Accepted Manuscript: Neuroscience
Accepted Manuscript: Neuroscience
Accepted Manuscript: Neuroscience
PII: S0306-4522(16)00079-8
DOI: http://dx.doi.org/10.1016/j.neuroscience.2016.01.051
Reference: NSC 16869
Please cite this article as: R. Atchley, D. Klee, T. Memmott, E. Goodrich, H. Wahbeh, B. Oken, Event-related
potential correlates of mindfulness meditation competence, Neuroscience (2016), doi: http://dx.doi.org/10.1016/
j.neuroscience.2016.01.051
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Authors: Rachel Atchley, PhD; Dan Klee, BS1; Tabatha Memmott, BA, BS1; Elena
Goodrich, MDiv1; Helané Wahbeh, ND, MCR1, and Barry Oken, MD, MS1.
Portland, OR 97239
Email: [email protected]
Phone: 503-494-5650
2
Abstract
detection task and a Breath Counting task. The Breath Counting task served as the
mindfulness meditation condition for the novice and experienced meditator groups.
Participants were instructed to respond to target tones with a button press in the first
task (Tones), and then ignore the primed tones while breath counting. The primary
outcomes were ERP responses to target tones, namely the N2 and P3, as markers of
groups during the Breath Counting task in comparison to the Tones task (p < .001).
There was a task by group interaction for P3 (p = .039). Both meditator groups
during the Tones condition and more pronounced reductions in P3 amplitudes during
instructed to ignore the same tones during the Breath Counting task. This study
meditation competence, and results suggest this may be a valid approach. This
3
treatment of anxiety, depression, and chronic pain (Kabat-Zinn et al., 1992; Miller et al.,
1995; Teasdale et al., 2000; Zeidan et al., 2010; Chiesa & Serretti, 2010; Grossman et
magnetic resonance imaging (MRI) (Chiesa & Serretti, 2010; Fox et al., 2014;
Dickenson et al., 2013; Kilpatrick et al., 2011; Cahn & Polich, 2006). A more
straightforward EEG marker could enable researchers to more accurately assess the
are emerging. More accurate assessment would further elucidate the brain mechanisms
delineated as the ability to attend to breathing while ignoring other stimuli. EEG is
appealing way to assess brain changes in meditation because it allows for brain activity
2007; Lutz et al., 2009), EEG may be of additional benefit since it can evaluate these
changes.
this aim, we investigated brain changes with EEG during mindfulness meditation
practice among participants with differing levels of experience: naïve, novice, and
experienced.
examined the ERP correlates of “paying attention”, not the motivational or emotional
processes that accompany paying attention. We acknowledge that there are many
delineating the ability to keep awareness in the present moment because we were
mindful attention to the present moment during daily living and cultivate concentrative
meditational techniques. The Body Scan and Sitting Meditation, which are the two
surrogate in order to be evaluated, and attention is an ideal marker given the results of
past studies (Brefcyznski-Lewis et al. 2007; Chan & Woollacott 2007; Chiesa et al.,
2011; Lutz et al., 2008). We used a breath counting task because non-meditators can
5
ERP components are predictable patterns of brain activity that occur in response
experience-related differences during a quiet, potentially meditative state. The first was
the P3, which generally indicates stronger attentional focus on a particular stimulus. We
earlier work (Brefcyznski-Lewis et al. 2007; Chan & Woollacott 2007; Chiesa et al.,
2011; Lutz et al., 2008). Thus we hypothesized that meditators would also have greater
meditators and non-meditators (Cahn & Polich 2009; Chiesa et al. 2011; Delgado-
Pastor et al. 2013; Tang et al., 2009), although the relationship between meditation
training and attentional priming effects remains unknown. We also predicted that P3
amplitudes would differ between experienced and novice meditators, expecting that
participants with the most meditation experience would also have the most attentional
control.
The second component of interest in this study was the N2, which is elicited by
stimuli similar to those that elicit the P3, specifically those that involve greater task-
related attention or novelty (Luck, 2014). The N2 is elicited in response to target tones
experienced meditators were expected to have the most pronounced difference from
6
naïve participants while novices’ performance would fall in the middle. To test these
naïve meditators during an odd-ball paradigm, initially while participants were instructed
to attend to the target tones and then while they were told to ignore the tones and focus
responses to target tones during the Breath Counting task and how these responses
Methods
area utilizing internet-based, flyer, and word-of-mouth strategies. All underwent a 30-
minute telephone screening. Inclusion criteria for participants in all groups were as
follows: 1) Age 25-75 years; 2) Good general past and present medical health; 3) Stable
on all medications for at least two months; and 4) Cognitively intact, as determined by a
score of ≥31 on the Telephone Interview for Cognitive Status (TICS) (Welsh et al.,
The naïve, novice, and experienced groups were carefully defined, and each
Information about lifetime hours of practice was collected via verbal self-report.
Meditation was defined as any practice of attention training, in which one is intentionally
7
working to improve his or her ability to pay attention to the present moment. Further
details about the types of practice are described by group below. Mind-body movement
practices were defined as any activity in which one is practicing attention training. Mind-
body movement-based practices included yoga, tai chi, martial arts, qi gong, mindful
eating, walking, running, and swimming. The practices included foci of attention were
The three groups were evaluated by specific criteria. Potential naïve subjects
were excluded if they had taken a meditation or other mind-body movement class within
the past two years or if they had a daily meditation practice of five minutes or longer in
the past 30 days. Novice subjects were included if they had some formal training,
meaning they attended classes that were described and approved by the principal
investigator, practiced at least three days a week, and had ≤1,000 hours’ lifetime
experience of combined meditation and mind-body practices. All novice meditators took
myriad of other methods, including the body scan, compassion practices, and
≥5,000 lifetime meditation and mind-body movement practice hours. All had ≥4,000
in addition to those practiced by the novices, including but not limited to the following:
non-conceptual awareness, and open awareness. The protocol for this study was
Our experiment was designed to measure changes in brain activity during Breath
Counting meditation and assess priming as a means of attentional focus; therefore, our
primary measures were the attentional N2/P3 ERP components and P3b specifically in
response to infrequent target tones across tasks. Given the age of our sample (M age =
49 years), it is worth noting that P3a and P3b tend to overlap as age increases (Alperin
et al., 2014) and that general P3 anteriorization occurs as age increases (Kopp et al.,
Tones Task. For the first cognitive task, participants were seated with eyes
closed for 15 minutes and asked to press a button when they identified an infrequent
high-pitched target tone (2000Hz). Participants also heard infrequent, non-target low
tones (low-500Hz) and frequent standard tones (1000Hz). Tones were presented at
1500-2500ms second intervals. In each block of 10 tones, there was 1 high frequency
target tone, 1 low frequency distractor tone, and 8 standard tones. The minimum
number of standard tones between each target tone was 2. On average, there were 45
target tones presented in 15 minutes. Participants practiced this task before beginning
the experiment.
meditators and non-meditators, there was a Breath Counting session with the eyes
closed. This task was described simply as breath counting to naïve participants and as
a breath counting meditation for meditators. The rationale for using Breath Counting as
participants in all three groups, and all novice and experienced meditators had
experience with meditation focusing on the breath. The same tones were presented in
the background during the Breath Counting task as during the Tones task, but
participants were instructed to ignore the tones and keep track of their breath count.
Importantly, the purpose of the Breath Counting task is to allow for between-
subjects comparisons of priming effects during a task that could be performed by both
were instructed to press a button if they lost count of their breaths and continue
counting using their best estimate of their breath count to that point. The Meditation
Depth Index (MEDI) (Piron, 2001) and Stanford Sleepiness Scale (SSS) (Herscovitch,
1981) were administered after the Breath Counting session. The MEDI assessed the
subjective quality of attentional focus to breath counting. The Stanford Sleepiness Scale
was administered after the Breath Counting sessions to assess potential differences
that might be attributed to drowsiness from prolonged eye closure, although none were
found. Additionally, we calculated theta and alpha power for one-second epochs prior to
Nomenclature (MCN) at AF3/4, F7/8, F3/4, FC1/2, FC5/6, T7/8, C3/4, CP1/2, CP5/6,
P7/8, P3/4, P03/4, O1/2, Oz, Fz, Cz, and Pz. All EEG data were acquired at a sampling
0.1-70.0Hz. Online recordings referenced a common mode sense (CMS) and driven
al., 2014) and also important for the specific nature of the Breath Counting meditative
task. It was measured with a light elastic piezoelectric belt (Ambu-Sleepmate, Maryland)
around the participant’s chest near the diaphragm. Respiration rate was analyzed in
breath was counted whenever the respiratory voltage reading crossed zero in a positive
direction.
Electrophysiological Analyses. Data were analyzed from the Fz, Cz, and Pz
midline electrode sites. During offline processing data were re-referenced to linked
mastoids. Data were filtered offline using a 70Hz low pass filter, a 0.1Hz high pass filter,
and a 60Hz notch filter and analyzed in BrainVision Analyzer. Visual, semi-automatic
allowed voltage step of 50µV/ms; maximal allowed absolute difference 125µV within
interval length of 50ms; maximum EEG amplitudes allowed was +/- 75 µV and the
lowest allowed EEG activity was .5µV within interval length of 100ms. The EEG activity
To generate the ERPs for processing of the N2 and P3 peaks, data were
segmented -200ms before to 1000ms after stimulus presentations. The tone types were
11
then separated using distinct markers, averaged, and baseline corrected using 200ms
using these intervals N2 (200-300ms) and P3 (275-450ms). All peak estimates were
subject to visual inspection, and temporal windows were adjusted and reapplied if
necessary. These criteria were decided on a case-by-case basis for target tones. Inter-
rater reliability was achieved by having two researchers separately view the data and
one naïve participant with no discernible N1, P2, or N2 during Breath Counting,
although there was no issue with this person’s P3. Two experienced meditators had no
approximate values were kept in an effort to represent a complete, objective data set.
Following detection, discrete peak voltage values were exported from Brain Vision
Analyzer for further processing. Final N2 and P3 values were computed as the change
in voltage from the previous peak estimate (i.e., N2final = P1raw – N2raw, and P3final =
P3raw – N2raw). This computation was intended to control for deceptive individual
differences in absolute peak amplitudes resulting from general positive or negative drift
EEG frequency analysis was utilized to assess drowsiness and thus ensure ERP
differences were not simply related to differences in levels of alertness. The analysis
was performed on one-second epochs prior to all stimulus tones using the same pre-
processing and filtering techniques as the ERPs. A periodic Hanning window was
applied with a tapering of 20%. The frequency spectrum was generated using the Fast
Fourier Transformation (FFT). The resulting epoch FFTs were averaged and exported,
12
then the square root of power in frontal-midline theta (4-8 Hz) and posterior alpha (8-13
Hz) were calculated. The square root transform was used to improve normality of FFT
Statistical Analyses. Results were assessed using mixed design ANOVAs for N2 and
P3 amplitudes and total task respiration counts (SPSS v.21). Mixed 2 (Tones or Breath
task and by group. Univariate ANOVAs were used to assess N2 and P3 difference
differences in these measures as well as the MEDI and SSS. A separate 2x2 mixed
ANOVA that pooled novice and experienced meditator groups was also calculated.
Results
of more than one race (Table 1). A one-way ANOVA determined there were no
significant demographic differences among the groups. Novices had been practicing
meditation and/or mind-body activities for an average of 2.4 (SD = 2.5) years and
currently practiced 12.6 (SD = 7.7) minutes per day. Experienced meditators had been
practicing meditation and/or mind-body activities for an average of 22.6 (SD = 13.1)
years and presently practiced an average of 122.1 (SD = 180.9) minutes per day. High-
pitched target tones were the focus of ERP analyses from the Fz, Cz, and Pz sites
because we were looking for N2/P3 priming effects from the Tones condition to the
Breath Counting condition (see Table 2 for task summary). The non-target infrequent
and standard tone results as well as the N1/P2 components are discussed separately.
13
Please note that one novice participant was excluded from Pz analyses due to electrode
P3 ERP. IN all three groups there was a main within-subjects effect of task on P3
amplitudes elicited by infrequent target tones, F(1,39) = 58.02, p < .001, with primed P3
amplitudes attenuated during the Breath Counting task (M = 5.12µV) compared to the
Tones task (M = 5.96µV) across the Fz, Cz, and Pz midline electrode sites. There were
further assess the effects of meditation experience, we pooled novice and experienced
meditators into one meditation group and repeated the above analyses. For the pooled
meditator group, there was a priming effect on P3 amplitude following infrequent target
tones at the Fz site: F(1,40) = 42.34, p < .001; Cz site: F(1,40) = 34.31; p < .001; and Pz
site: F(1,40) = 42.23, p < .001. There was an interaction for target P3s at the Cz site as
well, F(1,40) = 4.56, p = .039 (Figure 1), with meditators showing a greater change in
peak-to-trough P3 amplitudes from the Tones task to the Breath Counting task. See
Figure 2 for average ERP waveforms elicited by target tones at the Cz site. Figures 3
N2 ERP. With three groups there were interactions for N2 responses to target
tones at the Cz site, F(2,39) = 3.96, p = .027, and Pz site, F(2,38) = 3.25, p = .05. With
pooled meditators, these group interactions were still present at the Cz site, F(1,40) =
6.25, p = .017, and Pz site, F(1,39) = 4.32, p = .044, for high/infrequent target tones
(Figures 5 & 6). At the Cz electrode site the effect was more pronounced, with
Tones task to the Breath Counting task. In both cases meditators on average had
greater N2 amplitudes during the Tones task and more attenuated N2 amplitudes during
Exploratory ERPs. This section will cover results for N1 and P2 ERPs as well as
responses to low infrequent non-target tones and frequent standard tones. These
analyses are exploratory, as N2/P3 responses to target tones were our primary
analyses. Thus, only group effects are of interest with these variables. We will report
pooled group results (meditators versus naïve participants) as they were the strongest.
Additional analyses on standard and low tones for P3 revealed no group effects
or interactions regarding low or standard tones. For N2 at the Pz site, there was a
responses to low tones than naive participants (M = -3.46µV) during the Tones task.
Meditators (M = -6.43µV) also had higher amplitude N2s than naïve participants (M = -
4.27µV) during Breath Counting. There were no significant results for N2 responses to
standard tones.
For N1, there was a general reduction in amplitude from the Tones task to the
Breath Counting task for all tone types (standard, high, low) at all electrode sites of
interest (Fz, Cz, Pz), all p values < .005, with the exception of Pz low tones, for which
participants and meditators was observed for low tones at the Cz midline site, F(1,40) =
5.94, p = .019. During Tones, meditators (M = -11.67µV) exhibited higher amplitude N1s
P2 results were more scattered. P2 amplitudes went down from Tones to Breath
Counting but only for standard tones across Fz, Cz, and Pz, with all p values < .008.
Like N1, there was a group effect for low tones at the Cz site, F(1,40) = 4.53, p = .040,
but the effect was for the Breath Counting task as meditators (M = 15.72µV) exhibited
waveform graphs are included for standard and low tones (Figures 7 & 8). These results
will not be discussed further since they were exploratory and separate from our original
research question.
meditator, between subjects) mixed ANOVAs revealed a main effect of task on total
automated respiration count for the Breath Counting session after the Tones task,
F(1,41) = 51.78, p < 001. Total respiration count decreased during the Breath Counting
task (M = 128.67) in comparison to the Tones task (M = 203.70). These tasks were
equivalent in length at 15 minutes. When the tasks were further divided into three
equivalent segments, there were significant respiration differences between the tasks at
each time point for the first segment, F(1,41) = 49.10, p < 001, second segment, F(1,41)
= 34.75, p < 001, and final segment, F(1,39) = 40.79, p < 001. Overall, there were no
Breath Counting tasks in the frequency content analyzed. We also assessed theta/alpha
there were no differences across groups in drowsiness measures. When theta and
alpha levels were measured separately however, there was a significant task by group
theta interaction, F(2,36) = 5.12, p = 01. When broken down by t-tests, we see that
naïve participants had greater theta (Theta M = .94) than experienced meditators (Theta
M = .54) during the Breath Counting task, potentially suggesting a less vigilant state
(Oken et al., 2006), although drowsiness does not explain the N2/P3 difference between
groups.
(Meditation Depth Index = MEDI) using t-tests. After the Breath Counting session, naïve
participants reported the lowest scores (M = 24), novices were in the middle (M = 27),
and experienced meditators had the highest MEDI scores (M = 28). The difference
between the naïve participants and experienced meditators was significant, p = .024,
ceiling effect. The average correct identification rate for target tones was 98% for
meditators and 97% for naïve participants, as measured by button press responses.
Misses due to time outs and false alarms were both taken into account in error rates.
There were no significant group differences in any of these factors. We did not assess
reaction time for the Tones task because participants were not instructed to press the
button as quickly as they could. One naïve group participant had to be excluded after
behavioral analyses revealed that they did not follow instructions. This person
responded to the infrequent low tones as targets in addition to high tones as targets,
thus their data had to be removed from all ERP analyses since the goal of the priming
17
task was compromised. Importantly, P3 data were only calculated from correct
Discussion
they were relevant versus irrelevant in order to capture mindful cognitive states across
naïve, novice, and experienced meditation groups. The Breath Counting session
accomplished a controlled state that was meditative as assessed by the self-rated MEDI
scale.
Previous work strongly suggests that attentional control increases with meditation
experience (Cahn & Polich, 2006). On average, meditators in this experiment had
greater N2 and P3 amplitudes than non-meditators while attending to targets during the
Tones task, and greater attenuation of N2 and P3 while engaged in the breath counting
meditation and ignoring the primed tones. This strongly suggests that meditators had
greater attentional control both while they were specifically attending to target tones as
well as while ignoring them during the Breath Counting meditative task.
The lack of differences between the novice and experienced groups might
achieved relatively early on in practice, although the benefits of longer term meditative
perhaps the group definitions and/or sample sizes weakened the results. The findings
presented here are not conclusive on this matter. The novices in this experiment were
18
actually quite practiced in meditation with an average of 2.4 years of experience, and
some novices had rather extensive formal training. Perhaps greater differences would
Drowsiness was also an a priori concern in all of our groups since drowsiness
attenuates P3, and increased theta is associated with drowsiness. However, our
This study had some limitations. All novice meditators reported practicing
meditation on breath, and for most, it was their primary practice. In contrast, meditation
on breath was just one among many practices for the experienced meditators. An
experienced Zen meditator participant also provided valuable feedback that the Breath
Counting meditation was essentially a dual performance task since, in Zen meditation,
eyes are usually open without a focus on breath counting. Thus, although we were
constrained by the experimental need to create a replicable and simple meditation task,
Breath Counting may not have captured the more profound meditation states that
experienced meditators may achieve. This potential meditation state difference between
novice and experienced mediators during the Breath Counting meditation was
documented by self-report, but this issue may have contributed to the lack of differences
have other habitual conditions used for their meditation practice that were not present in
this study, and these issues may have also contributed to the lack of differences
between experienced and novice meditators in our study. In the future, it may be
experience levels were better able to direct their attention than naïve participants. This
responses to target tone stimuli when they were relevant to the task and decreased
regardless of experience level. The results of this study have important implications for
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20.00
Peak to trough amplitudes μV
16.00
12.00 Controls
Meditators
8.00
4.00
0.00
Tones Breath Counting
*For target tones this interaction was significant, p = .039, with meditators showing a
greater change in peak-to-trough P3 amplitudes from the Tones to the Breath Counting
task.
* With novice and experienced groups combined, meditators showed a greater peak-
responding to infrequent target tones. Data here are reported from the Cz electrode
site. Please note that the ERP component labels are approximate denotations of
-1.00
Peak to trough amplitudes μV
-3.00
-5.00
-7.00
Controls
Meditators
-9.00
-11.00
-13.00
-15.00
Tones Breath Counting
*
*This interaction was significant at the Cz site, p = .017, with a more pronounced effect
than at the Pz site and meditators exhibiting a greater difference in N2 peak-to-trough
amplitudes from the Tones Task to Breath Counting.
Figure 6
-1.00
-3.00
Peak to trough amplitudes μV
-5.00
-7.00
Controls
Meditators
-9.00
-11.00
-13.00
-15.00
Tones Breath Counting
*This interaction was significant at the Pz site, p = .044, with meditators on average
showing greater peak-to-trough N2 amplitudes during the Tones task and attenuated N2
amplitudes during the Breath Counting task in comparison to controls.
Figure 7
*For frequent standard tones there were significant changes in N1 and P2 peak-to-
trough values from the Tones task to the Breath Counting task, but there were no group
effects, as expected.
Figure 8
*At the Cz site, there were significant changes in amplitude in N1 and P3 responses to
infrequent non-targets as well as a group effect for N1 responses, with meditators
showing higher amplitudes during the Tones task, p = .02. There was an additional
group effect for P2 with meditators showing higher amplitudes during the Breath
Counting task, p = .04.
24
N 42 13 15 14