Khalsa 2008 Psychophysiology
Khalsa 2008 Psychophysiology
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 scientific 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 difficulty 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
Meditation is a form of mental training that has been practiced monly practiced under conditions of rest, the subjective experi-
for thousands of years that can be conceptualized as a family of ence of these interoceptive body sensations is also routinely
complex emotional and attentional regulatory training regimens modulated through manipulations of the breath and musculo-
developed for various ends, including the cultivation of well- skeletal posture, particularly during the practice of yoga exercises
being and emotional balance (Lutz, Dunne, & Davidson, 2007). (Arambula, Peper, Kawakami, & Gibney, 2001; Bhajan Y, 2000;
Although typically practiced in the context of spiritual traditions, Peng et al., 2004). Many traditions state that the practice of
there has been a notable increase in the therapeutic application of attending to interoceptive sensations results in enhanced aware-
meditation as a complement in alternative medicine. (Arias, ness of these sensations, and also assert that the meditation
Steinberg, Banga, & Trestman, 2006; Astin, Shapiro, Eisenberg, practice results in enhanced awareness of a variety of other in-
& Forys, 2003; Barnes, Powell-Griner, McFann, & Nahin, ternal events, such as the ongoing experience of thoughts and
2004). emotions (Kabat-Zinn, 1990; Kornfield, 1996; Nairn, 2000).
Most meditation traditions incorporate attention to internal The idea that a meditation practice would enhance inter-
body sensations as a component of the practice, particularly in oceptive awareness is certainly plausible, but there is no scientific
the beginning stages of instruction, possibly because the avail- evidence to support this claim. In the current study, we sought to
ability of these sensations from moment to moment makes them address this knowledge gap by studying interoceptive awareness
a convenient object to focus on. The most commonly attended in experienced meditators.
body sensations include the breath, the position of the joints Several methods for assessing interoceptive awareness have
(proprioception), the degree of muscle tension, and the heartbeat been described, including gastrointestinal distension (Holzl,
(Kabat-Zinn, 1990; Kornfield, 1996; Nairn, 2000; Selby, 1992). Erasmus, & Moltner, 1996), adrenergic stimulation (Cameron
Although attention to internal body sensations is most com- & Minoshima, 2002; Khalsa, Rudrauf, Sandesara, Olshansky, &
Tranel, in press), and heartbeat perception (Brener & Kluvitse,
We thank M. Ricard and A. Francis for assistance with participant 1988; Schandry, 1981; Whitehead, Drescher, & Heiman, 1977).
recruitment. The project was supported by NIH NCCAM F31AT003061 The latter, heartbeat perception, is considered the standard and
from the National Center For Complementary & Alternative Medicine preferred method for the noninvasive assessment of interoceptive
(NCCAM) (S.K.), by the Mind and Life Institute (S.K.), by NCCAM awareness, and factors modulating awareness of cardiac sensa-
U01AT002114-01A1 (A.L.), and by NIDA R01 DA022549 (D.T.). tions have been extensively studied (Brener, Liu, & Ring, 1993;
Address reprint requests to: Sahib S. Khalsa, B.S., Neuroscience
Graduate Program, Department of Neurology, University of Iowa,
Eichler & Katkin, 1994; Jones, 1994; Knapp, Ring, & Brener,
200 Hawkins Drive, Iowa City, IA 52242, USA. E-mail: sahib-khalsa 1997; Ring & Brener, 1992; Rouse, Jones, & Jones, 1988; Schan-
@[Link] dry, Bestler, & Montoya, 1993). Recently, functional neuro-
671
672 S.S. Khalsa et al.
imaging studies have demonstrated that heartbeat perception Table 1. Demographic Data for All Three Groups (Means SD)
tasks activate a network of brain regions including the insula,
primary somatosensory cortex, and the anterior cingulate cortex Tibetan
(Craig, 2002; Critchley, Wiens, Rotshtein, Ohman, & Dolan, Nonmeditators Kundalini Buddhist
2004; Pollatos, Schandry, Auer, & Kaufmann, 2007). These Sex 4 M:13 F 5 M:12 F 7 M:6 F
brain regions are considered necessary for the representation and Age (years) 50.6 9.6 52.1 8.6 48.8 10.1
maintenance of the internal state of the organism (Craig, 2002; Body mass index 24.8 5.1 24.0 5.2 22.3 3.3
Meditation practice 00 29.3 6.4 24.7 8.4
Critchley et al., 2004; Pollatos et al., 2007) and for the conscious (years)
experience of emotion and feelings (Damasio et al., 2000), lend- Cumulative 00 17,660 9128 24,903 14,270
ing further support to the notion that heartbeat perception is a meditation
good index of interoception. practice (hours)
Although there are several techniques for assessing heartbeat
perception, the most commonly used methods are heartbeat de-
tection and heartbeat tracking. During heartbeat detection, sub- ness would be reflected through more accurate subjective ratings
jects determine whether an exteroceptive stimulus, such as a light of interoceptive task performance in both groups of meditators
or a tone, is contemporaneous with their heartbeat sensation than in nonmeditators.
(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 Methods
true negatives), which also allows measurement of individual and
group response accuracy. Subjects are then classified as ‘‘good Participants
heartbeat detectors’’ when their performance lies above chance Seventeen nonmeditators, 17 Kundalini meditators, and 13 Ti-
according to the binomial distribution (Katkin, Wiens, & Oh- betan Buddhist meditators participated in the study (Table 1).
man, 2001; Schneider et al., 1998; Wiens & Palmer, 2001). Dur- Meditators were selected according to three criteria: (1) a min-
ing heartbeat tracking, subjects silently count their heartbeats imum of 15 years of formal meditation practice, (2) a self re-
during brief, fixed time periods. Performance is indexed by a ported strong daily practice, and (3) having attended at least one
cardiac perception score, in which the number of counted heart- meditation retreat during the previous year. Nonmeditators were
beats is contrasted with the number of actual heartbeats. Subjects identified as individuals who had never attended a formal yoga or
are classified as ‘‘good heartbeat perceivers’’ when their scores meditation course and did not practice self-taught meditation.
fall above a predetermined level (Herbert, Ulbrich, & Schandry, All groups were matched with respect to age and body mass
2007). Heartbeat detection has been the more commonly utilized index. Any participant reporting a history of neurological or
measure, perhaps because it appears to suffer from less method- psychiatric disease was excluded from the study. Based on this
ological confounds than heartbeat tracking. Such confounds in- criterion, 1 Kundalini meditator and 2 nonmeditators were pre-
clude the lack of a statistical measure to evaluate individual cluded from study participation. This study was approved by the
performance, the possible influence of a priori knowledge about University of Iowa’s Institutional Review Board, and all partic-
average heart rate on the rate of counting (Phillips, Jones, Rieger, ipants provided informed consent prior to participation.
& Snell, 1999; Ring & Brener, 1996), and the insensitivity of
heartbeat tracking tasks to changes in heart rate (Windmann, Tasks
Schonecke, Frohlig, & Maldener, 1999). Consequently, we se- Participants performed two types of tasks: a pulse detection fa-
lected heartbeat detection as an index of interoceptive awareness. miliarization task and a heartbeat detection task. Each task uti-
We identified experienced meditators from two different med- lized identical stimuli but required a different attentional focus.
itation traditions that are extensively practiced within the United During pulse detection, participants took their nondominant
States: Tibetan Buddhism and Kundalini yoga. These traditions wrist pulse and were required to judge whether a train of ext-
were selected to examine whether the effects of the meditation eroceptive stimuli (800-Hz, 50-ms tones) were simultaneous or
practice on interoceptive awareness were consistent across tra- nonsimultaneous with pulse sensations. During heartbeat detec-
ditions, despite the fact that each tradition adopts slightly differ- tion participants were not allowed to take their pulse and were
ing approaches to the cultivation of interoceptive awareness. For required to judge whether the tones were simultaneous or non-
example, in Tibetan Buddhism interoceptive awareness is more simultaneous with perceived heartbeat sensations.
commonly cultivated while meditating under resting physiolog-
ical conditions, whereas in Kundalini yoga interoceptive aware- Tone Delivery
ness is more commonly cultivated during yoga exercises that elicit Tone delivery was triggered by each myocardial contraction, as
conditions of mild physiological arousal. measured (indirectly) from the R-wave of a lead II electrocar-
We hypothesized that the long-term practice of meditation diogram (MP100 acquisition unit, Biopac Systems, Inc.). During
leads to enhanced interoceptive awareness. On this basis, we simultaneous trials, tones were delivered at the same time as the
predicted that experienced meditators from both traditions participant’s own finger pulse, approximately 250–300 ms after
would display enhanced awareness of heartbeat sensations dur- the R-wave1 (corresponding to the R-wave to pulse interval, or
ing performance of a heartbeat detection task at rest. We further RPI). The finger pulse was measured with an infrared photo-
hypothesized that experienced meditators would display meta- 1
cognitive awareness of this enhancement, that is, knowledge of This delay, around 250 to 300 ms, has been shown to lead to the
perception by accurate heartbeat detectors that heartbeats and tones are
accurate self performance, based on the rationale that meditation ‘‘simultaneous’’ (Brener et al., 1993; Eichler & Katkin, 1994; Jones, 1994;
cultivates a monitoring of experience at levels beyond mere in- Knapp et al., 1997; Ring & Brener, 1992; Rouse et al., 1988; Schandry
teroceptive processing. We predicted that metacognitive aware- et al., 1993).
Meditation and interoception 673
Table 2. Cardiovascular Parameters for All Three Groups meditation instruction was given to the participants. We con-
(Means SD) trolled for breathing patterns during heartbeat detection for two
related reasons: (1) spontaneous respiratory manipulations have
Nonmeditators Kundalini Tibetan Buddhist been observed to occur in subjects in the absence of an instruction
Resting heart rate: 63.3 10.0 67.0 8.7 65.6 14.9 to breathe normally and have been suggested as a potential
Visit 1 (bpm) strategy for maximizing heartbeat sensations (Jones, 1994; We-
Resting heart rate: 65.8 8.4 68.8 11.5 65.3 15.3 isz, Balazs, & Adam, 1988), and (2) several meditators were ob-
Visit 2 (bpm) served to spontaneously display Ujjai breathing during the
R-wave to pulse 0.269 0.017 0.261 0.013 0.266 0.016
interval: Visit 1 (s)
piloting phase of the study and this, in and of itself, could be a
R-wave to pulse 0.266 0.015 0.260 0.014 0.264 0.014 basis for enhanced interoceptive accuracy. One Kundalini med-
interval: Visit 2 (s) itator was unable to perform the Ujjai breathing due to a pre-
existing respiratory condition and was excluded from the
heartbeat detection analysis.
Subjective Ratings
plethysmograph (TSD123B) attached to the distal phalange of Prior to performing each task, participants were asked to predict
the fifth digit of the dominant hand. The RPI was measured for task accuracy (e.g., ‘‘How good do you think you will be at [task
each participant by calculating the average delay between the X]?’’) and difficulty (‘‘How hard do you think [task X] will be?’’).
peak of the R-wave and the foot of the systolic upstroke mea- Upon completion of each task participants were also asked to
sured during a 2-min resting period. Mean resting heart rate and estimate task accuracy (‘‘How good do you think you were at
RPI intervals are listed in Table 2.2 During nonsimultaneous [task X]?’’) and difficulty (‘‘How hard do you think [task X]
trials, tones were delivered 400 ms after the RPI, approximately was?’’). Accuracy ratings could range from 1 (very bad) to 5 (very
650–700 ms after the R-wave. Thus, tone delivery was tempo- good). Difficulty ratings could range from 1 (very hard) to 5
rally linked to each participant’s actual heartbeat during each (very easy). To familiarize participants with each task, all par-
trial. Trial order was randomized within and across each block. ticipants were instructed to sample tones from each trial type
Tones were presented through noise canceling headphones (Qui- (i.e., one simultaneous and one nonsimultaneous trial) for an
etComfort, Bose Inc., Framingham, MA). All participants per- unlimited period prior to performing each task. In addition, task-
formed the tasks in the supine position with their eyes closed, and related feedback was withheld from all participants until the
they were given an unlimited time to respond during each trial. conclusion of the study.
Cardiovascular Parameters
A 3 2 repeated measures ANOVA did not reveal any group
differences in resting heart rate, F(2, 44) 5 0.42, p 5 .66. There
was no effect of visit on resting heart rate, F(1, 44) 5 2.18,
p 5 .15, and there were no Group Visit interactions, F(2,
44) 5 0.86, p 5 .43. The groups also did not differ with respect to
the R-wave to pulse interval, F(2, 44) 5 1.34, p 5 .26. There was
no effect of visit on the R-wave to pulse interval, F(1, 44) 5 0.10,
p 5 .75, and there were no Group Visit interactions, F(2,
44) 5 0.38, p 5 .69. Figure 1. Heartbeat detection and pulse detection accuracy across each
block for each group. HB1: heartbeat detection during normal breathing.
Accuracy Measures HB2: heartbeat detection during Ujjai breathing. NM: nonmeditators.
There were no group differences in accuracy on the pulse KM: Kundalini meditators. TB: Tibetan Buddhist meditators.
detection task, F (2, 44) 5 1.27, p 5 .29. A 3 2 2 ANOVA Performance accuracy could range from 0 to p, with chance
performance 5 p/2. Dotted line 5 chance, Error bars: SE.
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 43) 5 4.1, p 5 .023, Zp 2 ¼ :16, with both groups of meditators
Visit 2) as within-subject factors. There were no main effects rating their heartbeat detection performance to be more accurate
for group, F(2, 43) 5 0.30, p 5 .74, Zp 2 ¼ :01, block, F(1, and the task to be less difficult than the nonmeditators (Figures 2
43) 5 0.69, p 5 .41, or visit, F(1, 43) 5 1.38, p 5 .25, and there and 3). There were no other significant main effects or interac-
were no significant interactions between group and visit, F(2, tions for ratings of heartbeat detection accuracy. For ratings of
43) 5 0.77, p 5 .47, block and visit, F(1, 43) 5 .00, p 5 .99, or heartbeat detection difficulty, there was a significant effect of
group and block and visit, F(2, 43) 5 1.03, p 5 .37, (Figure 1). visit, F(2, 1) 5 4.5, p 5 .039, Zp 2 ¼ :10, with all groups rating
The lack of group differences was not accounted for by group both tasks as less difficult on the second visit. There was a sig-
differences in response bias, defined as the tendency to favor one nificant interaction between group and block, F(2, 2) 5 4.7,
particular response type over another, for either pulse detection, p 5 .015, Zp 2 ¼ :18, with both groups of meditators rating each
F(2, 44) 5 0.1, p 5 .91, or heartbeat detection, F(2, 43) 5 1.3, block to be less difficult than the nonmeditators. There was also a
p 5 .28. significant interaction between block and visit, F(2, 1) 5 4.3,
There were also no differences in the proportion of meditators p 5 .045, Zp 2 ¼ :10, with all groups rating blocks from the sec-
classified as good heartbeat detectors (Table 3). This was equally ond visit to be easier than the first visit.
true when the definition of good heartbeat detection performance
was restricted to above chance performance on two out of two Post Analysis
visits or loosened to above chance performance on at least one Both groups of meditators displayed higher subjective ratings of
out of two visits, for both tasks (Table 3). heartbeat detection accuracy and lower subjective ratings of
heartbeat detection difficulty than nonmeditators. Because these
Subjective Ratings findings occurred in the absence of an actual difference in heart-
There were no group differences in the ratings of pulse detection beat detection accuracy, we examined the relationship between
accuracy, F(2, 44) 5 0.12, p 5 .89, or pulse detection difficulty, the objective accuracy scores and the subjective accuracy ratings
F(2, 44) 5 .76, p 5 .48. However, a 3 2 2 ANOVA with two provided by each participant after the pulse and heartbeat de-
repeated measures factors revealed significant group differences tection tasks. Because maximum objective accuracy was almost
in ratings of heartbeat detection accuracy, F(2, 43) 5 5.77, always reached for pulse detection, we assumed that the subjec-
p 5 .007, Zp 2 ¼ :21, and heartbeat detection difficulty, F(2, tive accuracy ratings for pulse detection represented the maxi-
Table 3. Percentage of Individuals Classified as Good Heartbeat Detectors for Each Block of Heartbeat Detectiona
Figure 2. Mean ratings of pulse and heartbeat detection accuracy across Figure 3. Mean ratings of pulse and heartbeat detection difficulty across
each block for each group. Accuracy ratings could range from 1 (very each block for each group. Difficulty ratings could range from 1 (very
bad) to 5 (very good). NM: nonmeditators. KM: Kundalini meditators. hard) to 5 (very easy). NM: nonmeditators. KM: Kundalini meditators.
TB: Tibetan Buddhist meditators. Error bars: SE. TB: Tibetan Buddhist meditators. Error bars: SE.
mum possible range for subjective accuracy ratings in general. on interoceptive awareness. We conducted a power analysis
We then normalized each participant’s subjective heartbeat de- based on the observed main effect to determine the sample size
tection rating by the global average subjective pulse detection required to achieve a statistically meaningful result for heartbeat
accuracy ratings measured from all participants using the fol- detection. We found that group sizes would need to be increased
lowing formula: (individual heartbeat detection accuracy rating- by one order of magnitude before reaching the threshold of sig-
global mean pulse detection accuracy rating)/global mean pulse nificance. Thus if the sample sizes were increased 10-fold, the
detection accuracy rating. We also normalized each group’s main effect would be as follows: F(2, 457) 5 3.21, p 5 .041,
heartbeat detection accuracy scores (A 0 ) by the mean pulse de- Zp 2 ¼ :01. Even if this were the case, the presumed effect size
tection accuracy scores using this same procedure. Finally, we suggests that the influence of meditative experience on resting
examined the relationship between these normalized heartbeat awareness of heartbeat sensations would be quite small.
detection ratings and normalized accuracy scores for each group Sex differences in heartbeat detection ability have sometimes
for congruency. We found that, on average, meditators’ subjec- been reported in the literature (Jones & Hollandsworth, 1981;
tive accuracy ratings appeared more congruent with objective Katkin, Blascovich, & Goldband, 1981; Whitehead et al., 1977;
accuracy scores than the nonmeditators (Table 4). There was a but see Ring & Brener, 1992; Rouse et al., 1988). There were no
nearly significant interaction between group and scale, F(2, significant group differences between the proportion of males
2) 5 2.6, p 5 .08, Zp 2 ¼ :1, in support of this dissociation. and females in the current study. However, the sample sizes may
not be large enough to test whether sex differences influenced the
Discussion findings. In any event, it seems unlikely that sex played a role in
The current findings do not support the hypothesis that expe- the current findings: We examined whether there were any sex
rienced meditators would display increased interoceptive aware- related differences in interoceptive accuracy and found that none
ness, as meditators did not differ from nonmeditators in of the results differed with respect to sex.
heartbeat detection accuracy. The lack of an effect of medita- Although we believe that the current finding is reliable, it is
tion on awareness of heartbeat sensations appears to be a reliable important to consider alternatives that might explain it. First, it is
finding. It occurs in two different groups of experienced med- possible that awareness of heartbeat sensations alone is a poor
itators, measured at two time points, and with two different re- index of the type of interoceptive sensations cultivated by the
spiratory manipulation strategies. These results are consistent practice of meditation. Although attention to body sensations
with recent findings by Nielsen and Kaszniak (2006), who re- such as the heartbeat is practiced at some point of the training in
ported a lack of significant differences between a group of Bud- all meditation traditions, attention is more commonly directed
dhist meditators and a group of nonmeditators on a single session toward breathing. Any enhancement of interoceptive sensations
of standard heartbeat detection. The Nielsen and Kaszniak study that results from the long-term practice of meditation might be
had a small sample size, did not include comparison subjects specific only to the bodily signals that are attended. Thus the
matched for age or body mass (Rouse et al., 1988), and was current results do not rule out the possibility that meditation
conducted in a small number of sessions, limiting statistical cultivates interoceptive awareness for other body signals such as
power. The present study, however, did not suffer from any of breathing. Second, attention to nonbodily signals is also fre-
these limitations and still did not reveal any effect of meditation quently practiced in all meditation traditions. For example, in the
Table 4. Normalized Objective Heartbeat Detection Accuracy and Subjective Ratings of Heartbeat Detection Accuracya
Tibetan Buddhist tradition, attention is commonly focused on heartbeat detection difficulty than nonmeditators. In the absence
complex mental imagery or external visual objects during med- of an actual difference in heartbeat detection accuracy these
itation (Lutz et al., 2007), and the awareness that develops during findings were surprising. The ratings differences did not appear
such attention training might not translate readily into an en- to be due to a general rating bias, as there were no such group
hancement of interoceptive awareness. Third, the current study differences in the ratings of the pulse detection task. All groups
only examined interoceptive awareness under resting conditions. displayed accurate pulse detection performance, rated their ac-
We chose this starting point because the meditation practice most curacy accordingly, and found the task to be easy. With respect
commonly occurs during those conditions. It is possible that in- to heartbeat detection, the nonmeditators’ ratings were near the
teroceptive awareness for heartbeat sensations is limited at rest bottom of each scale, suggesting that they found the task to be
by a physiological mechanism not amenable to voluntary mod- difficult and felt that their performance was very poor. The
ulation, even through a long-standing meditation practice. Of meditators’ ratings were near the middle of the scale, suggesting
note, none of the groups in the current study displayed heartbeat that they found the task to be neither easy nor difficult and felt
detection rates above 50%. These rates are consistent with those that their performance was neither good nor bad. These rating
routinely reported in the heartbeat detection literature (Brener & differences could be explained either by the nonmeditators un-
Kluvitse, 1988; Eichler & Katkin, 1994; Jones, 1994; Knapp et derestimating their performance or the meditators overestimat-
al., 1997; Ring & Brener, 1992; Wiens & Palmer, 2001), sug- ing their performance. Even though both groups displayed
gesting that it is difficult for most individuals to display aware- performance within the normally reported range on the heartbeat
ness of heartbeat sensations at rest. However, the current finding detection task, ‘‘normal’’ performance is quite often below
does not guarantee that meditation would not be associated with chance, given the fact that heartbeat detection is most commonly
enhanced interoceptive awareness under other physiological measured at rest. Thus it could be argued that either the med-
conditions. Indeed, visceral sensations do not dominate con- itators’ or the nonmeditators’ ratings were congruent with the
scious experience under resting conditions, but quickly develop literature. An analysis of the relationship between each group’s
when conditions such as exercise or stress signal deviations in the objective accuracy scores and subjective ratings of accuracy sug-
homeostatic state (Cameron & Minoshima, 2002; Khalsa et al., gests it is more likely that the nonmeditators were underestimat-
in press). Thus it is still possible that meditators would display ing their heartbeat detection performance and provides support,
increased interoceptive awareness under these conditions. Such albeit limited, for the notion that experienced meditators’ sub-
considerations argue for the development of new measures of jective perceptions of interoceptive states are more in tune with
interoceptive awareness that take into account nonhomeostatic their performance on interoceptive tasks.
physiological body states. Overall, the results of this study provide evidence against the
Both groups of meditators displayed higher subjective ratings notion that practicing attention to internal body sensations, a core
of heartbeat detection accuracy and lower subjective ratings of feature of meditation, enhances resting interoceptive awareness.
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504–510. (Received November 14, 2007; Accepted December 13, 2007)