استاتیک مطرح شده و حالات برانگیخته صورت از احساسات در اسکیزوفرنی

Abstract Objective Impaired facial expressions of emotions have been described as characteristic symptoms of schizophrenia. Differences regarding individual facial muscle changes associated with specific emotions in posed and evoked expressions remain unclear. This study examined static facial expressions of emotions for evidence of flattened and inappropriate affect in persons with stable schizophrenia. Methods 12 persons with stable schizophrenia and matched healthy controls underwent a standardized procedure for posed and evoked facial expressions of five universal emotions, including happy, sad, anger, fear, and disgust expressions, at three intensity levels. Subjects completed self-ratings of their emotion experience. Certified raters coded images of facial expressions for presence of action units (AUs) according to the Facial Action Coding System. Logistic regression analyses were used to examine differences in the presence of AUs and emotion experience ratings by diagnosis, condition and intensity of expression.

. Introduction Facial expressions are shared in humans and animals, and are central for communication both within and across species (Darwin, 1872). Abnormal expressions of emotions have been described as characteristic symptoms of schizophrenia (Andreasen, 1984a and Bleuler, 1911) and may precede the onset of illness by many years (Walker et al., 1993). Affective flattening and other negative symptoms are present at onset of illness (Gelber et al., 2004 and Shtasel et al., 1992) more common in males, increase with illness duration (Shtasel et al., 1992) and appear distinct from depression (Kohler et al., 1998). In contrast to positive symptoms of schizophrenia, negative symptoms may not respond as well to antipsychotics and have been linked to impairment in psychosocial functioning (Edwards et al., 1999 and Ho et al., 1998). Whereas there are widely used and validated instruments that measure and parse aspects of cognitive dysfunction and its neurobiology in schizophrenia, clinical assessments of affective flattening and other negative symptoms have been limited to observer based rating scales. The ability to quantify emotional expression, especially in the face, has been enhanced by work aimed at measuring unique features of universal emotions. Six universal emotions are recognized across cultures in facial expressions — happiness, sadness, anger, fear, disgust and surprise (Eibl-Eibesfeldt, 1970, Ekman and Friesen, 1975 and Izard, 1994). Based on facial muscle movement, Ekman and Friesen (1978) developed the Facial Action Coding System (FACS), which identifies discrete facial muscle movements, called Action Units (AUs). FACS has been simplified and adapted for clinical research. Emotion FACS (EMFACS: Friesen, 1986) identifies AUs associated with the predicted expression of the particular emotion, and the Facial Expression Coding System (FACES: Kring et al., 1993 and Kring and Sloan, 2007), which rates overall dynamic facial changes, according to number of expressions, intensity and duration. Examinations of facial expressions beyond clinical rating scales in schizophrenia have reported on imitative expressions (Putnam and Kring, 2007, Schwartz et al., 2006 and Tremeau et al., 2005), deliberate or posed expressions (Berenbaum, 1992, Schwartz et al., 2006 and Tremeau et al., 2005), spontaneous expressions within dyadic interactions (Aghevli et al., 2003, Mattes et al., 1995, Schneider et al., 1990 and Steimer-Krause et al., 1990), expressions associated with emotional film clips ((Berenbaum and Oltmanns, 1992, Earnst et al., 1996, Kring et al., 1999 and Kring et al., 1993) or emotional experiences of the participants (Berenbaum and Oltmanns, 1992, Gottheil et al., 1970, Kring et al., 1993 and Tremeau et al., 2005). Media for capturing facial expressions have included still photographs (Gottheil et al., 1976 and Schwartz et al., 2006), videotapes (Aghevli et al., 2003, Berenbaum, 1992, Berenbaum and Oltmanns, 1992, Gaebel and Wolwer, 2004, Kring et al., 1993, Putnam and Kring, 2007, Steimer-Krause et al., 1990 and Tremeau et al., 2005), and electromyographic recordings (Earnst et al., 1996, Kring et al., 1999 and Mattes et al., 1995). Videotaped acquisition offers the advantage of capturing duration and frequency of emotion expressions. However, analyses of such lengthy data sets have been limited to global assessment of positive and negative emotion expressions, rather than changes in specific face regions. Other measurements of emotion expressions have included recognition rates of expressions (Gottheil et al., 1970, Gottheil et al., 1976, Putnam and Kring, 2007, Schneider et al., 1990 and Schwartz et al., 2006) and FACS derived measures without analysis of specific AUs (Aghevli et al., 2003, Berenbaum, 1992, Berenbaum and Oltmanns, 1992, Gaebel and Wolwer, 2004, Kring et al., 1993 and Tremeau et al., 2005). In addition, automated methods have included computerized face morphometry (Mattes et al., 1995 and Schneider et al., 1990) and electromyographic measurements (Earnst et al., 1996, Kring et al., 1999 and Mattes et al., 1995) that can measure minute muscle activations, albeit limited to select face regions. Most studies have supported affective flattening in general, rather than inappropriate affect. Studies that examined specific emotions reported on selective impairment in happy (Gottheil et al., 1976), sad(Putnam and Kring, 2007), angry (Gottheil et al., 1970 and Schwartz et al., 2006) and disgusted (Schwartz et al., 2006) expressions. Laterality differences of emotional expressions have not been reported, although acuity of illness may be associated with differential impairment in upper versus lower face expressions (Gaebel and Wolwer, 2004, Mattes et al., 1995 and Schneider et al., 1990). While affective flattening is considered characteristic of schizophrenia, comparisons with psychiatric (Berenbaum, 1992, Gaebel and Wolwer, 2004, Schneider et al., 1990 and Tremeau et al., 2005) and medical (Steimer-Krause et al., 1990) control groups have raised questions regarding specificity. Antipsychotics, particularly first-generation, are associated with extrapyramidal symptoms, but their influence on emotion expression remains unclear. Some studies indicated an adverse effect of medications on facial expression (Gaebel and Wolwer, 2004 and Schneider et al., 1992). Others (Earnst et al., 1996, Putnam and Kring, 2007 and Tremeau et al., 2005) examined patients both on and off antipsychotics and found no clear effect on expressivity. Previously, we investigated AUs in high intensity evoked expressions of universal emotions expressed by actors and determined AUs, which were essential for accurate recognition and increased recognition, when present in combinations (Kohler et al., 2004). The aim of the present study was to extend previous investigations on evidence of impaired affect in schizophrenia and to examine individual muscle movements in static facial expressions of emotions in persons with stable symptoms. We expected persons with schizophrenia to produce emotion expressions which include fewer AUs that are frequently present in expressions of controls and more AU that are infrequently present in controls. Matched groups of persons with stable schizophrenia and healthy controls underwent a standardized procedure of eliciting posed and evoked facial expressions of five universal emotions. We applied FACS to examine facial changes based on the presence of AUs within each emotion and condition, i.e. posed and evoked. Stratified by emotion, we examined the sum of frequent and infrequent AUs, combinations of frequent AUs, and differences in the presence of individual AUs. We expected different results for posed compared to evoked emotional expressions, as the former are regulated by cortical systems and are under greater volitional and cognitive control (Rinn, 1991). Specifically, we anticipated that impaired emotional expression in schizophrenia is more pronounced for evoked, rather than posed expressions.

. Conclusions Impaired facial expressions of emotions represent characteristic negative symptoms in schizophrenia and directly affect interpersonal engagement and social functioning. Previous clinical studies have characterized the enduring and pervasive nature of affective flattening in schizophrenia. Experimental studies have underscored these findings and expanded on this body of knowledge by examination of affective flattening in different conditions and in comparison with other patient groups. In the present study, involving persons with stable schizophrenia and case matched healthy controls, we applied ratings of specific facial changes associated with posed and evoked expressions of five universal emotions. Overall patterns of facial expressions of emotions were similar between patient and control groups in all emotions and, for each emotion, expression at higher intensities produced increased number of AUs in patient and control groups without differential findings. Differences in expression of AUs between groups support observations of altered facial expression of emotions in schizophrenia. Expressions of emotions usually result from activation of multiple AUs and for all emotions, except sadness, patients displayed fewer expressions with combinations of at least two frequent AUs. Most experimental studies in schizophrenia have supported affective flattening, rather than inappropriate affect, and experimental ratings of affective flattening in dynamic expressions correlated with clinical scales (Berenbaum, 1992, Putnam and Kring, 2007 and Tremeau et al., 2005). In our study, experimental measures of affective flattening based on the presence of frequent AUs failed to correlate with clinical ratings affective flattening. While this lack of finding was unexpected, it may relate to the research methodology of examining static, rather than dynamic, expressions and omission of intensity ratings from data analysis. Our prediction regarding inappropriate expressions was confirmed and in each emotion infrequent AUs were more commonly expressed in the schizophrenia group. In addition, experimental measures of inappropriate affect in happy, sad and fearful expressions correlated with clinical ratings in patients. The presence of even a single potentially erroneous AU in a particular emotion expression should not be underestimated. Whereas affective flattening may result in lack of recognition of the emotion expressed and misinterpretation as neutral or no emotion, inappropriate affect will result in misinterpretation of the emotional valence. Our prediction regarding a more selective impairment in evoked expressions was limited to happy expressions. The prediction could not be confirmed in the negative emotions tested, in particular disgust, where some frequent AUs were less common in posed expressions in the patient group. In happy expressions, patients commonly displayed upward turned lip corners, as the most common and characteristic feature of a smile. Other elements, which constitute the Duchenne smile and are necessary for a smile to appear sincere, such as eye lids tightened and cheeks raised, were less frequent. In all negative emotion expressions, furrowed or lowered brows were clearly less common in schizophrenia. The corrugator muscle, as the muscle associated with formation of a frown or scowl, represents a major constituent in the expression of negative emotion ( Larsen et al., 2003). Different from our finding, Kring et al. (1999) reported increased corrugator muscle activity, as measured by electromyography that can measure small changes beyond visual resolution, for both positive and negative emotional stimuli in schizophrenia. Considering similar subjective emotional experience within the two groups, our findings do not clearly support the hypotheses on the unidirectional relationship between emotion experience and expression according to either Darwin or James. Perhaps, our findings are more consistent with the concept of neuromotor dysfunction put forth by Dworkin et al. (1996), however, not all muscle movements were less frequent and there were specific differences found for each emotion. Although lower than during evoked expressions, levels of emotion experience during posed emotion expressions were elevated and in line with a previous study that reported on emotion experience and autonomic activity related to coached facial expressions in actors (Levenson et al., 1990). While subjective emotional experience cannot be readily quantified, our findings are in consistent with previous reports (Berenbaum and Oltmanns, 1992, Earnst and Kring, 1999, Kring et al., 1993 and Kring and Neale, 1996) and support the notion that flat affect in schizophrenia does not indicate diminished emotional experience. Limitations of our study pertain to subject selection, methodology for acquisition of facial expressions and data analysis. The small sample size is mediated by careful matching of patient and control groups, the intensive task design and complex analysis that accounted for presence and absence of every AU. We chose controls as comparisons, since actors or coached controls would magnify the difference found amongst groups. Given the limited power of our sample size and clinical stability of patients, the major concern was that the study would fail to detect differences and this did not occur. Due to the complexity of data, previous attempts to rate dynamic facial expressions using FACS were forced to limit analysis to global assessment of emotion expressions. Therefore to determine differences in individual muscle movements, we focused on rating static facial expressions. Inherent to this methodology is the possibility that photographs may be obtained which miss the intended emotion expression, despite extensive training — on synchronizing the different aspects of image acquisition. Emotion expressions were obtained in two conditions, posed and evoked. Advantages for obtaining more spontaneous or genuine emotion expressions rather than evoked expressions were weighed – against the need to keep acquisition methods for the two series similar – and the interference of speech on emotion expressions. The sequence of expressed emotions remained fixed and we decided against a randomized sequence of emotions where happy expressions could be affected by negative emotions and sad experiences could interfere with other expressions. Lastly, comparisons between groups were based on differences in AUs that were frequently or infrequently present in healthy controls, and did not include expression intensity ratings. Intensity ratings may have produced interesting findings regarding expression differences amongst groups, but the small sample size precluded meaningful comparisons. Applying FACS to larger groups with wider range of clinical symptomatology is needed to replicate our findings and investigate the effect of illness acuity and symptom clusters on facial expressions. Other future directions involving measurement of facial muscle movements may lie in further development of automated measurement of facial expressions and therapeutic application of measuring facial expressions. Over the past 15 years, several automated programs have been created with the aim to better quantitate facial regions (Bartlett et al., 1999 and Cohn et al., 1999). Based on MRI morphometry, our group (Verma et al., 2005) developed an automated program that examines facial changes in 10 regions that relate to the anatomic areas involved in AUs, as described by FACS. Such computerized methods will be able to provide a measure of the subtle changes in facial expression, which FACS is unable to quantify and may replace visual inspection as a more reliable and sensitive measure of facial expression of emotions. While simple feedback did not enhance emotion expression (Schwartz et al., 2006), more interactive remediation programs (Frommann et al., 2003) that utilize information about individual regional differences in expression of specific emotions, based on AUs or alternate muscle movement measurement, may enable remediation of emotion expression. Lastly, in the past decade identification of prodromal states in schizophrenia has received increased attention. Affective flattening may be present well before clinical onset of schizophrenia (Walker et al., 1993), increase during the prodromal phase (Malla et al., 2002) and represent a marker of vulnerability. In conjunction with other candidates for endophenotypes, facial expressions of emotions in persons with vulnerability to schizophrenia may inform us about risk of illness and assist in future efforts at prevention or postponement of onset of schizophrenia.