does meditation reduce pain through a unique neural mechanism

3
Journal Club Editor’s Note: These short, critical reviews of recent papers in the Journal, written exclusively by graduate students or postdoctoral fellows, are intended to summarize the important findings of the paper and provide additional insight and commentary. For more information on the format and purpose of the Journal Club, please see http://www.jneurosci.org/misc/ifa_features.shtml. Does Meditation Reduce Pain through a Unique Neural Mechanism? Tim V. Salomons 1 and Aaron Kucyi 1,2 1 Division of Brain, Imaging and Behaviour—Systems Neuroscience, Toronto Western Research Institute, Toronto, Ontario, Canada M5T 2S8, and 2 Institute of Medical Science, University of Toronto, Toronto, Ontario, Canada M5S 1A8 Review of Zeidan et al. The neuroscience of meditative practice has attracted considerable attention, in part be- cause it represents a unique juxtaposition of Western scientific practice and Eastern mys- tical tradition. Beyond cultural interest, however, lies the question of whether such study has clinical/therapeutic relevance. Pain research is an ideal testing ground for this question. Many chronic pain disorders are frustratingly resistant to treatments aimed at eliminating the sensory compo- nent of pain, prompting increased focus on reducing suffering by altering emo- tional and evaluative components of pain. Mindfulness-based meditative practices, which aim to focus attention on present experiences while reducing evaluative and affective responses, appear tailor-made for this task. Several studies have demonstrated bene- ficial effects of mindfulness-based interven- tions for both chronic and acute pain. Most of these have demonstrated effects of mind- fulness on the affective and evaluative com- ponents of pain (McCracken et al., 2007; Morone et al., 2008; Perlman et al., 2010), but some have also demonstrated effects on sensory thresholds (Grant et al., 2010, 2011) and perceived pain intensity (Grant and Ra- inville, 2009). Exploration of the biological mechanisms of such treatments may in- crease our ability to treat pain disorders by enhancing our understanding of endoge- nous pain regulation. Recent studies of healthy long-term meditation practitioners suggest that ex- tensive mental training can result in thick- ening of cortical regions associated with pain processing, including midcingulate cortex (MCC) and primary and secondary somatosensory cortices (Grant et al., 2010). A study of event-related potentials during anticipation of pain found that long-term meditation practice alters an- ticipatory evaluation and processing of pain in MCC and other pain regions (Brown and Jones, 2010). Functional im- aging demonstrated that during pain, practitioners had reduced activation in amygdala, hippocampus, and emotional/ evaluative regions of prefrontal cortex, as well as increased activation in the MCC, thalamus, and insula (Grant et al., 2011). Additionally, altered pain sensitivity was as- sociated with reduced functional connectiv- ity between MCC and dlPFC. Grant et al. (2011) interpreted these findings as consis- tent with the meditative goals of increasing attention to present sensory experience (in this case, pain) while reducing emotional and evaluative responses. Findings from long-term practitioners are of enormous theoretical interest as they demonstrate that intensive mental training can result in clinically beneficial neuroplasticity. Nevertheless, the level of training of the practitioners studied is be- yond the scope of what many individuals with clinical pain conditions might be able to achieve, leading to questions of whether brief mindfulness-based inter- ventions might also alter the way that pain is processed and experienced. In this respect, a recent study in The Journal of Neuroscience by Zeidan et al. (2011) is an important step forward. Zeidan et al. (2011) scanned 15 healthy volunteers with pulsed arterial spin label- ing (ASL), an MRI pulse sequence that provides a quantitative measure of cere- bral blood flow (CBF) using water as a flow tracer. Scan sessions occurred before and after a brief mindfulness-based train- ing intervention consisting of four 20 min sessions on successive days. In the first (pretraining) scan, subjects were stimu- lated with noxious (49°C) or innocuous (35°C) heat in both an attention-neutral and an attention-to-breath (ATB) control condition. Pain intensity and unpleasant- ness ratings were taken after each series of noxious heat delivery. The second (post- training) scan session was identical to the first except that subjects’ ability to focus on their breathing sensations while re- ducing distractions, judgments, and emo- tional responses had presumably been enhanced by mindfulness training. Thus, the ATB condition pretraining and the meditation condition posttraining were Received June 7, 2011; revised July 20, 2011; accepted July 21, 2011. This work was supported by the University of Toronto Centre for the Study of Pain (Clinician-Scientist award to T.V.S.) and Canadian Institutes of Health Research (Master’s Award to A.K.). We thank Karen Davis, Donal Maccoon, and Joshua Grant for comments on the manuscript. Correspondence should be addressed to Dr. Tim V. Salomons, Division of Brain, Imaging and Behaviour—Systems Neuroscience, Toronto Western Research Institute, Toronto Western Hospital, University Health Network, 399 Bathurst Street, Room MP14-303, Toronto, Ontario, Canada M5T 2S8. E-mail: [email protected]. DOI:10.1523/JNEUROSCI.2843-11.2011 Copyright © 2011 the authors 0270-6474/11/3112705-03$15.00/0 The Journal of Neuroscience, September 7, 2011 31(36):12705–12707 • 12705

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1 DivisionofBrain,ImagingandBehaviour—SystemsNeuroscience,TorontoWesternResearchInstitute,Toronto,Ontario,CanadaM5T2S8,and 2 InstituteofMedicalScience,UniversityofToronto,Toronto,Ontario,CanadaM5S1A8 TimV.Salomons 1 andAaronKucyi 1,2 JournalClub ReviewofZeidanetal. TheJournalofNeuroscience,September7,2011 • 31(36):12705–12707•12705 12706 • J.Neurosci.,September7,2011 • 31(36):12705–12707 SalomonsandKucyi•JournalClub SalomonsandKucyi•JournalClub J.Neurosci.,September7,2011 • 31(36):12705–12707•12707

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Page 1: Does meditation reduce pain through a unique neural mechanism

Journal Club

Editor’s Note: These short, critical reviews of recent papers in the Journal, written exclusively by graduate students or postdoctoralfellows, are intended to summarize the important findings of the paper and provide additional insight and commentary. For moreinformation on the format and purpose of the Journal Club, please see http://www.jneurosci.org/misc/ifa_features.shtml.

Does Meditation Reduce Pain through a Unique NeuralMechanism?

Tim V. Salomons1 and Aaron Kucyi1,2

1Division of Brain, Imaging and Behaviour—Systems Neuroscience, Toronto Western Research Institute, Toronto, Ontario, Canada M5T 2S8, and2Institute of Medical Science, University of Toronto, Toronto, Ontario, Canada M5S 1A8

Review of Zeidan et al.

The neuroscience of meditative practice hasattracted considerable attention, in part be-cause it represents a unique juxtaposition ofWestern scientific practice and Eastern mys-tical tradition. Beyond cultural interest,however, lies the question of whether suchstudy has clinical/therapeutic relevance.Pain research is an ideal testing ground forthis question. Many chronic pain disordersare frustratingly resistant to treatmentsaimed at eliminating the sensory compo-nent of pain, prompting increased focuson reducing suffering by altering emo-tional and evaluative components of pain.Mindfulness-based meditative practices,which aim to focus attention on presentexperiences while reducing evaluative andaffective responses, appear tailor-madefor this task.

Several studies have demonstrated bene-ficial effects of mindfulness-based interven-tions for both chronic and acute pain. Mostof these have demonstrated effects of mind-fulness on the affective and evaluative com-ponents of pain (McCracken et al., 2007;Morone et al., 2008; Perlman et al., 2010),

but some have also demonstrated effects onsensory thresholds (Grant et al., 2010, 2011)and perceived pain intensity (Grant and Ra-inville, 2009). Exploration of the biologicalmechanisms of such treatments may in-crease our ability to treat pain disorders byenhancing our understanding of endoge-nous pain regulation.

Recent studies of healthy long-termmeditation practitioners suggest that ex-tensive mental training can result in thick-ening of cortical regions associated withpain processing, including midcingulatecortex (MCC) and primary and secondarysomatosensory cortices (Grant et al.,2010). A study of event-related potentialsduring anticipation of pain found thatlong-term meditation practice alters an-ticipatory evaluation and processing ofpain in MCC and other pain regions(Brown and Jones, 2010). Functional im-aging demonstrated that during pain,practitioners had reduced activation inamygdala, hippocampus, and emotional/evaluative regions of prefrontal cortex, aswell as increased activation in the MCC,thalamus, and insula (Grant et al., 2011).Additionally, altered pain sensitivity was as-sociated with reduced functional connectiv-ity between MCC and dlPFC. Grant et al.(2011) interpreted these findings as consis-tent with the meditative goals of increasingattention to present sensory experience (inthis case, pain) while reducing emotionaland evaluative responses.

Findings from long-term practitionersare of enormous theoretical interest as

they demonstrate that intensive mentaltraining can result in clinically beneficialneuroplasticity. Nevertheless, the level oftraining of the practitioners studied is be-yond the scope of what many individualswith clinical pain conditions might beable to achieve, leading to questions ofwhether brief mindfulness-based inter-ventions might also alter the way that painis processed and experienced.

In this respect, a recent study in TheJournal of Neuroscience by Zeidan et al.(2011) is an important step forward.Zeidan et al. (2011) scanned 15 healthyvolunteers with pulsed arterial spin label-ing (ASL), an MRI pulse sequence thatprovides a quantitative measure of cere-bral blood flow (CBF) using water as aflow tracer. Scan sessions occurred beforeand after a brief mindfulness-based train-ing intervention consisting of four 20 minsessions on successive days. In the first(pretraining) scan, subjects were stimu-lated with noxious (49°C) or innocuous(35°C) heat in both an attention-neutraland an attention-to-breath (ATB) controlcondition. Pain intensity and unpleasant-ness ratings were taken after each series ofnoxious heat delivery. The second (post-training) scan session was identical to thefirst except that subjects’ ability to focuson their breathing sensations while re-ducing distractions, judgments, and emo-tional responses had presumably beenenhanced by mindfulness training. Thus,the ATB condition pretraining and themeditation condition posttraining were

Received June 7, 2011; revised July 20, 2011; accepted July 21, 2011.This work was supported by the University of Toronto Centre for the

Study of Pain (Clinician-Scientist award to T.V.S.) and Canadian Institutesof Health Research (Master’s Award to A.K.). We thank Karen Davis, DonalMaccoon, and Joshua Grant for comments on the manuscript.

Correspondence should be addressed to Dr. Tim V. Salomons, Division ofBrain, Imaging and Behaviour—Systems Neuroscience, Toronto WesternResearch Institute, Toronto Western Hospital, University Health Network,399 Bathurst Street, Room MP14-303, Toronto, Ontario, Canada M5T 2S8.E-mail: [email protected].

DOI:10.1523/JNEUROSCI.2843-11.2011Copyright © 2011 the authors 0270-6474/11/3112705-03$15.00/0

The Journal of Neuroscience, September 7, 2011 • 31(36):12705–12707 • 12705

Page 2: Does meditation reduce pain through a unique neural mechanism

matched in terms of instructions and di-vided attention (to breath) but differed interms of the individual’s ability to achievea nonjudgmental stance toward the painstimulus.

Zeidan et al. (2011) reported signifi-cant changes from pretraining to post-training (ATB vs meditation) in averagepain intensity and unpleasantness ratingsacross subjects [�40% and 57% reduc-tions, respectively, as inferred from thesimilarity observed in their Fig. 2 betweenratings for the rest condition posttrainingand the ATB condition pretraining]. Withinthe second (posttraining) MRI session, sig-nificant reductions in pain-induced CBFwere found in the contralateral primarysomatosensory cortex during meditationrelative to the attention-neutral condition.Training-induced reductions in pain in-tensity were correlated with meditation-induced activity (main effect includingmeditation with and without painfulstimulation) in the right anterior insulaand MCC. Training-induced reductionsin pain unpleasantness were correlatedwith orbitofrontal cortex (OFC) activa-tion and thalamic deactivation duringmeditation.

The use of ASL is a notable feature ofZeidan et al.’s (2011) study. Although ASLlacks the spatial and temporal resolutionof BOLD fMRI, it is well suited for exam-ining the neural mechanisms throughwhich meditation might affect clinicalpain conditions. One reason is that be-cause the ASL signal is sensitized to perfu-sion rather than blood oxygenation, it isnot susceptible to slow-drift artifacts thatare present in BOLD fMRI experimentswhen stimulus/task epochs exceed 1 min.This makes ASL ideal for studying bothchronic pain and meditation, which in-volve sustained neural activity. The recentapplication of ASL to monitor dynamicchanges in CBF over several minutes in amuscular pain model (Owen et al., 2010)highlights the suitability of ASL for exam-ining naturally occurring pain states. Thestudy by Zeidan and colleagues (2011)demonstrates advantageous use of ASLfor examining meditation, as the authorswere able to use longer functional epochs(e.g., 5 min, 55 s blocks of thermal stimu-lation) to examine a sustained meditativestate. Together, these studies suggest thatexamining the effects of a sustained med-itative state on naturally occurring painwould be a promising and clinically rele-vant future application of ASL.

Zeidan et al.’s (2011) study increasesour understanding of the neural mecha-nisms through which short-term meditative

training can affect the pain experience.The authors suggest that meditation alterspain through multiple mechanisms, someof which might be common to otherforms of cognitive modulation of pain(e.g., reappraisal, perceived control, ex-pectation of relief, etc.). Precise character-ization of the cognitive and biologicalmechanisms through which mindfulnessuniquely alters pain is a critical challengefor future research.

A cognitive mechanism that is thoughtto be unique to mindfulness is the combi-nation of increased attention and reducednegative evaluation. As anterior insulaand MCC play a role in salience detectionand motor preparedness (Menon and Ud-din, 2010), increased activation in theseregions may represent a neural substrateof increased attention to perceptuallysalient features of pain. Given that in-creased attention to pain and accompany-ing activation in these two regions is morecommonly associated with increased ex-perience of pain, the finding that activa-tion in these regions is associated withreduced pain intensity appears counterin-tuitive, but it is consistent with the find-ings of Grant and colleagues (2011) inexperienced meditators.

As increased attention and activationin MCC and insula would be expected toincrease the pain experience, the key toreported analgesic effects of meditationtraining might be the co-occurring reduc-tion in emotional and evaluative responses.Thus it is noteworthy that both Zeidan et al.(2011) and Grant et al. (2011) found activa-tion patterns in regions associated withdownregulation of negative affective re-sponses (Ochsner and Gross, 2005). Grantet al. (2011) found functional decoupling ofdlPFC and cingulate, which they attributedto dissociation between attention to painand evaluation of pain. Zeidan and col-leagues (2011) noted an inverse correlationbetween OFC activation and unpleasant-ness ratings, which was attributed to alteredprocessing of reward and hedonic experi-ences. The degree of concordance betweenthese studies suggests that meditative prac-tices may indeed reduce pain through aunique neural mechanism, one correspond-ing to increased attention and reduced eval-uative/emotional responses.

Although these patterns of activationappear consistent with the hypothesizedcognitive mechanisms of mindfulness, fu-ture work must verify these mechanismsempirically. Cognitive benefits of mind-fulness have been demonstrated (Lutz etal., 2008), but it should not be assumedthat these effects occur in all populations

or that they are the mechanism throughwhich meditative training affects painperception. For instance, it is noteworthythat Zeidan and colleagues (2011) ob-served an �57% decrease in unpleasant-ness ratings following meditative trainingbut only a 14% increase in self-reportedmindfulness. While psychometric factorscould explain this discrepancy, it clearlycannot be taken for granted that changesin pain experience can be attributed solelyto mindfulness. Coupling pain with wellestablished cognitive tasks that manipu-late and measure attention and affectiveresponses to pain is necessary to linkchanges in self-report and neural activa-tion with the purported cognitive mecha-nisms of mindfulness training.

A shortcoming of the Zeidan et al.(2011) study in terms of testing the mech-anistic specificity of mindfulness is thelack of an active-treatment control group.There has been considerable debate as towhether the benefits of particular psycho-therapeutic interventions result from cog-nitive factors specific to those therapies orto factors, such as expectation of efficacy,that are characteristic of all effective treat-ments (Wampold et al., 1997). As demon-strated by studies of placebo analgesia,strong belief in the stated benefits of atreatment such as mindfulness may havedirect benefits on the experience andprocessing of pain (Wiech et al., 2008).Furthermore, such beliefs may result inunconscious biases toward self-reportconsistent with these stated benefits (e.g.,reductions in unpleasantness ratings).Comparing mindfulness with psychothera-peutic interventions that do not contain amindfulness component but are otherwisematched for common factors such as de-gree of patient engagement and efficacybeliefs would provide a more precise un-derstanding of the degree to which themechanisms of mindfulness are distinctfrom other forms of cognitive modulationof pain.

In conclusion, Zeidan et al. (2011)provide important insights into the neuralmechanisms through which meditationalters the pain experience. The study isparticularly promising from the stand-point of clinical neuroscience, as theobserved effects are due to clinically plau-sible, short-term meditation training. Asboth meditation and chronic pain presentchallenges for traditional functional neu-roimaging, the use of ASL in the presentstudy is also highly promising. As the sci-entific investigation of meditative practicecontinues to expand, however, a key chal-lenge will be determining the degree to

12706 • J. Neurosci., September 7, 2011 • 31(36):12705–12707 Salomons and Kucyi • Journal Club

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which changes in both the experience ofpain and associated neural processing aredue to cognitive and biological mecha-nisms specific to mindfulness.

ReferencesBrown CA, Jones AK (2010) Meditation experi-

ence predicts less negative appraisal of pain:electrophysiological evidence for the involve-ment of anticipatory neural responses. Pain150:428 – 438.

Grant JA, Rainville P (2009) Pain sensitivity andanalgesic effects of mindful states in Zen med-itators: a cross-sectional study. PsychosomMed 71:106 –114.

Grant JA, Courtemanche J, Duerden EG, DuncanGH, Rainville P (2010) Cortical thicknessand pain sensitivity in Zen meditators. Emo-tion 10:43–53.

Grant JA, Courtemanche J, Rainville P (2011) Anon-elaborative mental stance and decou-

pling of executive and pain-related corticespredicts low pain sensitivity in Zen medita-tors. Pain 152:150 –156.

Lutz A, Slagter HA, Dunne JD, Davidson RJ(2008) Attention regulation and monitoringin meditation. Trends Cogn Sci 12:163–169.

McCracken LM, Gauntlett-Gilbert J, Vowles KE(2007) The role of mindfulness in a contex-tual cognitive-behavioral analysis of chronicpain-related suffering and disability. Pain131:63– 69.

Menon V, Uddin LQ (2010) Saliency, switching,attention and control: a network model of in-sula function. Brain Struct Funct 214:655–667.

Morone NE, Greco CM, Weiner DK (2008) Mind-fulnessmeditationforthetreatmentofchroniclowback pain in older adults: a randomized controlledpilot study. Pain 134:310–319.

Ochsner KN, Gross JJ (2005) The cognitive con-trol of emotion. Trends Cogn Sci 9:242–249.

Owen DG, Clarke CF, Ganapathy S, Prato FS, St

Lawrence KS (2010) Using perfusion MRI tomeasure the dynamic changes in neural acti-vation associated with tonic muscular pain.Pain 148:375–386.

Perlman DM, Salomons TV, Davidson RJ, Lutz A(2010) Differential effects on pain intensityand unpleasantness of two meditation prac-tices. Emotion 10:65–71.

Wampold BE, Mondin GW, Moody M, Stich F,Benson K, Ahn H (1997) A meta-analysis ofoutcome studies comparing bona fide psycho-therapies: empirically, “all must have prizes.”Psychol Bull 122:203–215.

Wiech K, Ploner M, Tracey I (2008) Neurocog-nitive aspects of pain perception. TrendsCogn Sci 12:306 –313.

Zeidan F, Martucci KT, Kraft RA, GordonNS, McHaffie JG, Coghill RC (2011) Brainmechanisms supporting the modulation ofpain by mindfulness meditation. J Neurosci31:5540 –5548.

Salomons and Kucyi • Journal Club J. Neurosci., September 7, 2011 • 31(36):12705–12707 • 12707