, and autonomic tone.
4) The five aspects of mindfulness practice overlap with other common contemplative practices including TM, the relaxation response, Hatha Yoga, compassion training, Zazen, imagery, recitation, forced breathing, and mindful movement, providing an overview of the mechanisms and potential benefits of these practices for mental health and well-being.
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IN THIS ISSUE
- 1What is Meditation Research? A Comprehensive Overview
- 2On the Neuroscience of Enlightenment
- 3Can Embodied Contemplative Practices Accelerate Resilience Training and Trauma Recovery?
- 4The Potency of Exposing Science in Yoga
- 5The subtle body: an interoceptive map of central nervous system function and meditative mind–brain–body integration
- 6Yoga Therapy and Polyvagal Theory: The Convergence of Traditional Wisdom and Contemporary Neuroscience for Self-Regulation and Resilience
- 7Understanding the Neurobiological Mechanisms of Mindfulness
- 8The Guide to Mindfulness Meditation: Contemplative Science and Buddhist Origins
- 9Allostasis, Plasticity, and Integration: The Neuroscience of Mindfulness