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Mindfulness-based training attenuates insula response to an aversive interoceptive challenge.
Open accessAbstract
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.
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“The insula is associated with greater dispositional mindfulness (Creswell et al., 2007; Murakami et al., 2012; Haase et al., 2016), and studies have consistently shown that mindfulness is linked with increased cortical thickness in the aINS (Farb et al., 2007, 2013, 2015; Paulus et al., 2011; Haase et al., 2016).”
From Mindfulness, Interoception, and the Body: A Contemporary Perspective (2019) · cites this paper as Haase et al., 2016
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“Controlled, rhythmic breathing provides a stream of sensory information that has an affective component (Davenport and Vovk, 2009; Haase et al., 2016).”
From Mindfulness, Interoception, and the Body: A Contemporary Perspective (2019) · cites this paper as Haase et al., 2016
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“Attenuation of the right anterior insula and ACC was related to the loaded breathing task (Haase et al., 2014).”
From Enhanced Resting-State Functional Connectivity With Decreased Amplitude of Low-Frequency Fluctuations of the Salience Network in Mindfulness Novices (2022) · cites this paper as Haase et al., 2014
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“Additionally, several studies have documented posterior cingulate cortex and medial prefrontal cortex deactivation in experienced meditators (Brewer et al., 2011, 2013; Taylor et al., 2011; Pagnoni, 2012), suggesting multiple brain regions are actively involved during meditation practices.”
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Mindfulness training affects attention—Or is it attentional effort?
Jensen, C. G., Vangkilde, S., Frokjaer, V., & Hasselbalch, S. G. (2012) · Journal of Experimental Psychology: General · doi:10.1037/a0024931 · Cited by 284 · cited 1×
“Research has shown that individuals who undergo meditation training show improved attention (Wenk-Sormaz, 2005; Jha et al., 2007; Tang et al., 2007; Jensen et al., 2012).”
BackgroundNeural correlates of establishing, maintaining, and switching brain states
Tang, Y., Rothbart, M. K., & Posner, M. I. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.05.001 · Cited by 271 · cited 2×
“…Kang et al., 2013) and functional (Cahn and Polich, 2006; Brefczynski-Lewis et al., 2007; Farb et al., 2007; IvesDeliperi et al., 2011; Zeidan et al., 2011; Tang et al., 2012; Dickenson et al., 2013) brain changes are associated with MT, particularly in the insula, ACC and prefrontal cortices.”
BackgroundCommentary and Opinion: II. Statistical Parametric Mapping: Ontology and Current Issues
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“, 1996) that modeled the prototypical 6–8 s delay hemodynamic response function (Friston, 1995) and the temporal dynamics of the hemodynamic response (typically 12–16 s; Cohen, 1997).”
BackgroundMethodWhat about the “Self” is Processed in the Posterior Cingulate Cortex?
Brewer, J. A., Garrison, K. A., & Whitfield-Gabrieli, S. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00647 · Cited by 263
Waugh, C. E., Fredrickson, B. L., & Taylor, S. F. (2008) · Journal of Research in Personality · doi:10.1016/j.jrp.2008.02.005 · Cited by 245 · cited 2×
“…towards positive emotions when faced with uncertain or negative emotions (Tugade and Fredrickson, 2004; Arce et al., 2009) and these individuals demonstrate faster recovery following the anticipation of an aversive stimulus (Waugh et al., 2008a), which may contribute to increased coping abilities.”
BackgroundKok, B. C., Herrell, R. K., Thomas, J. L., & Hoge, C. W. (2012) · Journal of Nervous & Mental Disease · doi:10.1097/nmd.0b013e3182532312 · Cited by 238 · cited 2×
“2% of operational infantry units following deployment to Iraqi and Afghanistan meet criteria for post-traumatic stress disorder (Kok et al., 2012).”
BackgroundInfluentialCortical and subcortical central neural pathways in respiratory sensations
Davenport, P. W., & Vovk, A. (2009) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2008.10.001 · Cited by 235 · cited 2×
“what is sensed) and affective information (i.e. how it feels; Davenport and Vovk, 2009).”
BackgroundJohnson, D. C., Thom, N. J., Stanley, E. A., Haase, L., Simmons, A. N., Shih, P.-A. B., Thompson, W. K., Potterat, E. G., Minor, T. R., & Paulus, M. P. (2014) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2014.13040502 · Cited by 227
Anterior insular cortex mediates bodily sensibility and social anxiety
Terasawa, Y., Shibata, M., Moriguchi, Y., & Umeda, S. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nss108 · Cited by 224 · cited 1×
“Activation in the anterior insula is associated with interoceptive awareness and level of anxiety, such that the level of attention to interoceptive body states was associated with increased levels of anxiety (Terasawa et al., 2013).”
BackgroundThe effect of meditation on brain structure: cortical thickness mapping and diffusion tensor imaging
Kang, D.-H., Jo, H. J., Jung, W. H., Kim, S. H., Jung, Y.-H., Choi, C.-H., Lee, U. S., An, S. C., Jang, J. H., & Kwon, J. S. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nss056 · Cited by 224 · cited 2×
“There is converging evidence to suggest anatomical (Lazar et al., 2005; Holzel et al., 2008; Grant et al., 2010; Kang et al., 2013) and functional (Cahn and Polich, 2006; Brefczynski-Lewis et al.”
BackgroundNeural correlates of focused attention during a brief mindfulness induction
Dickenson, J., Berkman, E. T., Arch, J., & Lieberman, M. D. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nss030 · Cited by 224 · cited 2×
“…Kang et al., 2013) and functional (Cahn and Polich, 2006; Brefczynski-Lewis et al., 2007; Farb et al., 2007; IvesDeliperi et al., 2011; Zeidan et al., 2011; Tang et al., 2012; Dickenson et al., 2013) brain changes are associated with MT, particularly in the insula, ACC and prefrontal cortices.”
BackgroundMcLean, C. P., & Foa, E. B. (2011) · Expert Review of Neurotherapeutics · doi:10.1586/ern.11.94 · Cited by 199 · cited 3×
“Post-traumatic stress disorder (PTSD)), such as cognitive processing therapy (CPT) (Resick and Schnicke, 1992) and prolonged exposure (McLean and Foa, 2011), MBSR is an evidence-based therapy that can be initiated prior to trauma exposure and thus may have potential as a preventative method.”
BackgroundThe neural substrates of mindfulness: An fMRI investigation
Ives-Deliperi, V. L., Solms, M., & Meintjes, E. M. (2010) · Social Neuroscience · doi:10.1080/17470919.2010.513495 · Cited by 194 · cited 1×
“, 2013) and functional (Cahn and Polich, 2006; Brefczynski-Lewis et al., 2007; Farb et al., 2007; Ives-Deliperi et al., 2011; Zeidan et al., 2011; Tang et al., 2012; Dickenson et al., 2013) brain changes are associated with MT, particularly in the insula, ACC and prefrontal cortices.”
BackgroundThe neural correlates of trait resilience when anticipating and recovering from threat
Waugh, C. E., Wager, T. D., Fredrickson, B. L., Noll, D. C., & Taylor, S. F. (2008) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsn024 · Cited by 180 · cited 3×
“…towards positive emotions when faced with uncertain or negative emotions (Tugade and Fredrickson, 2004; Arce et al., 2009) and these individuals demonstrate faster recovery following the anticipation of an aversive stimulus (Waugh et al., 2008a), which may contribute to increased coping abilities.”
BackgroundDevelopment and initial validation of the Response to Stressful Experiences Scale.
Johnson, D. C., Polusny, M. A., Erbes, C. R., King, D., King, L., Litz, B., Schnurr, P., Friedman, M., Pietrzak, R., & Southwick, S. (2011) · Military Medicine · doi:10.7205/milmed-d-10-00258 · Cited by 158 · cited 2×
“, 2006), designed to measure the five primary facets of mindfulness (observing, describing, acting with awareness, non-judging of inner experience and non-reactivity to inner experience); response to stressful experiences scale (RSES; Johnson et al., 2011) designed to measure six-processes that promote resilient respo…”
BackgroundA neuroscience approach to optimizing brain resources for human performance in extreme environments☆
Paulus, M. P., Potterat, E. G., Taylor, M. K., Orden, K. F. V., Bauman, J., Momen, N., Padilla, G. A., & Swain, J. L. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.05.003 · Cited by 146 · cited 2×
“Specifically, one approach is to improve interoception (Craig, 2002), that is, the processing of the body’s internal state and in particular the perturbation of this state as a result of external demands when an individual has to maintain goal-directed action and homeostatic balance (Paulus et al., 2009).”
BackgroundGreen, K. T., Calhoun, P. S., Dennis, M. F., & Beckham, J. C. (2010) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.09m05780blu · Cited by 121 · cited 2×
“…conceptualized as one’s ability to positively adapt to severe stress, trauma and adversity (Luthar et al., 2000), that may help to prevent the development of psychopathology (Campbell-Sills et al., 2006), particularly in individuals with combat exposure (Pietrzak et al., 2009; Green et al., 2010).”
BackgroundPagnoni, G. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.4135-11.2012 · Cited by 107 · cited 2×
“Additionally, several studies have documented posterior cingulate cortex and medial prefrontal cortex deactivation in experienced meditators (Brewer et al., 2011, 2013; Taylor et al., 2011; Pagnoni, 2012), suggesting multiple brain regions are actively involved during meditation practices.”
BackgroundPaulus, M. P., Flagan, T., Simmons, A. N., Gillis, K., Kotturi, S., Thom, N., Johnson, D. C., Van Orden, K. F., Davenport, P. W., & Swain, J. L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029394 · Cited by 100 · cited 7×
“In the support of this proposal, we have previously shown that highly resilient individuals, such as elite adventure racers (Paulus et al., 2012) and US NAVY Sea, Air and Land Forces (Simmons et al.”
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Fonzo, G. A., Flagan, T., Sullivan, S. A., Allard, C. B., Grimes, E. M., Simmons, A. N., Paulus, M. P., & Stein, M. B. (2012) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2012.08.006 · Cited by 89 · cited 2×
“…by guest on 30 July 2018 defined ROIs were constructed using a data-driven approach that combined Talairach stereotactic definition and grey matter probabilities based on high resolution T1 images from a group of 43 healthy adults (Fonzo et al., 2013).”
MethodThe impact of anxiety on the neural processing of respiratory sensations
von Leupoldt, A., Chan, P.-Y. S., Bradley, M. M., Lang, P. J., & Davenport, P. W. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.11.050 · Cited by 80 · cited 3×
“Affective reactions to breathing changes are experienced as equally or more aversive than negative visual stimuli (Pappens et al., 2010), and can serve as a source of threat, leading to increased anxiety (von Leupoldt et al., 2011).”
BackgroundGottfried, S. B., Altose, M. D., Kelsen, S. G., Fogarty, C. M., & Cherniack, N. S. (1978) · CHEST Journal · doi:10.1378/chest.73.2_supplement.286 · Cited by 57 · cited 1×
“One effective method of inducing experimental breathing change is through loaded inspiratory breathing, which can be operationally defined as the degree to which an individual experiences resistance during inspiration (Lopata et al., 1977; Gottfried et al., 1978).”
MethodEffects of flow-resistive loading on mouth occlusion pressure during CO2 rebreathing.
Lopata, M., Fata, J. L., Evanich, M. J., & Lourenço, R. V. (1977) · PubMed · doi:10.1164/arrd.1977.115.1.73 · Cited by 55 · cited 2×
“One effective method of inducing experimental breathing change is through loaded inspiratory breathing, which can be operationally defined as the degree to which an individual experiences resistance during inspiration (Lopata et al., 1977; Gottfried et al., 1978).”
MethodArce, E., Simmons, A. N., Stein, M. B., Winkielman, P., Hitchcock, C. A., & Paulus, M. P. (2008) · Journal of Affective Disorders · doi:10.1016/j.jad.2008.08.015 · Cited by 53 · cited 2×
“…resilience are associated with a bias towards positive emotions when faced with uncertain or negative emotions (Tugade and Fredrickson, 2004; Arce et al., 2009) and these individuals demonstrate faster recovery following the anticipation of an aversive stimulus (Waugh et al., 2008a), which…”
BackgroundThe Wiley Blackwell handbook of mindfulness
Ie, A., Ngnoumen, C. T., & Langer, E. J. (2014) · Wiley-Blackwell eBooks · Cited by 45
Paulus, M. P., Simmons, A. N., Fitzpatrick, S. N., Potterat, E. G., Orden, K. F. V., Bauman, J., & Swain, J. L. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010096 · Cited by 45 · cited 3×
“Moreover, self-reported resilience during emotion processing task is associated with differential activation of insula, ACC and amygdala (Waugh et al., 2008b; Paulus et al., 2010).”
BackgroundPappens, M., den Bergh, O. V., Peuter, S. D., Bresseleers, J., Vansteenwegen, D., & Diest, I. V. (2010) · Biological Psychology · doi:10.1016/j.biopsycho.2010.02.006 · Cited by 36 · cited 4×
“Affective reactions to breathing changes are experienced as equally or more aversive than negative visual stimuli (Pappens et al., 2010) and can serve as a source of threat, leading to increased anxiety (von Leupoldt et al.”
BackgroundInfluentialRespiration, metabolic balance, and attention in affective picture processing.
Gomez, P., Shafy, S., & Danuser, B. (2008) · Biological Psychology · doi:10.1016/j.biopsycho.2008.01.013 · Cited by 34 · cited 2×
“…breathing loads are organized along the dimensions of valence and arousal, and represent a homeostatic balance between metabolic activity and affective arousal (Gomez et al., 2008) are experienced as aversive (Pappens et al., 2010), and can result in increased anxiety (von Leupoldt et al., 2011).”
BackgroundNeural correlates of anxiety sensitivity during masked presentation of affective faces
Killgore, W. D. S., Britton, J. C., Price, L. M., Gold, A. L., Deckersbach, T., & Rauch, S. L. (2011) · Depression and Anxiety · doi:10.1002/da.20788 · Cited by 33 · cited 1×
“Self-reported anxiety, particularly concerns regarding the physical features of anxiety, is associated with increased anterior insula activation in response to negatively valenced stimuli (Killgore et al., 2011).”
BackgroundAltered insula activation in anticipation of changing emotional states
Simmons, A. N., Fitzpatrick, S. N., Strigo, I. A., Potterat, E. G., Johnson, D. C., Matthews, S. C., Orden, K. F. V., Swain, J. L., & Paulus, M. P. (2012) · Neuroreport · doi:10.1097/wnr.0b013e3283503275 · Cited by 29 · cited 5×
“, 2012) and US NAVY Sea, Air and Land Forces (Simmons et al., 2012), demonstrate improved performance and attenuated insular activation during an aversive interoceptive breathing and emotion detection tasks.”
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Thom, N. J., Johnson, D. C., Flagan, T., Simmons, A. N., Kotturi, S., Orden, K. F. V., Potterat, E. G., Swain, J. L., & Paulus, M. P. (2012) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nss127 · Cited by 26 · cited 2×
“, elite athletes and special operations forces) and demonstrated differential activation of the insula and ACC in response to emotional processing and loaded inspiratory breathing (Paulus et al., 2010, 2012; Simmons et al., 2012; Thom et al., 2012).”
BackgroundStanley, E. A. (2014) · Wiley eBooks · doi:10.1002/9781118294895.ch50 · Cited by 25 · cited 1×
“See Stanley (2014) for details.”
Hayen, A., Herigstad, M., Kelly, M., Okell, T. W., Murphy, K., Wise, R. G., & Pattinson, K. T. S. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.10.049 · Cited by 24 · cited 2×
“While inspiratory breathing loads (IBL) result in increased activation in the primary and secondary somatosensory cortices and the cerebellum, IBLs do not modulate task-specific brain activation (Hayen et al., 2012).”
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“Breathing is an interoceptive process that is modulated in the periphery through several sensory airway receptors (Adriaensen and Timmermans, 2011) providing continuous sensory information, which provides discriminative (i.”
BackgroundEffect of elastic loading on mouth occlusion pressure during CO2 rebreathing in man.
Shekleton, M., Lopata, M., Evanich, M. J., & Lourenço, R. V. (1976) · PubMed · doi:10.1164/arrd.1976.114.2.341 · Cited by 15
Research works printed but not linked: 2
- 10.1378/chest.73.2.286 · DOI
- 10.1097/00001756-200005150-00041 · DOI · Paper page
Cited by
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Mindfulness Meditation and Psychopathology
Wielgosz, J., Goldberg, S. B., Kral, T. R. A., Dunne, J. D., & Davidson, R. J. (2019) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-021815-093423 · Cited by 435
“One way this may occur is through improved interoception, or the perception of internal bodily states (Farb et al. 2012, 2015), although evidence for MM-related improvements in interoception has been mixed (Farb et al. 2015, Haase et al. 2016, Khalsa et al. 2008).”
BackgroundMindfulness and Behavior Change
Schuman-Olivier, Z., Trombka, M., Lovas, D. A., Brewer, J. A., Vago, D. R., Gawande, R., Dunne, J. P., Lazar, S. W., Loucks, E. B., & Fulwiler, C. (2020) · Harvard Review of Psychiatry · doi:10.1097/hrp.0000000000000277 · Cited by 435
Gotink, R. A., Meijboom, R., Vernooij, M. W., Smits, M., & Hunink, M. G. M. (2016) · Brain and Cognition · doi:10.1016/j.bandc.2016.07.001 · Cited by 338
“Seven studies, however, reported increased activity in relation to mindfulness-based tasks (Creswell et al., 2007; Haase et al., 2015; Haase et al., 2016; Herwig et al., 2010b; Modinos et al., 2010; Murakami et al., 2015; Zeidan et al., 2015).”
BackgroundMindfulness, Interoception, and the Body: A Contemporary Perspective
Gibson, J. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.02012 · Cited by 278
NOW vs LATER brain circuits: implications for obesity and addiction
Volkow, N. D., & Baler, R. D. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.04.002 · Cited by 237
Metadata
- Authors
- Haase, L., Thom, N. J., Shukla, A., Davenport, P. W., Simmons, A. N., Stanley, E. A., Paulus, M. P., & Johnson, D. C.
- Affiliations
- University of California San Diego (US)
- Naval Health Research Center (US)
- University of Florida (US)
- Georgetown University (US)
- Venue
- Social Cognitive and Affective Neuroscience
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-04-08
- Volume
- 11
- Issue
- 1
- Pages
- 182-190
- ISSN
- 1749-5016 (ISSN-L)
- 1749-5024
- PMC
- PMC4692309
- OpenAlex
- W2108033418
- Cited by
- 124
- References
- 94
- Citations by year
- 2026: 6 · 2025: 17 · 2024: 14 · 2023: 8 · 2022: 11 · 2021: 10 · 2020: 10 · 2019: 13 · 2018: 12 · 2017: 4 · 2016: 12 · 2015: 7
- FWCI
- 9.05
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Social Cognitive and Affective Neuroscience (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Defense
- Center of Excellence for Stress and Mental Health
- University of California, San Diego
- Office of Naval Research
- National Institute of Mental Health (T32-MH018399-26, MH018399, T32MH018399)
- Bureau of Medicine and Surgery
- Topics
- Social Sciences › Psychology › Clinical Psychology › Mindfulness and Compassion Interventions
- Health Sciences › Medicine › Psychiatry and Mental health › Psychosomatic Disorders and Their Treatments
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Keywords
- mindfulness training, insula, anterior cingulate cortex, interoception, emotion regulation, attentional control, military personnel, pre-deployment training, deployment stress, resilience
- MeSH terms
- Self-Control, Arousal, Attention, Cerebral Cortex, Dominance, Cerebral, Emotions, Female, Gyrus Cinguli, Humans, Magnetic Resonance Imaging, Male, Military Personnel, Nerve Net, Resilience, Psychological, Young Adult, Mindfulness, Interoception
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