Voluntary facial displays of pain increase suffering in response to nociceptive stimulation.

Abstract

Facial expressions of pain are an important part of the pain response, signaling distress to others and eliciting social support. To evaluate how voluntary modulation of this response contributes to the pain experience, 29 subjects were exposed to thermal stimulation while making standardized pain, control, or relaxed faces. Dependent measures were self-reported negative effect (valence and arousal) as well as the intensity of nociceptive stimulation required to reach a given subjective level of pain. No direct social feedback was given by the experimenter. Although the amount of nociceptive stimulation did not differ across face conditions, subjects reported more negative effects in response to painful stimulation while holding the pain face. Subsequent analyses suggested the effects were not due to preexisting differences in the difficulty or unpleasantness of making the pain face. These results suggest that voluntary pain expressions have no positively reinforcing (pain attenuating) qualities, at least in the absence of external contingencies such as social reinforcement, and that such expressions may indeed be associated with higher levels of negative affect in response to similar nociceptive input. PERSPECTIVE: This study demonstrates that making a standardized pain face increases negative affect in response to nociceptive stimulation, even in the absence of social feedback. This suggests that exaggerated facial displays of pain, although often socially reinforced, may also have unintended aversive consequences.

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Voluntary Facial Displays of Pain Increase Suffering in Response
to Nociceptive Stimulation
Tim V. Salomons,*,†James A. Coan,*,?S. Matthew Hunt,* Misha-Miroslav Backonja,§
and Richard J. Davidson*,†,‡
*Waisman Laboratory for Brain Imaging and Behavior, Waisman Center,
†Department of Psychology,
‡Department of Psychiatry, and
§Department of Neurology, the University of Wisconsin-Madison, Madison, Wisconsin; and
?University of Virginia Department of Psychology, Charlottesville, Virginia.
Abstract: Facial expressions of pain are an important part of the pain response, signaling distress to
others and eliciting social support. To evaluate how voluntary modulation of this response contrib-
utes to the pain experience, 29 subjects were exposed to thermal stimulation while making stan-
dardized pain, control, or relaxed faces. Dependent measures were self-reported negative effect
(valence and arousal) as well as the intensity of nociceptive stimulation required to reach a given
subjective level of pain. No direct social feedback was given by the experimenter. Although the
amount of nociceptive stimulation did not differ across face conditions, subjects reported more
negative effects in response to painful stimulation while holding the pain face. Subsequent analyses
suggested the effects were not due to preexisting differences in the difficulty or unpleasantness of
making the pain face. These results suggest that voluntary pain expressions have no positively
reinforcing (pain attenuating) qualities, at least in the absence of external contingencies such as social
reinforcement, and that such expressions may indeed be associated with higher levels of negative
affect in response to similar nociceptive input.
Perspective:Thisstudydemonstratesthatmakingastandardizedpainfaceincreasesnegativeaffect
in response to nociceptive stimulation, even in the absence of social feedback. This suggests that
exaggerated facial displays of pain, although often socially reinforced, may also have unintended
aversive consequences.
© 2008 by the American Pain Society
Key words: Pain, facial displays, directed facial action task.
F
use as a complementary indicator of pain in clinical set-
tings, particularly in infants or adults with limited lin-
guistic ability.8
Considerable research has been dedicated to under-
standing the origin and maintenance of facial expressions
acial displays are one of the clearest indicators that
an individual is experiencing pain. Precise character-
ization of these facial displays has facilitated their
of pain. The operant model of pain behavior,14for exam-
ple,hasemphasizedtheroleofreinforcementintheestab-
lishment and maintenance of pain behaviors including fa-
cial displays. Within this framework, the positive social
reinforcementelicitedbyfacialdisplaysofpainisviewedas
a primary factor in their etiology and continuance. Based
onobservationsofpaindisplaysinawidevarietyofspecies
and in infants as young as 25 days, Williams19has compel-
lingly argued that many of the morphological characteris-
tics of facial pain displays are reflexive and have evolution-
ary origins. Nevertheless, actions that are not voluntary or
explicitly social in nature can be recruited for instrumental
purposes,8,9suggesting that pain displays may include a
component that is voluntary, or at least under the control
of social contingencies consistent with the operant model,
as this may confer advantages such as increased social sup-
port or decreased suffering.
ReceivedNovember4,2007;RevisedJanuary4,2008;AcceptedJanuary7,
2008.
Supported by NIMH grant P50-MH069315 and by a gift from William
Heckrodt.
Addressreprintrequeststo:TimSalomons,WaismanLaboratoryforBrain
Imaging and Behavior, Waisman Center, 1500 Highland Drive, A-132,
Madison, WI 53705. E-mail: tvsalomons@wisc.edu
1526-5900/$34.00
© 2008 by the American Pain Society
doi:10.1016/j.jpain.2008.01.330
The Journal of Pain, Vol 9, No 5 (May), 2008: pp 443-448
Available online at www.sciencedirect.com
443

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From a clinical perspective, the critical question that
arises is the degree to which deliberate augmentation of
a particular pain behavior is an adaptive strategy for
coping with pain. Operant treatments for chronic pain
seek to identify the specific reinforcers and punishments
associated with each behavior. Although social feedback
may represent a reinforcer, it is possible that there are
negative consequences of this behavior that counteract
these benefits. To properly assess this question in a lab-
oratory setting, the effect of pain behaviors on the sub-
jectiveexperienceofpainmustbedisentangledfromthe
effect of positive reinforcers such as social support. To-
ward this goal, the present study tests the effect of a
voluntary facial display of pain on the affective response
to pain in the absence of social reinforcement.
In addition to limiting social reinforcement, this study
aimed to reduce demand characteristics by using stan-
dardized facial movements. Previous studies that have
examined this question7,15,17have instructed subjects to
exaggerate or inhibit their response to a pain stimulus.
Although this technique has the advantage of external
validity (as the manipulation is based upon the subject’s
own natural response to pain), it may lead to biased
results due to the effect of demand characteristics, as
instructions to exaggerate the facial response to pain
may implicitly suggest to the subject that pain ratings
should also be increased.
The present study used the Directed Facial Action
(DFA) Task,10a set of instructions developed to guide
subjects through the voluntary performance of discrete
musclemovements,orActionUnits(AUs),fromtheFacial
Action Coding System (FACS).11,12Using AUs commonly
associated with pain,8,19we compared a “pain face”
withastandard“controlface”todeterminetheeffectof
the pain face on pain tolerance and subjective reports of
distress in the absence of social reinforcement.
Previous studies of the effects of voluntary facial ex-
pressions on emotional responding have been criticized
for paying insufficient attention to the impact of preex-
isting differences between facial expressions on results.1
To address this issue, we have also assessed the degree to
which pre-existing differences between the faces (ie,
face specific difficulty and unpleasantness ratings) could
account for their effects on pain perception.
Materials and Methods
Participants
Twenty-nine participants (19 female, mean age/SD ?
23/4.16) provided informed consent and completed the
study. Subjects were screened for medications and med-
icalorpsychiatricconditionsthatcouldalterpainpercep-
tion.
Facial Action Training
Subjects were trained to make the pain and control
faces (Fig 1) based on AUs of the FACS.6The pain face
consisted of 5 AUs: Brow lower (AU4), cheek raise (AU6),
upper lip raise (AU10), lip corner pull (AU20), and lips
apart (AU25).8The control face was valence-neutral and
matched with the pain face in numbers of AUs: Brow
raise (AU1 and AU2), one eye closed (Unilateral AU43),
lips puckered (AU18), and cheeks filled (AU34). In addi-
tion to these 2 faces, subjects also received thermal stim-
ulation while sitting calmly (referred to subsequently as
the “relaxed face”).
Subjects were given no information about the faces,
which were referred to by number throughout the ex-
periment (eg, “make face #2”). No feedback other than
repetition of the standardized instruction script was pro-
vided. Immediately after facial training, participants
Figure 1. Subjects held the pain face (left) or control face (right) for 15 seconds before the onset of thermal stimulation. Subjects
stopped the stimulus themselves when it reached a predetermined level. (Figure printed with permission.)
444
Voluntary Facial Displays

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rated the difficulty and unpleasantness of the faces on a
7-point scale (0 ? not at all difficult or unpleasant, re-
spectively; 6 ? extremely difficult or unpleasant, respec-
tively). These ratings formed the basis of the analysis of
preexisting differences between the faces (see Results
section).
Heat Stimulus
Heat stimuli were generated by a thermal stimulator
(TSA-II; Medoc Advanced Medical Systems, Haifa, Israel)
through a 30 ? 30-mm Peltier device that was attached
to the subject’s nondominant forearm. Stimulation be-
ganat34°Candincreasedby0.3°C/s.Subjectswereasked
to stop the stimulation by pressing a button when their
pain reached an 8 on a standard 11-point numeric pain
scale, (0 ? “no pain”, 10 ? “the worst pain imaginable”).
To obtain baseline threshold temperatures, this proce-
dure was repeated 4 times before the experiment.
Subjects who reached the maximum temperature al-
lowed in the experiment (49°C) were eliminated from
the study.
Experimental Trials and Assessment
The experiment took place in a windowless room. To
prevent unintentional social feedback from the experi-
menter, subjects were instructed to focus on a small
piece of colored paper on the wall.
Beforetheonsetofthethermalstimulus,subjectswere
instructed which face to make. When the desired AUs
were present, subjects held the face for 15 seconds be-
fore heat onset and for the duration of thermal stimula-
tion.
The experimenter observed the participants face for
the duration of the trial and rated the face accuracy on
completion. Accuracy ratings were made on a 7-point
scale (0 ? completely wrong, 6 ? perfect). To assess in-
terrater reliability, 2 trained raters were present for a
subset (n ? 5) of the study participants. Cronbach’s ? was
0.67,consistentwithreliabilitiesobservedinsimilarstud-
ies.6
Thirtysecondsafterpainoffset,emotionalvalenceand
arousal were assessed using the Self-Assessment Mani-
kin, an experimentally validated measure of affective
responding (SAM).2The SAM measures valence and
arousal on separate scales ranging from 1 to 5 for each
dimension.
Subjects received 4 presentations of the thermal stim-
ulus under each of the 3 face conditions (pain, control,
and relaxed faces) in quasirandom order.
The study was approved by the Health Sciences Institu-
tional Review Board at the University of Wisconsin-Mad-
ison.
Results
Threerepeated-measuresANOVAswereconductedfor
the purpose of assessing the effects of Face (control,
pain, relaxed) and Time (measurements 1 through 4) on
pain tolerance and ratings of valence and arousal on
each pain trial (Table 1). Where appropriate, tests were
Huynh-Feldt–adjusted to correct for violated assump-
tions of sphericity.
Temperature
There were no effects of Face on pain tolerance [mean
(SD) for pain face ? 47.16 (1.27)°C, control face ? 47.12
(1.26) °C, resting condition ? 47.03 (1.41)°C; all P’s for
planned comparisons ?0.1]. The effect of Time was also
not significant but approached significance, F(3, 84) ?
3.52, P ? .06, ?2? .11, ? ? .42, with pain tolerance
increasing from times 1 through 4 (means, 46.92°C,
46.93°C, 47.21°C, and 47.35°C, respectively). There was
no significant Face by Time interaction.
Perceived Aversiveness (Valence Ratings)
There was a significant main effect of Face on valence
ratings [F(2, 56) ? 12.34, P ? .00, ?2? .31, ? ? .95], with
pain face trials rated as more aversive than control face
trials (P ? .01), and both face trials more aversive than
relaxed face trials (all P ? .03) (Table 1). Planned compar-
isons revealed that pain face trials were rated as more
aversive than control face trials (P ? .01) and that both
types of faces were rated as more aversive than relaxed
face trials (all P ? .03; Fig 2). The effect of time was also
significant [F(3, 84) ? 6.72, P ? .01], with all trials becom-
2
2.5
3
RelaxedControlPain
P < .03
P < .01
P < .00
Pain Trial Aversiveness (Valence) Ratings
Figure 2. Main effect of face on pain trial aversiveness (va-
lence) ratings [F(2, 56) ? 12.34, P ? .00, ?2? .31, ? ? .95], with
pairwise comparisons.
Table 1. Effects of 3 Repeated-Measures
ANOVAs, With Face (Control, Pain, and
Relaxed), Time, and Their Interaction,
Predicting Pain Trial Unpleasantness Ratings
DFFPH2
Pain Trial Unpleasantness
Face
Time
Face by Time
2, 56
3, 84
6, 168
12.34
6.72
1.85
.00
.00
.10
0.31
0.19
0.06
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ing more unpleasant with time. This finding is notewor-
thy given the trend toward increased tolerance over
time. A possible explanation for this potentially incon-
sistent finding is that because of reduced peripheral sen-
sitivity over time, subjects required more stimulation to
achieve the same level of pain but that this pain was
perceived as more unpleasant due to the cumulative ef-
fort of making the faces. The Face by Time interaction
was not significant.
Toensurethattheseeffectscouldnotbeaccountedfor
by temperature differences, we ran a hierarchical linear
model (see below for methodological details), with tem-
perature entered first. Even after accounting for Tem-
perature, the effect of Face was still highly significant
[F(2,227) ? 9.47, P ? .00].
Emotional Arousal (Arousal Ratings)
There were no significant effects on arousal, although
the effect of Face approached significance [F(2, 56) ?
2.72, P ? .09], with a trend toward both the pain and
control faces being more arousing than the relaxed face.
Covariate Analyses of Nuisance Variables
As demonstrated in Table 2, there were significant dif-
ferences between the faces in difficulty and unpleasant-
ness (both measured before the experiment) as well as
the accuracy with which they made the faces (measured
during the experiment). The degree to which effects on
valence ratings were due to these differences was as-
sessed. Because the SPSS (SPSS, Inc., Chicago, IL) GLM
module does not handle changing covariates, covariate
analyses were performed with the use of SPSS Mixed
Model utility. Importantly, all covariate models were
specified hierarchically using a Type 1 sum of squares,
with the nuisance variable entered first. This method
prioritized shared variance to the nuisance covariates,
making this a very conservative set of analyses. As indi-
cated in Table 3, in all models in which face was entered
with 1 of the nuisance variables, the nuisance variable
was significant but the effect of face remained even af-
ter accounting for this effect. There were no significant
interactions, which is somewhat surprising in the case of
face accuracy, as effects of DFA tasks are frequently de-
pendent on face performance (Ekman, personal commu-
nication with J.A.C., March 22, 2005). Restriction of
rangeontheperformancevariablemayexplainthisfind-
ing.
In addition to the 3 models presented in Table 3, an
additional model was calculated with all nuisance vari-
ables (face unpleasantness, face difficulty, and face per-
formance) entered in the same model. This was a highly
conservative test of the robustness of the face effect.
With all nuisance variables in the model, main effects of
difficulty, unpleasantness, and performance fall away,
but main effects of face [F(1,14) ? 11.88, P ? .01] and
time [F(1,57) ? 9.06, P ? .01] remain. In this model, no
interaction effects were observed.
The fact that the effects of face on valence ratings re-
mains even after accounting for the effects of nuisance
variables in these models strongly suggests that these ef-
fects cannot be accounted for by preexisting differences
between the faces in unpleasantness or difficulty or by dif-
ferences in the accuracy of subjects’ facial expressions.
Discussion
Using the Directed Facial Action task, we found that in
the absence of social reinforcement a voluntary facial
display of pain altered the affective response to painful
stimulation but not the stimulus intensity required to
reach a particular subjective level of pain (8 of 10). In
addition to providing no experimenter feedback and
having subjects focus on a spot on the wall, the effect of
social feedback was controlled in 2 ways. First, by having
subjects make and hold an extreme facial display before
the onset of pain, we obviated the facial information
conveyed during the actual pain experience. Finally, by
allowing subjects to control the duration and tempera-
ture of the nociceptive stimulus, we were able to limit
the need for subjects to use social support as a means of
gaining control over their pain experience.
Our findings indicate that in the absence of social re-
inforcement, voluntary facial displays of pain increase
the negative affect resulting from nociceptive input. By
Table 2. Pre-existing Differences Between the
Faces in Difficulty and Unpleasantness and
Differences in the Accuracy With Which the
Subjects Made the Two Faces During the
Experiment
PAIN FACE
CONTROL FACE
F (1,28)PMEAN
SDMEAN
SD
Difficulty
Unpleasantness
Accuracy
4.35
3.69
5.00
.24
.21
.48
3.07
2.59
4.56
.20
.24
.59
24.47
37.04
20.04
? .01
? .01
? .01
Table 3. Results of Covariate Analyses, Entering Face, and a Nuisance Variable in a Model
Predicting Valence Ratings
NUISANCE VARIABLE
EFFECT OF NUISANCE VARIABLE WITHIN MODEL
EFFECT OF FACE WITHIN MODEL, F (DF)FACE *NUISANCE VARIABLE INTERACTION
Difficulty
Unpleasantness
Accuracy
F(1, 52) ? 4.15, P ? .05
F(1, 157) ? 6.98, P ? .01
F(1, 156) ? 5.02, P ? .03
F(1, 75) ? 12.18, P ? .01
F(1, 169) ? 4.60, P ? .03
F(1, 178) ? 19.29, P ? .01
NS
NS
NS
Note that denominator degrees of freedom are estimated from Satterthwaite approximations without exact F distributions.
446
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indicating that voluntary facial displays of pain incur
costs in terms of increased negative affect, these results
argue against the notion that the operant properties of
voluntary pain displays are determined solely by social
contingencies. For example, while social contingencies
may reinforce the facial expression of pain, these bene-
fits may be offset by an increase in subjective suffering.
From a clinical standpoint, this suggests that increasing
or exaggerating pain behaviors may be a maladaptive
strategy for pain control, particularly for individuals who
are highly sensitive to social reinforcement or who are
otherwise strongly reinforced for expressing pain.
One difficulty with drawing conclusions from the DFA
task concerns the degree to which pre-existing differ-
ences between the faces are responsible for results ob-
tained. We found, for example, that control and pain
faces differed in terms of both difficulty and unpleasant-
ness, even in the absence of concomitant painful stimuli.
Similar differences are common in DFA tasks, with previ-
ous investigators observing differences between faces in
both subjective ratings and autonomic nervous system
activation.10These findings have generated some con-
troversy as to whether effects observed in DFA experi-
ments are better explained by variables such as face dif-
ficulty (Boiten,11996; and rebuttal by Levenson and
Ekman,162002). In the present study, effects of face on
valence ratings survived conservative covariate analyses
testing the effects of face-specific difficulty, unpleasant-
ness, and accuracy, both singly and in combination, sug-
gesting that the effect of the pain face on the subjective
experience of pain cannot be solely attributed to any of
these pre-existing differences between the faces.
These results ultimately suggest that voluntary facial
displays of pain increase the negativity of the affective
response to painful stimulation and that these effects
cannot be accounted for by the difficulty or unpleasant-
ness of making such a face in the absence of nociceptive
input. Nevertheless, there are some caveats that should
be considered in the interpretation of these data. For
example, although the present experiment limited the
impact of demand characteristics by making the instruc-
tions opaque with respect to the experimental question
and using an archetypal pain face that was unlikely to
mimic the subject’s own natural facial response, it is dif-
ficult to completely eliminate such effects due to the
possibility that some subjects may have inferred that it
was an approximation of a facial pain response.
The conclusions drawn from these data would also be
strengthened by future study determining their specificity
to the pain face. The control face used in this preliminary
investigationwasaffectivelyneutralandmatchedthepain
face only in terms of the number of movements. A logical
next step will be to compare the pain face to other nega-
tively valenced, but not pain-specific, faces (eg, fear).
Althoughthepresentstudyfoundnoeffectofthepain
face on pain tolerance, future study may investigate
these effects further with more comprehensive testing,
not only of tolerance but pain threshold, which might be
more sensitive to such effects. Performing such testing
might also help to clarify the suggestion made by these
data that voluntary facial expressions of pain seem to
affect the affective response to pain while having no
effect on sensory processing.
If findings such as those reported here are found to be
specific to biologically relevant facial displays of pain,
future work must determine the mechanisms by which
they affect subjective responses to pain stimuli. Several
theorists have considered this question, proposing direct
feedback from facial afferents as well as central connec-
tions between motor cortex and other neural centers
directing peripheral pain responses,10but none of these
potentialexplanationshavebeenconclusivelysupported
experimentally. A small number of studies suggest that
voluntary emotional facial expressions can alter CNS
functioning in ways that are consistent with the emo-
tional valence of those expressions. For example, Ekman
and Davidson13observed that voluntary smiles, includ-
ingflexionoftheorbicularismusclesurroundingtheeye,
corresponded with increases in left prefrontal cortex
(PFC) activity, a pattern often observed to follow the
elicitation positive affect.18Similarly, Coan et al5ob-
served that voluntary facial expressions of fear and sad-
ness resulted in decreases in left, and increases in right,
PFC activity, a pattern of PFC activity that has long been
associated with both anxiety and depression.3Impor-
tantly, Coan and Allen4reported that changes in PFC
activity appeared to mediate associations between vol-
untary facial movement and self-reported emotional ex-
perience for both positive and negative emotions. Fu-
ture studies, combining measures of CNS activation (eg,
EEG, ERP, and fMRI) and peripheral autonomic nervous
system arousal may clarify the way voluntary facial dis-
plays of pain affect the neural processing and subjective
experience of pain.
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