Elsevier

NeuroImage

Volume 25, Issue 1, March 2005, Pages 312-319
NeuroImage

Rapid Communication
Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain

https://doi.org/10.1016/j.neuroimage.2004.11.043Get rights and content

Abstract

Recent neuroimaging and neuropsychological work has begun to shed light on how the brain responds to the viewing of facial expressions of emotion. However, one important category of facial expression that has not been studied on this level is the facial expression of pain. We investigated the neural response to pain expressions by performing functional magnetic resonance imaging (fMRI) as subjects viewed short video sequences showing faces expressing either moderate pain or, for comparison, no pain. In alternate blocks, the same subjects received both painful and non-painful thermal stimulation. Facial expressions of pain were found to engage cortical areas also engaged by the first-hand experience of pain, including anterior cingulate cortex and insula. The reported findings corroborate other work in which the neural response to witnessed pain has been examined from other perspectives. In addition, they lend support to the idea that common neural substrates are involved in representing one's own and others' affective states.

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)

  • K.M. Prkachin

    The consistency of facial expressions of pain: a comparison across modalities

    Pain

    (1992)
  • K.M. Prkachin et al.

    Pain expression in patients with shoulder pathology: validity, coding properties and relation to sickness impact

    Pain

    (1989)
  • K.M. Prkachin et al.

    Encoding and decoding of pain expressions: a judgment study

    Pain

    (1994)
  • P. Vuilleumier et al.

    Effects of attention and emotion on face processing in the human brain. An event-related fMRI study

    Neuron

    (2001)
  • B. Wicker et al.

    Both of us are disgusted in my insula: the common neural basis of seeing and feeling disgust

    Neuron

    (2003)
  • J.S. Winston et al.

    Common and distinct neural responses during direct and incidental processing of multiple facial expressions

    NeuroImage

    (2003)
  • R.J.R. Blair et al.

    Dissociable neural responses to facial expressions to facial expressions of sadness and anger

    Brain

    (1999)
  • C. Buchel et al.

    Brain systems mediating aversive conditioning: an event related fMRI study

    Neuron

    (1998)
  • K.D. Craig et al.

    The facial expression of pain

  • H. Critchley et al.

    Explicit and implicit neural mechanisms for processing of social information from facial expressions: a functional magnetic imaging study

    Hum. Brain Mapp.

    (2000)
  • M. Davis

    The role of the amygdala in conditioned and unconditioned fear and anxiety

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