Elsevier

NeuroImage

Volume 53, Issue 1, 15 October 2010, Pages 355-363
NeuroImage

Brain responses to facial expressions of pain: Emotional or motor mirroring?

https://doi.org/10.1016/j.neuroimage.2010.05.037Get rights and content

Abstract

The communication of pain requires the perception of pain-related signals and the extraction of their meaning and magnitude to infer the state of the expresser. Here, BOLD responses were measured in healthy volunteers while they evaluated the amount of pain expressed (pain task) or discriminated movements (movement task) in one-second video clips displaying facial expressions of various levels of pain. Regression analysis using subjects' ratings of pain confirmed the parametric response of several regions previously involved in the coding of self-pain, including the anterior cingulate cortex (ACC) and anterior insula (aINS), as well as areas implicated in action observation, and motor mirroring, such as the inferior frontal gyrus (IFG) and inferior parietal lobule (IPL). Furthermore, the pain task produced stronger activation in the ventral IFG, as well as in areas of the medial prefrontal cortex (mPFC) associated with social cognition and emotional mirroring, whereas stronger activation during the movement task predominated in the IPL. These results suggest that perception of the pain of another via facial expression recruits limbic regions involved in the coding of self-pain, prefrontal areas underlying social and emotional cognition (i.e. ‘mentalizing’), and premotor and parietal areas involved in motor mirroring.

Introduction

Pain behavior is vital to pain communication: how we move our bodies and our faces in response to a noxious stimulus provides observers with key information about our experience/inner state. Current neuroimaging techniques have allowed us to begin to investigate neural processes involved in the perception of pain in others. It has been demonstrated that certain brain regions previously identified as involved in processing the affective dimension of pain in the self, namely, the posterior (supracallosal) part of the anterior cingulate cortex (ACC; BA 24) and the anterior insula (aINS) (Apkarian et al., 2005) are also engaged when individuals view cues indicating that a loved one is receiving a painful stimulus (Singer et al., 2004), images of limbs receiving noxious stimuli (Jackson et al., 2005, Lamm et al., 2007b, Morrison et al., 2004) or images and/or videos of people in painful situations (Ochsner et al., 2008).

As the facial expression of pain is the most prominent non-verbal pain behavior, it has an enormous impact on the social communication of pain (Hadjistavropoulos and Craig, 2002). The few studies that have looked at brain responses to the observation of facial expressions of pain have also found engagement of brain regions underlying self-pain, even in the absence of information about the nature of the painful stimulus (Botvinick et al., 2005, Saarela et al., 2007). These findings have been discussed in the context of “shared representations” theories of empathy, which assert that empathic processes, from emotional contagion to cognitive empathy, begin with a mapping of the perceived emotional state of the expresser on a representation of the corresponding state in the observer [e.g. (Keysers and Gazzola, 2009, Preston and de Waal, 2002)]. When pain states are communicated through facial expression, the neurobiological substrate of this shared representation may involve the human “mirror neuron” system (MNS) (Fadiga et al., 1995, Grafton et al., 1996, Iacoboni et al., 1999, Rizzolatti et al., 1996), perhaps via interactions with brain areas involved in emotions (Iacoboni, 2009). However, empathy could potentially occur without the involvement of the classic (motor) MNS (e.g. Chakrabarti et al., 2006) and mirroring processes may be common across several brain areas beyond the motor system (Keysers and Gazzola, 2009).

It should be noted that the basic processing of facial expression of emotions may not be sufficient to activate the MNS system reliably and this system is generally not included as a part of the basic brain network underlying the perception of emotional faces (see review by Vuilleumier and Pourtois, 2007). However, several recent studies have reported overlapping engagement of areas of this network during the observation/evaluation and execution of facial expressions of emotion, specifically the inferior frontal gyrus (IFG) (Carr et al., 2003, Enticott et al., 2008, Hennenlotter et al., 2005, Leslie et al., 2004, van der Gaag et al., 2007) and the inferior parietal lobule (IPL) (Montgomery and Haxby, 2008). Furthermore, the response of an adjacent and more dorsal part of the IFG to the passive viewing of facial expressions of basic emotions has been associated with individual scores on an empathy questionnaire (Chakrabarti et al., 2006). In the specific case of pain expressions, one study found that subjective ratings of acute versus chronic pain expressions correlated with activation in the left inferior parietal lobule (IPL) (Saarela et al., 2007), one area posited as part of the human MNS (Iacoboni, 2005).

The facial expressions of pain and emotions have at least two dimensions: dynamic facial movements, and an affective meaning. As these two components are strongly linked, it is not clear if brain activation evoked by the viewing of pain expressions is driven by the amount of pain expressed (the affective dimension), the magnitude of the movement of facial features (the motor dimension), or both. Therefore, studies of brain responses during the perception of pain expressions must consider and attempt to separate these two dimensions.

The first aim of the current study was to expand and improve on earlier pain face studies by examining the modulation of brain activation by the amount of pain perceived. Secondly, we wanted to investigate the underlying mechanisms involved in the observation of pain in others while differentiating between the contribution of the affective and dynamic motor dimensions of the expressions. In order to differentiate between the observer's responses reflecting the affective meaning conveyed by the expressions and the perception of facial movements coding for the expressions, we used two tasks intended to manipulate the attention allocated to those separate dimensions of the facial expressions. The first was a pain evaluation task in which subjects reported the amount of pain expressed (i.e. attentional focus on meaning), and the second was a movement discrimination task in which subjects compared the movement in the upper versus lower regions of the face (i.e. attentional focus on movements). This is, to our knowledge, the first study looking at pain facial expressions that has not only used an explicit, online evaluation task, but that has also contrasted it with a control task condition.

We hypothesized that the explicit processing of the meaning of facial expressions of pain would engage cortical areas also involved in the experience of pain in the self, and that activity in a subset of these areas would correlate with the amount of pain perceived. Moreover, we expected that brain activation in response to the facial expression of pain would differ depending on task demands and attentional focus. Specifically, we expected that explicitly attending to and evaluating pain in others would activate midline prefrontal areas believed to be involved in social cognition and, specifically, “mentalizing”—that is, thinking about the emotional states of others (Amodio and Frith, 2006, Frith and Frith, 2006), whereas attending to and evaluating movement would lead to greater activation in areas believed to code for motor aspects of observed action, such as the premotor cortex (BA 6) (Morin and Grezes, 2008), as well as the ventral IFG and IPL (Iacoboni, 2005, Iacoboni, 2009, Kilner et al., 2009).

Section snippets

Subjects

Subjects were 18 healthy, right-handed volunteers (9 women) between 18 and 25 years of age, with no history of neurological or psychiatric disorder. Data from one participant were discarded due to excessive movement during scanning. Subjects were informed as to the purpose and procedures of the study, and written consent was obtained prior to the experiment. The study was approved by the research ethics committee of the Institut Universitaire de Gériatrie de Montréal.

Stimuli

The stimuli used in this

Behavioral results

In the PT trials, subject ratings for the amount of pain expressed (0–100) matched the pre-defined levels—neutral/no pain (pain 0; mean ± SD = 1.68 ± 3.48), mild (pain 1; 22.25 + 10.17), moderate (pain 2; 46.41 + 13.98), and strong (pain 3; 70.01 + 13.08), showing that subjects not only differentiated significantly between the levels (F(3,51) = 463.81; p  0.001), but that they also perceived the intended pain level of the stimuli. There was no effect of the gender of the subjects or of the actors on pain

Discussion

The results of the present study support, strengthen, and go beyond earlier work in several important ways. For the first time, we looked at the evaluation of pain in others in a paradigm combining dynamic pain expressions (rather than static images), several well-controlled discrete levels of pain including a neutral expression, and a target task involving the online rating of pain perceived in each stimulus (as opposed to passive viewing and post-scan stimuli evaluation). Most importantly, we

Conclusion

In conclusion, we first confirmed earlier findings that implicate the ACC and INS in the perception and evaluation of pain in others. Second, we found that the explicit evaluation of pain expression engages areas considered to be important for general, high-level social cognition—specifically, thinking about what others are feeling. Third, and most significantly, we find that areas recently posited to be part of a human mirror neuron system are differently engaged, depending on the specific

Acknowledgments

This work was supported by grants from the Canadian Institutes of Health Research (CIHR) and the National Sciences and Engineering Research Council of Canada (NSERC). The authors thank other members of the pain research lab and staff of the Functional Neuroimaging Unit for their help in the validation of the stimuli and in fMRI data acquisition (T.N. Ly, M.J. Roy, E. Jakmakjian, L. Tenbokum, J. Chen, C. Hurst, and A. Cyr). We also thank A. Heinecke and F. Esposito at Brain Innovation, Inc. for

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