Khalsa Et Al 2008 Psychophysiology
Khalsa Et Al 2008 Psychophysiology
Khalsa Et Al 2008 Psychophysiology
Department of Neurology and Neuroscience Program, University of Iowa, Iowa City, Iowa, USA
Brain and Creativity Institute, Department of Psychology and Neurology, University of Southern California, Los Angeles, California, USA
c
W. M. Keck Laboratory for Functional Brain Imaging and Behavior, Waisman Center, and Laboratory for Affective Neuroscience, Department of
Psychology, University of Wisconsin, Madison, Wisconsin, USA
b
Abstract
Attention to internal body sensations is practiced in most meditation traditions. Many traditions state that this practice
results in increased awareness of internal body sensations, but scientic studies evaluating this claim are lacking. We
predicted that experienced meditators would display performance superior to that of nonmeditators on heartbeat
detection, a standard noninvasive measure of resting interoceptive awareness. We compared two groups of meditators
(Tibetan Buddhist and Kundalini) to an age- and body mass index-matched group of nonmeditators. Contrary to our
prediction, we found no evidence that meditators were superior to nonmeditators in the heartbeat detection task, across
several sessions and respiratory modulation conditions. Compared to nonmeditators, however, meditators consistently
rated their interoceptive performance as superior and the difculty of the task as easier. These results provide evidence
against the notion that practicing attention to internal body sensations, a core feature of meditation, enhances the
ability to sense the heartbeat at rest.
Descriptors: Meditation, Interoception, Heartbeat detection, Awareness, Respiration
monly practiced under conditions of rest, the subjective experience of these interoceptive body sensations is also routinely
modulated through manipulations of the breath and musculoskeletal posture, particularly during the practice of yoga exercises
(Arambula, Peper, Kawakami, & Gibney, 2001; Bhajan Y, 2000;
Peng et al., 2004). Many traditions state that the practice of
attending to interoceptive sensations results in enhanced awareness of these sensations, and also assert that the meditation
practice results in enhanced awareness of a variety of other internal events, such as the ongoing experience of thoughts and
emotions (Kabat-Zinn, 1990; Korneld, 1996; Nairn, 2000).
The idea that a meditation practice would enhance interoceptive awareness is certainly plausible, but there is no scientic
evidence to support this claim. In the current study, we sought to
address this knowledge gap by studying interoceptive awareness
in experienced meditators.
Several methods for assessing interoceptive awareness have
been described, including gastrointestinal distension (Holzl,
Erasmus, & Moltner, 1996), adrenergic stimulation (Cameron
& Minoshima, 2002; Khalsa, Rudrauf, Sandesara, Olshansky, &
Tranel, in press), and heartbeat perception (Brener & Kluvitse,
1988; Schandry, 1981; Whitehead, Drescher, & Heiman, 1977).
The latter, heartbeat perception, is considered the standard and
preferred method for the noninvasive assessment of interoceptive
awareness, and factors modulating awareness of cardiac sensations have been extensively studied (Brener, Liu, & Ring, 1993;
Eichler & Katkin, 1994; Jones, 1994; Knapp, Ring, & Brener,
1997; Ring & Brener, 1992; Rouse, Jones, & Jones, 1988; Schandry, Bestler, & Montoya, 1993). Recently, functional neuro-
672
imaging studies have demonstrated that heartbeat perception
tasks activate a network of brain regions including the insula,
primary somatosensory cortex, and the anterior cingulate cortex
(Craig, 2002; Critchley, Wiens, Rotshtein, Ohman, & Dolan,
2004; Pollatos, Schandry, Auer, & Kaufmann, 2007). These
brain regions are considered necessary for the representation and
maintenance of the internal state of the organism (Craig, 2002;
Critchley et al., 2004; Pollatos et al., 2007) and for the conscious
experience of emotion and feelings (Damasio et al., 2000), lending further support to the notion that heartbeat perception is a
good index of interoception.
Although there are several techniques for assessing heartbeat
perception, the most commonly used methods are heartbeat detection and heartbeat tracking. During heartbeat detection, subjects determine whether an exteroceptive stimulus, such as a light
or a tone, is contemporaneous with their heartbeat sensation
(Brener & Kluvitse, 1988; Schneider, Ring, & Katkin, 1998;
Whitehead et al., 1977). Performance is indexed by the number of
correct responses reported by the subject (e.g., true positives and
true negatives), which also allows measurement of individual and
group response accuracy. Subjects are then classied as good
heartbeat detectors when their performance lies above chance
according to the binomial distribution (Katkin, Wiens, & Ohman, 2001; Schneider et al., 1998; Wiens & Palmer, 2001). During heartbeat tracking, subjects silently count their heartbeats
during brief, xed time periods. Performance is indexed by a
cardiac perception score, in which the number of counted heartbeats is contrasted with the number of actual heartbeats. Subjects
are classied as good heartbeat perceivers when their scores
fall above a predetermined level (Herbert, Ulbrich, & Schandry,
2007). Heartbeat detection has been the more commonly utilized
measure, perhaps because it appears to suffer from less methodological confounds than heartbeat tracking. Such confounds include the lack of a statistical measure to evaluate individual
performance, the possible inuence of a priori knowledge about
average heart rate on the rate of counting (Phillips, Jones, Rieger,
& Snell, 1999; Ring & Brener, 1996), and the insensitivity of
heartbeat tracking tasks to changes in heart rate (Windmann,
Schonecke, Frohlig, & Maldener, 1999). Consequently, we selected heartbeat detection as an index of interoceptive awareness.
We identied experienced meditators from two different meditation traditions that are extensively practiced within the United
States: Tibetan Buddhism and Kundalini yoga. These traditions
were selected to examine whether the effects of the meditation
practice on interoceptive awareness were consistent across traditions, despite the fact that each tradition adopts slightly differing approaches to the cultivation of interoceptive awareness. For
example, in Tibetan Buddhism interoceptive awareness is more
commonly cultivated while meditating under resting physiological conditions, whereas in Kundalini yoga interoceptive awareness is more commonly cultivated during yoga exercises that elicit
conditions of mild physiological arousal.
We hypothesized that the long-term practice of meditation
leads to enhanced interoceptive awareness. On this basis, we
predicted that experienced meditators from both traditions
would display enhanced awareness of heartbeat sensations during performance of a heartbeat detection task at rest. We further
hypothesized that experienced meditators would display metacognitive awareness of this enhancement, that is, knowledge of
accurate self performance, based on the rationale that meditation
cultivates a monitoring of experience at levels beyond mere interoceptive processing. We predicted that metacognitive aware-
Sex
Age (years)
Body mass index
Meditation practice
(years)
Cumulative
meditation
practice (hours)
Nonmeditators
Kundalini
Tibetan
Buddhist
4 M:13 F
50.6 9.6
24.8 5.1
00
5 M:12 F
52.1 8.6
24.0 5.2
29.3 6.4
7 M:6 F
48.8 10.1
22.3 3.3
24.7 8.4
00
17,660 9128
24,903 14,270
Methods
Participants
Seventeen nonmeditators, 17 Kundalini meditators, and 13 Tibetan Buddhist meditators participated in the study (Table 1).
Meditators were selected according to three criteria: (1) a minimum of 15 years of formal meditation practice, (2) a self reported strong daily practice, and (3) having attended at least one
meditation retreat during the previous year. Nonmeditators were
identied as individuals who had never attended a formal yoga or
meditation course and did not practice self-taught meditation.
All groups were matched with respect to age and body mass
index. Any participant reporting a history of neurological or
psychiatric disease was excluded from the study. Based on this
criterion, 1 Kundalini meditator and 2 nonmeditators were precluded from study participation. This study was approved by the
University of Iowas Institutional Review Board, and all participants provided informed consent prior to participation.
Tasks
Participants performed two types of tasks: a pulse detection familiarization task and a heartbeat detection task. Each task utilized identical stimuli but required a different attentional focus.
During pulse detection, participants took their nondominant
wrist pulse and were required to judge whether a train of exteroceptive stimuli (800-Hz, 50-ms tones) were simultaneous or
nonsimultaneous with pulse sensations. During heartbeat detection participants were not allowed to take their pulse and were
required to judge whether the tones were simultaneous or nonsimultaneous with perceived heartbeat sensations.
Tone Delivery
Tone delivery was triggered by each myocardial contraction, as
measured (indirectly) from the R-wave of a lead II electrocardiogram (MP100 acquisition unit, Biopac Systems, Inc.). During
simultaneous trials, tones were delivered at the same time as the
participants own nger pulse, approximately 250300 ms after
the R-wave1 (corresponding to the R-wave to pulse interval, or
RPI). The nger pulse was measured with an infrared photo1
This delay, around 250 to 300 ms, has been shown to lead to the
perception by accurate heartbeat detectors that heartbeats and tones are
simultaneous (Brener et al., 1993; Eichler & Katkin, 1994; Jones, 1994;
Knapp et al., 1997; Ring & Brener, 1992; Rouse et al., 1988; Schandry
et al., 1993).
673
Kundalini
Tibetan Buddhist
10.0
67.0 8.7
65.6 14.9
8.4
68.8 11.5
65.3 15.3
0.266 0.016
0.264 0.014
meditation instruction was given to the participants. We controlled for breathing patterns during heartbeat detection for two
related reasons: (1) spontaneous respiratory manipulations have
been observed to occur in subjects in the absence of an instruction
to breathe normally and have been suggested as a potential
strategy for maximizing heartbeat sensations (Jones, 1994; Weisz, Balazs, & Adam, 1988), and (2) several meditators were observed to spontaneously display Ujjai breathing during the
piloting phase of the study and this, in and of itself, could be a
basis for enhanced interoceptive accuracy. One Kundalini meditator was unable to perform the Ujjai breathing due to a preexisting respiratory condition and was excluded from the
heartbeat detection analysis.
Subjective Ratings
Prior to performing each task, participants were asked to predict
task accuracy (e.g., How good do you think you will be at [task
X]?) and difculty (How hard do you think [task X] will be?).
Upon completion of each task participants were also asked to
estimate task accuracy (How good do you think you were at
[task X]?) and difculty (How hard do you think [task X]
was?). Accuracy ratings could range from 1 (very bad) to 5 (very
good). Difculty ratings could range from 1 (very hard) to 5
(very easy). To familiarize participants with each task, all participants were instructed to sample tones from each trial type
(i.e., one simultaneous and one nonsimultaneous trial) for an
unlimited period prior to performing each task. In addition, taskrelated feedback was withheld from all participants until the
conclusion of the study.
Accuracy Measures
Accuracy scores were calculated using A 0 5 [1/21((HR
FP)(11HR FP))/(4HR(1 FP))], a nonparametric signal detection analog of d 0 ideal for signal detection conditions with low
trial numbers (Grier, 1971). In this formula, HR 5 hit rate and
FP 5 false positive. Following methods commonly utilized in
heartbeat detection studies (Brener et al., 1993; Jones, OLeary,
& Pipkin, 1984; Rouse et al., 1988), A 0 scores were normalized
using the following formula: 2arcsin (sqrt A 0 ), such that performance ranged from 0 to p (chance 5 p/2). Participants were further classied as good heartbeat detectors if they displayed
above chance performance during a block of testing, dened
as 16 out of 23 trials correct, po.05 per binomial test, again
following the approach of previous studies (Katkin et al., 2001;
Schneider et al., 1998; Wiens & Palmer, 2001). Because no
differences were predicted between the two groups of meditators,
the overall analyses examined the three groups separately. All
univariate repeated measures ANOVA tests were assessed for
violations of the sphericity assumption, and when violated, were
corrected with the HuynhFeldt method. In these instances the
corrected p values are reported, along with the HuynhFeldt
e correction.
Results
Participants
Both groups of meditators reported signicantly more years of
meditation practice, F(2, 44) 5 120.5, po.001, and hours of
cumulative meditation practice, F(2, 44) 5 31.9, po.001, than
the nonmeditators. The groups did not differ with respect to age
F(2, 44) 5 .45, p 5 .64, or BMI F(2, 44) 5 1.07, p 5 .35, (Table 1).
There were also no differences between the proportion of men
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Accuracy Measures
There were no group differences in accuracy on the pulse
detection task, F (2, 44) 5 1.27, p 5 .29. A 3 2 2 ANOVA
was run on heartbeat detection accuracy with group (Kundalini,
Tibetan Buddhist, nonmeditators) as the between-subjects factor
and with block (Block 1 and Block 2) and visit (Visit 1 and
Visit 2) as within-subject factors. There were no main effects
for group, F(2, 43) 5 0.30, p 5 .74, Zp 2 :01, block, F(1,
43) 5 0.69, p 5 .41, or visit, F(1, 43) 5 1.38, p 5 .25, and there
were no signicant interactions between group and visit, F(2,
43) 5 0.77, p 5 .47, block and visit, F(1, 43) 5 .00, p 5 .99, or
group and block and visit, F(2, 43) 5 1.03, p 5 .37, (Figure 1).
The lack of group differences was not accounted for by group
differences in response bias, dened as the tendency to favor one
particular response type over another, for either pulse detection,
F(2, 44) 5 0.1, p 5 .91, or heartbeat detection, F(2, 43) 5 1.3,
p 5 .28.
There were also no differences in the proportion of meditators
classied as good heartbeat detectors (Table 3). This was equally
true when the denition of good heartbeat detection performance
was restricted to above chance performance on two out of two
visits or loosened to above chance performance on at least one
out of two visits, for both tasks (Table 3).
Subjective Ratings
There were no group differences in the ratings of pulse detection
accuracy, F(2, 44) 5 0.12, p 5 .89, or pulse detection difculty,
F(2, 44) 5 .76, p 5 .48. However, a 3 2 2 ANOVA with two
repeated measures factors revealed signicant group differences
in ratings of heartbeat detection accuracy, F(2, 43) 5 5.77,
p 5 .007, Zp 2 :21, and heartbeat detection difculty, F(2,
Table 3. Percentage of Individuals Classied as Good Heartbeat Detectors for Each Block of Heartbeat Detectiona
No. of visits above chance
Good heartbeat detectors: HB1
NM (n 5 17)
KM (n 5 17)
w21 1=2 visits
w21 2=2 visits
TB (n 5 13)
w21 1=2 visits
w21 2=2 visits
0/2
1/2
2/2
0/2
1/2
2/2
47% (8)
35% (6)
18% (3)
47% (8)
w21 :49, p 5 .24
35% (6)
17% (3)
47% (8)
38% (6)
35% (6)
13% (2)
46% (6)
23% (3)
w1 5 .002, p 5 .48
w21 0, p 5 .49
31% (4)
18% (3)
50% (8)
w21 :31, p 5 .29
31% (4)
38% (5)
w1 5 .28, p 5 .30
w1 5 .02, p 5 .44
w1 5 .14, p 5 .35
31% (4)
w1 5 .11, p 5 .37
a
The numbers of individuals meeting each criterion are listed in parentheses. A Chi-square with one degree of freedom compares whether the proportion
of meditators classied as good heartbeat detectors differs from the nonmeditators. NM: nonmeditators. KM: Kundalini meditators. TB: Tibetan
Buddhist meditators. Only 16 Kundalini meditators completed testing in Block 2.
675
Discussion
The current ndings do not support the hypothesis that experienced meditators would display increased interoceptive awareness, as meditators did not differ from nonmeditators in
heartbeat detection accuracy. The lack of an effect of meditation on awareness of heartbeat sensations appears to be a reliable
nding. It occurs in two different groups of experienced meditators, measured at two time points, and with two different respiratory manipulation strategies. These results are consistent
with recent ndings by Nielsen and Kaszniak (2006), who reported a lack of signicant differences between a group of Buddhist meditators and a group of nonmeditators on a single session
of standard heartbeat detection. The Nielsen and Kaszniak study
had a small sample size, did not include comparison subjects
matched for age or body mass (Rouse et al., 1988), and was
conducted in a small number of sessions, limiting statistical
power. The present study, however, did not suffer from any of
these limitations and still did not reveal any effect of meditation
Table 4. Normalized Objective Heartbeat Detection Accuracy and Subjective Ratings of Heartbeat Detection Accuracya
Nonmeditators
Kundalini
Tibetan Buddhist
0.45 (0.10)
0.27 (0.08)
0.40 (0.10)
0.51 (0.09)
0.46 (0.14)
0.51 (0.10)
676
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(Received November 14, 2007; Accepted December 13, 2007)