Impact of mindfulness-based stress reduction training on intrinsic brain connectivity
Research highlights
►MBSR training enhances functional connectivity within sensory networks. ►MBSR subjects show greater auditory/visual reciprocal modulation. ►MBSR training alters connectivity between attention and sensory networks.
Introduction
Mindfulness meditation is an attention-training technique that is receiving increased research and public interest in the West (Ludwig and Kabat-Zinn, 2008, Lutz et al., 2008b). It consists of training practitioners in how to be mindful, an attentional stance of openly and non-judgmentally observing one's moment-by-moment experiences. A growing body of evidence suggests that mindfulness meditation training may reduce stress and improve some aspects of physical and psychological health in patient populations (Brown et al., 2007, Chiesa and Serretti, 2009, Chiesa and Serretti, 2010, Creswell et al., 2009). Moreover, new neuroimaging studies suggest that mindfulness meditation training, such as that offered in the standardized and manualized 8-week Mindfulness-Based Stress Reduction (MBSR) intervention (Kabat-Zinn, 1990), can alter functional neural responding to affective tasks in healthy individuals (Farb et al., 2010).
A major component of mindfulness meditation training is focusing and refocusing awareness on present moment internal and external experience (e.g., breathing, thoughts, ambient sounds, interoceptive sensations) as opposed to mind wandering or active problem solving. MBSR training includes breath awareness, body awareness, attention to the transient nature of sensory experience, and shifting attention across sensory modalities. It is therefore hypothesized that meditation practice should lead to altered functioning of brain networks involved in attention and sensitivity to internal and external sensations and emotions. To date only a small number of studies examined brain mechanisms involved in mindfulness meditation using functional brain imaging. Although the results across these small studies are not completely consistent they do suggest mindfulness meditation leads to increased activations in frontal brain regions involved in attention (Farb et al., 2007, Goldin and Gross, 2010, Holzel et al., 2007) and increased activations in temporal regions during processing of sounds (Lutz et al., 2008a). In addition, mindfulness meditation experience is associated with increased cortical thickness in anterior insula (involved in interoception), frontal cortex (Brodmann's area 9/10; involved in the integration of emotion and cognition) and sensory cortices (Lazar et al., 2005). Thus there is evidence that mindfulness meditation is associated with changes in attention and perceptual processing circuits, perhaps reflecting the emphasis on conscious direction and redirection of attention to present moment experience and increased awareness of sensory stimuli.
The examination of intrinsic connectivity networks (ICNs), sometimes referred to as resting state networks (Seeley et al., 2007), provides information about the integrity and organization of major functional systems of the brain. Even in the absence of explicit, phasic changes induced by a sensory or cognitive task, intrinsic brain activity is characterized by slow fluctuations in the BOLD signal (< 0.1 Hz) which exhibit a high degree of spatial structure reminiscent of task-related activation maps (Damoiseaux et al., 2006, Smith et al., 2009). Coherent functional networks most consistently identified by fcMRI include the default mode network (DMN) associated with episodic memory and self-referential processing; the executive control network associated with salience processing; lateralized frontoparietal networks associated with working memory and attentional processes; and sensory-related networks (medial visual, lateral visual, auditory, sensorimotor) (Damoiseaux et al., 2006, Smith et al., 2009).
Intrinsic connectivity fMRI has been used to characterize neural networks in healthy and patient populations (Buckner et al., 2008, Greicius, 2008), and it may be also particularly relevant for the study of changes in functional connectivity that are hypothesized to result from regular practice of mindfulness meditation. Intrinsic connectivity reflects both anatomically constrained spontaneous fluctuations and state-dependent activity (Gopinath et al., 2010) and is well suited for studying states such as meditation. Intrinsic activity has been shown to be modulated in terms of connectivity, amplitude or spectral power distribution by various conditions such as rest with eyes open or closed, sleep, transcutaneous electrical nerve stimulation, muscle fatigue and by pharmological manipulations (Bianciardi et al., 2009, Esposito et al., 2010, Gopinath et al., 2010, Horovitz et al., 2008, Peltier et al., 2005, Rack-Gomer et al., 2009, Yan et al., 2009). Also, intrinsic connectivity changes have been found following intense training on a difficult visual discrimination task (Lewis et al., 2009). Thus, fcMRI provides a tool for examining training-related plasticity and neural mechanisms underlying states such as meditation. The aim of the present study was to determine if Mindfulness-Based Stress Reduction (MBSR) training alters the functional connectivity of intrinsic connectivity networks during mindful awareness of auditory sensation. Given that the formal practice of MBSR highlights attention to sensory experience, we hypothesized that ICNs associated with attention and sensory processing would show training-related changes.
Section snippets
Subjects
Thirty-two healthy, meditation-naïve women (ages 21–55; mean = 34.1; standard deviation = 9.8) were recruited by advertisement. Subjects were screened via medical exam for absence of significant health or psychiatric conditions. All study protocols were performed after approval by UCLA and informed consent was obtained from all subjects. Subjects were compensated for participation by the provision of the MBSR training program free of charge. One additional subject completed the MBSR training;
MBSR training compliance
All MBSR subjects completed at least six of the eight classes. Meditation diaries were not received from two MBSR subjects. Of the remaining 15 MBSR subjects, 10 attended all eight classes; three attended seven classes; two attended six classes and 10 attended the daylong retreat. Diary data indicated that MBSR subjects completed an average of 2716.5 min of meditation during the course (± 184.6 standard error; range: 1520–3925 min).
MAAS
MAAS scores for three of the wait list control subjects were not
Discussion
The results indicate that a course of MBSR training in healthy subjects impacts regional functional connectivity within auditory/salience and medial visual intrinsic connectivity networks during instructed mindful awareness to auditory stimuli. MBSR subjects, relative to wait list controls, displayed increased functional connectivity of the parietal operculum and the dmPFC (BA9/32) in the auditory/salience ICN and increased functional connectivity of retrosplenial cortex in the medial visual
Conclusions
Intrinsic connectivity fMRI allows for an examination of the functional connectivity of basic brain processing systems during meditation states. The current findings extend the results of prior studies that showed meditation-related changes in specific brain regions active during attention and sensory processing by providing evidence that MBSR trained compared to untrained subjects, during a focused attention instruction, have increased connectivity within sensory networks and between regions
Acknowledgments
This study is supported by funds from G. Oppenheimer Family Foundation, National Institutes of Health grants AT 00268 and DK64531, and the UCLA Ahmanson-Lovelace Brain Mapping Center.
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