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Differences in facial expressions of four universal emotions

Psychiatry Research, 2004
The facial action coding system (FACS) was used to examine recognition rates in 105 healthy young men and women who viewed 128 facial expressions of posed and evoked happy, sad, angry and fearful emotions in color photographs balanced for gender and ethnicity of poser. Categorical analyses determined the specificity of individual action units for each emotion. Relationships between recognition rates for different emotions and action units were evaluated using a logistic regression model. Each emotion could be identified by a group of action units, characteristic to the emotion and distinct from other emotions. Characteristic happy expressions comprised raised inner eyebrows, tightened lower eyelid, raised cheeks, upper lip raised and lip corners turned upward. Recognition of happy faces was associated with cheek raise, lid tightening and outer brow raise. Characteristic sad expressions comprised furrowed eyebrow, opened mouth with upper lip being raised, lip corners stretched and turned down, and chin pulled up. Only brow lower and chin raise were associated with sad recognition. Characteristic anger expressions comprised lowered eyebrows, eyes wide open with tightened lower lid, lips exposing teeth and stretched lip corners. Recognition of angry faces was associated with lowered eyebrows, upper lid raise and lower lip depression. Characteristic fear expressions comprised eyes wide open, furrowed and raised eyebrows and stretched mouth. Recognition of fearful faces was most highly associated with upper lip raise and nostril dilation, although both occurred infrequently, and with inner brow raise and widened eyes. Comparisons are made with previous studies that used different facial stimuli....Read more
Differences in facial expressions of four universal emotio Christian G. Kohler a, * , Travis Turner b , Neal M.Stolar a , Warren B. Bilker c , Colleen M. Brensinger c , Raquel E. Gur a , Ruben C. Gur a a Neuropsychiatry, Department of Psychiatry, 10th Floor Gates Bldg., University of Pennsylvania, 3400 Spruce St., Philadelphia, PA 19104-4283, USA b Department of Psychology, University of California, San Diego, CA, USA c Department of Biostatistics and Epidemiology, University of Pennsylvania, Philadelphia, PA,USA Received 27 June 2003; received in revised form 25 June 2004; accepted 10 July 2004 Abstract The facial action coding system (FACS) was used to examine recognition rates in 105 healthy young men an viewed 128 facial expressions of posed and evoked happy, sad, angry and fearful emotions in color photograph gender and ethnicity of poser. Categorical analyses determined the specificity of individual action units for each emotion. Relationships between recognition rates for different emotions and action units were evaluated using a logistic Each emotion could be identified by a group of action units, characteristic to the emotion and distinct from other emotions. Characteristic happy expressions comprised raised inner eyebrows, tightened lower eyelid, raised cheeks, uppe corners turned upward. Recognition of happy faces was associated with raised cheek, lid tightening and raised outer brow. Characteristic sad expressions comprised furrowed eyebrow, opened mouth with upper lip being raised, lip cor turned down, and chin pulled up. Only lower brow and raised cheek were associated with sad recognition. Char expressions comprised lowered eyebrows, eyes wide open with tightened lower lid, lips exposing teeth and stre Recognition of angry faces was associated with lowered eyebrows, raised upper lids and lower lip depression. C expressions comprised eyes wide open, furrowed and raised eyebrows and stretched mouth. Recognition of fearful faces was most highly associated with raised upper lip and nostril dilation, although both occurred infrequently, and with and widened eyes. Comparisons are made with previous studies that used different facial stimuli. D 2004 Elsevier Ireland Ltd. All rights reserved. Keywords: Action unit; Facial emotion expression; Emotion recognition 1. Introduction Facial expressions are used in humans and animal for communication, in particularto convey one’s emotional state ( Darwin,1965). This communication can be reflexive, as situations may evoke emotions 0165-1781/$ - see front matter D 2004 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.psychres.2004.07.003 * Corresponding author. Tel.:+1 215 614 0161; fax:+1 215 662 7903. E-mail address: kohler@bbl.med.upenn.edu (C.G. Kohler). Psychiatry Research 128 (2004) 235 – 244 www.elsevier.com/locate/psychres
that are spontaneously expressed on the face. In other instances, particularly in humans, facialexpressions may be volitional signals intended for communication and may not reflectthe true emotional state ofthe person (Ekman and Friesen, 1975).Impairment in emotional processing, specifically emotion recogni- tion, has beendescribed inpsychiatricdisorders including schizophrenia, depression and bipolar dis- order,and in neurological disorders (review: Kohler et al., 2004).Since the earliestdescriptionsof schizophrenia, decreased and muted facial expres- sions of emotions have been reported as a hallmark of the illness; however, there have been few attempts to investigate this impairment further in schizophre- nia and other psychiatric disorders. Six basic emotions—happiness, sadness, anger, fear,disgustand surprise—and their corresponding facial expressions are recognized across different cultures (Huber, 1931;Eibl-Eibesfeldt, 1970;Izard, 1971;Ekman and Friesen, 1975).Descriptions have been made about which facial muscles are involved in the formation of each of the basic emotions ( Huber, 1931;Plutchik,1962;Ekman and Friesen, 1975; Gosselin et al., 1997). For happy expressions, Ekman and Friesen (1975) described facial expressions of tense lower eyelids,raised cheeks and lip corners pulled up; for sad expressions, inner eyebrows raised and drawn together, and lip corners pulled down; for anger expressions, lowered eyebrows drawn together, tense lower eyelids, pressed lips or lips parted in a square shape; for fearexpressions, eyebrows raised and drawn together, wide open eyes with tense lower eyelidsand stretched lips. Based on facial muscle movement, Ekman and Friesen (1978) developed the FacialAction Coding System (FACS) by identifying thepresenceof specificactionsof facialmuscles called Action Units (AUs). Gosselin etal. (1997) tested Ekman and Friesen’s predictions about facial expressions of six emotions in two conditions—posed or unfelt and evoked or felt. In that study, actors used two different methods of displaying facial expressions of six emotions—trying toexperience the target emotion according to the Stanislawski technique, while expressing the emotion (evoked emotion) or merely displaying the emotion without the emotional experience (posed emotion). FACS analyses of facial expressions by a single rater revealed that AUs for eachemotionwere concordant with Ekman and Friesen’s descriptions. Occurrence rates of AUs for evoked and posed facial expressions showed consid- erable overlap, in particular for happy and surprise expressions. Otherstudiesthatinvestigated facial landmark changes associated with emotional expres- sion focused on measurement of muscle activity wit electromyography (EMG). Limitations of this meth- odology include that only select muscle groups, such as corrugator supercilii orbicularis oculi and zygoma ticus major have been measured, showing the corrugator to be associated with sad and the zygom ticus with happy emotions (Schwartz et al., 1976). Tassinaryand Cacioppo(1989) elucidatedthat expressions of action units involving brow and chee regionsare associated with discrete facialmuscle activity as measured by surface EMG. More recently considerable overlap has been shown between surfa and intramuscular recordings of facialEMG during happy, sad and angry expressions ( Aniss and Sachd 1996). In our study, three certified FACS raters examined 128 images of extremely happy, sad, angry and fea facesthatwere selected foruse in a functional imaging study and piloted for recognition in a group of healthy subjects. Disgust was not included becau of our assumption that it may notpresent a pure emotion,butrathera mixtureof otheruniversal emotions (Kohleret al., 2003).Surprisewas not included because its valence depends entirely on th triggering event and itcan therefore be any of the other emotions, with a rapid onset. The purpose of o study was to investigate which facial changes are m frequent in happy, sad, angry and fearful expression and which facial changes are essential for accurate recognition ofthe particularemotion.The study included thefollowing specificaims:(1) Which action units characterize the different emotions? We hypothesized that each emotion can be defined by t presence of action units common to faces with the particular emotion. (2) Which action units distinguis different emotions from each other? We hypothesize thatfacialexpressions of each emotion consist of uniqueactionunits that are distinctfrom other emotions. (3) How do posed and evoked emotions differ with respect to action units? We hypothesized that different action units are used for the expressio of posed and evoked emotions. (4) Do men and women utilize different action units for the expressio C.G. Kohler et al. / Psychiatry Research 128 (2004) 235–244 236
Psychiatry Research 128 (2004) 235 – 244 www.elsevier.com/locate/psychres Differences in facial expressions of four universal emotions Christian G. Kohlera,*, Travis Turnerb, Neal M. Stolara, Warren B. Bilkerc, Colleen M. Brensingerc, Raquel E. Gura, Ruben C. Gura a Neuropsychiatry, Department of Psychiatry, 10th Floor Gates Bldg., University of Pennsylvania, 3400 Spruce St., Philadelphia, PA 19104-4283, USA b Department of Psychology, University of California, San Diego, CA, USA c Department of Biostatistics and Epidemiology, University of Pennsylvania, Philadelphia, PA, USA Received 27 June 2003; received in revised form 25 June 2004; accepted 10 July 2004 Abstract The facial action coding system (FACS) was used to examine recognition rates in 105 healthy young men and women who viewed 128 facial expressions of posed and evoked happy, sad, angry and fearful emotions in color photographs balanced for gender and ethnicity of poser. Categorical analyses determined the specificity of individual action units for each emotion. Relationships between recognition rates for different emotions and action units were evaluated using a logistic regression model. Each emotion could be identified by a group of action units, characteristic to the emotion and distinct from other emotions. Characteristic happy expressions comprised raised inner eyebrows, tightened lower eyelid, raised cheeks, upper lip raised and lip corners turned upward. Recognition of happy faces was associated with raised cheek, lid tightening and raised outer brow. Characteristic sad expressions comprised furrowed eyebrow, opened mouth with upper lip being raised, lip corners stretched and turned down, and chin pulled up. Only lower brow and raised cheek were associated with sad recognition. Characteristic anger expressions comprised lowered eyebrows, eyes wide open with tightened lower lid, lips exposing teeth and stretched lip corners. Recognition of angry faces was associated with lowered eyebrows, raised upper lids and lower lip depression. Characteristic fear expressions comprised eyes wide open, furrowed and raised eyebrows and stretched mouth. Recognition of fearful faces was most highly associated with raised upper lip and nostril dilation, although both occurred infrequently, and with raised inner brow and widened eyes. Comparisons are made with previous studies that used different facial stimuli. D 2004 Elsevier Ireland Ltd. All rights reserved. Keywords: Action unit; Facial emotion expression; Emotion recognition 1. Introduction * Corresponding author. Tel.: +1 215 614 0161; fax: +1 215 662 7903. E-mail address: kohler@bbl.med.upenn.edu (C.G. Kohler). Facial expressions are used in humans and animals for communication, in particular to convey one’s emotional state (Darwin, 1965). This communication can be reflexive, as situations may evoke emotions 0165-1781/$ - see front matter D 2004 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.psychres.2004.07.003 236 C.G. Kohler et al. / Psychiatry Research 128 (2004) 235–244 that are spontaneously expressed on the face. In other instances, particularly in humans, facial expressions may be volitional signals intended for communication and may not reflect the true emotional state of the person (Ekman and Friesen, 1975). Impairment in emotional processing, specifically emotion recognition, has been described in psychiatric disorders including schizophrenia, depression and bipolar disorder, and in neurological disorders (review: Kohler et al., 2004). Since the earliest descriptions of schizophrenia, decreased and muted facial expressions of emotions have been reported as a hallmark of the illness; however, there have been few attempts to investigate this impairment further in schizophrenia and other psychiatric disorders. Six basic emotions—happiness, sadness, anger, fear, disgust and surprise—and their corresponding facial expressions are recognized across different cultures (Huber, 1931; Eibl-Eibesfeldt, 1970; Izard, 1971; Ekman and Friesen, 1975). Descriptions have been made about which facial muscles are involved in the formation of each of the basic emotions (Huber, 1931; Plutchik, 1962; Ekman and Friesen, 1975; Gosselin et al., 1997). For happy expressions, Ekman and Friesen (1975) described facial expressions of tense lower eyelids, raised cheeks and lip corners pulled up; for sad expressions, inner eyebrows raised and drawn together, and lip corners pulled down; for anger expressions, lowered eyebrows drawn together, tense lower eyelids, pressed lips or lips parted in a square shape; for fear expressions, eyebrows raised and drawn together, wide open eyes with tense lower eyelids and stretched lips. Based on facial muscle movement, Ekman and Friesen (1978) developed the Facial Action Coding System (FACS) by identifying the presence of specific actions of facial muscles called Action Units (AUs). Gosselin et al. (1997) tested Ekman and Friesen’s predictions about facial expressions of six emotions in two conditions—posed or unfelt and evoked or felt. In that study, actors used two different methods of displaying facial expressions of six emotions—trying to experience the target emotion according to the Stanislawski technique, while expressing the emotion (evoked emotion) or merely displaying the emotion without the emotional experience (posed emotion). FACS analyses of facial expressions by a single rater revealed that AUs for each emotion were concordant with Ekman and Friesen’s descriptions. Occurrence rates of AUs for evoked and posed facial expressions showed considerable overlap, in particular for happy and surprise expressions. Other studies that investigated facial landmark changes associated with emotional expression focused on measurement of muscle activity with electromyography (EMG). Limitations of this methodology include that only select muscle groups, such as corrugator supercilii orbicularis oculi and zygomaticus major have been measured, showing the corrugator to be associated with sad and the zygomaticus with happy emotions (Schwartz et al., 1976). Tassinary and Cacioppo (1989) elucidated that expressions of action units involving brow and cheek regions are associated with discrete facial muscle activity as measured by surface EMG. More recently, considerable overlap has been shown between surface and intramuscular recordings of facial EMG during happy, sad and angry expressions (Aniss and Sachdev, 1996). In our study, three certified FACS raters examined 128 images of extremely happy, sad, angry and fearful faces that were selected for use in a functional imaging study and piloted for recognition in a group of healthy subjects. Disgust was not included because of our assumption that it may not present a pure emotion, but rather a mixture of other universal emotions (Kohler et al., 2003). Surprise was not included because its valence depends entirely on the triggering event and it can therefore be any of the other emotions, with a rapid onset. The purpose of our study was to investigate which facial changes are most frequent in happy, sad, angry and fearful expressions, and which facial changes are essential for accurate recognition of the particular emotion. The study included the following specific aims: (1) Which action units characterize the different emotions? We hypothesized that each emotion can be defined by the presence of action units common to faces with the particular emotion. (2) Which action units distinguish different emotions from each other? We hypothesized that facial expressions of each emotion consist of unique action units that are distinct from other emotions. (3) How do posed and evoked emotions differ with respect to action units? We hypothesized that different action units are used for the expression of posed and evoked emotions. (4) Do men and women utilize different action units for the expression C.G. Kohler et al. / Psychiatry Research 128 (2004) 235–244 of emotions? We hypothesized that certain emotions, in particular anger, are expressed differently by men and women. (5) Which action units are associated with recognition of each emotion? We hypothesized that the presence of characteristic action units is associated with proper detection of the particular emotion. We propose that findings based on accurate descriptions of facial muscle groups in people without psychiatric disorders will facilitate investigations into the effects of psychiatric illness on facial emotion expression in persons with psychiatric disorders. This knowledge will lead to better understanding of how interpersonal nonverbal communication is affected in psychiatric disorders. In particular, this will give us information about whether disorders, such as schizophrenia or affective disorders, are associated with muted, but appropriate facial muscle movement or recruitment of different muscle groups. 2. Methods 2.1. Task construction Color slide photographs which were acquired during a study of facial displays of emotion (Gur et al., 2002a) and which totaled over 5000 pictures, were digitally scanned. They were then processed in PhotoShopn to remove background features and reduce distinguishing hair and clothing cues. Evoked and posed images from eight male and eight female actors were selected for each emotion (Happy, Sad, Anger, and Fear). Based on our finding that disgust expressions, in particular of extreme intensity, were poorly recognized (Kohler et al., 2003), we decided to limit the current task to the universal emotions of happiness, sadness, anger, and fear. Only extreme intensity images and only faces with opened eyes that were unaffected by spontaneous eye blinks were used in this study. Faces used in our study were screened by a group of raters (n=11), and only faces that were correctly identified by N55% (6/11) of raters were included in this task. Each actor (n=64) was assigned to one emotion and photographed in both posed and evoked expressions. Assignments were balanced for gender, age, and race (Caucasian versus non-Caucasian). A total of 128 images of emotional expressions 237 (32 per emotion) were used in the emotion identification tasks. There was no planned overlap in the stimuli used in the present study and recent studies (Gur et al., 2002b,c; Kohler et al., 2003, 2004) that employed stimuli from the archival set of over 5000 pictures. The facial stimuli in this project were piloted for a functional magnetic resonance imaging (fMRI) study of emotion recognition and face memory. 2.2. Emotion recognition testing Healthy control subjects were recruited from undergraduate introductory psychology courses at Drexel University in Philadelphia. Testing sessions were conducted in a closed on-campus computer laboratory over a 1-week period. Participants completed a brief screening form that included demographic and health-related questions. The sample consisted of 63 men (meanFS.D. age=19.7F1.63 years) and 42 women (meanFS.D. age=19.9F2.88 years) who met inclusion criteria (Erwin et al., 1992). There were 71 Caucasian, 9 African-American, 4 Hispanic/Latino, and 21 Asian-American participants. Subjects were asked to press one button if the face displayed the target emotion, another button if the face shown was neutral or displayed a different emotion. Percentages of subjects making correct identifications were used to generate recognition rates for each image. 2.3. Facial action coding system ratings (FACS) Images used in the emotion recognition test (Section 2.2) were presented via digital video projection to three certified FACS raters in pseudorandom order. To serve as a baseline comparison, neutral images were presented next to emotional images of the same person. FACS scoring was performed independently by each rater. For purposes of this study, we were interested in the presence rather than the intensity of AUs, and intensity ratings were not included in the analysis. Laterality was collapsed so that if an AU was scored for one side; it was qualified on both. Ratings were transformed to binomial data, with the presence of an AU being recorded with 1, absence with 0. According to the agreement of at least two raters, an AU was rated as present or absent. The number of occurrences for each 238 C.G. Kohler et al. / Psychiatry Research 128 (2004) 235–244 AU was calculated for each image, grouped by emotion and only AUs that occurred in at least 10% of the images in a particular emotion were included for further analysis. AUs occurring in at least 25% of the images in an emotion were considered to be characteristic of the expression. 2.4. Data analysis Fisher’s Exact tests were performed to determine specificity of AUs, defined as uniquely present or absent, for each emotion and to explore differences in gender and condition (posed and evoked). To understand interactions between emotions and cluster effects of AUs within emotions, co-occurrence rates were calculated for all AU pairs with the following formula: CoR of AU x with y=(# mutual occurrences of AU x and y)/(# occurrences AU x)+(# occurrences AU y). On the basis of the emotion recognition testing from the 105 Drexel students, multivariable logistic regression analyses with backward elimination were performed to determine the impact of action units on the odds of accurate identification, broken down by evoked and posed conditions. The logistic regression was fit using generalized estimating equations (GEE) with an exchangeable correlation structure, in order to account for the non-independence or clustering of the multiple faces assessed by each student. The results are expressed as odds ratios for comparing odds of correct recognition when the AU was present vs. absent. To further examine the effect of characteristic AUs on accurate recognition of Sad, Angry and Fearful faces, odds ratios (ORs) were calculated for recognition faces lacking one, two or three characteristic AUs for the respective emotion. For Happy faces, this analysis could only be performed for recognition of faces lacking one or two characteristic action units. 3. Results 3.1. Characterization of emotional expressions FACS ratings revealed separate profiles for Happy, Sad, Anger and Fear expressions (Fig. 1, Table 1). Characteristic, uniquely absent and present AUs were found for each emotion. Expressions of Anger and Sad shared the most characteristic AUs (5), while Fear and Happy shared the fewest (2). Characteristic AUs for Happy included in descending order of frequency 12, 7, 26, 6, 10, 1 and 25. AUs 6 and 12 were uniquely present, while AUs 4 and 20 were uniquely absent in Happy expressions. Characteristic AUs for Sad included 4, 7, 20, 10, 17, 25, 1 and 15. AU 17 was unique for Sad expressions while AU 26 was specifically absent. Characteristic AUs for Anger Fig. 1. Facial expressions of emotion. C.G. Kohler et al. / Psychiatry Research 128 (2004) 235–244 Table 1 FACS of emotions (number present of 32 faces per category) AU Name Fisher’s Exacta Happy Sad Anger Fear 1 2 4 5 6 7 9 10 12 15 16 17 20 23 24 25 26 27 38 Pb0.001 Pb0.001 Pb0.001 Pb0.001 Pb0.001 Pb0.001 P=0.001 P=0.038 Pb0.001 P=0.050 Pb0.001 Pb0.001 n.s. n.s. n.s. n.s. Pb0.001 n.s. P=0.006 9 7 2** 2 20* 23 2 17 32* 0 1 0 4** 0 0 8 23 0 0 1** 1 26 12 2 20 9* 17 1 6 16* 4 11 5 3 13 9 1 0 Inner Brow Raiser Outer Brow Raiser Brow Lower Upper Lid Raiser Cheek Raiser Lid Tightener Nose Wrinkler Upper Lip Raiser Lip Corner Puller Lip Corner Depressor Lower Lip Depressor Chin Raiser Lip Stretcher Lip Tightener Lip Pressor Lips Part Jaw Drop Mouth Stretch Nostril Dilator 10 0 24 1 3 21 0 14 3 8 0 12* 15 1 3 12 4** 0 0 18 13* 14 28 0 6** 0 4** 2 1 0 1 9 0 0 3 23 5 6* n.s.= not significant. a df=3; all P values after Bonferroni correction. * Unique qualifying AU. ** Unique disqualifying AU. included AUs 4, 7, 10, 16, 25, 5, 20, 9 and 26. AUs 9 and 16 were uniquely present in Anger, while AU 1 was uniquely absent. Characteristic AUs for Fear included AUs 5, 26, 1, 4, 2 and 20. AUs 5 and 2 were uniquely present, while AUs 7 and 10 were uniquely absent in Fear. 3.2. Co-occurrence of action units AUs occurring together more than 75% of the time were considered to be clustered. In Happy, we found a clustering of AU 1 with 2 (88%), and AU 12 with 6 (77%), AU 7 (84%) and 26 (84%); in Sad, AU 4 with 7 (76%) and 20 (77%); in Anger, AU 4 with 7 (78%); in Fear, AU 1 with 2 (77%), and AU 26 with 5 (78%). 3.3. Condition of expression Effects of condition—evoked or posed—were only significant in expressions of Anger. AU 16 (Fisher’s Exact=8.00, df=1, P=0.012) and AU 20 (Fisher’s Exact=11.22, df=1, P=0.002) were more frequent in 239 evoked than posed expressions. After correction for multiple comparisons, the finding for AU 20 remained significant. 3.4. Gender of face No significant differences between male and female posers were found for expressions of Happy, Sad, Anger and Fear. 3.5. Recognition of emotions Recognition rates for Happy faces were 91.2%, for Sad faces 84.0%F10.6 (S.D.), for Anger faces 68.9%F24.3 (S.D.) and for Fear faces 67.9%F22.6 (S.D.). These rates are similar to recognition rates in our previous publications, which employed different faces from the same archival set of pictures and different testing paradigms (Kohler et al., 2003, 2004). 3.6. Effect of condition on recognition of emotions Recognition rates were similar for posed and evoked expressions of Happy faces. Recognition rates for Sad faces were 82.4% in the posed condition and 85.6% in the evoked condition (OR=0.79, P=0.01). For example, this means that posed sad faces were less likely—specifically 0.79 times as likely to be correctly identified, when compared with evoked sad faces. Recognition rates for Angry faces were 65.6% in the posed and 72.2% in the evoked condition (OR=0.74, Pb0.001). Recognition rates for Fearful faces were 61.7% in the posed and 74.2% in the evoked condition (OR=0.56, Pb0.001). 3.7. Relationship between recognition of emotion and presence of AUs The relationship between emotion recognition and presence of AUs was assessed using multivariable GEE logistic regression models, adjusting for the multiple faces assessed by each rater. Happy: Since AU 12 was always present, no correlation could be calculated. Of the remaining characteristic AUs, the presence of 6, 7, and 26 was positively associated with happy recognition. The OR of 4.27 for AU 6 being present means that correct identification of happy faces is more than four times greater when AU 240 C.G. Kohler et al. / Psychiatry Research 128 (2004) 235–244 6 is present than when AU 6 is absent. Of the noncharacteristic AUs, the presence of AU 2 was positively and AU 20 was negatively associated with happy recognition. Sad: Of the characteristic AUs, 4, 17 and 25 were positively associated; AUs 1, 7, 10 and 20 were not correlated and AU 15 was negatively associated with sad recognition. Anger: Of the characteristic AUs, 4, 5 and 16 were positively associated; AUs 7, 9, 10, 20, 25, and 26 were not associated with anger recognition. Of the non-characteristic AUs, AUs 15 and 24 were pos- itively, while the presence of AU 23 was negatively associated with anger recognition. Anger was better recognized in the posed than in the evoked condition. Fear: Of the characteristic AUs, 5, 1 and 26 were positively associated, AUs 2 and 20 were not associated, and AU 4 was negatively associated with fear recognition. Of the non-characteristic AUs, AU 10 and 38 were positively associated with fear recognition. Fear was less often recognized in the posed (OR=0.56, Pb0.001) than in the evoked condition. The presence of AUs and significant ORs are described in Table 2. Table 2 Presence of action units and correct emotion recognition AU Happy cAU OR, 95% Sad cAU OR, 95% Anger cAU OR, 95% Fear cAU OR, 95% 1 ! n.s. CI 4 5 2.37, 1.65–3.40 ! n.s. CI ! 1.88, 1.50–2.36 CI ! 7.27, 5.10–10.38 ! 1.81, 1.48–2.22 CI AU Happy cAU OR, 95% Sad cAU OR, 95% Anger cAU OR, 95% Fear cAU OR, 95% 2 ! 3.01, 2.54–3.58 ! n.s. ! 0.65, 0.55–0.77 ! 3.48, 2.45–4.95 16 17 20 23 ! 1.41, 1.11–1.80 CI ! 4.27, 2.92–6.24 ! 3.81, 2.93–4.95 ! n.s. 10 12 ! 2.34, 1.81–3.04 ! n.s. ! n.a. ! n.s. ! n.s. ! n.s. 9 ! n.s. 15 ! 0.60, 0.48–0.75 ! n.s. 2.18, 1.64–2.89 4.43, 3.01–6.52 24 ! n.s. ! n.s. CI 7 0.57, 0.43–0.78 CI CI 6 25 26 ! n.s. ! 1.93, 1.41–2.65 27 38 ! 1.38, 1.09–1.75 0.67, 0.55–0.82 3.03, 2.26–4.06 ! n.s. ! n.s. ! 1.51, 1.31–1.74 1.61, 1.38–1.89 cAU=characteristic action unit. OR=odds ratios for recognition, when AU present (all P-values b0.001, except for AU25 in Sad: P=0.007). n.a.=not applicable, could not be calculated. n.s.=not significant OR for recognition when characteristic AU present. C.G. Kohler et al. / Psychiatry Research 128 (2004) 235–244 Table 3 Recognition rates and odds ratios for emotional faces without characteristic action units (cAU)* Happy Sad Anger Fear cAU No cAUs present (%/OR) 1 cAU present (%/OR) 2 cAUs present (%/OR) 3 cAUs present (%/OR) 12,6,7 4,17,25 4,5,16 1,5,26 n.a./– 68.7/– 24.8/– 32.0/– 71.3/– 84.0/2.38 60.7/4.72 54.3/2.45 90.5/3.76 86.6/2.89 77.5/10.47 65.0/3.83 95.2/7.79 90.2/4.16 85.9/18.42 80.4/8.37 n.a. since AU 12 is always present. OR=odds ratio for recognition of faces with one, two or three characteristic AU present for the specific emotion when compared to faces without these characteristic AU (Sad, Anger and Fear) and one characteristic AU present (Happy). * Limited to cAU with positive correlations with recognition. 3.8. Relationship between recognition of emotion and absence of characteristic AUs In an effort to examine the recognizability of emotional faces lacking key components—or characteristic AUs—for the specific emotion, we present odds ratios for recognition of Sad, Angry and Fear faces with none, one, two or three of the characteristic AU present that are associated with recognition (Section 3.6) (Table 3). In Happy faces, AU 12 was always present and the effect of its absence on recognition of Happy could not be examined. 4. Discussion This study examined the presence of action units (AUs) in four universal emotions, how these AUs differ according to gender of poser and condition, and the relationship between presence or absence of AUs and recognition of the expressed emotion. In Happy faces, we found characteristic expressions to consist of raised inner eyebrows, tightened lower eyelid, raised cheeks, upper lip raised and lip corners turned upward. Recognition of Happy faces was associated with characteristic AUs, such as cheek raised and lid tightening, and, although infrequently present, with outer brow raised. Since lip corner pull was present in all faces and lip stretch was negatively was associated with recognition, we conclude that the former is essential for the facial expression of happiness. 241 In Sad faces, we found characteristic expressions to consist of furrowed eyebrows, opened mouth with upper lip being raised, lip corners stretched and turned down, and pulled up chin. Of eight characteristic AUs for Sad, only brow lower and chin raised was associated with recognition, but these correlations were much lower than what was found for other emotions. It appears that most of the frequent AUs in Sad were common to other emotions as well and did not contribute to its recognition. In addition, lip corner depression, which because of findings by Ekman and Gosselin was thought to be essential to Sad, was present in only 25% of Sad faces and was associated negatively with recognition. In our set of faces, it appears that recognition of Sad is less dependent on the presence of single AUs, but on the combination of AUs or the bGestaltQ of facial expression. In Anger faces, we found characteristic expressions to consist of furrowed—or lowered—eyebrows, eyes wide open with tightened lower lid, raised upper and turned lower lips exposing teeth, and stretched lip corners. Recognition of Anger faces was associated with only three of nine characteristic or frequent AUs—brow lower, lower lip depression and upper lid raised—but with three non-characteristic AUs. Although infrequent in Anger faces, lips being pressed together (9%) and lip corners turned down (19%) was associated positively with recognition, whereas tightened lips (16%) impeded recognition. In Fear faces, we found characteristic expressions to consist of eyes wide open with furrowed and raised eyebrows and stretched mouth. Recognition of Fear faces was associated most highly with upper lip raised (13%) and to a lesser extent with nostril dilation (19%), both of which occurred infrequently in Fear faces. Of the characteristic AUs, fear recognition was associated with inner—but not outer—brow being raised and widened eyes and was impeded by brow lower, a frequent AU (43%) in Fear. In addition, we found in every emotion, except Anger, opening of the mouth, as represented by lips parted or jaw dropped, to correlate with improved recognition. Examining recognition of faces lacking one, two or three characteristic AUs that are associated with recognition of the specific emotion, we found Happy and Sad faces to be well recognized with none or only one of the characteristic AUs being present. This was 242 C.G. Kohler et al. / Psychiatry Research 128 (2004) 235–244 different for Anger and Fear faces, which were poorly recognized when no characteristic AUs were present; however, recognition improved markedly with the presence of just one or two characteristic AUs. In comparison with previous studies (Table 4), there was considerable agreement about the presence of AUs in each emotion as predicted by Ekman and Friesen (1978, 1982) and as determined experimentally by Gosselin et al. (1997) and the present study. Among the three groups, there is unanimous agreement for the presence of cheek raise and lip corner pull in Happy; eyebrow lower and lip corner depressed in Sad; eyes wide open, eyebrow lower and mouth open in both Anger and Fear expressions. Differences among the studies regarding which AUs were found to be characteristic may be due to different methodologies in how facial expressions were obtained. In Gosselin’s study, actors were presented with scenarios meant to evoke felt emotions, while in our study actors chose personal events. The unfelt condition in Gosselin’s study used scenarios as well; in our posed condition, actors were simply Table 4 Comparison of characteristic action units from three studies AU Happy E 1 2 4 5 6 7 9 10 11 12 15 16 17 20 23 24 25 26 27 * G * Sad K E * * X * ** * * Anger G K E G * *F * * * *F * * * * * * * Fear K E X * * * * * * * ** * G K * * * ** * * *F X X * * * ** * *U * * ** * X *U * * * * * * * X * * * * * *F *U *F ** * * *F *F * * * * * * * * E=predictions by Ekman and Friesen (1978, 1982). G=findings by Gosselin et al. (1997) (N10% occurrence). K=findings by Kohler et al. *=frequently present AU. **=unique qualifying AU. X=unique disqualifying AU. F=felt (evoked) condition. U=unfelt (posed) condition. instructed to convey a target emotion with their face. Lastly, whereas Gosselin’s study used videotaped acquisition, our study used still photos. With respect to evoked versus posed conditions, we were surprised to only find differences for anger, where lip stretch was more common in the evoked state. This finding is consistent with few differences between felt and unfelt encoding conditions reported in the Gosselin study and indicates that better recognition of evoked Sad, Anger and Fear expressions result from differences in intensities of expression. Unexpectedly, differences for gender were limited to mouth open being more commonly in male sad faces. Overall, these findings offer support that possible condition and gender related differences in the expression of emotions are not based on qualitatively different facial expressions. Such differences, if present, may be related to quantitative differences, i.e. differences in intensities in facial expressions, which were not investigated in our study. An argument can be made that visual inspection of action units has limited sensitivity to detect small and fleeting facial changes and certainly microexpressions, which are defined as emotion specific muscle patterns in the absence of overt expression (Tassinary and Cacioppo, 1992). In our study, all expressions were of extreme intensity to minimize below threshold activation of action units and ambiguous expressions. In addition, all expressions were judged to represent the intended target expression during the acquisition phase (Gur et al., 2002a,b,c) and selected as a representative expression upon construction of the fMRI task. Another potential limitation is that photos capture emotional expressions at a fixed point in time and the possibility that the most valent expression or the sequence of facial changes essential for the expression of a particular emotion were not obtained. The photographic stimuli used were carefully assembled from an archive of over 150 people and over 5000 pictures that underwent standardized procedures for expression of emotion, and images with closed eyes or marked head tilt were not included. In the present study, we did not compare intensity ratings and laterality ratings. Our investigation examined whether facial changes were present, rather than the degree of presence or the presence on one side of the face. Previous research has shown posed and C.G. Kohler et al. / Psychiatry Research 128 (2004) 235–244 deliberate emotions to include more asymmetric muscle activity than evoked emotions (Ekman et al., 1981, 1982) and the left side of the face to be more expressive (Sackeim et al., 1978; Indersmitten and Gur, 2003). Since we examined facial expressions of extreme emotional intensity, we did not explore the effect of intensity of emotional experience on facial expression. Future directions to evaluate facial expression of emotions based on FACS in healthy persons and persons with psychiatric disorders may explore issues of data acquisition, selection of stimuli and methods of facial ratings. Data acquisition with facial EMG using multiple electrodes may yield more comprehensive and accurate findings regarding facial movements, in particular with respect to subtle movements, chronological sequence and facial laterality of action units. Laterality of facial expressions of different intensity emotions and their effect on recognition can be investigated by assembling right-right and left-left composite faces. A potential limitation of assembling composite faces is based in the natural asymmetry of faces and the need for accurate three-planar alignment of the images, which, if not performed correctly, can produce odd and unnatural looking composites. Since FACS represents a laborious and inexact method to measure facial changes, attempts have been made to create automated programs that measure facial muscle movements. Cohn et al. (1999) and Bartlett et al. (1999) reported on isolated and simple combinations of posed facial action units, but this analysis has not been applied to emotional faces. These methodologies provide qualitative AU-based analyses during the course of an expression; however, they are unable to further quantify a change in facial expression. Quantification of fine-grained structural—or pointwise—changes in the face, employing advanced morphometric tools, is needed to capture the subtlety of human expression. To pursue this aim, we have developed a novel methodology for quantitative analysis of facial expressions, which is capable of measuring expansions and contractions of select facial regions and their boundaries (Verma et al., in press). In psychiatric disorders, qualitative and quantitative impairment of facial expression of emotions have received limited attention, while a large body of literature exists on emotion recognition deficits, 243 particularly in schizophrenia. In schizophrenia but not affective illness, impaired facial expressions of emotions constitute characteristic symptoms of the illness. It remains to be investigated whether persons with psychiatric illness, such as schizophrenia or affective disorders, display muted facial expressions of emotions or recruit facial muscle movements which in people without mental illness are not particular to the expression of the target emotion. While the former will be associated with lack of recognition of the expressed emotion, the latter will lead to misidentification or misattribution of another emotion with pronounced effects on non-verbal communication. Acknowledgments This work was supported by NIMH MH01839 and MH43880. 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