Neural mechanisms of attentional control in mindfulness meditation

Peter Malinowski, Peter Malinowski

Abstract

The scientific interest in meditation and mindfulness practice has recently seen an unprecedented surge. After an initial phase of presenting beneficial effects of mindfulness practice in various domains, research is now seeking to unravel the underlying psychological and neurophysiological mechanisms. Advances in understanding these processes are required for improving and fine-tuning mindfulness-based interventions that target specific conditions such as eating disorders or attention deficit hyperactivity disorders. This review presents a theoretical framework that emphasizes the central role of attentional control mechanisms in the development of mindfulness skills. It discusses the phenomenological level of experience during meditation, the different attentional functions that are involved, and relates these to the brain networks that subserve these functions. On the basis of currently available empirical evidence specific processes as to how attention exerts its positive influence are considered and it is concluded that meditation practice appears to positively impact attentional functions by improving resource allocation processes. As a result, attentional resources are allocated more fully during early processing phases which subsequently enhance further processing. Neural changes resulting from a pure form of mindfulness practice that is central to most mindfulness programs are considered from the perspective that they constitute a useful reference point for future research. Furthermore, possible interrelations between the improvement of attentional control and emotion regulation skills are discussed.

Keywords: Stroop; attention; attentional control; meditation; mindfulness.

Figures

Figure 1
Figure 1
The Liverpool Mindfulness Model.
Figure 2
Figure 2
Effortful attention regulation during meditation. Panel (A) provides a schematic representation of the meditation process. The inner circle outlines the phenomenological layer, presenting the typical sequence (clockwise) a meditator will go through. The middle circle relates the attentional processes that lie underneath, while the outer circle represents the different brain networks that are involved in carrying out these functions. The different attentional processes and the brain networks are represented as partially overlapping to indicate that in many instances more than one process/network is involved. Panel (B) outlines the main brain areas involved in each of the five networks. Anatomical details are discussed in the main text.
Figure 3
Figure 3
Behavioral and ERP results from the Stroop task as a function of meditation practice. (A) Performance differences between meditators and non-meditators in a cross-sectional comparison (Moore and Malinowski, 2009). (B) Outline of the Stroop task. (C) and (D) Results from a longitudinal study (Moore et al., 2012) showing effects of meditation training on ERPs during the Stroop task for the N2 (C) and P3 (D) ERP components. The glass brain slices show activation differences between T1 and T3 for each group and congruency. Salmon-colored areas indicate a decrease in activation and green areas indicate activation increase. On the right hand side ERPs (line graphs) and ERP-component amplitudes (bar graphs) are depicted for left and right posterior sites (C) and for posterior central sites (D).

References

    1. Aarts E., Roelofs A., Van Turennout M. (2008). Anticipatory activity in anterior cingulate cortex can be independent of conflict and error likelihood. J. Neurosci. 28, 4671–4678 10.1523/JNEUROSCI.4400-07.2008
    1. Adorni R., Proverbio A. M. (2009). New insights into name category-related effects: is the age of acquisition a possible factor? Behav. Brain Funct. 5:33 10.1186/1744-9081-5-33
    1. Allen M., Dietz M., Blair K. S., Van Beek M., Rees G., Vestergaard-Poulsen P., et al. (2012). Cognitive-affective neural plasticity following active-controlled mindfulness intervention. J. Neurosci. 32, 15601–15610 10.1523/JNEUROSCI.2957-12.2012
    1. Anderson N. D., Lau M. A., Segal Z. V., Bishop S. R. (2007). Mindfulness-based stress reduction and attentional control. Clin. Psychol. Psychother. 14, 449–463
    1. Baron Short E., Kose S., Mu Q., Borckardt J., Newberg A., George M. S., et al. (2010). Regional brain activation during meditation shows time and practice effects: an exploratory FMRI study. Evid. Based Complement. Alternat. Med. 7, 121–127 10.1093/ecam/nem163
    1. Bishop S. R., Lau M. A., Shapiro S. L., Carlson L. E., Anderson N. D., Carmody J., et al. (2004). Mindfulness: a proposed operational definition. Clin. Psychol. Sci. Pract. 11, 230–242
    1. Boroojerdi B., Bushara K. O., Corwell B., Immisch I., Battaglia F., Muellbacher W., et al. (2000). Enhanced excitability of the human visual cortex induced by short-term light deprivation. Cereb. Cortex 10, 529–534 10.1093/cercor/10.5.529
    1. Brefczynski-Lewis J. A., Lutz A., Schaefer H. S., Levinson D. B., Davidson R. J. (2007). Neural correlates of attentional expertise in long-term meditation practitioners. Proc. Natl. Acad. Sci. U.S.A. 104, 11483–11488 10.1073/pnas.0606552104
    1. Brickenkamp R., Zilmer E. (1998). D2 Test of Attention: Manual. Oxford: Hogrefe and Huber
    1. Brown K. W., Ryan R. M., Creswell J. D. (2007). Mindfulness: theoretical foundations and evidence for its salutary effects. Psychol. Inq. 18, 211–237
    1. Buckner R. L., Andrews-Hanna J. R., Schacter D. L. (2008). The brain's default network: anatomy, function, and relevance to disease. Ann. N.Y. Acad. Sci. 1124, 1–38 10.1196/annals.1440.011
    1. Cardaciotto L., Herbert J. D., Forman E. M., Moitra E., Farrow V. (2008). The assessment of present-moment awareness and acceptance: the Philadelphia Mindfulness Scale. Assessment 15, 204–223 10.1177/1073191107311467
    1. Chan D., Woollacott M. (2007). Effects of level of meditation experience on attentional focus: is the efficiency of executive or orientation networks improved? J. Altern. Complement. Med. 13, 651–657 10.1089/acm.2007.7022
    1. Chiesa A., Malinowski P. (2011). Mindfulness based interventions: are they all the same? J. Clin. Psychol. 67, 404–424 10.1002/jclp.20776
    1. Cohen L., Dehaene S. (2004). Specialization within the ventral stream: the case for the visual word form area. Neuroimage 22, 466–476 10.1016/j.neuroimage.2003.12.049
    1. Cohen L., Lehericy S., Chochon F., Lemer C., Rivaud S., Dehaene S. (2002). Language-specific tuning of visual cortex? Functional properties of the visual word form area. Brain 125, 1054–1069 10.1093/brain/awf094
    1. Conners C. K. (2000). Continuous Performance Test II: Technical Guide and Software Manual. Toronto, ON: Multi-Health Systems
    1. Corbetta M., Shulman G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–215 10.1038/nrn755
    1. Davis L., Kurzban S. (2012). Mindfulness-based treatment for people with severe mental illness: a literature review. Am. J. Psychiatr. Rehabil. 15, 202–232
    1. Dosenbach N. U., Fair D. A., Miezin F. M., Cohen A. L., Wenger K. K., Dosenbach R. A., et al. (2007). Distinct brain networks for adaptive and stable task control in humans. Proc. Natl. Acad. Sci. U.S.A. 104, 11073–11078 10.1073/pnas.0704320104
    1. Dosenbach N. U., Visscher K. M., Palmer E. D., Miezin F. M., Wenger K. K., Kang H. C., et al. (2006). A core system for the implementation of task sets. Neuron 50, 799–812 10.1016/j.neuron.2006.04.031
    1. Eimer M. (1997). An event-related potential (ERP) study of transient and sustained visual attention to color and form. Biol. Psychol. 44, 143–160 10.1016/S0301-0511(96)05217-9
    1. Falkenstein M., Hoormann J., Christ S., Hohnsbein J. (2000). ERP components on reaction errors and their functional significance: a tutorial. Biol. Psychol. 51, 87–107 10.1016/S0301-0511(99)00031-9
    1. Fan J., McCandliss B. D., Fossella J., Flombaum J. I., Posner M. I. (2005). The activation of attentional networks. Neuroimage 26, 471–479 10.1016/j.neuroimage.2005.02.004
    1. Fan J., McCandliss B. D., Sommer T., Raz A., Posner M. I. (2002). Testing the efficiency and independence of attentional networks. J. Cogn. Neurosci. 14, 340–347 10.1162/089892902317361886
    1. Ganushchak L. Y., Schiller N. O. (2008). Motivation and semantic context affect brain error-monitoring activity: an event-related brain potentials study. Neuroimage 39, 395–405 10.1016/j.neuroimage.2007.09.001
    1. Grossman P., Niemann L., Schmidt S., Walach H. (2004). Mindfulness-based stress reduction and health benefits A meta-analysis. J. Psychosom. Res. 57, 35–43 10.1016/S0022-3999(03)00573-7
    1. Hanslmayr S., Pastotter B., Bauml K. H., Gruber S., Wimber M., Klimesch W. (2008). The electrophysiological dynamics of interference during the Stroop task. J. Cogn. Neurosci. 20, 215–225 10.1162/jocn.2008.20020
    1. Hasenkamp W., Wilson-Mendenhall C. D., Duncan E., Barsalou L. W. (2012). Mind wandering and attention during focused meditation: a fine-grained temporal analysis of fluctuating cognitive states. Neuroimage 59, 750–760 10.1016/j.neuroimage.2011.07.008
    1. Hölzel B. K., Lazar S. W., Gard T., Schuman-Olivier Z., Vago D. R., Ott U. (2011). How does mindfulness meditation work? Proposing mechanisms of action from a conceptual and neural perspective. Perspect. Psychol. Sci. 6, 537–559
    1. Jha A. P., Krompinger J., Baime M. J. (2007). Mindfulness training modifies subsystems of attention. Cogn. Affect. Behav. Neurosci. 7, 109–119
    1. Kabat-Zinn J. (2003). Mindfulness-based interventions in context: past, present, and future. Clin. Psychol. Sci. Pract. 10, 144–156
    1. Kabat-Zinn J. (2011). Some reflections on the origins of MBSR, skillful means, and the trouble with maps. Contemp. Buddh. Interdiscipl. J. 12, 281–306
    1. Kabat-Zinn J., Lipworth L., Burney R. (1985). The clinical use of mindfulness meditation for the self-regulation of chronic pain. J. Behav. Med. 8, 163–190
    1. Kabat-Zinn J., Massion A. O., Kristeller J. L., Peterson L. G., Fletcher K. E., Pbert L., et al. (1992). Effectiveness of a meditation-based stress reduction program in the treatment of anxiety disorders. Am. J. Psychiatry 149, 936–943
    1. Kozasa E. H., Sato J. R., Lacerda S. S., Barreiros M. A., Radvany J., Russell T. A., et al. (2012). Meditation training increases brain efficiency in an attention task. Neuroimage 59, 745–749 10.1016/j.neuroimage.2011.06.088
    1. Kristeller J. L., Wolever R. Q. (2011). Mindfulness-based eating awareness training for treating binge eating disorder: the conceptual foundation. Eat. Disord. 19, 49–61 10.1080/10640266.2011.533605
    1. Kuyken W., Byford S., Taylor R. S., Watkins E., Holden E., White K., et al. (2008). Mindfulness-based cognitive therapy to prevent relapse in recurrent depression. J. Consult. Clin. Psychol. 76, 966–978 10.1037/a0013786
    1. Liotti M., Woldorff M. G., Perez R., Mayberg H. S. (2000). An ERP study of the temporal course of the Stroop color-word interference effect. Neuropsychologia 38, 701–711 10.1016/S0028-3932(99)00106-2
    1. Lutz A., Slagter H. A., Dunne J. D., Davidson R. J. (2008). Attention regulation and monitoring in meditation. Trends Cogn. Sci. 12, 163–169 10.1016/j.tics.2008.01.005
    1. Macleod C. M. (1991). Half a century of research on the Stroop effect: an integrative review. Psychol. Bull. 109, 163–203
    1. Malinowski P. (2008). Mindfulness as psychological dimension: concepts and applications. Irish J. Psychol. 29, 155–166
    1. Malinowski P. (2012). Wirkmechanismen der Achtsamkeitspraxis. Wie fördert Meditation positive psychologische Veränderungen? [Mechanisms of mindfulness. How meditation fosters positive psychological change], in Achtsamkeit: Ein buddhistisches Konzept erobert die Wissenschaft [Mindfulness: A Buddhist concept conquers science], eds Zimmermann M., Spitz C., Schmidt S. (Berlin: Hans Huber; ), 91–100
    1. Malinowski P. (2013). Flourishing through meditation and mindfulness, in Oxford Handbook of Happiness, eds David S., Boniwell I., Conley Ayers A. (Oxford: Oxford University Press; ), 384–396
    1. Marois R., Ivanoff J. (2005). Capacity limits of information processing in the brain. Trends Cogn. Sci. 9, 296–305 10.1016/j.tics.2005.04.010
    1. Mason M. F., Norton M. I., Van Horn J. D., Wegner D. M., Grafton S. T., Macrae C. N. (2007). Wandering minds: the default network and stimulus-independent thought. Science 315, 393–395 10.1126/science.1131295
    1. Miyake A., Friedman N. P., Emerson M. J., Witzki A. H., Howerter A., Wager T. D. (2000). The unity and diversity of executive functions and their contributions to complex “Frontal Lobe” tasks: a latent variable analysis. Cogn. Psychol. 41, 49–100 10.1006/cogp.1999.0734
    1. Moore A., Gruber T., Derose J., Malinowski P. (2012). Regular, brief mindfulness meditation practice improves electrophysiological markers of attentional control. Front. Hum. Neurosci. 6:18 10.3389/fnhum.2012.00018
    1. Moore A., Malinowski P. (2009). Meditation, mindfulness and cognitive flexibility. Conscious. Cogn. 18, 176–186 10.1016/j.concog.2008.12.008
    1. Pagnoni G., Cekic M. (2007). Age effects on gray matter volume and attentional performance in Zen meditation. Neurobiol. Aging 28, 1623–1627 10.1016/j.neurobiolaging.2007.06.008
    1. Pitskel N. B., Merabet L. B., Ramos-Estebanez C., Kauffman T., Pascual-Leone A. (2007). Time-dependent changes in cortical excitability after prolonged visual deprivation. Neuroreport 18, 1703–1707 10.1097/WNR.0b013e3282f0d2c1
    1. Polich J. (2007). Updating P300: an integrative theory of P3a and P3b. Clin. Neurophysiol. 118, 2128–2148 10.1016/j.clinph.2007.04.019
    1. Posner M. I., Petersen S. E. (1990). The attention system of the human brain. Annu. Rev. Neurosci. 13, 25–42 10.1146/annurev.ne.13.030190.000325
    1. Posner M. I., Rothbart M. K. (2007). Research on attention networks as a model for the integration of psychological science. Annu. Rev. Psychol. 58, 1–23 10.1146/annurev.psych.58.110405.085516
    1. Raz A., Buhle J. (2006). Typologies of attentional networks. Nat. Rev. Neurosci. 7, 367–379 10.1038/nrn1903
    1. Robertson I. H., Manly T., Andrade J., Baddeley B. T., Yiend J. (1997). ‘Oops!’: performance correlates of everyday attentional failures in traumatic brain injured and normal subjects. Neuropsychologia 35, 747–758 10.1016/S0028-3932(97)00015-8
    1. Roelofs A., Van Turennout M., Coles M. G. (2006). Anterior cingulate cortex activity can be independent of response conflict in Stroop-like tasks. Proc. Natl. Acad. Sci. U.S.A. 103, 13884–13889 10.1073/pnas.0606265103
    1. Sahdra B. K., Maclean K. A., Ferrer E., Shaver P. R., Rosenberg E. L., Jacobs T. L., et al. (2011). Enhanced response inhibition during intensive meditation training predicts improvements in self-reported adaptive socioemotional functioning. Emotion 11, 299–312 10.1037/a0022764
    1. Schmertz S. K., Anderson P. L., Robins D. L. (2008). The relation between self-report mindfulness and performance on tasks of sustained attention. J. Psychopathol. Behav. Assess. 31, 60–66
    1. Schooler J. W., Smallwood J., Christoff K., Handy T. C., Reichle E. D., Sayette M. A. (2011). Meta-awareness, perceptual decoupling and the wandering mind. Trends Cogn. Sci. 15, 319–326 10.1016/j.tics.2011.05.006
    1. Seeley W. W., Menon V., Schatzberg A. F., Keller J., Glover G. H., Kenna H., et al. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 27, 2349–2356 10.1523/JNEUROSCI.5587-06.2007
    1. Shapiro K. L., Arnell K. M., Raymond J. E. (1997). The attentional blink. Trends Cogn. Sci. 1, 219–296
    1. Shapiro S. L., Carlson L. E., Astin J. A., Freedman B. (2006). Mechanisms of mindfulness. J. Clin. Psychol. 62, 373–386 10.1002/jclp.20237
    1. Shaywitz B. A., Shaywitz S. E., Blachman B. A., Pugh K. R., Fulbright R. K., Skudlarski P., et al. (2004). Development of left occipitotemporal systems for skilled reading in children after a phonologically- based intervention. Biol. Psychiatry 55, 926–933 10.1016/j.biopsych.2003.12.019
    1. Slagter H. A., Davidson R. J., Lutz A. (2011). Mental training as a tool in the neuroscientific study of brain and cognitive plasticity. Front. Hum. Neurosci. 5:17 10.3389/fnhum.2011.00017
    1. Slagter H. A., Lutz A., Greischar L. L., Francis A. D., Nieuwenhuis S., Davis J. M., et al. (2007). Mental training affects distribution of limited brain resources. PLoS Biol. 5:e138 10.1371/journal.pbio.0050138
    1. Slagter H. A., Lutz A., Greischar L. L., Nieuwenhuis S., Davidson R. J. (2009). Theta phase synchrony and conscious target perception: impact of intensive mental training. J. Cogn. Neurosci. 21, 1536–1549 10.1162/jocn.2009.21125
    1. Sridharan D., Levitin D. J., Menon V. (2008). A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc. Natl. Acad. Sci. U.S.A. 105, 12569–12574 10.1073/pnas.0800005105
    1. Stroop J. R. (1935). Studies of interference in serial verbal reactions. J. Exp. Psychol. 18, 643–661
    1. Suedfeld P. (1975). Society The Benefits of Boredom: sensory Deprivation Reconsidered: the effects of a monotonousenvironment are not always negative; sometimes sensory deprivation has high utility. Am. Sci. 63, 60–69
    1. Tang Y. Y., Ma Y., Wang J., Fan Y., Feng S., Lu Q., et al. (2007). Short-term meditation training improves attention and self-regulation. Proc. Natl. Acad. Sci. U.S.A. 104, 17152–17156 10.1073/pnas.0707678104
    1. Tang Y. Y., Posner M. I. (2009). Attention training and attention state training. Trends Cogn. Sci. 13, 222–227 10.1016/j.tics.2009.01.009
    1. Tang Y. Y., Rothbart M. K., Posner M. I. (2012). Neural correlates of establishing, maintaining, and switching brain states. Trends Cogn. Sci. 16, 330–337 10.1016/j.tics.2012.05.001
    1. Teper R., Inzlicht M. (2013). Meditation, mindfulness and executive control: the importance of emotional acceptance and brain-based performance monitoring. Soc. Cogn. Affect. Neurosci. 8, 85–92 10.1093/scan/nss045
    1. Valentine E. R., Sweet P. L. G. (1999). Meditation and attention: a comparison of the effects of concentrative and mindfulness meditation on sustained attention. Ment. Health Relig. Cult. 2, 59–70
    1. Wallace B. A. (1999). The Buddhist tradition of samatha: methods for refining and examining consciousness. J. Conscious. Stud. 6, 175–187
    1. Wallace B. A. (2006). The Attention Revolution: Unlocking the Power of the Focused Mind. Somerville, MA: Wisdom Books
    1. Wallace B. A., Shapiro S. (2006). Mental balance and well-being: building bridges between Buddhism and Western Psychology. Am. Psychol. 61, 690–701 10.1037/0003-066X.61.7.690
    1. Weinberg A., Riesel A., Hajcak G. (2012). Integrating multiple perspectives on error-related brain activity: the ERN as a neural indicator of trait defensive reactivity. Motiv. Emot. 36, 84–100
    1. Wenk-Sormaz H. (2005). Meditation can reduce habitual responding. Altern. Ther. Health Med. 11, 42–58
    1. Wickens C., Kramer A., Vanasse L., Donchin E. (1983). Performance of concurrent tasks: a psychophysiological analysis of the reciprocity of information-processing resources. Science 221, 1080–1082 10.1126/science.6879207
    1. Yeung N., Botvinick M. M., Cohen J. D. (2004). The neural basis of error detection: conflict monitoring and the Error-Related Negativity. Psychol. Rev. 111, 931–959 10.1037/0033-295X.111.4.939
    1. Zylowska L., Ackerman D. L., Yang M. H., Futrell J. L., Horton N. L., Hale T. S., et al. (2008). Mindfulness meditation training in adults and adolescents with ADHD: a feasibility study. J. Atten. Disord. 11, 737–746 10.1177/1087054707308502

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