Social laughter is correlated with an elevated pain threshold

Abstract

Although laughter forms an important part of human non-verbal communication, it has received rather less attention than it deserves in both the experimental and the observational literatures. Relaxed social (Duchenne) laughter is associated with feelings of wellbeing and heightened affect, a proximate explanation for which might be the release of endorphins. We tested this hypothesis in a series of six experimental studies in both the laboratory (watching videos) and naturalistic contexts (watching stage performances), using change in pain threshold as an assay for endorphin release. The results show that pain thresholds are significantly higher after laughter than in the control condition. This pain-tolerance effect is due to laughter itself and not simply due to a change in positive affect. We suggest that laughter, through an endorphin-mediated opiate effect, may play a crucial role in social bonding.

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doi: 10.1098/rspb.2011.1373
, 1161-1167 first published online 14 September 2011279 2012 Proc. R. Soc. B
Stow, Giselle Partridge, Ian MacDonald, Vincent Barra and Mark van Vugt
R. I. M. Dunbar, Rebecca Baron, Anna Frangou, Eiluned Pearce, Edwin J. C. van Leeuwen, Julie
Social laughter is correlated with an elevated pain threshold
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Social laughter is correlated with an
elevated pain threshold
R. I. M. Dunbar1,*, Rebecca Baron3, Anna Frangou4,
Eiluned Pearce2, Edwin J. C. van Leeuwen5, Julie Stow6,
Giselle Partridge6, Ian MacDonald7, Vincent Barra6
and Mark van Vugt1,5
1
British Academy Centenary Research Project, and
2
Institute of Cognitive and
Evolutionary Anthropology, University of Oxford, 64 Banbury Road, Oxford OX2 6PN, UK
3
Magdalen College, Oxford OX1 4AU, UK
4
Lady Margaret Hall, Oxford OX2 6QA, UK
5
Department of Social and Organizational Psychology, VU University Amsterdam,
57 van der Boechorsstraat 1, 1081 BT Amsterdam, The Netherlands
6
School of Biological Sciences, University of Liverpool, Crown Street, Liverpool L69 3BX, UK
7
Department of Biological Sciences, Binghamton University (SUNY), Vestal Parkway East,
Binghamton, NY 13902, USA
Although laughter forms an important part of human non-verbal communication, it has received rather
less attention than it deserves in both the experimental and the observational literatures. Relaxed social
(Duchenne) laughter is associated with feelings of wellbeing and heightened affect, a proximate expla-
nation for which might be the release of endorphins. We tested this hypothesis in a series of six
experimental studies in both the laboratory (watching videos) and naturalistic contexts (watching stage
performances), using change in pain threshold as an assay for endorphin release. The results show that
pain thresholds are significantly higher after laughter than in the control condition. This pain-tolerance
effect is due to laughter itself and not simply due to a change in positive affect. We suggest that laughter,
through an endorphin-mediated opiate effect, may play a crucial role in social bonding.
Keywords: laughter; positive affect; pain threshold; endorphins; social bonding
1. INTRODUCTION
Despite the fact that laughter is a human universal that can
occur at very high rates under natural conditions and plays
an important role in regulating social interaction (including
conversation) in humans, it has been little studied [1,2].
While having a number of unique properties, laughter is a
feature that we share with the other great apes (in particu-
lar, its use in play contexts [3,4]), and this suggests that it
has at least as ancient a heritage as any other aspect of
our non-verbal behaviour [2]. Not surprisingly, given this
lack of attention, the function and evolutionary significance
of laughter remains ambiguous. One suggestion has been
that laughter conveys signals of social (and especially
mating) interest in a companion [5–7]. A more general ver-
sion of this hypothesis is that laughter induces a positive
attitude in the observer, thereby facilitating interaction by
reducing threat [7–9]. An alternative is that laughter
induces states of positive affect in the laugher, and this
facilitates the capacity to learn new things from others
(Fredrickson’s [10] ‘broaden-and-build’ hypothesis).
Another possibility is that laughter plays a more generalized
role in social bonding at the group level [2], thereby facili-
tating the enhanced prosociality and cooperation that has
played such a crucial role in the evolution of modern
humans with their exceptionally large groups [11,12].
None of these explanations, however, provides a plaus-
ible biological mechanism for how laughter might enhance
affect and produce the proposed effects. A tentative ans-
wer derives from the fact that humour can have analgesic
properties: patients allowed to watch comedy videos
required less pain medication than those who watched con-
trol videos [13–15]. However, whether patients laughed
was never explicitly tested in these experiments. We suggest
that it is the physical action of laughing that generates
positive affect by triggering activation of the endorphin
system. Endorphins are a class of endogenous opioid pep-
tides produced in the central nervous system (CNS) that
not only function as neurotransmitters [16] but also play
a crucial role in the management of pain through their
analgesic properties:
b
-endorphin, in particular, appears
to play a critical role in buffering the organism against the
effects of physiological and psychological stress [17–24].
More importantly, in the present context, endorphins are
also thought to play a central role in social bonding,
especially in primates [25–27].
Because CNS endorphins do not cross the blood– brain
barrier [28,29], it has been common practice to assay
endorphin levels using pain threshold [20,22,30–34].
This assay assumes that high levels of CNS endorphins
will be associated with an elevated pain threshold. Using
pain thresholds as a proxy for endorphin release, we
*Author for correspondence (robin.dunbar@anthro.ox.ac.uk).
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rspb.2011.1373 or via http://rspb.royalsocietypublishing.org.
Proc. R. Soc. B (2012) 279, 1161–1167
doi:10.1098/rspb.2011.1373
Published online 14 September 2011
Received 30 June 2011
Accepted 26 August 2011 1161 This journal is q2011 The Royal Society
on September 27, 2012rspb.royalsocietypublishing.orgDownloaded from

report a set of six experiments that test the hypothesis that,
compared with a control condition, laughter elevates
endorphin titres.
2. METHODS
Because pain thresholds vary between individuals, we used a
within-subjects comparison: subjects took a pain threshold
test, undertook an experimental or control task and then
repeated the pain assay. In five experimental studies, the task
involved watching either a comedy video or a non-humorous
factual documentary. In a sixth study, we sampled actors and
audiences at live performances under completely naturalistic
conditions. Details of the videos and selection of subjects are
given in the electronic supplementary material.
(a)Experiments 1 – 3
Experiments 1 – 3 use different experimental designs to con-
firm the main effect of laughter on pain threshold. Because
humans do not laugh readily when watching even the funni-
est performances alone [1,35] and laughter is 30 times more
likely to occur in social contexts than when alone [36], all
subjects were tested in groups.
In experiment 1, 15 females and 20 males were tested in
groups of 2–6 in a between-subjects design, with half
acting as the experimental group (watching a comedy
video) and half as the control group (watching a factual
documentary). Experiment 2 used a within-subjects design
to confirm that subjects responded differentially to comedy
and neutral videos when tested on both. In this experiment,
10 females and six males were tested in five groups of 3 – 4
individuals in a within-subject design with each subject
acting as their own control (each group was tested twice,
first in the control condition and then in the experimental
condition). In experiment 3, three males and two females
(mean age ¼23.2 years, range 22 – 24) formed the exper-
imental group, and eight males and three females (mean
age ¼24.6 years, range ¼20 – 32) the control group.
Pain tolerance was assayed using a frozen vacuum wine
cooler sleeve (frozen to 2168C for the start of each trial;
maximum duration 180 s) in experiments 1 and 2, and a mer-
curial sphygmomanometer (inflated to a maximum pressure of
260– 280 mmHg) in experiment 3. In each case, subjects were
asked to indicatewhen they could no longer stand the pain (see
electronic supplementary material).
In experiments 1 and 2, we estimated how much time par-
ticipants spent laughing while watching videos by scan
sampling each participant at 15 s intervals, recording
whether or not they were laughing.
(b)Experiments 4 and 5
In experiments 1–3, all subjects were tested in groups, making
it difficult to determine whether the change in pain
threshold was due to some kind of group effect rather than to
laughter. Experiment 4 tested for this confound by separating
out the two effects. In this experiment, 21 males (mean
age ¼25.7 +9.4 years, range 18– 55) and 41 females
(mean age ¼24.0 +8.7 s.d. years, range 18–58) were ran-
domly assigned to one of three conditions in which they
watched either a neutral video alone, a comedy video alone
or a comedy video in a group of four (each of 15 min dur-
ation). Laughter was recorded on individual dictaphones
hung from each subject’s neck, and subsequently scan-
sampled for the presence/absence of laughter at 15 s intervals.
Owing to equipment malfunction, laughter data are available
only for 58 subjects and pain threshold data for 60.
A second possible confound relates to the interface between
affect and endorphins. Although endorphins are known to
mediate affect [21], the change in pain threshold might be
due to changes in affect rather than the laughter itself. Exper-
iment 5 separated out these two effects. In this experiment,
14 males (mean age ¼23.0 years, range 18–32) and 36
females (mean age ¼19.9 years, range 18–27) were randomly
assigned to watch one of the three 15 min video clips (neutral,
positive affect and comedy). Participants in the neutral
condition either watched the film alone in a small cubicle
(n¼10) or in single-sex groups of four (n¼8). Those in the
affect and comedy conditions watched the videos only in
single sex groups of four. Participants were audio-recorded
with a hidden microphone. The absolute number of laughter
bouts for the group as a whole was scored from the audio
recordings without differentiating who was laughing.
In both experiments, pain tolerance was assessed following
the procedure used in experiment 3. Subjects completed a
positive and negative affect scale (PANAS) [37] before and
after watching the video to measure the change in positive
and negative affect.
(c)Experiment 6
In order to determine whether the results of experiments 1– 3
generalized to the real world outside the laboratory, we used
live theatrical performances at the Edinburgh Fringe Festival
in August 2008 as an outdoor laboratory. In this experiment,
27 performers and technical crew members (10 females, 17
males: mean age ¼21.6 years, range 18–30) participated in
this experiment over a period of 18 days. Several of these
appeared as both actor and audience on different days
(depending on whether they were performing), yielding a
total of 41 cases in all. Four experimental conditions were cre-
ated: comedy actors (six female, 11 male), comedy audience (six
female, 11 male), drama actors (one female, three male) and
drama audience (one female, two male).
In each condition, participants were required to complete
a pain test at least an hour before performing or watching the
show and to repeat this immediately after the show. Because
experiment 6 was conducted outside the laboratory, we used
a standard ski exercise as a pain assay: subjects lean against a
wall with their legs at right angles (as if sitting on a straight-
backed chair) until it becomes too painful and they collapse
onto the ground [38,39]. Subjects completed a questionnaire
self-reporting how much they had laughed during the
performance (on a 0 – 5 scale).
Because individual subjects were sampled at several per-
formances (mean 2.9, range 1 – 6) in any given condition,
all analyses are based on mean values for individual subjects
in each condition. However, to determine whether there
was any habituation effect, we correlated difference in the
time for which the position was held with order of perform-
ance for all subjects who had three or more trials. Of the 11
subjects who met this criterion, six exhibited positive corre-
lations and five negative correlations, suggesting that there
was no consistent bias owing to multiple trials (binomial
test: n.s.).
(d)Statistical analysis
Change in pain threshold was normally distributed in all
but one of 16 conditions across the six experiments, and
overall, does not differ from a normal distribution (Fisher’s
1162 R. I. M. Dunbar et al. Laughter and pain
Proc. R. Soc. B (2012)
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meta-analysis:
x
2
¼24.76, d.f. ¼2k¼32, p¼0.857; see
electronic supplementary material). Percentage of time
spent laughing was significantly different from a normal dis-
tribution, but ln-transforms of (%laugh þ1) (to remove 0
values) was not; so ln-transformed data are used for analysis
in this case. All statistical tests are two-tailed except in
respect of the variable condition: as a directional hypothesis
is being tested in this case (comedy .neutral), a one-tailed
test is appropriate.
3. RESULTS
(a)Laughter rates
To establish that laughter rates differ across experimental
and control conditions in the way predicted, we first
tested for an effect of video type on laughter rates in the
three experiments where laughter by individual subjects
was sampled by scan-sampling (experiments 1, 2 and 4).
Subjects spent significantly more time laughing in the
comedy condition than in the control condition (electronic
supplementary material, figure S1). Condition (video type)
is the only factor that significantly affects the dependent
variable (study: F
1,115
¼1.31, p¼0.275; condition:
F
3,115
¼166.92, p,0.001; gender: F
1,115
¼1.69, p¼
0.196; condition gender: F
3,115
¼0.36, p¼0.670).
Scheffe
´post hoc tests confirm that laughter rates (i) are sig-
nificantly higher in all the comedy conditions than in all the
control conditions, (ii) are significantly higher in the
comedy-alone condition than in the control conditions,
(iii) are significantly higher in all the group comedy con-
ditions than in the comedy-alone condition (all at p,
0.001), and (iv) do not differ significantly between the
experimental (comedy) conditions across experiments
(p.0.600).
(b)Laughter and pain tolerance
Figure 1 plots the difference in pain tolerance before and
after viewing the video for the control (neutral) versus the
experimental (comedy) groups for experiments 1– 3.
Condition is the only factor that has a significant effect,
with change in pain tolerance being significantly higher
in experimental (comedy video) conditions than in con-
trol (neutral video) conditions (condition: F
1,77
¼4.09,
p¼0.024; study: F
2,77
¼1.01, p¼0.370; gender:
F
2,77
¼3.91, p¼0.051; condition gender: F
1,77
¼
1.15, p¼0.287). Note that there is a marginally signifi-
cant effect of gender (p¼0.051). This effect is not,
however, consistent across experiments: in the exper-
imental condition, females showed a stronger effect than
males in experiments 1 and 2, but the reverse was the
case in experiment 3.
The critical test for the endorphin hypothesis is that
there should be a significantly elevated pain threshold in
the experimental conditions, but no change (
d
¼0) in
the control conditions. We tested this by comparing the
distribution of pain threshold differences (after minus
before) in a one-sample t-test against the null hypothesis
that
d
¼0. Taken together, change in pain threshold is
significantly greater than zero in the three experimental
conditions (experiment 1: t
16
¼2.12, p¼0.007; exper-
iment 2: t
15
¼1.12, p¼0.140; experiment 3: t
4
¼9.46,
p,0.001; Fisher’s meta-analysis:
x
2
¼30.44, d.f. ¼6,
p,0.00001), but not significantly greater than zero in
the three control conditions (experiment 1: t
17
¼1.50,
p¼0.924; experiment 2: t
15
¼1.09, p¼0.146; exper-
iment 3: t
10
¼1.79, p¼0.948; Fisher’s meta-analysis:
x
2
¼6.91, d.f. ¼6, p¼0.329).
(c)Group and affect confounds
In experiment 4, we checked whether the elevated pain
thresholds in the comedy condition were due simply to
being tested in a group or whether there is a parametric
effect of the amount of laughter. Ln-transformed laughter
rates varied significantly across conditions (electronic sup-
plementary material, figure S1; F
2,55
¼94.29, p,0.001),
with all differences between conditions being significant
(group comedy .comedy alone .neutral alone: Scheffe
´
post hoc tests, p,0.001). Positive affect scores did not
differ significantly between conditions, although they
were in the same direction (F
2,59
¼2.96, p¼0.060). Con-
dition has a significant effect on pain threshold (figure 2;
F
2,56
¼5.56, p¼0.007), but gender does not (F
1,56
¼
0.97, p¼0.318); there is a significant condition gender
interaction (F
1,56
¼5.33, p¼0.008), but this may reflect
the rather small sample size for males in the group
comedy condition. Scheffe
´post hoc tests for condition indi-
cate that threshold changes in the neutral-alone condition
are significantly smaller than that in the group comedy
(p¼0.043), but the comedy-alone condition does not
differ significantly from either the neutral-alone condition
(p¼0.861) or the group comedy condition (p¼0.110),
indicating that laughter exhibits something closer to a
dose–response effect than a step change due solely to a
group effect: experiencing comedy in a group ramps up
the laughter response, and this is reflected in a proportional
change in pain threshold.
Experiment 5 sought to determine whether the change
in pain threshold is due to laughter or to affect alone. It
did this by asking subjects to view a non-humorous positive
affect video, as well as the usual neutral and comedy videos.
Ln-transformed laughter rates varied significantly across
conditions (F
3,46
¼46.64, p,0.001), with all differences
between conditions being significant (comedy group .
60
40
difference in pain threshold
20
0
–20
experiment 1 experiment 2 experiment 3
Figure 1. Experiments 1– 3: mean (+s.e.) difference in pain
threshold (post-test minus pre-test) under the two conditions
(control: neutral video, open symbols; experimental: comedy
video, solid symbols). Experiments 1 and 3 were between-
subjects designs; experiment 2 was a within-subjects design.
Pain threshold was indexed using a frozen wine cooler sleeve
(experiments 1 and 2) or a sphygmomanometer (experiment
3). Experiment 3 demonstrates that alternative indices of
pain threshold yield similar results. Sample sizes (left to
right): 18, 17, 16, 16, 11, 5.
Laughter and pain R. I. M. Dunbar et al. 1163
Proc. R. Soc. B (2012)
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neutral group .affect group .neutral alone: Scheffe
´post
hoc tests, p0.031). Positive PANAS scores showed a
broadly similar pattern across conditions (F
3,46
¼3.54,
p¼0.022), but only the scores in the group comedy con-
dition were significantly (p¼0.022) higher than those in
the other three conditions (which did not themselves
differ: p0.198). The differences in mean pain threshold
across the four conditions are shown in figure 3. We first
tested whether pain thresholds in the positive affect con-
dition are significantly different from those in the two
neutral conditions (they are not: F
2,27
¼0.16, p¼0.856),
and then whether pain thresholds in the group comedy
condition are significantly greater than the neutral and
affect conditions combined (they are: F
1,48
¼4.95, p¼
0.016 one-tailed). Thus, laughter can be differentiated
from positive affect per se in its effect on pain threshold,
even though laughter may enhance (or be correlated
with) enhanced positive affect.
(d)Laughter under natural conditions
(experiment 6)
As a final test of the hypothesis, we ran a version of the
experiment under natural conditions at live theatrical
performances. Mean self-report laughter scores in the
comedy condition were 3.5 +0.87 for actors and 3.38 +
1.12 for audience members (modal value ¼4 for both,
on a Likert scale of 1– 5), indicating that both performers
and audience actively laughed during the sampled sessions.
Subjects in the drama events did not laugh at all (all
scores ¼0). Figure 4 plots the change in pain threshold
separately for actors and audience in the comedy and
drama events. There was a significant effect of condition
(comedy versus drama: F
1,38
¼3.86, p¼0.022 one-
tailed), but no effect owing to status (actor versus audience:
F
1,38
¼0.16, p¼0.901). More importantly, the difference
in pain threshold is significantly greater than
d
¼0 for both
actors (t
16
¼3.983, p,0.001) and audience (t
16
¼2.742,
p¼0.007) in the comedy events, but not in the drama
events (though sample sizes are small in the latter; actors:
t
3
¼21.022, p¼0.618; audience: t
2
¼1.932, p¼0.193;
all tests one-tailed).
4. DISCUSSION
We tested the hypothesis that social laughter elevates pain
thresholds both in the laboratory and under naturalistic
150
100
difference in pain threshold
50
0
–50
alone/neutral alone/comedy group/comedy
Figure 2. Experiment 4: mean (+s.e.) change in pain
threshold (post-test minus pre-test) for females (open sym-
bols) and males (solid symbols) under three different
conditions: neutral video watched alone, comedy video
watched alone and comedy video in groups of four. Pain
threshold was indexed using a sphygmomanometer. Sample
sizes (left to right): 18, 8, 17, 7, 8, 2.
20
10
0
–10
difference in pain threshold
–20
–30
–40
neutral affect comedy
Figure 3. Experiment 5: mean (+s.e.) change in pain
threshold (post-test minus pre-test) under three conditions
(neutral video, positive affect-only video and comedy
video) for subjects who watched the video alone (open sym-
bols) or in groups of four (solid symbols). Pain threshold was
indexed using a sphygmomanometer. Sample sizes (left to
right): 10, 8, 12, 20.
80
60
difference in pain threshold (s)
40
20
0
comed
y
drama
–20
Figure 4. Experiment 6: mean (+s.e.) difference in pain
threshold (post-test minus pre-test) for actors (open sym-
bols) and audience (solid symbols) in live theatre
performances of stand-up comedy versus drama (no laughter
condition). Pain threshold indexed using the Madsen et al.
[38] skiing task and the measure is the time for which the
position was held (in seconds). Sample sizes (left to right):
17, 17, 4, 3.
1164 R. I. M. Dunbar et al. Laughter and pain
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conditions. In both cases, the results confirmed that when
laughter is elicited, pain thresholds are significantly
increased, whereas when subjects watched something
that does not naturally elicit laughter, pain thresholds
do not change (and are often lower). These results can
best be explained by the action of endorphins released
by laughter.
An important distinction is drawn between Duchenne
laughter (relaxed, unforced laughter that is stimulus-
driven and emotionally valent, involving involuntary
contraction of the orbicularis oculi muscles) and non-
Duchenne laughter (context-driven and emotionless, with
no orbicularis oculi involvement) [1,2,40,41]. Neuroima-
ging evidence suggests that these two types of laughter
involve different neural pathways [42]. The involuntary
nature of Duchenne laughter is largely responsible for the
well-known contagion effect whereby we are stimulated to
laugh just by others laughing. Precisely because Duchenne
laughter is intensely social and contagious [1,40], it is likely
that the endorphin effect is limited to this form of laughter.
Indeed, only Duchenne laughter has the capacity to
mitigate negative emotions and stress [40].
Most of the phenomena that trigger endorphin release
involve physical exercise (running, circuit-training, rowing,
etc. [18,33,43–45]) or other forms of pressure on the
body surface (e.g. grooming and massage [46]). In the
case of laughter, we assume that the functional mechanism
is the muscular exertion involved in sustained laughter. As
the sonograms in Davila Ross et al. [4] illustrate, ape laugh-
ter typically consists of a series of alternating exhalations and
inhalations, whereas that of humans typically consists of a
sustained series of exhalations without drawing breath (see
also [1]). (This capacity to maintain a long series of exhala-
tions is crucial to speech [1,47,48].) It is this long series of
exhalations that appears to be exhausting (hence triggering
endorphin release), and this might be either because the
physicaleffort involved is itself significant or because empty-
ing the lungs in an uninterrupted series of exhalations
is taxing.
Although it has been argued that positive affect plays
an important role in the bonding of groups of individuals
[49], experiment 5 suggests that affect alone may be
insufficient to create a significant endorphin surge.
Given that neuroimaging studies have demonstrated a
direct relationship between endorphin uptake at receptor
sites and perceptions of affect [21], our results suggest
that the sense of heightened affect in this context probably
derives from the way laughter triggers endorphin uptake.
Although laughter plays an important role in regulating
conversation in humans [1], it may also play a significant
role in facilitating social bonding among groups of in-
dividuals [2,11,12,50]. In both primates and humans, for
example, laughter plays an important signalling role
during social play [1–3]. The capacity to sustain laughter
for periods of several minutes at a time may exaggerate
the opioid effects, thus ramping up the sense of heightened
affect that humans experience in these contexts. A key
aspect of this may be that social (or Duchenne) laughter
is highly socially synchronized [1]. In a study of physical
exercise (rowing), synchronized activity ramped up endor-
phin production (as indexed by change in pain threshold)
by a factor of two over that generated by exercise alone
[33]. If the opiate effects of endorphins create a sense of
wellbeing, synchronized activity might then lead to
enhanced prosociality, and hence group bonding and
cooperation [50]. Indeed, even simple behavioural syn-
chrony is sufficient to enhance cooperative behaviour in
subjects [51]. As we might anticipate a similar effect arising
from social laughter, a promising future development
would be to test whether sustained laughter in groups
enhances prosociality or altruistic behaviour.
Laughter contrasts with many more conventional
aspects of non-verbal communication in one important
respect: it seems to create euphoric states in the performer
similar to those experienced in communal music-making,
dancing and some of the rituals of religion [52]. There is
some evidence to suggest that these euphoric states are
also associated with the release of endorphins [11,53].
Singing, dancing and rituals have long been recognized as
important components in the process of bonding whole
communities in traditional societies, a process referred to
variously in the anthropological literature as ‘effervescence’
[54] and ‘communitas’ [55]. An obvious hypothesis is that
all these activities exploit the same psychopharmacological
mechanism (the release of endorphins) as social grooming
does in primates [25,26], and so provide a bridging mech-
anism (i.e. a form of grooming at a distance) that enables
humans to bond social communities that are much larger
than those that primates can bond by social grooming
alone [12–25,56]. This possibility awaits detailed testing.
This research was supported by the British Academy
Centenary Research Project.
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