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Neuroscience 281 (2014) 195–201

INFLUENCE OF LONG-TERM SAHAJA YOGA MEDITATION PRACTICE


ON EMOTIONAL PROCESSING IN THE BRAIN: AN ERP STUDY
N. V. REVA, * S. V. PAVLOV, K. V. LOKTEV, psychosomatic diseases (for reviews see Barnes and
V. V. KORENYOK AND L. I. AFTANAS Orme-Johnson, 2012; Chen et al., 2012; Hagins et al.,
Federal State Budgetary Institution ‘‘Scientific Research Institute 2013; Khoury et al., 2013), although little is known about
of Physiology and Basic Medicine’’ under the Siberian Branch of underlying brain mechanisms. According to a transac-
the Russian Academy of Medical Sciences, Timakova Street tional model of stress and coping (Lazarus and
4, 630117 Novosibirsk, Russia Folkman, 1984), individuals on an unconscious level, or
deliberately, produce appraisals of events with respect
Abstract—Despite growing interest in meditation as a tool for to their importance for well-being and the availability of
alternative therapy of stress-related and psychosomatic resources necessary for coping with these events. When
diseases, brain mechanisms of beneficial influences of med- a given stimulus is initially appraised as challenging,
itation practice on health and quality of life are still unclear. harmful, or threatening, an activation of physiological sys-
We propose that the key point is a persistent change in tems involved in the stress response co-occurs with a
emotional functioning, specifically the modulation of the subjective experience of distress. A persistent trend of
early appraisal of motivational significance of events. The overestimating the significance of the negative events
main aim was to study the effects of long-term meditation leads to excessive emotional reactivity and to wear-and-
practice on event-related brain potentials (ERPs) during
tear of visceral systems (McEwen and Gianaros, 2010).
affective picture viewing. ERPs were recorded in 20 long-term
Sahaja Yoga meditators and 20 control subjects without
It is likely that the beneficial effects of meditation
prior experience in meditation. The meditators’ mid-latency practices on health may be mediated by reduction of
(140–400 ms) ERPs were attenuated for both positive and negative affect along with an increase in positive
negative pictures (i.e. there were no arousal-related increases emotional attitude toward oneself and others, i.e.
in ERP positivity) and this effect was more prominent over the positive affectivity (Cahn and Polich, 2006; Wadlinger
right hemisphere. However, we found no differences in the and Isaacowitz, 2011). A plausible way to reach this state
long latency (400–800 ms) responses to emotional images, is the reduction of the significance of negative events dur-
associated with meditation practice. In addition we found ing the evaluative stage of emotional response. Indeed,
stronger ERP negativity in the time window 200–300 ms for the metacognitive stance of mindfulness, inherent in
meditators compared to the controls, regardless of picture
many meditative styles, can moderate the impact of
valence. We assume that long-term meditation practice
enhances frontal top-down control over fast automatic
potentially distressing psychological content. It may be
salience detection, based on amygdala functions. assumed that the process of mindfulness extricates atten-
Ó 2014 IBRO. Published by Elsevier Ltd. All rights reserved. tion from being fixated on evaluative language, enabling
nonjudgmental, metacognitive awareness of thoughts
and feelings, so one is able to let go of clinging to memo-
ries of the past and hopes and fears of the future, based
Key words: meditation, mindfulness, emotion, ERP, affective on habitual patterns of thought (Garland et al., 2009).
images. Therefore, we assume that due to meditation practice
the process of appraisal of an event’s motivational signif-
icance undergoes a change which allows an individual to
INTRODUCTION
control emerging emotions; moreover, this change gradu-
Recent years have seen growing interest in meditation as ally becomes automatic.
a tool for alternative therapy of stress-related and The event-related brain potential (ERP) findings of
Sobolewski et al. (2011) provide some support for different
*Corresponding author. Address: Laboratory Psychophysiology, Fed- emotional processing in Buddhist meditation practitioners:
eral State Budgetary Institution ‘‘Scientific Research Institute of meditators were less affected by stimuli with adverse emo-
Physiology and Basic Medicine’’ under the Siberian Branch of the tional load (the effect of greater late positive potential (LPP)
Russian Academy of Medical Sciences, Timakova Street 4, 630117,
Novosibirsk, Russia. Tel: +7-383-335-98-55, +7-383-335-97-37; amplitude for negative International Affective Picture Sys-
fax: +7-383-335-97-54. tem (IAPS) images was not replicated in the case of medi-
E-mail addresses: n.v.reva@physiol.ru, iph@physiol.ru (N. V. Reva). tators’ frontal scalp regions), while processing of positive
Abbreviations: ANOVAs, analysis of variances; C, central; CP,
centroparietal; Cz, central midline; EEG, electroencephalography;
stimuli remained unaltered. In another ERP research1
ERPs, event-related brain potentials; F, frontal; FC, frontocentral; Fz,
frontal midline; IAPS, International Affective Picture System; LPP, late
1
positive potential; P, parietal; P3a, early P300. The research was not published as a journal article.

http://dx.doi.org/10.1016/j.neuroscience.2014.09.053
0306-4522/Ó 2014 IBRO. Published by Elsevier Ltd. All rights reserved.

195
196 N. V. Reva et al. / Neuroscience 281 (2014) 195–201

(Marhe, 2007) no effects of meditation on emotional pro- negative or positive emotions or being in a neutral
cessing were indicated for Sudarshan Kriya Yoga. Thus, emotional state.
the data obtained are insufficient to draw any conclusions
about the impact of meditation practice on the evaluative Procedure
component of emotional responses.
Therefore in this study we aimed to investigate the It should be noted that this study was a part of the
influence of long-term Sahaja Yoga meditation on the emotional regulation study, so rationale for block-wise
ERP response to affective pictorial stimuli. This stimulus presentation and cueing was defined by task
technique, more related to mindfulness than a requirements (for details see Pavlov et al., 2014b). Only
concentrative type of meditation, is characterized by a unregulated trials were analyzed in this study.
mental state of ‘‘thoughtless awareness’’, or ‘‘mental During the experiment participants sat in a
silence’’ and is accompanied by the experience of bliss. comfortable chair in a dimmed room. After attachment
In general, the outcome of this meditative technique, as of the sensors, a 7-min resting period (2 min with closed
most others, is a sense of relaxation and positive mood eyes and 5 min with open eyes) was recorded. Then,
and a feeling of benevolence toward oneself and others participants were given instructions describing the
(Rai, 1993; Aftanas and Golocheikine, 2001; Manocha experimental procedure and performed a practice block
et al., 2012). Moreover, in recent eye-tracking research (not used for further analyses) including 10 trials. Each
the shift of attention toward happy faces was obtained trial was composed of four events: cue word (look,
for Sahaja Yoga meditators, evidencing positive affective increase, decrease) (2.5 s), image (neutral, negative,
bias (Pavlov et al., 2014a). positive) (5 s), subjective emotional report (3–4 s), blank
Because it was recently shown that within the scope of screen (2.5 s). While the image remained on the screen,
standard categories the amplitude of the LPP significantly participants performed the operations specified by the
depends on the image content (Anokhin et al., 2006; prior instructional cue. During unregulated trials (cue
Weinberg and Hajcak, 2010; Ferri et al., 2012), we used word ‘‘look’’) participants were instructed simply to look
a homogeneous set of images depicting people (the at the image and let themselves respond naturally. All
objects for empathy) in appropriate life situations trials were broken down into four experimental blocks.
(Pavlov et al., 2014b). Each of the four experimental blocks included five
We assume that in the case of negative emotions the sequentially presented series, consisting of eight trials
arousal-related increase in positive components of ERP, with similar instructional cues (i.e., eight unregulated
in particular LPP, will be reduced, reflecting less neutral, eight unregulated positive, eight unregulated
motivational significance of this stimuli for Sahaja Yoga negative, eight regulated positive, and eight regulated
meditators. Since long-term meditation practice favors negative trials). Series of sequences were
developing of positive affective bias, we assume higher counterbalanced across blocks. There was a break of
ERP reactivity (increase in positivity) in response to 5 min after each experimental block.
positive images in Sahaja Yoga meditators versus
controls. MEASURES
Subjective emotional report
EXPERIMENTAL PROCEDURES After the image offset, two dimensions of valence and
Participants arousal (in a nine-point scale for each dimension) were
assessed using a computerized Self-Assessment
Two groups of healthy right-handed males participated in Manikin (SAM) (Bradley and Lang, 1994).
our study. The experimental group included 20
experienced long-term Sahaja Yoga meditators
Electroencephalography (EEG)
(meditators, mean age = 36.30, SD = 9.41; mean
meditation experience = 11.45 years, SD = 4.35) and EEG recordings (62-channel, bandpass 0.08–120 Hz,
20 age-matched healthy controls with no meditation sampling frequency 1000 Hz) were obtained
experience (controls, mean age = 33.55, SD = 5.48). monopolarly using the BrainProduct Acquisition 1.1
The age difference between meditators and controls program and a QuickAmp (Brain Products GmBh,
was insignificant (two tailed t-test, t = 0.99, p < 0.33). Munich, Germany) system via a modified 64-channel
All the subjects gave written informed consent and were cap with inbuilt Ag/AgCl electrodes (QuikCap,
paid for participation. NeuroSoft, Inc., Charlotte, NC, USA). A common
average reference was used. Electrode impedances
were kept at <5 kO. Horizontal and vertical
Stimuli
electrooculographic activity (EOG) was measured in a
One hundred and sixty images (151 from free websites, 9 bipolar configuration laterally at the outer canthi of each
from the International Affective Picture System (IAPS, eye and above and below the right eye, off-line
Lang et al., 1999)), including 32 neutral (people in emo- correction of EEG recordings was performed with
tionally neutral situations), 64 negative (loss, accidents), Gratton’s algorithm (Gratton et al., 1983). ERP epochs
and 64 positive (attractive women, family) photos were were extracted from 200 to 2000 ms relative to stimulus
selected for the study. All pictures included people with presentation onset, visually checked for residual oculo-
well-distinguishable facial expressions, experiencing motor, myographic, motor, DC-drift and other artifacts,
N. V. Reva et al. / Neuroscience 281 (2014) 195–201 197

and low-pass filtered at 20 Hz (48 dB/oct). Segments rated positive images as significantly more pleasant as
were baseline corrected to the 200-ms pre-stimulus per- compared to negative and neutral, and negative images
iod. Stimulus-locked ERPs were constructed by sepa- were rated as significantly more unpleasant than neutral
rately averaging trials for each emotion category in the (all p < .001). Arousal was rated significantly higher for
free-viewing condition and for positive and negative pic- positive and negative images in comparison to neutral
tures that followed reappraisal instructions. The ERP images (all p < .001). No differences in arousal ratings
was quantified as mean level of activity within five sepa- were found between positive and negative images (all
rate time windows: 80–140 ms for N100, 140–200 ms p > .54).
for N170 and P200; 200–300 ms for N200 and early
P300 (P3a), 300–400 ms for late P300 (P3b), and 400– ERP
800 ms for LPP. The window analysis was preferred to
peak analysis for the following reasons. Contrary to For the 80–140-ms time window no effects or interactions
strictly defined cognitive paradigms, in case of complex with Group or Emotional Category factors were obtained
emotional visual stimuli the main ERP components may (Fig. 1).
overlap, resulting in difficulties in component recognition. The main effect of Group was revealed for the time
Moreover, the recognizability of the components can differ window 200–300 ms (F(1,38) = 7.21; p < 0.011,
systematically depending on group affiliation. The window gp2 = .16), evidencing more negative potential values
analysis makes it possible to overcome these problems for meditators regardless of stimulus category (Fig. 2).
and to test whether ERP segments without consistent In spite of non-significant interactions with topographic
peaks are statistically different across groups or condi- factors, the ANOVAs for separate electrodes showed
tions (Hoormann et al., 1998). For statistical analyses that group differences were located predominantly over
the data of 25 electrodes, less sensitive to low-frequency central cortical regions (C3, C1, Cz, C2, C4, CP3, CP1;
artifacts, were used (F3, F1, frontal midline (Fz), F2, F4, all p < 0.05).
FC3, FC1, FCz, FC2, FC4, C3, C1, central midline (Cz), The Group  Emotional Category interactions were
C2, C4, CP3, CP1, CPz, CP2, CP4, P3, P1, Pz, P2, P4). revealed for 140–200-ms (F(2,76) = 3.41; p < 0.041,
gp2 = .08) and 200–300-ms (F(2,76) = 3.54; p < 0.035,
gp2 = .09) time windows, along with the Group 
Data analysis. Group differences in the effects of
Emotional Category  Sagittality interactions for 140–
emotional salience on the subjective emotional report
200-ms (F(8,304) = 2.78; p < 0.026, gp2 = .07), 200–
were analyzed for valence and arousal scores using
300-ms (F(8,304) = 3.30; p < 0.014, gp2 = .08), and
repeated measures analysis of variances (ANOVAs)
300–400-ms (F(8,304) = 2.89; p < 0.020, gp2 = .07)
with factors of Group (meditators, controls) and Emotion
time windows. According to these interactions the
Category (neutral, negative and positive).
arousal-related increases in positivity were less
Effects of emotional salience on ERP were analyzed
pronounced in meditators than in controls mainly in the
for each time window using repeated measures
right hemisphere (Fig. 3). The latter was confirmed with
ANOVAs with Emotion Category (neutral, negative and
the Group  Emotional Category interactions, revealed
positive), Caudality (frontal—F (F3, F1, Fz, F2, F4),
in the right hemisphere both for medial (140–200 ms:
frontocentral—FC (FC3, FC1, FCz, FC2, FC4), central—
F(2,76) = 8.51; p < 0.001, gp2 = .18; 200–300 ms:
C (C3, C1, Cz, C2, C4), centroparietal—CP (CP3, CP1,
F(2,76) = 8.96; p < 0.001, gp2 = .19; 300–400 ms:
CPz, CP2, CP4), parietal—P (P3, P1, Pz, P2, P4)) and
F(2,76) = 4.98; p < 0.011, gp2 = .12) and lateral (140–
Sagittality (left lateral (F3, FC3, C3, CP3, P3), left medial
200ms: F(2,76) = 5.44; p < 0.007, gp2 = .13; 200–300
(F1, FC1, C1, CP1, P1), medial (Fz, FCz, Cz, CPz, Pz),
ms: F(2,76) = 7.32; p < 0.002, gp2 = .16; 300–400 ms:
right medial (F2, FC2, C2, CP2, P2), right lateral (F4,
F(2,76) = 6.25; p < 0.004, gp2 = .14) cortical regions.
FC4, C4, CP4, P4)) as within-subject factors and Group
Post-hoc analyses revealed that in the time window
(meditators, control) as the independent factor.
140–200 ms controls demonstrated a higher level of
For all analyses, degrees of freedom were
potential for positive stimuli in comparison with neutral
Greenhouse–Geisser corrected where appropriate. All
ones (p < 0.001) and a lack of difference between
the post hoc comparisons were evaluated by means of
negative and neutral stimuli, whereas meditators showed
the Tukey test. Effect sizes are reported using partial
no difference between positive and neutral stimuli along
eta squared (g2p ).
with a lower potential level for negative stimuli in
comparison with neutral ones (p < 0.027). For the time
RESULTS windows 200–300 ms and 300–400 ms controls showed
higher positivity for both types of emotional stimuli in
Subjective emotional report
comparison to neutral ones (all p < 0.001), whereas no
Mean valence and arousal scores for neutral, negative significant differences among stimulus categories were
and positive images for meditators and controls are obtained for meditators. Concerning the left hemisphere
shown in Table 1. ANOVAs did not reveal significant and the midline only common effects of Emotional
effects of group and Group  Emotion Category Category were revealed, on the whole evidencing higher
interactions, but revealed significant effects of Emotion positivity level for emotional stimuli than for neutral.
Category for valence (F(2,76) = 304.10, p < .001, For the 400–800-ms time window no effects or
gp2 = .89) and arousal (F(2,76) = 46.38, p < .001, interactions with Group factor were obtained, although
gp2 = .55), showing that both meditators and controls the effects of Emotional Category (F(2,76) = 54.10;
198 N. V. Reva et al. / Neuroscience 281 (2014) 195–201

Table 1. Mean valence and arousal scores for neutral, negative and positive images for meditators and controls

Group Controls (N = 20) Meditators (N = 20)


Images Valence Arousal Valence Arousal
M SD M SD M SD M SD

Neutral 5.13 0.43 3.23 2.15 5.75 0.95 2.80 2.04


Negative 3.20 0.67 5.26 2.10 3.07 0.76 4.80 2.25
Positive 7.24 0.79 5.86 1.88 7.53 0.80 4.42 2.13
Note: M, mean values; SD, standard deviation.

Fig. 1. ERP waveforms for neutral, negative and positive images


from midline leads, averaged across all subjects.

Fig. 3. Difference ERP waves (emotional vs. neutral) from right


hemisphere leads for the meditation and control group.

DISCUSSION
Fig. 2. (A) ERP waveforms of the meditation and control group from
the Cz lead averaged across emotional categories. (B) Difference In the present study we found no differences between
map (meditation vs. control) for the 200–300-ms time window. long-term Sahaja Yoga meditators and controls for the
time interval, corresponding to LPP (400–800 ms),
however, we revealed between-group ERP effects in the
p < 0.0001, gp2 = .59) and Emotional Category  earlier time windows (140–400 ms). In the time window
Caudality interaction (F(8,304) = 24.28; p < 0.0001, 200–300 ms predominantly over the central sites the
gp2 = .39) were highly significant. Post-hoc analyses meditation group demonstrated higher mean negative
revealed that both types of emotional stimuli elicited amplitudes than the control group, regardless of picture
more positive potential levels than neutral ones (Fig. 1). valence. We also found that meditators’ mid-latency
For the positive stimuli significant differences were (140–400 ms) ERPs were attenuated for both positive
located across the head except parietal regions (all and negative pictures (there was no increase in the
p < 0.0001), for the negative stimuli – over central, positivity or decrease in negativity of emotional ERP in
centroparietal and parietal areas (all p < 0.0001). The comparison to neutral pictures) and these effects were
higher potential level for positive stimuli in comparison more prominent over the right hemisphere.
to negative stimuli were revealed over frontal, The former finding is in accordance with the ERP
frontocentral and central cortical regions (all p < 0.009), research of Sudarshan Kriya meditators by Marhe
along with the lower levels over parietal loci (p < 0.002). (2007), where group differences were found at central
N. V. Reva et al. / Neuroscience 281 (2014) 195–201 199

(higher negative amplitudes) and parietooccipital (higher and prefrontal areas during the meditation state (Cahn
positive amplitudes) brain regions in the 200–400-ms time and Polich, 2006). Moreover, the longitudinal decrease
window for pictorial (IAPS) stimuli regardless of its in right amygdala activation in response to affective
valence. The ERP component, which contributes most images was revealed after training subjects in mindful-
to negativity in the 200–300-ms time window, apparently attention meditation (Desbordes et al., 2012).
belongs to the family of attention-related N2 components The peculiar process inherent in most meditation
that are maximal over frontal or central scalp sites when practices is the so-called labeling, i.e. verbal non-
elicited by visual stimuli. In the Pritchard et al. (1991) clas- emotional categorization of incoming external
sification scheme, the N2b was larger for nontargets than information. The process of verbally labeling affective
for targets, but elicited by both, had a central scalp distri- stimuli may disrupt or inhibit automatic affective
bution in both the auditory and visual modality, and was responses, reducing their intensity and duration along
accompanied by a P3a. Patel and Azzam (2005) defined with more effective cognitive [detached] recognition of
the N2b as a negativity of central cortical distribution seen emotions. According to functional magnetic resonance
only during conscious stimulus attention. Folstein and imaging (fMRI) data an experimental task consisting in
Van Petten (2008) adopt neutral terms of anterior N2, rating or verbally labeling emotions reduced activation in
referring to a negative-going wave with a frontal or central the amygdala and activated the right ventrolateral
scalp maximum and corresponding to Pritchard et al.’s prefrontal cortex compared to passive viewing or to a
(1991) N2b. They further divide N2 subcomponents into match-to-sample task (Hariri et al., 2000; Taylor et al.,
the deviance-related or novelty N2 (for which they advo- 2003; Lieberman et al., 2007). Moreover, strong negative
cate the name ‘‘N2b’’) and the control-related N2. It is associations were found between areas of prefrontal cor-
notable that in young adults, but not in older adults, the tex and right amygdala responses during affect labeling in
novel stimuli elicited a very large N2, which was of maxi- participants high in mindfulness but not in participants low
mal amplitude at the Cz, slightly smaller at the Fz, and in mindfulness (Creswell et al., 2007). Thus, we can
barely visible at both the prefrontal and occipital midline assume that labeling is the suitable candidate process
sites (Fpz and Oz) (Folstein and Van Petten, 2008). Tak- for mediating mindfulness effects on early appraisals of
ing into account that long-term meditation practice emotional information.
improves attention toward cognitive tasks (Srinivasan It should be noted that the data obtained contradict
and Baijal, 2007; Lutz et al., 2008, 2009; Chiesa et al., with our hypothesis about higher positivity of ERP
2011; van Leeuwen et al., 2012; Moore et al., 2012), we components in response to positive stimuli in
can interpret higher central negativity in meditators as meditators. The possible explanation is that meditators
an increased N2b component, characterizing the focus on internally generated positive experience (Rai,
enhanced efficiency of selective information processing 1993). It is noteworthy, that a recent eye-tracking study
(Patel and Azzam, 2005; Folstein and Van Petten, 2008). of this sample of meditators revealed positive affective
It is well established that emotional arousal elicits a bias (preference of happy faces) during maintenance of
positive-going waveform, and the underlying factor attention, but not in initial orienting (Pavlov et al., 2014a).
determining amplitude modulations is selective attention Since we found no difference in LPP (400–800 ms)
toward objects within the affective image that are response to arousing images between meditators and
assumed to be of intrinsic relevance (for review see control participants, we believe that voluntary attention,
Olofsson et al., 2008). Processing within the 150–300- initial memorization and experience remain unchanged
ms latency range mainly reflects automatic (‘‘bottom- in meditators (Olofsson et al., 2008). The lack of group dif-
up’’) stimulus discrimination, whereas the later segments ferences in subjective ratings is in agreement with this
of the affective ERP (i.e. P300 and LPP/slow wave) are interpretation. Apparently the emotional stability of Sahaja
sensitive to ‘‘top-down’’ control. The latter is confirmed Yoga meditators can hardly be seen as general flattening
by modulations of these components by concurrent cogni- of the emotional responses to external events, but rather
tive tasks or by emotional regulation such as reappraisal as the ability to prevent intense experiences and full-
(Polich, 2007; Olofsson et al., 2008; Hajcak et al., scale, potentially harmful, physiological reactions in
2010). Therefore we can assume that long-term Sahaja response to strong stimuli. Indeed, reduced emotional
Yoga meditators are characterized by changes in auto- arousal, indexed by alpha and gamma EEG oscillations,
matic ‘‘bottom-up’’ processes of salience detection. It is was shown for Sahaja Yoga meditators during aversive
known that early detection of motivational salience is film viewing (Aftanas and Golosheykin, 2005). We
mediated by amygdales, controlled by frontal/prefrontal hypothesize that emotional events of moderate intensity
cortical regions (Morrison and Salzman, 2010; Pessoa, (like those used in this study) can freely pass appraisal
2010; Ochsner et al., 2012). Moreover, the right inferior gates, accompanied by only transient early ERP modula-
frontal cortex in humans is critical for inhibiting response tions, whereas highly arousing stimuli would heavily acti-
tendencies in a variety of tasks (Aron et al., 2004, 2014; vate regulatory mechanisms, including LPP reduction.
Ochsner et al., 2012). Neurophysiologically we can As a whole our study provides support to the concept
expect that meditative attentional trainings will lead to that meditation practices improve attentional control and
sustained changes in the interactions between amygdales capacities for emotional regulation. We obtained ERP
and frontal cortical regions, with the redistribution of the evidence that long-term Sahaja Yoga meditation
leading role in favor of the latter. Indeed, recent practice enhances frontal top-down control over fast
neuroimaging research demonstrates activation of frontal automatic salience detection, based on amygdala
200 N. V. Reva et al. / Neuroscience 281 (2014) 195–201

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(Accepted 25 September 2014)


(Available online 2 October 2014)

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