Mindfulness-based training attenuates insula response to an aversive interoceptive challenge.

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Neuroimaging studies of mindfulness training (MT) modulate anterior cingulate cortex (ACC) and insula among other brain regions, which are important for attentional control, emotional regulation and interoception. Inspiratory breathing load (IBL) is an experimental approach to examine how an individual responds to an aversive stimulus. Military personnel are at increased risk for cognitive, emotional and physiological compromise as a consequence of prolonged exposure to stressful environments and, therefore, may benefit from MT. This study investigated whether MT modulates neural processing of interoceptive distress in infantry marines scheduled to undergo pre-deployment training and deployment to Afghanistan. Marines were divided into two groups: individuals who received training as usual (control) and individuals who received an additional 20-h mindfulness-based mind fitness training (MMFT). All subjects completed an IBL task during functional magnetic resonance imaging at baseline and post-MMFT training. Marines who underwent MMFT relative to controls demonstrated a significant attenuation of right anterior insula and ACC during the experience of loaded breathing. These results support the hypothesis that MT changes brain activation such that individuals process more effectively an aversive interoceptive stimulus. Thus, MT may serve as a training technique to modulate the brain's response to negative interoceptive stimuli, which may help to improve resilience.

Affiliation

Department of Psychiatry, University of California, San Diego, CA, USA, Warfighter Performance Department, Navel Health Research Center, San Diego, CA, USA.

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Neuroimaging studies of mindfulness training (MT) modulate anterior cingulate cortex (ACC) and insula among other brain regions, which are important for attentional control, emotional regulation and interoception. Inspiratory breathing load (IBL) is an experimental approach to examine how an individual responds to an aversive stimulus. Military personnel are at increased risk for cognitive, emotional and physiological compromise as a consequence of prolonged exposure to stressful environments and, therefore, may benefit from MT. This study investigated whether MT modulates neural processing of interoceptive distress in infantry marines scheduled to undergo pre-deployment training and deployment to Afghanistan. Marines were divided into two groups: individuals who received training as usual (control) and individuals who received an additional 20-h mindfulness-based mind fitness training (MMFT). All subjects completed an IBL task during functional magnetic resonance imaging at baseline and post-MMFT training. Marines who underwent MMFT relative to controls demonstrated a significant attenuation of right anterior insula and ACC during the experience of loaded breathing. These results support the hypothesis that MT changes brain activation such that individuals process more effectively an aversive interoceptive stimulus. Thus, MT may serve as a training technique to modulate the brain's response to negative interoceptive stimuli, which may help to improve resilience.

Military deployment can have profound effects on physical and mental health. Few studies have examined whether interventions prior to deployment can improve mechanisms underlying resilience. Mindfulness-based techniques have been shown to aid recovery from stress and may affect brain-behavior relationships prior to deployment. The authors examined the effect of mindfulness training on resilience mechanisms in active-duty Marines preparing for deployment.
Eight Marine infantry platoons (N=281) were randomly selected. Four platoons were assigned to receive mindfulness training (N=147) and four were assigned to a training-as-usual control condition (N=134). Platoons were assessed at baseline, 8 weeks after baseline, and during and after a stressful combat training session approximately 9 weeks after baseline. The mindfulness training condition was delivered in the form of 8 weeks of Mindfulness-Based Mind Fitness Training (MMFT), a program comprising 20 hours of classroom instruction plus daily homework exercises. MMFT emphasizes interoceptive awareness, attentional control, and tolerance of present-moment experiences. The main outcome measures were heart rate, breathing rate, plasma neuropeptide Y concentration, score on the Response to Stressful Experiences Scale, and brain activation as measured by functional MRI.
Marines who received MMFT showed greater reactivity (heart rate [d=0.43]) and enhanced recovery (heart rate [d=0.67], breathing rate [d=0.93]) after stressful training; lower plasma neuropeptide Y concentration after stressful training (d=0.38); and attenuated blood-oxygen-level-dependent signal in the right insula and anterior cingulate.
The results show that mechanisms related to stress recovery can be modified in healthy individuals prior to stress exposure, with important implications for evidence-based mental health research and treatment.

This study examined neural processes of resilience during aversive interoceptive processing. Forty-six individuals were divided into three groups of resilience Low (LowRes), high (HighRes), and normal (NormRes), based on the Connor-Davidson Resilience Scale (2003). Participants then completed a task involving anticipation and experience of loaded breathing during functional magnetic resonance imaging (fMRI) recording. Compared to HighRes and NormRes groups, LowRes self-reported lower levels of interoceptive awareness and demonstrated higher insular and thalamic activation across anticipation and breathing load conditions. Thus, individuals with lower resilience show reduced attention to bodily signals but greater neural processing to aversive bodily perturbations. In low resilient individuals, this mismatch between attention to and processing of interoceptive afferents may result in poor adaptation in stressful situations.

The insula and cingulate cortices are implicated in emotional, homeostatic/allostatic, sensorimotor, and cognitive functions. Non-human primates have specific anatomical connections between sub-divisions of the insula and cingulate. Specifically, the anterior insula projects to the pregenual anterior cingulate cortex (pACC) and the anterior and posterior mid-cingulate cortex (aMCC and pMCC); the mid-posterior insula only projects to the posterior MCC (pMCC). In humans, functional neuroimaging studies implicate the anterior insula and pre/subgenual ACC in emotional processes, the mid-posterior insula with awareness and interoception, and the MCC with environmental monitoring, response selection, and skeletomotor body orientation. Here, we tested the hypothesis that distinct resting state functional connectivity could be identified between (1) the anterior insula and pACC/aMCC; and (2) the entire insula (anterior, middle, and posterior insula) and the pMCC. Functional connectivity was assessed from resting state fMRI scans in 19 healthy volunteers using seed regions of interest in the anterior, middle, and posterior insula. Highly correlated, low-frequency oscillations (< 0.05 Hz) were identified between specific insula and cingulate subdivisions. The anterior insula was shown to be functionally connected with the pACC/aMCC and the pMCC, while the mid/posterior insula was only connected with the pMCC. These data provide evidence for a resting state anterior insula-pACC/aMCC cingulate system that may integrate interoceptive information with emotional salience to form a subjective representation of the body; and another system that includes the entire insula and MCC, likely involved in environmental monitoring, response selection, and skeletomotor body orientation.

Neuroimaging research has demonstrated that ventromedial prefrontal cortex (vmPFC) encodes value signals that can be modulated by top-down cognitive input such as semantic knowledge, price incentives, and monetary favors suggesting that such biases may have an identified biological basis. It has been hypothesized that mindfulness training (MT) provides one path for gaining control over such top-down influences; yet, there have been no direct tests of this hypothesis. Here, we probe the behavioral and neural effects of MT on value signals in vmPFC in a randomized longitudinal design of 8 weeks of MT on an initially naïve subject cohort. The impact of this within-subject training was assessed using two paradigms: one that employed primary rewards (fruit juice) in a simple conditioning task and another that used a well-validated art-viewing paradigm to test bias of monetary favors on preference. We show that MT behaviorally censors the top-down bias of monetary favors through a measurable influence on value signals in vmPFC. MT also modulates value signals in vmPFC to primary reward delivery. Using a separate cohort of subjects we show that 8 weeks of active control training (ACT) generates the same behavioral impact also through an effect on signals in the vmPFC. Importantly, functional connectivity analyses show that value signals in vmPFC are coupled with bilateral posterior insula in the MT groups in both paradigms, but not in the ACT groups. These results suggest that MT integrates interoceptive input from insular cortex in the context of value computations of both primary and secondary rewards.

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Affiliation Details

  • Department of Psychiatry, University of California, San Diego, CA, USA, Warfighter Performance Department, Navel Health Research Center, San Diego, CA, USA.
  • Department of Psychiatry
Affiliation Department of Psychiatry, University of California, San Diego, CA, USA, Warfighter Performance Department, Navel Health Research Center, San Diego, CA, USA.