Rapid CommunicationViewing facial expressions of pain engages cortical areas involved in the direct experience of pain
Introduction
The interpretation of facial expressions, and in particular expressions of emotion, is critical to everyday social functioning (Ekman, 1999). In recent years, a number of studies have begun to investigate the neural substrates for perceiving facial expressions, using neuroimaging and other modalities (see Adolphs, 2002, Murphy et al., 2003). Specific expressions that have been studied include those of fear, anger, sadness, happiness, and disgust (e.g., George et al., 1996, Gur et al., 2002, Kesler-West et al., 2001, LaBar et al., 2003, Phillips et al., 1997, Winston et al., 2003). However, one basic category of facial expression that has not yet been investigated is that of pain.
Facial expressions of pain have been the focus of considerable behavioral research (Craig et al., 2001). Such work has documented that pain expressions, like other affective facial expressions, play an important role in social communication (Hadjistavropoulos and Craig, 2002, Prkachin and Craig, 1994, Williams, 2003). From early in life, people display a keen sensitivity to the occurrence of pain in others (Deyo et al., 2004), eventually developing a highly refined, though sometimes interestingly biased, ability to evaluate pain intensity from facial displays (Prkachin et al., 1994). Although this ability has been characterized in some detail at the behavioral level, the neural substrates for the processing of pain expressions have not been previously investigated.
In approaching this question, one intriguing hypothesis is that viewing facial expressions of pain might engage neural systems that are also activated during the direct experience of pain. We might predict, specifically, that pain expressions would engage the dorsal anterior cingulate cortex (ACC) and the insula, regions reliably activated during first-person pain (Peyron et al., 2000, Rainville, 2003).
In fact, a strong motivation for this idea is provided by previous empirical work. For example, Wicker et al. (2003) showed that viewing facial expressions of disgust activated regions that were also activated as subjects inhaled disgusting odors. The researchers concluded that “there is a common mechanism for understanding the emotion in others and feeling the same emotions ourselves” (p. 661). If this were true, then it should be expected that facial expressions of pain would engage brain areas activated by the first-hand experience of pain.
This expectation is further bolstered by the results of three studies that examined neural responses as subjects viewed not the expression of pain, but the infliction of pain on another. Hutchison et al. (1999) measured single cell activity in the ACC during painful vibratory stimulation and found that some cells that responded to pain also responded to the sight of the vibratory stimulus being applied to the examiner. More recently, Singer et al. (2004) used fMRI to study brain activation as subjects viewed their own hand and the hand of their spouse, as each received painful electrical stimulation. Here again, pain-responsive brain structures (ACC and insula) were activated both by pain and by viewing the infliction of pain. Finally, in another recent fMRI study, Jackson et al. (2004) presented subjects with pictures of body parts in painful situations (e.g., a hand caught in a door), finding, consistent with the previous two studies, that this engaged pain-related regions, including ACC and insula.
It should be noted that the focus of these previous studies was on the witnessing of pain-inducing events rather than on pain-related behavior. In particular, none of the studies just summarized involved viewing facial expressions of pain. Existing data thus do not provide any direct information concerning how such expressions are processed in the brain. Nevertheless, the studies reviewed do provide an indirect motivation for the expectation that facial expressions of pain might activate pain-responsive brain areas.
In order to test this hypothesis, we performed fMRI as normal subjects viewed short video sequences showing facial expressions of pain. In order to identify areas responding to the first-person experience of pain, the same subjects also received, during alternate blocks, painful and non-painful thermal cutaneous stimulation. Our prediction was that regions engaged by first-person pain, specifically the dorsal ACC and anterior insula, would also show increased activation during the viewing of facial expressions of pain. A secondary question was whether pain expressions would also activate regions associated with the processing of other affective facial expressions, but not typically activated in the setting of first-person pain, such as the amygdala and orbitofrontal cortex (Adolphs, 2002).
Section snippets
Participants
Participants included 12 women recruited from the University of Pennsylvania community through an electronic newsgroup posting. All were native English speakers with no history of neurological illness. Ages ranged from 20 to 30. Participants gave informed consent and were paid for their participation. The experimental protocol was approved by the University of Pennsylvania Institutional Review Board.
Materials
Videotaped recordings of facial expressions were selected from a novel archive of participants
Results
As anticipated, greater activation was observed in all three a priori regions of interest during painful thermal stimulation than during non-painful stimulation (ACC, t(11) = 3.13, P < 0.01; left insula, t(11) = 3.77, P < 0.005; right insula, t(11) = 3.94, P < 0.005). More relevant to the present hypotheses was the question of whether these regions would also show higher activity during the viewing of facial expressions of pain than during viewing of neutral expressions. This prediction was
Discussion
In the present fMRI study, facial expressions of pain were found to induce a relative activation in cortical areas associated with the first-hand experience of pain. Regions of interest were selected in the dorsal ACC and bilateral insulae, based on previous research into the neural response to pain. The involvement of these areas in pain processing, for our subject group, was confirmed by the finding of higher activation in response to noxious thermal stimulation than to innocuous stimulation.
Acknowledgments
Financial support for this research was provided by U.S. National Institutes of Health Grant MH-16804 (M.B.), Canadian Institutes of Health Research Operating Grant MOP-53301 (K.M.P., P.E.S.), and a grant from the University of Pennsylvania Research Foundation (A.P.J.).
References (42)
Neural systems for recognizing emotion
Curr. Opin. Neurobiol.
(2002)- et al.
Development of sensitivity to facial expression of pain
Pain
(2004) - et al.
Neural activation during covert processing of positive facial expressions
NeuroImage
(1996) - et al.
Gender differences in regional cerebral blood flow during transient self-induced sadness or happiness
Biol. Psychiatry
(1996) - et al.
Brain activation during facial emotion processing
NeuroImage
(2002) - et al.
A theoretical framework for understanding self-report and observational measures of pain: a communications model
Behav. Res. Ther.
(2002) - et al.
Neural substrates of facial emotion processing using fMRI
Cogn. Brain Res.
(2001) - et al.
Dissociable neural pathways are involved in the recognition of emotion in static and dynamic facial expressions
NeuroImage
(2003) - et al.
An fMRI study of the anterior cingulate cortex and surrounding medial wall activations evoked by noxious cutaneous heat and cold stimuli
Pain
(2000) - et al.
Functional imaging of brain responses to pain. A review and meta-analysis
Clin. Neurophysiol.
(2000)
The consistency of facial expressions of pain: a comparison across modalities
Pain
Pain expression in patients with shoulder pathology: validity, coding properties and relation to sickness impact
Pain
Encoding and decoding of pain expressions: a judgment study
Pain
Effects of attention and emotion on face processing in the human brain. An event-related fMRI study
Neuron
Both of us are disgusted in my insula: the common neural basis of seeing and feeling disgust
Neuron
Common and distinct neural responses during direct and incidental processing of multiple facial expressions
NeuroImage
Dissociable neural responses to facial expressions to facial expressions of sadness and anger
Brain
Brain systems mediating aversive conditioning: an event related fMRI study
Neuron
The facial expression of pain
Explicit and implicit neural mechanisms for processing of social information from facial expressions: a functional magnetic imaging study
Hum. Brain Mapp.
The role of the amygdala in conditioned and unconditioned fear and anxiety
Cited by (459)
Activity increases in empathy-related brain regions when children contribute to peers’ sadness and happiness
2024, Journal of Experimental Child PsychologyA developmental neurocognitive perspective on conduct disorder: current status and future directions
2023, Encyclopedia of Mental Health, Third Edition: Volume 1-3Visual perspective and body ownership modulate vicarious pain and touch: A systematic review
2024, Psychonomic Bulletin and ReviewVicarious facilitation of facial responses to pain
2024, European Journal of Pain (United Kingdom)Emotion processing in youths with conduct problems: an fMRI meta-analysis
2023, Translational Psychiatry