Pain 107 (2004) 16–21 www.elsevier.com/locate/pain Development of sensitivity to facial expression of pain Kathleen S. Deyoa, Kenneth M. Prkachina,*, Susan R. Mercerb a Department of Psychology, University of Northern British Columbia, 3333 University Way, Prince George, British Columbia, Canada V2N 4Z9 b University of Otago, Dunedin, Otago, New Zealand Received 25 October 2002; received in revised form 13 March 2003; accepted 10 June 2003 Abstract The ability to perceive pain in others is an important human capacity. Its development has not been studied. The present study examined the development of sensitivity to evidence of pain from childhood to early adulthood. One hundred and thirty-four males and females from four age groups (5 – 6, 8 – 9, 11 – 12 years and young adult) took part. They judged the amount of pain displayed on videotaped excerpts of the facial expressions of pain patients. Excerpts were selected to display no pain, some pain and strong pain, based on facial measurements, and were displayed to participants in a signal-detection paradigm. All participant groups were more sensitive to evidence of strong than some pain. The ability to detect pain expressions increased across the young, middle and older groups of children, but older children did not differ from adults. Increasing age was generally associated with increasing sensitivity to more subtle facial signs of pain. The results indicate that the ability to perceive pain in others is already significantly developed by the ages of five to six, but refinements in the ability continue through to early adulthood. These findings represent the first description of the development of the ability to perceive pain in others. Important areas for future research into the neurobiological, personal and social determinants of this ability are highlighted. q 2003 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. Keywords: Pain; Expression; Facial expression; Facial action coding system; Development Suffering produced by pain is often evident on the face of its victim. The sufferer’s behavior commands attention from others and can provoke behavior changes, such as offering assistance, and emotional responses, such as concern, sympathy, empathy and distress (Prkachin and Craig, 1994). There is evidence that rudiments of the capacity to recognize distress in and empathize with others are present from a very young age (Eisenberg and Fabes, 1998). For example, Martin and Clark (1982) reported that neonates will cry when exposed to the cries of other human infants but not to those of other primates or themselves. Zahn-Waxler et al. (1992) found that behavioral evidence of concern for others increased between the ages of 14 and 20 months among children exposed to experimental simulations of distress. There is considerable evidence that empathic and sympathetic responding are present by the age of 2 –3 years (Eisenberg, 2000). Behavioral and affective responses indicative of empathic or sympathetic responding to another’s pain * Corresponding author. Tel.: þ 250-960-6633; fax: þ 250-960-5536. E-mail addresses: [email protected] (K.M. Prkachin); susan.mercer@ stonebow.otago.ac.nz (S.R. Mercer). presuppose the ability to detect and identify pain in others. Although it is evident that both adults and children are able to identify and respond to painful distress in others, little is known about the development of this capacity. Knowledge of how this capacity develops may play an important role in helping us understand not only pain, but phenomena as varied as empathy and clinical decision making on the one hand and the perceptual integration of experience and expression on the other. A substantial body of research has described facial changes that occur during pain and their important role in social communication (Craig et al., 2001; Prkachin and Craig, 1994). A limited set of changes—principally contraction of the muscles surrounding the eye and drawing together of the eyebrows—occurs on the face when a person is in pain (Prkachin, 1992a). These actions are graded in intensity (Prkachin and Mercer, 1989) and convey evidence of the subjective intensity of pain experience (Prkachin et al., 1994). During painful experiences, homologous changes occur in the faces of children and newborns, even those born prematurely (Craig et al., 1993, 1994; Grunau and Craig, 1987; Grunau et al., 1990; Johnston et al., 1993, 0304-3959/$20.00 q 2003 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. doi:10.1016/S0304-3959(03)00263-X K.S. Deyo et al. / Pain 107 (2004) 16–21 1995). This suggests that the behavioral capacity to register pain and its neurological substrates are present from the earliest moments of sentient existence. Observers are sensitive to variations in pain expression in adults (Poole and Craig, 1997; Prkachin et al., 1983; Prkachin and Craig, 1985; Prkachin, 1992b) and children (Craig et al., 1988; Hadjistavropoulos et al., 1994, 1997) although there are documented shortcomings in their performance (Prkachin et al., 1994, 2001). The capacity to recognize and take action upon the suffering of others is of obvious adaptive benefit to the species (Prkachin, 1986, 1997; Williams, in press). Individuals who can perceive evidence of pain in others are in a position to render them assistance, thus enhancing their fitness, or to protect themselves from a threat shared with the afflicted. Thus, sensitivity to evidence of pain in others should be a nearly universal human capacity. Despite this, virtually nothing is known about the influences upon this capacity. Is it present from an early age? When does it achieve its zenith? Does it change across the life-span? There have been, to our knowledge, no descriptive studies of the development of the capacity to perceive pain in others. Accordingly, the purpose of the present study was to collect basic descriptive information concerning the development of the ability to perceive pain in others. Study of the development of this ability presents certain methodological obstacles common to the study of perceptual processes in children. It is necessary first to construct procedures sensitive to the ability to perceive pain in others and to individual and group differences in those abilities. In addition, the procedures must be sufficiently interesting to sustain the attention and motivation of the youngest participants and sufficiently undemanding to avoid fatigue. Since any study of perception is dependent on the ability to observe a differential response associated with the stimuli of interest, the capacity to respond appropriately is a critical issue. Most often, perceptual sensitivity is indexed by a verbal response. It follows that the response demands for a developmental study must be consistent with the verbal and cognitive capacities of the youngest participants. Moreover, the response demands must be consistent across the age ranges under investigation in order for age comparisons to be valid. In the present study we describe a method for investigating age differences in the perception of pain in others. Observers from four age categories: young, middle and older children and adults judged the pain of others in a signal-detection paradigm (Swets, 1996). 1. Method 1.1. Participants One hundred and thirty-four children and adults from four age groups took part. Young children were 5- and 17 6-year-olds (16 boys, 17 girls), middle children were 8- and 9-year-olds (17 boys, 18 girls) and older children were 11and 12-year-olds (16 boys, 17 girls). A group of young adults, 17 men, 16 women (age, M ¼ 22, SD ¼ 6), also took part. The children were recruited from a number of sources: a participating school, summer day camps, by referral and from personal contacts. The adults were university students. 1.2. Materials Participants viewed videotaped excerpts of the facial expressions of patients undergoing assessment of their shoulder injuries by active and passive range of motion tests. The excerpts were sampled from records taken in a previous study (Prkachin and Mercer, 1989), which had been coded for the amount of pain expression displayed by the patients. Pain expression scores were based on measurements performed using Ekman and Friesen’s (1978) Facial Action Coding System. All excerpts had been assigned a score that was the sum of the products of the intensity and duration of four facial actions—brow lowering, orbit tightening, lipraising/nose-wrinkling and eye closure—that have been associated with pain (Prkachin, 1992a; Prkachin and Craig, 1994). Excerpts were selected from the Prkachin and Mercer (1989) archive if they fell into one of three categories defined by their pain expression scores: no pain, some pain and a lot of pain. Pain expression scores ranged from 0 to 150 (M ¼ 7:97; SD ¼ 15.23). Excerpts were categorized as no pain if their pain expression score was 0, some pain if their score ranged from 1 to 10 and a lot of pain if their scores exceeded 10. Thirty excerpts were selected from each category and assembled on a videotape. The excerpts were randomized in blocks such that each three excerpts contained one example of every category. The order of presentation of patients and patient gender was also random. The excerpts were 2 s in length. They were preceded by a number, identifying the trial, and followed by 5 s of black screen. This test series was itself preceded by 12 practice trials. The total time of the tape was just under 13 min. 1.3. Procedure Participants viewed the videotape on a portable, 13-inch television/video cassette player. They sat at a self-selected distance from the screen. The majority of children (80) were tested in their own homes. The rest were tested in another place familiar to them—a friend’s or relative’s home, a daycare or a day camp. The adults were tested in a room at the university. Pilot testing had established that even the youngest children were capable of making use of a five category rating scale if the experimenter recorded the responses. Participants were told that they were to watch each face on the video and decide if the person they saw hurt. The five category rating scale was explained. A laminated sheet of paper showing the five categories (0 ¼ no pain, 1 ¼ maybe 18 K.S. Deyo et al. / Pain 107 (2004) 16–21 pain or cannot tell, 2 ¼ a little amount, 3 ¼ a middle amount or moderate pain and 4 ¼ a lot of pain) was placed in front of the participant. Participants viewed each stimulus and gave their ratings aloud. The ratings were recorded by the experimenter. 2. Results Participants’ ratings of the three levels of pain were analyzed using the methods of signal-detection theory. For ease of description, the three levels of pain expression manipulated will be referred to as none, mild and strong. Two indices of sensitivity, one to mild pain expressions and one to strong pain expressions were calculated, using the ratings of no pain as a reference category for each. The conditional probabilities of using each rating-scale category to refer to no, mild or strong pain were first calculated. These probabilities were then accumulated from the highest to the lowest category, in this manner treating the rating-scale categories as a series of successively less stringent response criteria. The measure of sensitivity to pain expression was P(A) (McNicol, 1972), an estimate of the area under the receiver – operating – characteristic curve formed when the cumulative probability of using each category to describe a ‘signal’ (in this case, mild or strong pain expressions) is represented on the ordinate, while the cumulative probability of using each category to describe ‘noise’ (in this case, no pain expression) is represented on the abscissa. Thus, two measures of the ability to discriminate pain expressions were calculated, one representing the ability to distinguish mild pain from noise and one representing the ability to distinguish strong pain from noise. These values, referred to as P(A)M and P(A)S could vary between 0 and 1.0. A value of 0.5 represents chance performance. An initial analysis was conducted to determine whether participants were, in fact, able to detect pain expressions at above-chance levels. Single-sample t-tests were used to evaluate whether the mean P(A)M and P(A)S value for each age group differed from the chance value of 0.5. Because this entailed eight separate comparisons an alpha level of 0.007 was set as the criterion for statistical significance in order to adjust for Type 1 error. All the statistical tests were significant (lowest t (32) ¼ 7.04, p , 0:001). Thus, both mild and strong pain expressions were clearly discriminable from no pain across all participant age groups. P(A)M and P(A)S values were then entered as dependent variables in a 2 (sex) £ 4 (age) £ 2 (intensity) analysis of variance (ANOVA) with repeated measures on the last factor. The analysis revealed a significant effect for intensity, Fð1; 126Þ ¼ 291:91, p , 0:001, h ¼ 0.70. There was also a significant main effect for age, Fð3; 126Þ ¼ 85:22, p , 0:001, h ¼ 0.67. Both effects can be observed in Fig. 1, which shows that facial expressions of strong pain were clearly more discriminable than facial expressions of mild pain. Older participants were also clearly more sensitive to variations in pain expression. Post-hoc tests revealed that middle children were more sensitive than young children, while older children were more sensitive than middle children. However, the average performance of older children and adults did not differ significantly. A further analysis was conducted in order to examine how participants in the different age groups made use of the facial cues. Each participant’s pain rating was correlated with each patient’s scores on the component facial actions contributing to the pain expression index. Because mouth opening was related to pain in the original study from which the pain expression excerpts were sampled (Prkachin and Mercer, 1989), and because, from observation, it was Fig. 1. Mean (^ se) discriminability of the mild and strong pain expressions of shoulder pain patients, judged by four age groups: young children (ages 5–6 years, n ¼ 33), middle children (ages 8 –9 years, n ¼ 35), old children (ages 11 –12, n ¼ 33) and adults (Mean age ¼ 22 years, n ¼ 33). K.S. Deyo et al. / Pain 107 (2004) 16–21 Table 1 Average correlations between component facial actions and participants pain ratings across four age groups (standard errors in parentheses) Facial action Young children Middle children Older children Brow lowering 0.31* (0.02) 0.46* (0.02) 0.52* (0.02) Orbit tightening 0.17 (0.02) 0.35* (0.02) 0.39* (0.02) Lip-raising/ 0.18 (0.02) 0.28* (0.02) 0.31* (0.02) nose-wrinkling Eye closing 0.18 (0.01) 0.33* (0.01) 0.33* (0.01) Mouth opening 0.29* (0.02) 0.41* (0.02) 0.45* (0.02) Adults 0.49* (0.02) 0.40* (0.02) 0.31* (0.02) 0.35* (0.01) 0.43* (0.02) *Average p , 0:01. Note: data were subject to r-to-z transformations prior to averaging. Values represent z-to-r back-transformations subsequent to averaging. a salient feature of the excerpts, the measure of degree of mouth opening was also included. Individual participants’ action-rating correlations were subjected to r-to-z transformations. A 2 (sex) £ 4 (groups) £ 5 (actions) ANOVA, with repeated measures on the last factor was performed on z-transformed r values. This analysis resulted in a significant main effect for group, Fð3; 126Þ ¼ 44:09, p , 0:001, h ¼ 0.51, and a significant group – action interaction, Fð9; 377Þ ¼ 3:10, p , 0:001, h ¼ 0.07. Posthoc analysis of the interaction by Tukey’s B-test indicated that, for each component action, the youngest participants’ average correlations were significantly lower than those of the other three age groups, which did not differ. The backtransformed average correlations between each component facial action and pain ratings for the four separate age groups are shown in Table 1. It can be seen that, except for the correlations between orbit tightening, lip-raising/nosewrinkling, eye closing and pain ratings among the youngest participants, the average correlations were all significant. For the youngest participants, only two facial actions— brow lowering and mouth opening—were related to pain judgements. 3. Discussion Children as young as 5 –6 years of age are clearly sensitive both to the occurrence of and quantitative variation in pain expression. Despite this, the ability to detect facial evidence of pain in others increases in a linear fashion to the pre-adolescent years, at which age performance resembles that of young adults. By the age of 8– 9 years, the relation between children’s pain judgements and the facial movements that contribute to a pain expression suggests that children are sensitive to, and make use of, the suite of changes that occur on the face during pain. The findings provide evidence of a process of maturation of the ability to detect pain in others that unfolds over time and is largely in place by late childhood. There were significant improvements in the ability to detect both levels 19 of pain expression between the young and the middle children and the middle and the older children. The improvement between the young and middle groups was accompanied by a change in the relationship between their pain judgements and the facial signals that differentiated the pain levels. The judgements of the youngest children reflected primarily two actions—the degree of brow lowering and mouth opening on the patients’ faces. Children who were, on average, 3 years older, appeared to make independent use of all the facial changes involved in pain expression. Thus, the improvement in ability to detect pain expression over this time appears to reflect the emergence of differential sensitivity to a more comprehensive array of information. The fact that children in the older age group were more sensitive to the different levels of pain expression than the middle children, suggests that the older children may employ a more effective algorithm for weighing the array of information available in the facial displays. Adults, who were not significantly better at detecting pain than the older children, also made use of the full array of information in the processing of their judgements. The findings suggest that the maturation of sensitivity to pain expression unfolds sequentially across the age spectrum examined in this study. It is interesting to note the relative similarity across ages of the correlations with pain ratings associated with each facial action. For all participant groups the correlations associated with brow lowering and mouth opening were of greatest magnitude and differed only slightly. These appear, therefore, to be the most salient cues to observers of all ages. The correlations associated with orbit tightening, eye closing and nose-wrinkling/lip-raising were likewise comparable across age groups, though lower in magnitude. This pattern of findings is somewhat curious, since orbit tightening is the action that has shown the strongest and most consistent relationship to sufferers’ reports of pain in empirical studies of the subject (Craig et al., 2001). This kind of sub-optimal cue utilization has also been shown in judgement studies employing untrained adult observers (Prkachin et al., 1994) and adults with varying types of experience with pain sufferers (Prkachin et al., 2001). This may not be surprising, given that the facial signs associated with orbit tightening (and nose-wrinkling/lip-raising) are more subtle than the other changes (Ekman and Friesen, 1978). Nevertheless, from an adaptational perspective, it is difficult to explain why observers would be relatively insensitive to a more reliable indicator. Although it may not be surprising that sensitivity to evidence of pain in others improves with age, the findings nevertheless highlight the importance and the possibility of understanding the processes that contribute to this development. In addition, the data from the very youngest participants indicated that they were surprisingly adept at making discriminations between apparent pain states. The ability to detect suffering in others is clearly already functional to a significant degree at the ages of five and six. Indeed, despite the fact that pilot work had established that 20 K.S. Deyo et al. / Pain 107 (2004) 16–21 children in the youngest age group studied could make use of the rating scale employed in this study, it is also true that the use of quantitative ratings is quite a sophisticated procedure for children of this age. This could have limited the magnitude of the sensitivity indices obtained in the present study. With improved methodology, it may be possible to document sensitivity to evidence of suffering in others at an even earlier age. What are the sources of such sensitivity and its development over time? It is likely that some elements of the capacity to perceive suffering in others, as a component of our evolutionary heritage, are innate. A general tendency to know that others are hurt would clearly confer an adaptive advantage to the group, insofar as the perceptual ability is linked to lending assistance or feeling threatened in situations of peril. It is known that children as young as 4– 7 months of age are sensitive to the occurrence of some facial expressions of emotion (Labarbera et al., 1976; Nelson and de Haan, 1996). This suggests that, at a very early age, children are differentially responsive to social signals that have implications for their well-being and provides reason to believe that the ability to perceive some social signals is either inherent, or requires relatively little in the way of experience to develop. As an experience that has clear implications for well-being, whether it is occurring to oneself or someone else, pain would seem to be in the same category. Recent findings from the study of emotion may have implications here. Pain has several properties in common with emotions. It is an unpleasant state, it is accompanied by an expressive signal and it organizes a variety of behaviors whose goal is to manage it and to facilitate survival. Consequently, it is not implausible to expect that aspects of pain expression and the ability to perceive its expression would be regulated in ways that resemble the regulation of comparable emotional processes. There is increasing evidence from neuropsychological and neuroimaging studies that specific emotional states and the ability to perceive the expression of comparable emotional states in others are regulated in comparable brain sites. For example Adolphs and colleagues have reported that bilateral damage to the amygdala, a region that has been implicated in the regulation of fear (LeDoux, 1995), was associated with impaired ability to detect facial expressions of fear (Adolphs et al., 1994, 1995). Likewise PET and fMRI studies have shown enhanced activity in the amygdala among normal participants processing facial expressions of fear (Morris et al., 1998; Phillips et al., 1997). Given the parallels in properties of pain and emotional expression, it may well be that the ability to perceive pain expression in others is regulated by specific brain sites and that development of the capacity would be dependent on development of the associated neural structures. No doubt experiential influences play a role in development of the capacity to perceive pain in others. In fact, recent findings suggest that variations between people in the nature of their exposure to the pain of others can affect adults’ abilities to perceive pain expression (Prkachin et al., 2001). Precisely what kinds of experience may affect development of the ability to perceive pain expression in the age range examined in the present study is unclear. Von Baeyer et al. (1998) have documented the frequent experience of pain in the natural environments of children. Such exposure would appear to provide the critical environmental conditions for learning the signals associated with pain in others. In a related context, it should be emphasized that in the present study sensitivity to others’ pain expressions was examined by exposing participants to the displays of adult patients. It is not unreasonable to think that aspects of the perception of pain expressions of children may differ from perception of the expressions of adults. It seems likely that further study of the development of the ability to perceive pain in others and of individual differences in this ability would provide valuable information not just about the natural ecology of pain, but also about other important human processes. Sensitivity to suffering is a hallmark of sympathy and empathy. Consequently, learning about the factors that may increase or decrease such sensitivity would undoubtedly advance understanding of this important human capacity. Pain theorists have suggested that responses of members of the social environment to evidence of suffering may contribute to the development or maintenance of chronic pain problems (Fordyce, 1976). Pain-evoked social responses, such as sympathy or encouraging forbearance presuppose the ability to perceive variations in pain expression (Prkachin and Craig, 1994). Thus, studies of the determinants of sensitivity to pain expression are potentially of great importance to advance understanding of how social experience may affect pain. This study demonstrates a method for addressing these and other important issues. Acknowledgements This paper is based on a thesis submitted in partial fulfilment of requirements for the M.Sc. in Psychology at the University of Northern British Columbia. Some of the findings were presented at the Annual Meeting of the Canadian Psychological Association, Edmonton, Alberta, 1998. We gratefully acknowledge the assistance provided by Glenda Prkachin and Reiko Graham in the preparation of videotape materials and helpful commentary by Sherry Beaumont and Judith Lapadat. References Adolphs R, Tranel D, Damasio H, Damasio AR. 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