Mindfulness and dynamic functional neural connectivity in children and adolescents

Abstract

Background

Interventions that promote mindfulness consistently show salutary effects on cognition and emotional wellbeing in adults, and more recently, in children and adolescents. However, we lack understanding of the neurobiological mechanisms underlying mindfulness in youth that should allow for more judicious application of these interventions in clinical and educational settings.

Methods

Using multi-echo multi-band fMRI, we examined dynamic (i.e., time-varying) and conventional static resting-state connectivity between core neurocognitive networks (i.e., salience/emotion, default mode, central executive) in 42 children and adolescents (ages 6–17).

Results

We found that trait mindfulness in youth relates to dynamic but not static resting-state connectivity. Specifically, more mindful youth transitioned more between brain states over the course of the scan, spent overall less time in a certain connectivity state, and showed a state-specific reduction in connectivity between salience/emotion and central executive networks. The number of state transitions mediated the link between higher mindfulness and lower anxiety, providing new insights into potential neural mechanisms underlying benefits of mindfulness on psychological health in youth.

Conclusions

Our results provide new evidence that mindfulness in youth relates to functional neural dynamics and interactions between neurocognitive networks, over time.

Introduction

How often do you reach the bottom of a page and realize that you “zoned out”, and were thinking of the past or future instead of the task at hand? The propensity to mind-wander, or to shift attention away from the present moment and toward internal information, appears to be a “default mode” of processing. Incredibly, nearly 50% of our awake life is spent mind-wandering [1]. Yet, mind-wandering is associated with lower levels of happiness [1], possibly through pathological forms of self-referential thought focused on the past or future, such as rumination or worry [2]. These data have prompted interest in understanding present-centered mental states, and ways in which such states can be cultivated.

One such method is mindfulness, which is typically defined as the ability to stay aware of and focus attention on experiences in the present moment, in an accepting, nonjudgmental manner [3]. Mindfulness can be considered a mental capacity that differs between individuals, i.e., trait mindfulness [4], [5], and importantly, can be strengthened through a variety of methods. For instance, interventions that promote mindfulness (e.g., meditation practices) are shown to have broad positive effects on health and wellbeing, including enhanced cognitive functioning, alleviation of pain, and improved mood. Meta-analyses show consistent benefits of mindfulness-based interventions in patients with a variety of conditions, including chronic pain, anxiety disorders, depression, and cancer [6], [7], [8], as well as in nonclinical samples [9].

The benefits of mindfulness are firmly established in adults, and exciting emerging data also support the use of mindfulness to improve physical and mental health in children and adolescents. Indeed, recent meta-analyses indicate that mindfulness training relates to improvements in cognitive performance, emotion regulation, and stress resilience, as well as reductions in symptoms of anxiety and depression in clinical and nonclinical youth samples [10], [11]. It is not surprising, then, that there has been increased interest in integrating mindfulness practices into education and mainstream pediatric health services. We have recently shown that Kids Kicking Cancer (KKC, www.kidskickingcancer.org), a martial arts therapy that includes mindfulness based meditative practices, appears to be an effective interventional therapeutic modality for reducing pediatric cancer pain, with over 85% reporting reductions in pain with an average decrease of 40% [12]. KKC and other mindfulness-based interventions are particularly well suited for children because they can be used as a non-pharmacological strategy for early, preventive intervention with little or no adverse side effects. In addition to improving psychological wellbeing, such interventions may reduce morbidity, health care costs, and caregiver and family distress by improving patient adherence to medical procedures.

As the empirical evidence for mindfulness-based approaches continues to grow, there is a critical need to understand the neural correlates underlying positive intervention response. Greater understanding of the underlying neural correlates in youth could enhance the strength and efficacy of mindfulness-based interventions for improving long-term health outcomes, and allow for more judicious application of these techniques in clinical and educational settings. Recent neuroimaging studies in adults suggest that at least three large-scale neural networks play a pivotal role in mindfulness: the default mode network (DMN), the salience and emotion network (SEN), and the central executive network (CEN), implicated in self-referential processing and mind-wandering, present moment awareness, and shifting and sustaining attentional focus, respectively [13]. Although prior studies in adults find that trait mindfulness relates to altered connectivity between these networks [e.g.,14], such associations are typically measured using static functional connectivity approaches, which treat network interactions as fixed over time. Such an approach is at odds with the increasingly recognized dynamic nature of functional neural networks [15], [16], [17], [18], and of mindfulness, which may relate to greater mental and neural flexibility. Indeed, one neuroimaging study in adults [13] identified four accompanying mental or neural “states” associated with mindful meditation: (1) mind-wandering (DMN), (2) attentional awareness of mind-wandering (SEN), (3) shift of attention back to the present moment (CEN), and (4) focus on the present moment (CEN). It is likely that these states correspond with different patterns of connectivity among neural networks, and that mindfulness relates to more flexible transitioning between these brain states and/or altered coordination between networks over time. These functional neural patterns may be better captured with a complementary dynamic, or time-varying approach to neural connectivity [see review by 19].

Although it is now clear that mindfulness has similar salutary effects in youth, the neural correlates of these effects are largely unknown. As a first step, the present study evaluates both dynamic and conventional static neural connectivity to test how mindfulness in children relates to interactions between large-scale neural networks (DMN, SEN, CEN). We focus on trait mindfulness as a broad psychological indicator of health and well-being, associated with increased quality of life, academic competence, and social skills, and decreased somatic complaints and internalizing symptoms in youth [20]. Thus, we will also test for associations among mindfulness, neural connectivity, and indices of psychological health (anxiety, depression) in the sample.

Functional connectivity was measured during the resting-state in order to identify individual differences in trait-like neural patterns that may influence day-to-day life, beyond a meditative state. Indeed, resting-state functional connectivity is thought to reflect habitual network activations [21] that can be remodeled by long-term [e.g.,22] and even brief [e.g.,14] mindfulness training. Further, similar patterns of functional connectivity have been reported during meditation and a non-meditative (resting) state [13], suggesting that the neural substrates underlying trait mindfulness are the same ones that can be strengthened through mindfulness-based practices. We also evaluate amount of present-centered thought during the scan, as measured on a post-scan questionnaire, to assess convergence between state and trait measures and to aid interpretation of observed dynamic connectivity states.

Notably, the study sample was economically and racially diverse, with a large number of youth at risk for emotional psychopathology via socioeconomic disadvantage (i.e., lower income) and/or early threat exposures (i.e. violence, abuse exposure, intensive medical treatments; see Supplemental Material). This served to (1) increase the generalizability of findings, and (2) improve our ability to draw initial links among mindfulness, brain connectivity, and indices of psychological health.