Grant Et Al Bi Psychol 2013

You might also like

Download as pdf or txt
Download as pdf or txt
You are on page 1of 8

(This is a sample cover image for this issue. The actual cover is not yet available at this time.

This article appeared in a journal published by Elsevier. The attached


copy is furnished to the author for internal non-commercial research
and education use, including for instruction at the authors institution
and sharing with colleagues.
Other uses, including reproduction and distribution, or selling or
licensing copies, or posting to personal, institutional or third party
websites are prohibited.
In most cases authors are permitted to post their version of the
article (e.g. in Word or Tex form) to their personal website or
institutional repository. Authors requiring further information
regarding Elsevier’s archiving and manuscript policies are
encouraged to visit:
http://www.elsevier.com/copyright
Author's personal copy

Biological Psychology 92 (2013) 275–281

Contents lists available at SciVerse ScienceDirect

Biological Psychology
journal homepage: www.elsevier.com/locate/biopsycho

Cortical thickness, mental absorption and meditative practice: Possible


implications for disorders of attention
Joshua A. Grant a,b,c,d,∗ , Emma G. Duerden a,b,c,d , Jérôme Courtemanche c,d,e , Mariya Cherkasova f ,
Gary H. Duncan b,g,h , Pierre Rainville b,c,d,g
a
Département de Physiologie, Université de Montréal, Montréal, QC, Canada
b
Le Groupe de Recherche sur le Système Nerveux Central (GRSNC), Montréal, QC, Canada
c
Centre de Recherche en Neuropsychologie et Cognition (CERNEC), Montréal, QC, Canada
d
Centre de Recherche de l’Institut Universitaire de Gériatrie de Montréal (CRIUGM), Montréal, QC, Canada
e
Département de Psychologie, Université de Montréal, Montréal, QC, Canada
f
Research Institute of the McGill University Health Centre, Montréal, QC, Canada
g
Département de Stomatologie, Université de Montréal, Montréal, QC, Canada
h
Department of Neurology and Neurosurgery, McGill University, Montréal, QC, Canada

a r t i c l e i n f o a b s t r a c t

Article history: Mental training techniques rooted in meditation are associated with attention improvement, increased
Received 11 May 2012 activation and cortical thickening of attention/executive-related brain areas. Interestingly, attention-
Accepted 12 September 2012 deficit/hyperactivity disorder (ADHD) is associated with behavioural deficits, hypo-activation and cortical
Available online xxx
thinning of similar networks. This study assessed the relationship between prior meditative training,
attentional absorption, and cortical thickness. Grey matter thickness was measured in 18 meditators
Keywords:
and 18 controls. Subjective reports of attentional absorption were modestly higher in meditators and
Cortical thickness
across the entire sample correlated positively with cortical thickness in several regions corresponding
Attentional absorption
Meditation
to cingulo-fronto-parietal attention networks. Within these regions the meditation group had greater
Attention deficit hyperactivity disorder cortical thickness which was positively related to the extent of prior training. Evidence suggesting that
Mindfulness meditative practice activates these cortical areas, improves attention and may ameliorate symptoms of
Mental training ADHD by targeting vulnerable brain regions is discussed.
© 2012 Elsevier B.V. All rights reserved.

1. Introduction 2010; Holzel et al., 2008, 2010; Lazar et al., 2005; Luders et al.,
2009; Vestergaard-Poulsen et al., 2009). In all cases meditators have
The term meditation refers to a family of mental exercises been found to have more grey matter, in specific regions, than non-
aimed at enhancing the practitioner’s ability to attain and main- meditators. Further, several of these effects have involved regions
tain a target state, often attentional or affective in nature (e.g. implicated in attention/executive processing (e.g. ACC, superior
sustained attention or a state of compassion) (Lutz et al., 2008). and middle frontal gyri and orbitofrontal regions) (Grant et al.,
Although often viewed as spiritual, many such techniques are, 2010; Holzel et al., 2008; Lazar et al., 2005; Luders et al., 2009;
for the most part, completely secular and are gaining recogni- Vestergaard-Poulsen et al., 2009). Behaviourally, practitioners of
tion as clinically relevant (Chiesa and Serretti, 2010). Functional meditation have been shown to perform significantly better on
imaging studies have reported that meditating in an MRI scanner attention and executive function tasks such as the Attention Net-
activates attention-related cortices such as the anterior cingulate work Task (ANT), the Stroop Task, attentional blink, Symbol Digit
cortex (ACC) and frontoparietal networks (Brefczynski-Lewis et al., Modalities Test, verbal fluency, and the n-back task (Prakash et al.,
2007; Manna et al., 2010). A number of studies have also reported 2010; Zeidan et al., 2010; Tang et al., 2007; van Leeuwen et al.,
regional grey matter differences between individuals who medi- 2009). While it is certainly possible that there are pre-existing
tate and those who do not (Pagnoni and Cekic, 2007; Grant et al., differences in meditators, there is now evidence from longitu-
dinal studies that improvement in attention performance (Lutz
et al., 2009; Tang et al., 2007; Zeidan et al., 2010) and increases
in grey matter (Holzel et al., 2010, 2011) occur over the course
∗ Corresponding author. Present address: Department of Social Neuroscience,
of meditative training. Importantly, preliminary evidence suggests
Max Planck Institute for Human Cognitive and Brain Sciences, Stephanstrasse 1a,
04103 Leipzig, Germany. Tel.: +49 341 9940 2653; fax: +49 341 9940 2356. that meditative training may be an effective adjunct treatment
E-mail address: grant@cbs.mpg.de (J.A. Grant). for patients suffering from attention-deficit/hyperactivity disorder

0301-0511/$ – see front matter © 2012 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.biopsycho.2012.09.007
Author's personal copy

276 J.A. Grant et al. / Biological Psychology 92 (2013) 275–281

(ADHD). Following an 8 week meditation program, improvements further examine this connection we also administered the Five Facet Mindfulness
were observed on the ANT, the Stroop Task and the Trail Making Questionnaire (FFMQ) (Baer et al., 2008). The FFMQ measures skills associated with
the construct of mindfulness, namely, the tendencies to be observant (OBS), non-
Test, as well as in self-reported ADHD symptoms (Zylowska et al.,
judgmental (NJ) and nonreactive (NR) toward one’s experiences as well as aware in
2008). the present moment (AWARE). A meditation experience questionnaire was admin-
In the literature there are parallels between meditative practice istered sampling years, hours and frequency (days per week) of lifetime practice.
and ADHD at several levels. ADHD is characterized by inatten-
tion, impulsiveness and hyperactivity. Neuroimaging studies have
strongly implicated the fronto-striato-thalamic circuitry in the 2.3. MRI acquisition and cortical thickness measurement

pathophysiology of this disorder (Bush et al., 2005; Seidman et al., A single high-resolution (voxel size = 1 mm3 ) T-1 weighted structural MRI image
2005). Functional MRI studies of ADHD have repeatedly shown (MP-RAGE) was acquired for each participant on a 3 Tesla Siemens Trio MR scanner
hypo-activation of the anterior cingulate, dorsolateral and inferior (Siemens, Erlangen, Germany). An automated cortical thickness analysis pipeline
prefrontal cortices as well as the basal ganglia, thalamus, and pari- was employed (Montréal Neurological Institute (MNI)) (Lerch and Evans, 2005).
Images were linearly registered, transformed into MNI space and corrected for
etal cortices (Dickstein et al., 2006). Morphometric brain imaging
non-uniformity artifacts (Collins et al., 1994; Sled et al., 1998). Images were then
studies have likewise found structural differences, such as corti- segmented into grey and white matter and cerebrospinal fluid (Zijdenbos et al.,
cal thinning, in many of these same areas, in populations of both 2002). Grey and white matter surfaces were produced using constrained Laplacian
adults and children with ADHD (Shaw and Rabin, 2009; Seidman anatomic segmentation using proximities (Kim et al., 2005). A surface deforma-
et al., 2005). Furthermore, cortical thinning of a subset of these tion algorithm (MacDonald et al., 2000) then expanded the white matter surfaces
to the surface boundary between grey matter and cerebrospinal fluid, allowing the
regions has been associated with poor clinical outcome 5 years later calculation of cortical thickness. Thickness data were smoothed following surface
(Shaw et al., 2006). While ADHD and cortical thickness have sub- curvature using a blurring kernel of 20 mm.
stantial heritability (Durston et al., 2004; Forero et al., 2009; Rimol
et al., 2010), morphometric longitudinal studies suggest regional
grey matter may also vary as a function of training and perfor- 2.4. Statistical analyses
mance (Draganski and May, 2008). One particularly notable study
Questionnaires were analysed with independent sample t-tests and correlated
found that training naïve participants to juggle resulted in grey with cortical thickness estimates using Pearson correlations in SPSS. Cortical thick-
matter density increases, concomitant with performance gains, in ness data were analysed with the general linear model (GLM), controlling for age and
brain regions previously implicated in processing visual motion gender, in SurfStat (www.stat.uchicago.edu/∼worsley/surfstat) and with additional
(Draganski et al., 2004). Findings such as these suggest that, despite multiple linear regressions in SPSS. Given our explicitly unidirectional hypotheses,
1-tailed tests were used for all analyses.
the high likelihood of a genetic predisposition, it may be possible to Estimates of cortical thickness at 81,924 vertices covering the entire cortical
combat the functional deficits of a disorder like ADHD by targeting mantle were regressed on attentional absorption scores across the whole sample.
the vulnerable cortices with a suitable training intervention. As dis- For this full brain analysis the significance threshold was set to p < 0.05, corrected for
cussed above, one potential candidate to bolster both grey matter multiple comparisons using the random-field theory (Worsley et al., 1996) to strictly
control type I error. Regions meeting this strict criterion (i.e. showing a relation
thickness and attention/executive function is meditative practice.
between absorption and cortical thickness) were then defined as absorption-ROIs.
The present study provides initial evidence that cortical, Mean thickness within each ROI was computed. These values were compared
attention-related brain regions, that appear to be sensitive to thin- between groups and correlated with meditation experience in SPSS. To examine
ning in ADHD, are related to an experiential measure of attention the proximity of the present results with respect to previously reported structural
and are thicker in practitioners of meditation. The analysis took findings in ADHD, MNI coordinates were acquired from Shaw et al. (2006). In the
original study these regions exhibited cortical thinning in patients with ADHD and
place over two phases. We were first interested in testing the
included the right superior medial PFC, temporal pole, left superior medial PFC, pre-
hypothesis that an experiential measure of attention would (a) central gyrus and left medial PFC/cingulate. Circular ROIs with a 15 mm radius were
differ between meditators and controls and (b) relate to grey mat- created using SurfStat and compared visually by overlaying the respective maps.
ter thickness in attention-related brain regions. With evidence to Euclidian distance between the peak coordinates from the two studies was also
computed.
support these hypotheses a post hoc analysis was performed exam-
Finally, we performed a full brain exploratory search for each of the FFMQ sub-
ining the physical overlap between the present results and a report scales as well as regressions with mean cortical thickness within absorption-ROIs.
of grey matter thinning observed in a study of ADHD (Shaw et al., The main effects of group and meditation experience, at the full brain level, have
2006). been reported as part of the original study from which this data was acquired,
investigating the structural correlates of pain sensitivity (Grant et al., 2010).
2. Materials and methods

2.1. Participants
3. Results
Eighteen Zen meditators (14 male/4 female) were recruited, that had been
practicing between 2 and 30 years and had accumulated a minimum of 1000 h of life- 3.1. Self report measures
time practice (mean = 6406, SD = 1955, min = 1010, max = 39,439). Eighteen age- and
gender-matched control subjects (14 males/4 female) were subsequently recruited.
All participants provided informed written consent, approved by a local Ethics Com- Scores for all questionnaires were normally distributed based on
mittee (CMER-RNQ 05-06-020). Meditators were recruited from meditation centres the Shapiro–Wilk test. Meditators scored slightly higher than con-
in the Montréal area and had an average age of 37.1 yrs (SD = 10.9, range 22–57) and trols on the TAS (t(34) = 1.91, p < 0.05, d = 0.64) indicating a tendency
did not differ from controls (average age 37.9 yrs, SD = 10.5, range = 21–55). With the to be more absorbed in their experience. Meditators also scored
exception of one monk and one nun, all participants were lay practitioners. Control
subjects were also from Montreal and had no previous experience with meditation
higher than controls on three of the subscales of the FFMQ (OBS:
or yoga. t(34) = 3.30, p < 0.01, d = 1.09, NR: t(34) = 3.64, p < 0.001, d = 1.20 and
AWARE: t(34) = 2.03, p < 0.05, d = 0.67) indicating a greater tendency
2.2. Self report measures to be mindful. Across the entire sample TAS scores were positively
correlated with OBS scores (r(34) = 0.39, p < 0.01) and NR scores
Participants’ trait attentional absorption was measured with the 34-item
Tellegen Absorption Scale (TAS), a True/False subscale of the Multidimensional (r(34) = 0.32, p < 0.05) suggesting that absorption and mindfulness
Personality Questionnaire (Tellegen and Atkinson, 1974). The TAS measures one’s may have shared experiential dimensions. Absorption scores in the
tendency for “episodes of ‘total’ attention that fully engage one’s representational meditation group were predicted by the number of days of practice
(i.e. perceptual, enactive, imaginative and ideational) resources” (Tellegen and per week (r(16) = 0.41, p < 0.05) while years of practice predicted NR
Atkinson, 1974). Two previous studies have reported higher absorption scores for
meditators using this scale (Davidson et al., 1976; Holzel and Ott, 2006), the later also
scores (r(16) = 0.47, p < 0.05) with more experience being associated
finding correlations between absorption and meditation depth and mindfulness. To with less reactivity.
Author's personal copy

J.A. Grant et al. / Biological Psychology 92 (2013) 275–281 277

Fig. 1. Cortical thickness correlations with self-reported absorption. Areas in orange-red (t-threshold = 3.6) are Bonferonni-corrected for multiple comparison over the cortical
surface. Regions where thinner grey matter was associated with more absorption (blue-green clusters) did not reach significance. (Right) Relationship between thickness
and absorption within specific regions. R-values correspond to the partial correlations after controlling for age and gender. S.R. = standardized residuals. (For interpretation
of the references to colour in this figure legend, the reader is referred to the web version of the article.)

3.2. Cortical thickness: whole brain analysis of absorption 3.3. Cortical thickness: group and meditation-related effects
within absorption-ROIs
For the whole brain analysis, higher absorption was associated
with thicker grey matter in nodes of the cingulo-fronto-parietal The large cluster spanning left SFG, medial frontal and cingulate
(CFP) attention networks (Fig. 1 and Table 1). A large and highly sig- gyri in the absorption analysis was split into three components
nificant cluster of absorption-related cortical thickness was found (SFG, ACC and PCC), based on clearly visible borders, for the
in the left superior frontal gyrus extending into supra-callosal parts remainder of the analyses with the absorption-ROIs. Within these
of the medial frontal and cingulate gyri. Additional significant clus- ROIs, meditators had greater cortical thickness than controls in
ters were found in the middle frontal gyri and superior parietal left SFG (t(32) = 1.90, p < 0.05), SMG (t(32) = 2.37, p < 0.05) and SPL
lobule bilaterally, the left supramarginal gyrus as well as the right (t(32) = 1.85, p < 0.05) (Fig. 2 and Table 1). It must be noted that this
precuneus. These regions were defined as absorption-ROIs. No sig- analysis is not independent of the procedure used to derive the
nificant negative correlations between TAS scores and thickness absorption ROIs. With knowledge that the meditators scored higher
were observed. on the absorption questionnaire the analysis becomes circular and

Table 1
Full brain thickness/absorption correlations and effects of group and meditation in absorption-ROIs.

Location Vertices (#) Cluster (t, p) Peak-MNI (x, y, z) Meditation training (r/p) Group dif (t/p) Closest ADHD-peak
(mm-structure)

Frontal
SFG-Cing L 1220 4.60, <0.001*
SFG −7, 9, 69 0.42, <0.05 (yr) 1.95, <0.05 6.2 SFG/Med-PFC L
ACC −7, 16, 40 0.49, <0.05 (yr) ns 8.8 Med-PFC/ACC L
PCC −12, −24, 43 ns ns 38.2 Med-PFC/ACC L
MFG R 132 4.60, <0.05* 35, 31, 38 0.43, <0.05 (yr) ns 24.1 SFG/Med-PFC R
MFG L 446 4.51, =0.01* −25, 40, 39 0.53, <0.05 (yr) ns 41.0 SFG/Med-PFC L
Parietal
SMG L 533 4.64, <0.001* −45, −35, 26 ns 2.35, <0.05 >50
SPL R 369 4.55, <0.001* 32, −50, 53 ns ns >50
SPL L 211 4.26, <0.05* −4, −53, 55 0.44, <0.05 (yr) 1.95, <0.05 49.3 PreCG L
PrCun R 240 4.21, =0.01* 18, −83, 45 0.55, <0.05 (h) ns >50

Data are from 18 meditators and 18 controls. SFG-Cing refers to a large contiguous region which was divided into superior frontal, anterior and posterior cingulate regions.
Reported r-values are partial correlation coefficients, that is, representing unique variance after accounting for age and gender in the regression model. ACC, anterior cingulate
cortex; med-PFC, medial prefrontal cortex; MFG, middle frontal gyrus; MNI, Montreal Neurological Institute; PCC, posterior cingulate cortex; PreCG, precentral gyrus; PrCun,
precuneus; MFG, left medial frontal gyrus; SFG-Cing, superior frontal gyrus-cingulate; SPL, superior parietal lobule; SMG, supramarginal gyrus.
*
Indicates p-values Bonferonni-corrected for multiple comparison over the entire cortical surface based on the random-field theory.
Author's personal copy

278 J.A. Grant et al. / Biological Psychology 92 (2013) 275–281

Fig. 2. Group differences and meditation experience correlations within the absorption-ROIs. (Upper panels) Meditators had significantly thicker grey matter in the superior
frontal gyrus (SFG), superior parietal lobule (SPL) and supramarginal gyrus (SMG) all of the left side. M = meditators, C = controls. (Lower panels) Partial regression plots show
the standardized residuals (S.R.) of cortical thickness and years of practice after accounting for age, separately for each variable. The R-value is the partial coefficient and the
best fit line maintains the true relationship between the variables. More years of experience was associated with greater thickness of left SFG, SPL, anterior cingulate cortex
(ACC) and middle frontal gyrus (MFG). For additional regions see Table 1.

should be interpreted with some caution. Within the meditation To examine possible relations between absorption and mindful-
group, years of training (after accounting for age) was positively ness, mean cortical thickness of the absorption-ROIs was regressed
associated with thickness of the left SFG (r(13) = 0.42, p < 0.05), ACC on the FFMQ revealing positive associations between OBS scores
(r(13) = 0.49, p < 0.05), SPL (r(13) = 0.44, p < 0.05) and MFG bilater- and left SFG (r(33) = 0.46, p < 0.01), MFG (r(33) = 0.34, p < 0.05), SPL
ally (left: r(13) = 0.53, p < 0.05; right: r(13) = 0.43, p < 0.05) (Fig. 2 (r(33) = 0.48, p < 0.01) and SMG (r(33) = 0.37, p < 0.05). NR scores
and Table 1). Hours of experience was associated with thickness of were associated with mean thickness in the same regions with
the right precuneus (r(13) = 0.50, p < 0.05). There were no group dif- the exception of the SMG (left SFG: r(33) = 0.37, p < 0.05; MFG:
ferences or correlations with total hemispheric grey matter volume r(33) = 0.31, p < 0.05; SPL: r(33) = 0.34, p < 0.05). In each of these
reinforcing the focal nature of the effects. Significant overlap was cases, greater thickness was associated with higher self-reported
observed between the main effect of absorption and ADHD-related mindfulness. The AWARE and NJ subscales were not associated
cortical thinning observed previously by another group (Shaw et al., with mean thickness in any of the absorption network ROIs. Subse-
2006) (Fig. 3). The physical distance between the peaks observed quent full brain searches revealed a correlation between NR scores
in the present study and those observed by Shaw et al. (2006) are and cortical thickness in the right fusiform gyrus but no additional
listed in Table 1. regions were found for OBS, NJ or AWARE scores. As reported in
Grant et al. (2010) a global search contrasting meditators and con-
trols revealed that the right dorsal ACC was significantly thicker in
meditators and a single region on the right precentral gyrus was
found to be related to hours of meditation experience.

4. Discussion

Attentional absorption has been described as one’s tendency


for “episodes of ‘total’ attention that fully engage one’s represen-
tational resources” (Tellegen and Atkinson, 1974). Consistent with
previous reports (Davidson et al., 1976; Holzel and Ott, 2006), medi-
tators had a greater, albeit modest, tendency to become absorbed in
their experiences than control subjects. Further, absorption scores
of meditators were related to the frequency of their practice sug-
gesting the trait may be malleable and sensitive to training. Across
Fig. 3. Overlap between absorption and ADHD. Red: regions where absorption cor- the entire sample of meditators and controls, absorption positively
related with grey matter thickness across the entire sample of the present report. correlated with grey matter thickness, at multiple nodes of cingulo-
Yellow: ROIs derived from Shaw et al. (2006) where attention-deficit hyperactivity fronto-parietal (CFP) attention/executive networks. Within these
disorder (ADHD) was associated with thinner cortex and worse outcome. Orange:
regions meditators had thicker cortex which was also related to
overlap between the main effect of absorption and cortical thinning in ADHD. (For
interpretation of the references to colour in this figure legend, the reader is referred the extent of training. We suggest below, based on these and
to the web version of the article.) other structural, functional and behavioural results, that there is
Author's personal copy

J.A. Grant et al. / Biological Psychology 92 (2013) 275–281 279

substantial evidence indicating that meditative training has a pos- in meditators, within regions where absorption correlated with
itive impact on attention. We further describe the remarkable grey matter thickness. This suggests that absorption and aspects
correspondence, albeit in opposing directions, between meditation of mindfulness, such as the tendency to be observant and non-
and ADHD and speculate about the use of this form of mental train- reactive, may share common neural substrates. Similar to other
ing to bolstering grey matter thickness in highly susceptible cortical skills, changes in brain function and structure resulting from train-
regions implicated in the disorder. ing in meditation should have a corresponding behavioural effect.
Structurally, the present report shows that individuals’ propen- Evidence also suggests meditative practice is associated with per-
sity for attentional absorption is related to the grey matter formance improvements on attention and executive control tasks.
thickness of left ACC, SFG, SMG and bilateral MFG and SPL. These Behaviourally, substantial evidence now exists, from both lon-
regions are all parts of attention and executive control networks gitudinal and cross-sectional studies, that meditative training can
known under various formulations as the dorsal attention network enhance performance on attention/executive tasks such the ANT,
(Bush et al., 2000; Cabeza and Nyberg, 2000; Corbetta and Shulman, Stroop, attentional blink, a cued-response task, the Symbol Digit
2002), the frontoparietal control system (Vincent et al., 2008) or the Modalities Test, verbal fluency, and the n-back task (Prakash et al.,
executive control network (Seeley et al., 2007). These systems have 2010; Zeidan et al., 2010; Hodgins and Adair, 2010; Tang et al.,
been postulated to coordinate attention under competing condi- 2007; van Leeuwen et al., 2009). Taken as a whole, the existent lit-
tions. In absolute terms, meditators had thicker grey matter than erature suggests meditative practice functionally and structurally
controls in each of the above-mentioned regions, significantly so in alters attention and executive control networks and improves per-
the left SFG, SMG and SPL. Further, the years of practice of individ- formance on tasks which engage these regions. Interestingly, in all
ual meditators, after controlling for age, predicted the thickness of three domains the story is the reverse for ADHD.
left SFG, ACC, SPL and MFG bilaterally. One possible interpretation In the present report, the thickness of cortical regions asso-
of these results is that repeatedly engaging in meditative practice ciated with absorption and mindfulness overlapped with regions
leads, overtime, to increases in grey matter thickness in brain reported to undergo cortical thinning in ADHD populations, specif-
regions important for the control and maintenance of attention ically the cingulate, prefrontal and parietal cortices (Shaw et al.,
(an alternative is discussed below). This interpretation is consis- 2006) (Fig. 3). Of particular interest, cortical thinning of the cingu-
tent with a growing body of work, including a longitudinal training late cortex, measured longitudinally, has been found to be related to
study, reporting thicker or more dense grey matter for meditators worse outcome in patients (Shaw et al., 2006). In the present report
compared to controls (Grant et al., 2010; Holzel et al., 2008, 2010, we created a region of interest centred on the peak from that study
2011; Lazar et al., 2005; Luders et al., 2009; Vestergaard-Poulsen and found direct overlap with the main effect of absorption. In the
et al., 2009). Indeed, several of these studies have reported effects same ACC cluster, a positive relationship was observed between
of meditation in attention/executive regions such as ACC, superior, thickness and the extent of meditators’ training. Additional reports
middle and orbito-frontal regions. Importantly, functional imag- of cortical thinning in adults with ADHD (Makris et al., 2007) have
ing studies have also shown that engaging in meditative practice implicated the ACC, DLFPC and parietal lobules where again, in the
activates these same networks. present report, absorption was associated with thicker grey matter
The main effect of absorption and cortical thickness in left ACC, and meditation experience.
SFG, SMG and bilateral MFG and SPL corresponds well with atten- It is within these same networks that the majority of functional
tion and executive control networks. Functional MRI studies of abnormalities have been observed in children, adolescents, and
meditation have reported engagement of these networks during adults with ADHD while performing cognitive tasks tapping atten-
practice (Lutz et al., 2008). Brefczynski-Lewis et al. (2007) found tion and executive function (Bush et al., 2010). A meta-analysis of 16
greater activation of left MFG, DLPFC, SMG, right SFG and SPL functional imaging studies of ADHD reported significant patterns
bilaterally during sustained attention in advanced Tibetan medi- of hypo-activity of anterior cingulate, dorsolateral and inferior pre-
tators compared to novices. Similarly, Manna et al. (2010) reported frontal cortices as well as basal ganglia, thalamus, and the parietal
stronger cingulate and medial PFC activation during meditation cortex in sufferers of the disorder (Dickstein et al., 2006). As dis-
for Theravadin monks compared to controls. Interestingly, a brain- cussed above, activation of many of these regions is enhanced in
imaging study from our group examining attentional absorption meditators (Brefczynski-Lewis et al., 2007; Manna et al., 2010).
stemming from hypnotic induction reported absorption-specific Finally, preliminary behavioural results suggest that an 8 week, sec-
increases in regional cerebral blood flow in the ACC as well as bilat- ular, meditation-based program can improve symptoms of ADHD
erally in the SFG, MFG, IFG and IPL (Rainville et al., 2002). Thus, and scores on measures of attention and executive control such as
networks functionally activated during both absorption and medi- the ANT, Stroop and the Trail Making Test in adults and adolescents
tative practice, appear to overlap substantially with those observed (Zylowska et al., 2008).
in the present study to relate, structurally, to attentional absorp- Taken as a whole, existing behavioural, functional and structural
tion. This lends further support to the idea that meditation is a imaging studies provide a link between meditation and ADHD; the
trainable skill that is reflected in anatomical and functional brain former being associated with performance enhancement, increased
changes. activation and thicker cortex while the later is associated with per-
The idea that repeated practice or skill learning can result in formance decrement, hypoactivation and cortical thinning. This
functional and structural changes in the brain is certainly not new could potentially indicate that the cognitive processes engaged
(Buonomano and Merzenich, 1998). However it has only been in and strengthened by meditation, possibly reflected by cortical
the past decade that MRI technology and analyses have become thickening, are similar to those impaired in ADHD and associated
advanced enough to show, in living humans, that skills such as with functional and structural abnormalities. The contribution of
juggling (Draganski et al., 2004), mirror reading (Ilg et al., 2008) the present results is that of a potential mechanism by which
or playing a musical instrument (Gaser and Schlaug, 2003) can meditative practice may act; via changes in cortical thickness,
influence the amount of grey matter in functionally relevant brain itself potentially induced from repeated functional activation of
regions. In a similar manner, learning the skills associated with the relevant circuits. While this interpretation admittedly exceeds
meditation, such as being mindful or sustaining one’s focus, may what is reasonable for the results presented here, it highlights the
increase grey matter in regions implicated in attention/executive remarkable consistency across studies and measures. Further sup-
processing. Fittingly, we also observed correlations between cor- port for this link can be found in other domains as well. Seeley
tical thickness and facets of mindfulness, which were stronger et al. (2007) used resting-state MRI under task-free conditions
Author's personal copy

280 J.A. Grant et al. / Biological Psychology 92 (2013) 275–281

to link the executive-control network (considerably overlapping and ultimately, link those changes with behavioural improvement.
with the present results) to prior performance of the Trail Mak- The substantial financial burden that this and related disorders
ing Test (TMT). The TMT is an executive task requiring one to place on health care systems (Guevara et al., 2001), raises the incen-
switch between competing attentional sets and has been shown tive, both socially and economically, for such a complementary
to improve in ADHD populations following meditation training. treatment option.
Finally, there is evidence that stimulant treatment for ADHD acts To conclude, the current study provides evidence that grey mat-
partly by staving off cortical thinning (Shaw et al., 2009). This ter thickness, overlapping with regions of the brain susceptible to
suggests that it may be the engagement of specific brain regions, thinning in disorders of attention, is associated with an individual’s
enabled via the treatment and verified by positive changes in experience of mental absorption or engagement in their experi-
behaviour, which prevents grey matter loss. ence. Individuals who practice meditation had thicker cortex in
several of these regions which was also related to the extent of their
training. We suggest that these results and the existent literature
5. Limitations provide ample justification for further inquiry into the potential
use of meditative practice as an adjunct treatment for ADHD.
Thus far we have argued that our results combined with
the existent literature point to meditation as a plausible causal
Financial disclosures
agent, positively influencing cortical thickness and potentially
modulating behaviour in turn. However, such causality cannot be
None of the authors have any financial or other relationship that
determined from a cross sectional study and indeed a case can be
might lead to a conflict of interest.
made for alternative interpretations. For example, it may be, and
is perhaps even likely, that there is a substantial genetic contribu-
tion to one’s tendency for absorption (Ott et al., 2005; Ott, 2007), as Acknowledgments
there is for both regional cortical thickness (Rimol et al., 2010) and
ADHD (Durston et al., 2004; Forero et al., 2009). It may be that, due This research was supported jointly by a Canadian Institutes
to such factors, a phenotype characterized by high absorption is of Health Research (CIHR) operating grant (P.R.) and a Mind and
attracted to, and perseveres in, the practice of meditation. Indeed, Life Institute Varela Grant (J.A.G.). J.A.G has also been supported
Holzel and Ott (2006) suggest it may be one’s propensity for absorp- by a fellowship from CIHR. We would like to thank L’Unité de
tion that influences the depth of the meditative state. Nonetheless, Neuroimagerie Fonctionnelle du Centre de recherche de l’Institut
contributions to complex mental phenomenon will likely never be universitaire de gériatrie de Montréal for technical help with scan-
purely genetic or environmental and the existing longitudinal evi- ning and members of the Duncan-Rainville labs.
dence suggests a significant contribution of meditative training to
changes in attention performance (Prakash et al., 2010; Zeidan et al., References
2010; Hodgins and Adair, 2010; Tang et al., 2007; van Leeuwen
et al., 2009) and grey matter (Holzel et al., 2010) over time. Baer, R.A., Smith, G.T., Lykins, E., Button, D., Krietemeyer, J., Sauer, S., Walsh, E.,
An unfortunate limitation of the present study is the lack of Duggan, D., Williams, J.M., 2008. Construct validity of the five facet mindfulness
questionnaire in meditating and nonmeditating samples. Assessment 35 (2),
a performance-based measure of attention. This stems from the 207–216.
fact that these data were collected for a study designed to assess Brefczynski-Lewis, J.A., Lutz, A., Schaefer, H.S., Levinson, D.B., Davidson, R.J., 2007.
the structural correlates of pain perception (Grant et al., 2010). Neural correlates of attentional expertise in long-term meditation practitioners.
Proceedings of the National Academy of Sciences of the United States of America
Such a measure would have certainly been helpful. Nonetheless, 104 (27), 11483–11488.
the strong correlation between absorption and cortical thickness, Buonomano, D.V., Merzenich, M.M., 1998. Cortical plasticity: from synapses to maps.
nearly exclusively in attention/executive networks, suggests that Annual Review of Neuroscience 21, 149–186.
Bush, G., 2010. Attention-deficit/hyperactivity disorder and attention networks.
the scale may indeed tap these processes. It is interesting to note
Neuropsychopharmacology 35 (1), 278–300.
that the measure of absorption employed in the present report Bush, G., Luu, P., Posner, M.I., 2000. Cognitive and emotional influences in anterior
depends on participants’ access to the quality or stability of their cingulate cortex. Trends in Cognitive Sciences 4 (6), 215–222.
Bush, G., Valera, E.M., Seidman, L.J., 2005. Functional neuroimaging of attention-
mental experience. This suggests that there is a definite relation-
deficit/hyperactivity disorder: a review and suggested future directions.
ship between brain structure and the experience one has of their Biological Psychiatry 57 (11), 1273–1284.
mental state, and further, that this is consistent across a modest Cabeza, R., Nyberg, L., 2000. Imaging cognition II: an empirical review of 275 PET
sample size. While an experiential-based construct like absorption and fMRI studies. Journal of Cognitive Neuroscience 12 (1), 1–47.
Chiesa, A., Serretti, A., 2010. A systematic review of neurobiological and clinical
is not likely to be useful diagnostically for attention-related dis- features of mindfulness meditations. Psychological Medicine 40 (8), 1239–1252.
orders, it does seem relevant. After all, whether highly focused or Collins, D.L., Neelin, P., Peters, T.M., Evans, A.C., 1994. Automatic 3D intersubject
inattentive, our mental experience encompasses all that we can registration of MR volumetric data in standardized Talairach space. Journal of
Computer Assisted Tomography 18 (2), 192–205.
ever consciously know, making the quality of that experience a Corbetta, M., Shulman, G.L., 2002. Control of goal-directed and stimulus-driven
motivating factor for treatment. attention in the brain. Nature Reviews Neuroscience 3 (3), 201–215.
It should also be noted that other disorders such as Alzheimer’s Davidson, R.J., Goleman, D.J., Schwartz, G.E., 1976. Attentional and affective concomi-
tants of meditation: a cross-sectional study. Journal of Abnormal Psychology 85
Disease involve similar networks and effects observed here may (2), 235–238.
more generally reflect a maintenance of cortical thickness in med- Dickstein, S.G., Bannon, K., Castellanos, F.X., Milham, M.P., 2006. The neural corre-
itation as suggested previously (Pagnoni and Cekic, 2007; Lazar lates of attention deficit hyperactivity disorder: an ALE meta-analysis. Journal
of Child Psychology and Psychiatry and Allied Disciplines 47 (10), 1051–1062.
et al., 2005) and resulting from any number of factors associated
Draganski, B., Gaser, C., Busch, V., Schuierer, G., Bogdahn, U., May, A., 2004. Neu-
with the practice or lifestyle. Nonetheless, given the prelimi- roplasticity: changes in grey matter induced by training. Nature 427 (6972),
nary evidence for the effectiveness of meditation as an adjunct 311–312.
Draganski, B., May, A., 2008. Training-induced structural changes in the adult human
treatment for ADHD (Zylowska et al., 2008), there seems to be
brain. Behavioural Brain Research 192 (1), 137–142.
adequate justification for larger longitudinal studies combining Durston, S., Hulshoff Pol, H.E., Schnack, H.G., Buitelaar, J.K., Steenhuis, M.P., Minderaa,
mental training via meditation with performance measures of R.B., Kahn, R.S., van Engeland, H., 2004. Magnetic resonance imaging of boys with
attention/executive control and MRI morphometry. Importantly, attention-deficit/hyperactivity disorder and their unaffected siblings. Journal of
the American Academy of Child and Adolescent Psychiatry 43 (3), 332–340.
clinical studies could also directly test the hypothesis that medita- Forero, D.A., Arboleda, G.H., Vasquez, R., Arboleda, H., 2009. Candidate genes
tive training will increase cortical thickness in sufferers of ADHD involved in neural plasticity and the risk for attention-deficit hyperactivity
Author's personal copy

J.A. Grant et al. / Biological Psychology 92 (2013) 275–281 281

disorder: a meta-analysis of 8 common variants. Journal of Psychiatry & Neuro- epistasis between 5-HT2a and COMT polymorphisms. American Journal of Med-
science 34 (5), 361–366. ical Genetics. Part B: Neuropsychiatric Genetics 137B (1), 29–32.
Gaser, C., Schlaug, G., 2003. Brain structures differ between musicians and non- Pagnoni, G., Cekic, M., 2007. Age effects on gray matter volume and attentional
musicians. Journal of Neuroscience 23 (27), 9240–9245. performance in Zen meditation. Neurobiology of Aging 28 (10), 1623–1627.
Grant, J.A., Courtemanche, J., Duerden, E.G., Duncan, G.H., Rainville, P., 2010. Cortical Prakash, R., Dubey, I., Abhishek, P., Gupta, S.K., Rastogi, P., Siddiqui, S.V., 2010. Long-
thickness and pain sensitivity in Zen meditators. Emotion 10 (1), 43–53. term Vihangam Yoga meditation and scores on tests of attention. Percept Mot
Guevara, J., Lozano, P., Wickizer, T., Mell, L., Gephart, H., 2001. Utilization and cost of Skills 110 (3 Pt. 2), 1139–1148.
health care services for children with attention-deficit/hyperactivity disorder. Rainville, P., Hofbauer, R.K., Bushnell, M.C., Duncan, G.H., Price, D.D., 2002. Hypnosis
Pediatrics 108 (1), 71–78. modulates activity in brain structures involved in the regulation of conscious-
Hodgins, H.S., Adair, K.C., 2010. Attentional processes and meditation. Consciousness ness. Journal of Cognitive Neuroscience 14 (6), 887–901.
and Cognition 19 (4), 872–878. Rimol, L.M., Panizzon, M.S., Fennema-Notestine, C., Eyler, L.T., Fischl, B., Franz, C.E.,
Holzel, B.K., Carmody, J., Evans, K.C., Hoge, E.A., Dusek, J.A., Morgan, L., Pitman, R.K., Hagler, D.J., Lyons, M.J., Neale, M.C., Pacheco, J., Perry, M.E., Schmitt, J.E., Grant,
Lazar, S.W., 2010. Stress reduction correlates with structural changes in the M.D., Seidman, L.J., Thermenos, H.W., Tsuang, M.T., Eisen, S.A., Kremen, W.S.,
amygdala. Social Cognitive and Affective Neuroscience 5 (1), 11–17. Dale, A.M., 2010. Cortical thickness is influenced by regionally specific genetic
Holzel, B.K., Carmody, J., Vangel, M., Congleton, C., Yerramsetti, S.M., Gard, T., Lazar, factors. Biological Psychiatry 67 (5), 493–499.
S.W., 2011. Mindfulness practice leads to increases in regional brain gray matter Seeley, W.W., Menon, V., Schatzberg, A.F., Keller, J., Glover, G.H., Kenna, H., Reiss,
density. Psychiatry Research 191 (1), 36–43. A.L., Greicius, M.D., 2007. Dissociable intrinsic connectivity networks for salience
Holzel, B.K., Ott, U., 2006. Relationships between meditation depth, absorption, processing and executive control. Journal of Neuroscience 27 (9), 2349–2356.
meditation practice and mindfulness: a latent variable approach. The Journal Seidman, L.J., Valera, E.M., Makris, N., 2005. Structural brain imaging of attention-
of Transpersonal Psychology 38 (2), 179–199. deficit/hyperactivity disorder. Biological Psychiatry 57 (11), 1263–1272.
Holzel, B.K., Ott, U., Gard, T., Hempel, H., Weygandt, M., Morgen, K., Vaitl, D., 2008. Shaw, P., Lerch, J., Greenstein, D., Sharp, W., Clasen, L., Evans, A., Giedd, J., Castellanos,
Investigation of mindfulness meditation practitioners with voxel-based mor- F.X., Rapoport, J., 2006. Longitudinal mapping of cortical thickness and clini-
phometry. Social Cognitive and Affective Neuroscience 3 (1), 55–61. cal outcome in children and adolescents with attention-deficit/hyperactivity
Ilg, R., Wohlschlager, A.M., Gaser, C., Liebau, Y., Dauner, R., Woller, A., Zimmer, C., Zihl, disorder. Archives of General Psychiatry 63 (5), 540–549.
J., Muhlau, M., 2008. Gray matter increase induced by practice correlates with Shaw, P., Rabin, C., 2009. New insights into attention-deficit/hyperactivity dis-
task-specific activation: a combined functional and morphometric magnetic order using structural neuroimaging. Current Psychiatry Reports 11 (5),
resonance imaging study. Journal of Neuroscience 28 (16), 4210–4215. 393–398.
Kim, J.S., Singh, V., Lee, J.K., Lerch, J., Ad-Dab’bagh, Y., MacDonald, D., Lee, J.M., Kim, Shaw, P., Sharp, W.S., Morrison, M., Eckstrand, K., Greenstein, D.K., Clasen, L.S., Evans,
S.I., Evans, A.C., 2005. Automated 3-D extraction and evaluation of the inner A.C., Rapoport, J.L., 2009. Psychostimulant treatment and the developing cortex
and outer cortical surfaces using a Laplacian map and partial volume effect in attention deficit hyperactivity disorder. American Journal of Psychiatry 166
classification. Neuroimage 27 (1), 210–221. (1), 58–63.
Lazar, S.W., Kerr, C.E., Wasserman, R.H., Gray, J.R., Greve, D.N., Treadway, M.T., Sled, J.G., Zijdenbos, A.P., Evans, A.C., 1998. A nonparametric method for automatic
McGarvey, M., Quinn, B.T., Dusek, J.A., Benson, H., Rauch, S.L., Moore, C.I., Fischl, correction of intensity nonuniformity in MRI data. IEEE Transactions on Medical
B., 2005. Meditation experience is associated with increased cortical thickness. Imaging 17 (1), 87–97.
Neuroreport 16 (17), 1893–1897. Tang, Y.Y., Ma, Y., Wang, J., Fan, Y., Feng, S., Lu, Q., Yu, Q., Sui, D., Rothbart, M.K., Fan,
Lerch, J.P., Evans, A.C., 2005. Cortical thickness analysis examined through power M., Posner, M.I., 2007. Short-term meditation training improves attention and
analysis and a population simulation. Neuroimage 24 (1), 163–173. self-regulation. Proceedings of the National Academy of Sciences of the United
Luders, E., Toga, A.W., Lepore, N., Gaser, C., 2009. The underlying anatomical corre- States of America 104 (43), 17152–17156.
lates of long-term meditation: larger hippocampal and frontal volumes of gray Tellegen, A., Atkinson, G., 1974. Openness to absorbing and self-altering experi-
matter. Neuroimage 45 (3), 672–678. ences (absorption), a trait related to hypnotic susceptibility. Journal of Abnormal
Lutz, A., Slagter, H.A., Dunne, J.D., Davidson, R.J., 2008. Attention regulation and Psychology 83 (3), 268–277.
monitoring in meditation. Trends in Cognitive Sciences 12 (4), 163–169. van Leeuwen, S., Muller, N.G., Melloni, L., 2009. Age effects on attentional blink
Lutz, A., Slagter, H.A., Rawlings, N.B., Francis, A.D., Greischar, L.L., Davidson, R.J., 2009. performance in meditation. Consciousness and Cognition 18 (3), 593–599.
Mental training enhances attentional stability: neural and behavioral evidence. Vestergaard-Poulsen, P., van Beek, M., Skewes, J., Bjarkam, C.R., Stubberup, M., Ber-
Journal of Neuroscience 29 (42), 13418–13427. telsen, J., Roepstorff, A., 2009. Long-term meditation is associated with increased
MacDonald, D., Kabani, N., Avis, D., Evans, A.C., 2000. Automated 3-D extraction gray matter density in the brain stem. Neuroreport 20 (2), 170–174.
of inner and outer surfaces of cerebral cortex from MRI. Neuroimage 12 (3), Vincent, J.L., Kahn, I., Snyder, A.Z., Raichle, M.E., Buckner, R.L., 2008. Evidence for
340–356. a frontoparietal control system revealed by intrinsic functional connectivity.
Makris, N., Biederman, J., Valera, E.M., Bush, G., Kaiser, J., Kennedy, D.N., Caviness, Journal of Neurophysiology 100 (6), 3328–3342.
V.S., Faraone, S.V., Seidman, L.J., 2007. Cortical thinning of the attention and exec- Worsley, K.J., Marrett, S., Neelin, P., Vandal, A.C., Friston, K.J., Evans, A.C., 1996. A uni-
utive function networks in adults with attention-deficit/hyperactivity disorder. fied statistical approach for determining significant signals in images of cerebral
Cerebral Cortex 17 (6), 1364–1375. activation. Human Brain Mapping 4 (1), 58–73.
Manna, A., Raffone, A., Perrucci, M.G., Nardo, D., Ferretti, A., Tartaro, A., Londei, A., Zeidan, F., Johnson, S.K., Diamond, B.J., David, Z., Goolkasian, P., 2010. Mindfulness
Del Gratta, C., Belardinelli, M.O., Romani, G.L., 2010. Neural correlates of focused meditation improves cognition: evidence of brief mental training. Conscious-
attention and cognitive monitoring in meditation. Brain Research Bulletin 82 ness and Cognition 19 (2), 597–605.
(1–2), 46–56. Zijdenbos, A.P., Forghani, R., Evans, A.C., 2002. Automatic pipeline analysis of 3-D
Ott, U., 2007. States of absorption: in search of neurobiological founda- MRI data for clinical trials: application to multiple sclerosis. IEEE Transactions
tions. In: Jamieson, G. (Ed.), Hypnosis and Consciousness States: The on Medical Imaging 21 (10), 1280–1291.
Cognitive-neuroscience Perspective. Oxford University Press, New York, Zylowska, L., Ackerman, D.L., Yang, M.H., Futrell, J.L., Horton, N.L., Hale, T.S., Pataki, C.,
pp. 257–270. Smalley, S.L., 2008. Mindfulness meditation training in adults and adolescents
Ott, U., Reuter, M., Hennig, J., Vaitl, D., 2005. Evidence for a common biologi- with ADHD: a feasibility study. Journal of Attention Disorders 11 (6), 737–746.
cal basis of the absorption trait, hallucinogen effects, and positive symptoms:

You might also like