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Social anxiety disorder women easily recognize fearfull, sad and happy faces: The influence of gender
Journal of Psychiatric Research 44 (2010) 535–540
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Social anxiety disorder women easily recognize fearfull, sad and happy faces: The influence of gender Kátia C. Arrais a, João Paulo Machado-de-Sousa a,b, Clarissa Trzesniak a,b, Alaor Santos Filho a,b, Maria Cecília F. Ferrari a,b, Flávia L. Osório a,b, Sonia R. Loureiro a,b, Antonio E. Nardi b,c, Luiz Alberto B. Hetem a, Antonio W. Zuardi a,b, Jaime Eduardo C. Hallak a,b, José Alexandre S. Crippa a,b,* a b c
Department of Neuroscience and Behavior of the Ribeirão Preto Medical School, University of São Paulo, Brazil INCT, Translational Medicine, CNPq, Brazil Laboratory of Panic and Respiration, Institute of Psychiatry, Federal University of Rio de Janeiro, Brazil
a r t i c l e
i n f o
Article history: Received 28 August 2009 Received in revised form 27 October 2009 Accepted 3 November 2009
Keywords: Social phobia Social anxiety disorder Gender Recognition Emotion Face
a b s t r a c t Background: It has been suggested that individuals with social anxiety disorder (SAD) are exaggeratedly concerned about approval and disapproval by others. Therefore, we assessed the recognition of facial expressions by individuals with SAD, in an attempt to overcome the limitations of previous studies. Methods: The sample was formed by 231 individuals (78 SAD patients and 153 healthy controls). All individuals were treatment naïve, aged 18–30 years and with similar socioeconomic level. Participants judged which emotion (happiness, sadness, disgust, anger, fear, and surprise) was presented in the facial expression of stimuli displayed on a computer screen. The stimuli were manipulated in order to depict different emotional intensities, with the initial image being a neutral face (0%) and, as the individual moved on across images, the expressions increased their emotional intensity until reaching the total emotion (100%). The time, accuracy, and intensity necessary to perform judgments were evaluated. Results: The groups did not show statistically significant differences in respect to the number of correct judgments or to the time necessary to respond. However, women with SAD required less emotional intensity to recognize faces displaying fear (p = 0.002), sadness (p = 0.033) and happiness (p = 0.002), with no significant differences for the other emotions or men with SAD. Conclusions: The findings suggest that women with SAD are hypersensitive to threat-related and approval-related social cues. Future studies investigating the neural basis of the impaired processing of facial emotion in SAD using functional neuroimaging would be desirable and opportune. Ó 2009 Elsevier Ltd. All rights reserved.
1. Introduction Social phobia, also known as social anxiety disorder (SAD), is characterized by the excessive fear of humiliation or embarrassment in social or performance situations. The generalized form of the disorder is frequently a chronic, disabling condition (Davidson, 1993) marked by the phobic avoidance of most interaction situations, causing social, educational, professional and personal impairment (Schneier et al., 1994; Filho et al., 2009). The 12-month and lifetime DSM-IV prevalence rate of this disorder is high, of about 7.1% and 12.1%, respectively (Kessler et al., 2005; Ruscio et al., 2008). SAD is also associated with high rates of psychiatric
* Corresponding author. Address: Departamento de Neurociências e Ciências do Comportamento, Hospital das Clínicas da Faculdade de Medicina de Ribeirão Preto – USP, Av. dos Bandeirantes, 3900, 3° andar, CEP 14025-048, Brazil. Tel./fax: +55 16 3602 2201. E-mail address: [email protected] (José Alexandre S. Crippa). 0022-3956/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.jpsychires.2009.11.003
comorbidities, the most common being depression and substance abuse, among other anxiety disorders (Filho et al., 2009). One of the major aspects of SAD is the excessive fear of negative evaluation and criticism. Cognitive theories of this anxiety disorder (Beck et al., 1985; Clark and Wells, 1995; Rapee and Heimberg, 1997; Ito et al., 2008) suggest that the patient in the feared social situation, feel negatively evaluated by others to an exaggerated unrealistic extent, expecting to be negatively evaluated and hence conjuring rejection. Thus, they tend to focus their attention toward themselves, which interferes with normal processing of external social cues. This could lead to attentional and interpretational biases in detecting social threat, resulting in hypervigilance toward negative emotions (Leber et al., 2009). The adequate social functioning is related to the capacity to extract environmental information that is relevant to social outcome (Garner et al., 2006). In this process of evaluating and responding to environmental contingencies, the processing of facial expressions represent an important source of interpersonal information about positive or negative evaluations by others.
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Among the first systematic studies about the facial expression of emotions are the old reports by Charles Darwin (1872). In his work, Darwin demonstrated the evolutional importance and communicative value of facial expressions. Research in the area has gone a long way since then, dedicating great attention, especially after the 1970s, to the relation between mental disorders and the processing of facial information and particularly emotion. Thus, authors as Beck (1976) and Eysenck (1997) arrived at the concise proposition that the impaired ability to process emotional information from faces plays an important role in the etiology and maintenance of several mental conditions. In respect to the recognition of facial emotions by people with social anxiety, recent evidence suggests that a bias exist in the facial processing abilities of these individuals in the sense of a greater accuracy for recognition of facial expressions of negative emotions and more frequent wrong judgments of faces as negative (Winton et al., 1995; Lundh and Ost, 1996; Veljaca and Rapee, 1998; Mohlman et al., 2007; Yoon and Zinbarg, 2007, 2008). Also, people with social anxiety seem to take longer to recognize facial displays of happiness (Silvia et al., 2006), at the same that they require less emotional intensity to recognize angry (Joormann and Gotlib, 2006; Leber et al., 2009), sad (Leber et al., 2009), fear (Leber et al., 2009) and disgusted expressions (Montagne et al., 2006). In contrast, Philippot and Douilliez (2005) and Campbell et al. (2009) found no evidence of biased facial emotion recognition in individuals with SAD, and Hunter et al. (2009) reported that people with social phobia have a greater accuracy in the recognition of facial expressions in general, regardless of their emotional valence. Thus, although the majority of the studies suggest that people with SAD have an impaired capacity to recognize facial expressions of emotion; the reported conflicting findings may be due to the fact that most of them included small samples ranging from 12 to 29 subjects included in the experimental group, with most of patients selected from tertiary services (Lundh and Ost, 1996; Foa et al., 2000; Pérez-López and Woody, 2001; Mogg et al., 2004; Horley et al., 2004; Coles and Heimberg, 2005; Philippot and Douilliez, 2005; Joormann and Gotlib, 2006; Montagne et al., 2006; Mohlman et al., 2007; Gilboa-Schechtman et al., 2008; Campbell et al., 2009; Garner et al., 2009). Also, those studies do not report procedures to prevent the inclusion of patients with psychiatric comorbidities and on medication (Anderson et al., 2007; Arnone et al., 2009; Kerestes et al., 2009), which might have influenced the results obtained. Moreover, another important caveat of the former studies was that most of them did not take gender into account and there is evidence suggesting that gender-related differences exist in the recognition of facial expressions (Cellerino et al., 2004). Therefore, we assessed the recognition of facial expressions of the six basic emotions (happiness, sadness, disgust, anger, fear, and surprise) by individuals with SAD, in an attempt to overcome the limitations of previous studies.
2. Method 2.1. Participants The sample consisted of 78 patients with generalized SAD (30 men and 48 women; mean age 22.33 ± 5.11 years; mean education 13.03 ± 0.97 years; 79.70% participants reported their ethnicity as Caucasian, 18.05% as African descendant, 2.26% as Asian) in the experimental group and 153 healthy volunteers (53 men and 100 women, mean age 21.43 ± 3.63 years; mean education 12.95 ± 0.94; 78.04% participants reported their ethnicity as Caucasian, 13.55% as African descendant, 8.41% as Asian) enrolled in the control group (Table 1). All the subjects were recruited from the sample of an epidemiologic survey in which 2.319 university students completed self-
Table 1 Clinical and demographic characteristics of the SAD and healthy controls groups.
Male/female Age (years) Ethnicity (%) Education (years) SPIN (±SD) BSPS (±SD) DPS current LSRDS lifetime PHQ-2 (±SD) Age of SAD onset (years)
SAD (n = 78)
Controls (n = 153)
p
30/48 22.33 (±5.11) 79.70a/18.05b/ 2.26c 13.03 (±0.97) 35.18 (±13.18) 33.36 (±12.77) 8.63 (±6.65) 13.30 (±7.34) 2.24 (±1.75) 11.17 (±4.37)
53/100 21.43 (±3.63) 78.04a/13.55b/ 8.41c 12.95 (±0.94) 17.35 (±13.35) 14.78 (±10.92) 4.92 (±6.79) 6.79 (±6.77) 1.15 (±1.31)
0.32 0.052 0.98 0.32 <0.0001* <0.0001* <0.0001* <0.0001* <0.0001*
SD, standard deviation; SPIN, Social Phobia Inventory; BSPS, Brief Social Phobia Scale; DPS, Disability Profile Scale; LSRDS, Liebowitz Self-Rated Disability Scale; PHQ-2, Reduced Version of Patient Health Questionnaire. * Significant difference (p < 0.05). a Caucasian. b African descendant. c Asian.
assessment diagnostic instruments (Osório et al., 2007; Crippa et al., 2007, 2008). Out of those, 474 were selected and ascribed to two groups: (i) 237 individuals with a probable SAD diagnosis who, screened with the reduced version of the Social Phobia Inventory (MINI-SPIN – Connor, 2001), had a score of at least six points in the three items; and (ii) 237 volunteers with similar sociodemographic characteristics who scored zero in the three items of the MINI-SPIN. Afterwards, all 474 subjects were contacted by telephone and completed the Portuguese version (Del-Ben et al., 2001) of the anxiety mode of the Structured Clinical Interview for DSM-IV, clinical version (SCID-CV – First, 1997). Following the completion of the interview, the subjects were again distributed in two groups: (i) an experimental group composed by individuals with SAD; and (ii) a control group formed by health individuals. Finally, the full version of the SCID-CV was used for diagnostic confirmation and exclusion of comordid conditions (Crippa et al., 2008). The Brief Social Phobia Scale (BSPS) was used to assess SAD severity and the SPIN to rate SAD-related physiological symptoms of fear and avoidance. The Disability Profile Scale (DPS; Schneier et al., 1994) and the Liebowitz Self-Rated Disability Scale (LSRDS; Schneier et al., 1994), instruments designed to provide clinicianand patient-rated descriptive measures of current and lifetime functional impairment related to SAD. The reduced version of the Patient Health Questionnaire (PHQ-2), a brief self-administered scale, was used to assess the frequency of depressed mood and anhedonia symptoms over the two weeks prior to evaluation (Kroenke et al., 2003). Subjects were excluded from the sample who presented other psychiatric disorders, except for previous depressive episode, since it is a frequently comorbid condition with SAD (Stein and Stein, 2008; Filho et al., 2009). Additionally, we excluded individuals in treatment with psychotropic medication or in use of psychoactive substances, and the ones who presented with a general medical condition or who had received previous treatment for SAD (either pharmacological or psychotherapy). The research protocol was approved by the local ethics committee and all volunteers gave their signed informed consent to participate. 2.2. Material 2.2.1. Facial emotion recognition task We used a computerized task built with stimuli from the series Pictures of Facial Affect (Ekman and Friesen, 1976) depicting six basic emotions – happiness, sadness, fear, disgust, anger, surprise
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– and neutral faces. The chosen pictures displayed two men and two women to avoid gender interference, and were organized in 24 blocks (4 actors 6 emotions) with gradually increasing emotional intensity (Philippot and Douilliez, 2005), ranging from 0% (neutral face) to 100% (full emotion displayed). The participant was asked to label the emotion displayed on the computer screen as soon as he could recognize it, with no time restraint. Emotional intensity was increased by pushing a button on an eight-button pad developed for the study (six emotional labels, an ‘ADVANCE’ key to increase intensity, and an ‘ENTER’ key, used to start another block). The blocks were randomized in each session and a twoblock version was used for practice before the actual trial. At the end of the experiment, a performance report was generated informing the gender (actor) of each stimulus, time spent for each stimulus, total time, emotional label provided, and actual emotion displayed in each block. All participants were tested individually.
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Fig. 1. Mean number of frames advanced by women (intensity of emotion) to respond to each emotion. *Significant difference (MANOVA; p < 0.05).
2.3. Statistical analysis Clinical and demographic data were analyzed by t-test for continuous data and by the chi-squared test for nominal data. The time spent and the number of frames advanced until judgment (equivalent to emotional intensity) were calculated for each subject and analyzed by means of multivariate analysis of variance (MANOVA). Performance in the task and the interaction between gender and group were also analyzed by MANOVA. The influence of emotional valence – positive (happy, surprised) and negative (angry, sad, fearful, disgusted) facial expressions – was assessed by means of independent t-tests for both the time spent and the emotional intensity. The chi-square test was used to analyze emotional judgment accuracy. Since previous studies have shown that depression may be related to facial recognition abnormalities, particularly sadness (Gilboa-Schechtman et al., 2008), we further compared the results of SAD patients with or without past depression by means of the tstudent test. Additionally, Pearson’s and Spearman’s correlation coefficients were used to investigate interactions between the data from the scales and the emotion recognition task depending on whether they had a normal distribution (Pearson’s) or not (Spearman’s). The statistical analyses were performed using the SPSS 13.0 (SPSS –Incorporation, 2001) and the statistical level of significance was set at p < 0.05. 3. Results No significant differences were found between patients and controls in terms of their sociodemographic profile (gender, age, educational level and socioeconomic status), which attests to the adequacy of the matching procedure between the groups (Table 1). As expected, subjects with SAD presented higher scores than Controls on the self- (SPIN) and hetero- (BSPS) assessment social anxiety symptom scales, higher current (LSRDS) and lifetime (LSRDS) functional impairment, as well as higher frequency of depressed mood and anhedonia over two weeks (PHQ-2). 3.1. Facial emotion recognition The MANOVA for the intensity required for recognition showed significant differences for interaction (F3227 = 2.139; p = 0.050), but not for group (F3227 = 1.922; p = 0.078) and gender (F3227 = 1.337; p = 0.242). Therefore, a MANOVA was separately performed for gender. Women with SAD required less emotional intensity to recognize fear (F1146 = 10.210; p = 0.002), happiness (F1146 = 10.130; p = 0.002) and sadness (F1146 = 4.611; p = 0.033) (Fig. 1), but no dif-
Fig. 2. Mean number of frames advanced by men (intensity of emotion) to respond to each emotion. *Significant difference (MANOVA; p < 0.05).
ferences were found in males (Fig. 2). There were no significant effects for group (F3227 = 1.242; p = 0.286), gender (F3227 = 0.870; p = 0.517), and interaction (F3227 = 0.839; p = 0.541) for judgment accuracy or group (F3227 = 1.306; p = 0.256), gender (F3227 = 0.468; p = 0.831), and interaction (F3227 = 0.677; p = 0.669) for time spent to perform the task. The gender of the stimulus presented in the task also did not affect performance in terms of accuracy, time, and intensity required for recognition. Additionally, no statistical differences between the groups were found when the emotions were divided in two blocks according to their valence (positive and negative facial expressions), either in the time spent or emotional intensity. There were no differences for time spent (t = 0.235; p = 0.815), accuracy (t = 0.942; p = 0.351) or emotional intensity (t = 1.210; p = 0.233) when we compared SAD patients with or without depression. No correlations were found between the variables of the facial emotion recognition task and the clinical and subjective measures of social anxiety or depression. Finally, the results have shown that the recognition of facial emotion is unaffected by the gender of the stimulus. 4. Discussion This study was designed to investigate the recognition of facial expressions of emotion in patients with SAD and healthy controls, aiming to overcome the limitations of previous studies. As far as we know, this is the first study addressing the processing of facial affect in SAD patients with a large non-clinical, treatment-naïve sample with no current comorbities. The adoption of these parameters for the composition of the sample is important because recent studies suggest that treatments such as antidepressants can significantly reduce the response of the amygdala to faces of fear
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(Murphy et al., 2009) and could cause disinhibition in people with SAD that would eventually affect their ability to interact with other people (Valença et al., 2005). The performance of the patients in terms of the total time spent to assess the emotional task was similar to that of healthy controls. However, significant differences between the two groups were found regarding the emotional intensity required for judgment, represented by the number of frames advanced. The patients required lower emotional intensity to attain the same accuracy levels found in controls for the recognition of fear, sadness and happiness, with no differences for the other emotions. This effect was unrelated to previous depression episodes or depression symptoms scores. However, in an additional analysis to check the influence of gender on the recognition, we observed that this difference was significant only for the group of women. This finding is not unusual since several studies suggest that women with other disorders such as schizophrenia also perform better on tasks of recognition of facial expressions (Scholten et al., 2005). In the vast literature on the differentiated behavior of female and male subjects, it has been proposed that in selective attention tasks, female subjects’ processing entails more detailed elaboration of information than males (Meyers-Levy and Tybout, 1989; Meyers-Levy and Maheswaran, 1991 apud Güntekin and Basßar, 2007), and female subjects are more efficient in recognizing faces and facial expressions (Thayer and Johnsen, 2000; Cellerino et al., 2004 apud Güntekin and Basßar, 2007). By taking this trend in account, we could speculate that women with SAD have exacerbated this characteristic. The negative or contrasting findings of previous studies related to recognition biases for specific emotions by men or women with SAD may be due to the small sample size in many studies, which reduces the statistical power for this type of analysis. Several studies suggest that individuals with SAD show a bias for the recognition of negative expressions. However, in addition to differences related to the recognition of these expressions, this study found greater sensitivity to recognize positive emotions (happiness). A happy face is not just a learned stimulus; it is an emotion-laden social instrument to communicate friendly social alliance and a powerful social reward for showing assurance and acceptance and inviting collaboration (Oatley and Jenkins, 1996 apud Juth et al., 2005). Based on these data it is possible to conclude that the increased sensitivity demonstrated by women with SAD to recognize expressions of happiness could be associated with hypervigilance to detect signs of approval in facial expressions due to the desire for social acceptance, as a way to counterbalance the hypervigilance for negative expressions and the anxiety stemming from this bias. However, as suggested by Philippot and Douilliez (2005), recognition sensitivity could be unrelated to emotional valence and depend more on the individual’s personal concern about being judged, which could act as a signal to focus attention on his performance. The expression of fear is usually recognized as indicative of imminent threat, and the recognition of this expression was probably an advantage for the survival of the individual. Fear involves a withdrawal tendency (Davidson et al., 1990), but learning can attenuate, increase, or even replace this tendency with one of approach. The greater sensitivity for the recognition of fearful expressions could thus be attributed to the tendency of individuals with SAD to regard social or performance situations as threatening because of their excessive fear of humiliation or embarrassment in such situations. This increased sensitivity for the recognition of faces displaying fear may be an important factor in the maintenance of SAD, since the recognition of potential threat would lead the individual to decrease the frequency of social interactions due to regarding these as constant sources of threat. It is also important to emphasize that this hypervigilance to detect signs of threat or
approval in facial expressions may exacerbate the difficulty that people with SAD have to develop social skills (Levitan and Nardi, 2008). Different authors have proposed cognitive models to explain the way that people with social anxiety interact with their social environment. Clark and Wells (1995) state that people with social phobia, in the face of the situations they fear, tend to turn their attention toward themselves, making little use of available resources to monitor external stimuli as facial expressions of emotion, for example. Conversely, cognitive models of generalized social anxiety postulate an increase in the attention dedicated by the individuals to potentially threatening information (Mogg and Bradley, 1998; Mathews and Mackintosh, 1998). Thus, the social cues that are interpreted as critical and hostile can contribute to the maintenance of pathological levels of social anxiety (Leber et al., 2009). In addition to the happy and fearful faces, sadness was also recognized with less intensity, this gives further support to the hypothesis that SAD is related to a negative bias for the recognition of facial emotions. A possible explanation is that fearful and sad faces may be more easily recognized because they most closely represent the individual’s personal situational emotional state (Gilboa-Schechtman et al., 2008). Apparently, the emotional congruence between the stimulus and the beholder triggers related perceptual codes in memory, which facilitate the encoding of emotionally-congruent information (Bower, 1981; Niedenthal et al., 1997 apud Gilboa-Schechtman et al., 2008). Consistent with previous studies, our results suggest again that people with SAD and healthy controls differ in terms of their ability to recognize facial expressions of emotion. This difference is expressed in people with SAD by an apparent hypervigilance to fearful, sad, and happy faces, which would act as indicators of social threat and social reinforcement, in agreement with the disorder’s phenotype. In this study, no group differences were found related to the recognition of faces of disgust, anger or surprise. Although our work had a number of methodological strengths as compared to previous investigations, some limitations should be highlighted that could account for the discordant findings, especially in what concerns the expression of disgust, whose recognition seems to be most frequently reported as affected in SAD (e.g. Montagne et al., 2006). First, there were no time restraints and the stimuli remained on the screen until the volunteer provided a response The influence of the presentation time has been recognized as one of the factors that affect the recognition of facial expressions, since individuals with SAD submitted to brief expositions (500 ms) of facial expressions of emotion were shown to be more reactive to angry expressions, which did not occur when the presentation time of the stimuli was increased to 1250 ms (Mogg et al., 2004). Other studies also suggest that the processing of emotional stimuli is related to initial assessments of facial expressions (Simonian et al., 2001; Gilboa-Schechtman et al., 2005). Thus, with no time restraints for judgment, differences occurring at an early processing level (implicit processes) could be masked. Moreover, recent research shows evidence that the facial affect processing in social anxiety is influenced by experimental social threat conditions (Leber et al., 2009). Other limitations of our study were the non-acquisition of any other measures of anxiety other than social anxiety – which would be useful to investigate possible correlations with performance – and the adoption of static stimuli. Since emotional expressions are dynamic by nature, questions have been raised about the ecological adequacy of this stimulus design that was used in most of the studies to date (Sato and Yoshikawa, 2007 apud Johnston et al., 2008). Recent evidence suggests that emotional stimuli
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presented dynamically are recognized with greater accuracy as compared to static stimuli (Weyers et al., 2006 apud Johnston et al., 2008). Also, there is increasing evidence on the specialization of brain systems that are preferentially activated by biological movement, including the movement of facial features (Peuskens et al., 2005 apud Johnston et al., 2008). Despite these limitations, our findings suggest that SAD subjects are hypersensitive to threat-related and approval-related facial expressions. Future investigations to increase our knowledge in the field will benefit from the controlled inclusion of SAD patients in treatment, so that the potential effects of medication and psychotherapy – known to lead to symptom improvement – on the recognition of facial expressions of emotion can be evaluated. In addition, the neural basis of impaired processing of facial emotion could be explored using functional neuroimaging techniques, which would further our comprehension about the mechanisms of this disabling disorder. 5. Role of funding source K. Arrais, C. Trzesniak, M.C. Ferrari and J. Machado-de-Sousa are recipients of grants from the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Brazil). A.W. Zuardi (1C), S.R. Loureiro (1B), A.E. Nardi (1A) and J.A. Crippa (1C) are recipients of Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) productivity awards. This research was supported in part by a Fundação de Apoio ao Ensino, Pesquisa e Assistência do Hospital das Clínicas da Faculdade de Medicina de Ribeirão Preto da Universidade de São Paulo (FAEPA, Brazil) grant. Those funding had no further role in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication. 6. Contributors Crippa, Hallak, Loureiro and Machado-de-Sousa designed the study. Machado-de-Sousa, Trzesniak, Santos Filho, Ferrari and Osório were responsible for data collection. Arrais, Hallak, Crippa and Zuardi conducted the data analysis and interpretation of data. Arrais, Machado-de-Sousa, Zuardi, Hallak and Crippa managed the literature searches and wrote the initial drafts of the manuscript. Zuardi, Nardi and Hetem performed a critical revision of the manuscript for important intellectual content. All authors contributed to the final drafts of the manuscript and have approved the final version for publication. Conflict of interest statement The authors have no conflict of interest related to the topic of this trial. The grant for this research was provided by the Brazilian Council for Scientific and Technological Development (CNPq) and INCT Translational Medicine (CNPq). Acknowledgments The authors are grateful to Mrs. Sandra Bernardo for technical assistance and to Mr. Cássio dos Reis for help in statistical analysis. References Anderson IM, Del-Ben CM, Mckie S, Richardson P, Williams SR, Elliott R, et al. Citalopram modulation of neuronal responses to aversive face emotions: a functional MRI study. Neuroreport 2007;18(13):1351–5. Arnone D, Horder J, Cowen PJ, Harmer CJ. Early effects of mirtazapine on emotional processing. Psychopharmacology 2009;203:685–91. Beck AT. Cognitive therapy and the emotional disorders. New York: International Universities Press; 1976.
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Social anxiety disorder women easily recognize fearfull, sad and happy faces: The influence of gender Kátia C. Arrais a, João Paulo Machado-de-Sousa a,b, Clarissa Trzesniak a,b, Alaor Santos Filho a,b, Maria Cecília F. Ferrari a,b, Flávia L. Osório a,b, Sonia R. Loureiro a,b, Antonio E. Nardi b,c, Luiz Alberto B. Hetem a, Antonio W. Zuardi a,b, Jaime Eduardo C. Hallak a,b, José Alexandre S. Crippa a,b,* a b c
Department of Neuroscience and Behavior of the Ribeirão Preto Medical School, University of São Paulo, Brazil INCT, Translational Medicine, CNPq, Brazil Laboratory of Panic and Respiration, Institute of Psychiatry, Federal University of Rio de Janeiro, Brazil
a r t i c l e
i n f o
Article history: Received 28 August 2009 Received in revised form 27 October 2009 Accepted 3 November 2009
Keywords: Social phobia Social anxiety disorder Gender Recognition Emotion Face
a b s t r a c t Background: It has been suggested that individuals with social anxiety disorder (SAD) are exaggeratedly concerned about approval and disapproval by others. Therefore, we assessed the recognition of facial expressions by individuals with SAD, in an attempt to overcome the limitations of previous studies. Methods: The sample was formed by 231 individuals (78 SAD patients and 153 healthy controls). All individuals were treatment naïve, aged 18–30 years and with similar socioeconomic level. Participants judged which emotion (happiness, sadness, disgust, anger, fear, and surprise) was presented in the facial expression of stimuli displayed on a computer screen. The stimuli were manipulated in order to depict different emotional intensities, with the initial image being a neutral face (0%) and, as the individual moved on across images, the expressions increased their emotional intensity until reaching the total emotion (100%). The time, accuracy, and intensity necessary to perform judgments were evaluated. Results: The groups did not show statistically significant differences in respect to the number of correct judgments or to the time necessary to respond. However, women with SAD required less emotional intensity to recognize faces displaying fear (p = 0.002), sadness (p = 0.033) and happiness (p = 0.002), with no significant differences for the other emotions or men with SAD. Conclusions: The findings suggest that women with SAD are hypersensitive to threat-related and approval-related social cues. Future studies investigating the neural basis of the impaired processing of facial emotion in SAD using functional neuroimaging would be desirable and opportune. Ó 2009 Elsevier Ltd. All rights reserved.
1. Introduction Social phobia, also known as social anxiety disorder (SAD), is characterized by the excessive fear of humiliation or embarrassment in social or performance situations. The generalized form of the disorder is frequently a chronic, disabling condition (Davidson, 1993) marked by the phobic avoidance of most interaction situations, causing social, educational, professional and personal impairment (Schneier et al., 1994; Filho et al., 2009). The 12-month and lifetime DSM-IV prevalence rate of this disorder is high, of about 7.1% and 12.1%, respectively (Kessler et al., 2005; Ruscio et al., 2008). SAD is also associated with high rates of psychiatric
* Corresponding author. Address: Departamento de Neurociências e Ciências do Comportamento, Hospital das Clínicas da Faculdade de Medicina de Ribeirão Preto – USP, Av. dos Bandeirantes, 3900, 3° andar, CEP 14025-048, Brazil. Tel./fax: +55 16 3602 2201. E-mail address: [email protected] (José Alexandre S. Crippa). 0022-3956/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.jpsychires.2009.11.003
comorbidities, the most common being depression and substance abuse, among other anxiety disorders (Filho et al., 2009). One of the major aspects of SAD is the excessive fear of negative evaluation and criticism. Cognitive theories of this anxiety disorder (Beck et al., 1985; Clark and Wells, 1995; Rapee and Heimberg, 1997; Ito et al., 2008) suggest that the patient in the feared social situation, feel negatively evaluated by others to an exaggerated unrealistic extent, expecting to be negatively evaluated and hence conjuring rejection. Thus, they tend to focus their attention toward themselves, which interferes with normal processing of external social cues. This could lead to attentional and interpretational biases in detecting social threat, resulting in hypervigilance toward negative emotions (Leber et al., 2009). The adequate social functioning is related to the capacity to extract environmental information that is relevant to social outcome (Garner et al., 2006). In this process of evaluating and responding to environmental contingencies, the processing of facial expressions represent an important source of interpersonal information about positive or negative evaluations by others.
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Among the first systematic studies about the facial expression of emotions are the old reports by Charles Darwin (1872). In his work, Darwin demonstrated the evolutional importance and communicative value of facial expressions. Research in the area has gone a long way since then, dedicating great attention, especially after the 1970s, to the relation between mental disorders and the processing of facial information and particularly emotion. Thus, authors as Beck (1976) and Eysenck (1997) arrived at the concise proposition that the impaired ability to process emotional information from faces plays an important role in the etiology and maintenance of several mental conditions. In respect to the recognition of facial emotions by people with social anxiety, recent evidence suggests that a bias exist in the facial processing abilities of these individuals in the sense of a greater accuracy for recognition of facial expressions of negative emotions and more frequent wrong judgments of faces as negative (Winton et al., 1995; Lundh and Ost, 1996; Veljaca and Rapee, 1998; Mohlman et al., 2007; Yoon and Zinbarg, 2007, 2008). Also, people with social anxiety seem to take longer to recognize facial displays of happiness (Silvia et al., 2006), at the same that they require less emotional intensity to recognize angry (Joormann and Gotlib, 2006; Leber et al., 2009), sad (Leber et al., 2009), fear (Leber et al., 2009) and disgusted expressions (Montagne et al., 2006). In contrast, Philippot and Douilliez (2005) and Campbell et al. (2009) found no evidence of biased facial emotion recognition in individuals with SAD, and Hunter et al. (2009) reported that people with social phobia have a greater accuracy in the recognition of facial expressions in general, regardless of their emotional valence. Thus, although the majority of the studies suggest that people with SAD have an impaired capacity to recognize facial expressions of emotion; the reported conflicting findings may be due to the fact that most of them included small samples ranging from 12 to 29 subjects included in the experimental group, with most of patients selected from tertiary services (Lundh and Ost, 1996; Foa et al., 2000; Pérez-López and Woody, 2001; Mogg et al., 2004; Horley et al., 2004; Coles and Heimberg, 2005; Philippot and Douilliez, 2005; Joormann and Gotlib, 2006; Montagne et al., 2006; Mohlman et al., 2007; Gilboa-Schechtman et al., 2008; Campbell et al., 2009; Garner et al., 2009). Also, those studies do not report procedures to prevent the inclusion of patients with psychiatric comorbidities and on medication (Anderson et al., 2007; Arnone et al., 2009; Kerestes et al., 2009), which might have influenced the results obtained. Moreover, another important caveat of the former studies was that most of them did not take gender into account and there is evidence suggesting that gender-related differences exist in the recognition of facial expressions (Cellerino et al., 2004). Therefore, we assessed the recognition of facial expressions of the six basic emotions (happiness, sadness, disgust, anger, fear, and surprise) by individuals with SAD, in an attempt to overcome the limitations of previous studies.
2. Method 2.1. Participants The sample consisted of 78 patients with generalized SAD (30 men and 48 women; mean age 22.33 ± 5.11 years; mean education 13.03 ± 0.97 years; 79.70% participants reported their ethnicity as Caucasian, 18.05% as African descendant, 2.26% as Asian) in the experimental group and 153 healthy volunteers (53 men and 100 women, mean age 21.43 ± 3.63 years; mean education 12.95 ± 0.94; 78.04% participants reported their ethnicity as Caucasian, 13.55% as African descendant, 8.41% as Asian) enrolled in the control group (Table 1). All the subjects were recruited from the sample of an epidemiologic survey in which 2.319 university students completed self-
Table 1 Clinical and demographic characteristics of the SAD and healthy controls groups.
Male/female Age (years) Ethnicity (%) Education (years) SPIN (±SD) BSPS (±SD) DPS current LSRDS lifetime PHQ-2 (±SD) Age of SAD onset (years)
SAD (n = 78)
Controls (n = 153)
p
30/48 22.33 (±5.11) 79.70a/18.05b/ 2.26c 13.03 (±0.97) 35.18 (±13.18) 33.36 (±12.77) 8.63 (±6.65) 13.30 (±7.34) 2.24 (±1.75) 11.17 (±4.37)
53/100 21.43 (±3.63) 78.04a/13.55b/ 8.41c 12.95 (±0.94) 17.35 (±13.35) 14.78 (±10.92) 4.92 (±6.79) 6.79 (±6.77) 1.15 (±1.31)
0.32 0.052 0.98 0.32 <0.0001* <0.0001* <0.0001* <0.0001* <0.0001*
SD, standard deviation; SPIN, Social Phobia Inventory; BSPS, Brief Social Phobia Scale; DPS, Disability Profile Scale; LSRDS, Liebowitz Self-Rated Disability Scale; PHQ-2, Reduced Version of Patient Health Questionnaire. * Significant difference (p < 0.05). a Caucasian. b African descendant. c Asian.
assessment diagnostic instruments (Osório et al., 2007; Crippa et al., 2007, 2008). Out of those, 474 were selected and ascribed to two groups: (i) 237 individuals with a probable SAD diagnosis who, screened with the reduced version of the Social Phobia Inventory (MINI-SPIN – Connor, 2001), had a score of at least six points in the three items; and (ii) 237 volunteers with similar sociodemographic characteristics who scored zero in the three items of the MINI-SPIN. Afterwards, all 474 subjects were contacted by telephone and completed the Portuguese version (Del-Ben et al., 2001) of the anxiety mode of the Structured Clinical Interview for DSM-IV, clinical version (SCID-CV – First, 1997). Following the completion of the interview, the subjects were again distributed in two groups: (i) an experimental group composed by individuals with SAD; and (ii) a control group formed by health individuals. Finally, the full version of the SCID-CV was used for diagnostic confirmation and exclusion of comordid conditions (Crippa et al., 2008). The Brief Social Phobia Scale (BSPS) was used to assess SAD severity and the SPIN to rate SAD-related physiological symptoms of fear and avoidance. The Disability Profile Scale (DPS; Schneier et al., 1994) and the Liebowitz Self-Rated Disability Scale (LSRDS; Schneier et al., 1994), instruments designed to provide clinicianand patient-rated descriptive measures of current and lifetime functional impairment related to SAD. The reduced version of the Patient Health Questionnaire (PHQ-2), a brief self-administered scale, was used to assess the frequency of depressed mood and anhedonia symptoms over the two weeks prior to evaluation (Kroenke et al., 2003). Subjects were excluded from the sample who presented other psychiatric disorders, except for previous depressive episode, since it is a frequently comorbid condition with SAD (Stein and Stein, 2008; Filho et al., 2009). Additionally, we excluded individuals in treatment with psychotropic medication or in use of psychoactive substances, and the ones who presented with a general medical condition or who had received previous treatment for SAD (either pharmacological or psychotherapy). The research protocol was approved by the local ethics committee and all volunteers gave their signed informed consent to participate. 2.2. Material 2.2.1. Facial emotion recognition task We used a computerized task built with stimuli from the series Pictures of Facial Affect (Ekman and Friesen, 1976) depicting six basic emotions – happiness, sadness, fear, disgust, anger, surprise
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– and neutral faces. The chosen pictures displayed two men and two women to avoid gender interference, and were organized in 24 blocks (4 actors 6 emotions) with gradually increasing emotional intensity (Philippot and Douilliez, 2005), ranging from 0% (neutral face) to 100% (full emotion displayed). The participant was asked to label the emotion displayed on the computer screen as soon as he could recognize it, with no time restraint. Emotional intensity was increased by pushing a button on an eight-button pad developed for the study (six emotional labels, an ‘ADVANCE’ key to increase intensity, and an ‘ENTER’ key, used to start another block). The blocks were randomized in each session and a twoblock version was used for practice before the actual trial. At the end of the experiment, a performance report was generated informing the gender (actor) of each stimulus, time spent for each stimulus, total time, emotional label provided, and actual emotion displayed in each block. All participants were tested individually.
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Fig. 1. Mean number of frames advanced by women (intensity of emotion) to respond to each emotion. *Significant difference (MANOVA; p < 0.05).
2.3. Statistical analysis Clinical and demographic data were analyzed by t-test for continuous data and by the chi-squared test for nominal data. The time spent and the number of frames advanced until judgment (equivalent to emotional intensity) were calculated for each subject and analyzed by means of multivariate analysis of variance (MANOVA). Performance in the task and the interaction between gender and group were also analyzed by MANOVA. The influence of emotional valence – positive (happy, surprised) and negative (angry, sad, fearful, disgusted) facial expressions – was assessed by means of independent t-tests for both the time spent and the emotional intensity. The chi-square test was used to analyze emotional judgment accuracy. Since previous studies have shown that depression may be related to facial recognition abnormalities, particularly sadness (Gilboa-Schechtman et al., 2008), we further compared the results of SAD patients with or without past depression by means of the tstudent test. Additionally, Pearson’s and Spearman’s correlation coefficients were used to investigate interactions between the data from the scales and the emotion recognition task depending on whether they had a normal distribution (Pearson’s) or not (Spearman’s). The statistical analyses were performed using the SPSS 13.0 (SPSS –Incorporation, 2001) and the statistical level of significance was set at p < 0.05. 3. Results No significant differences were found between patients and controls in terms of their sociodemographic profile (gender, age, educational level and socioeconomic status), which attests to the adequacy of the matching procedure between the groups (Table 1). As expected, subjects with SAD presented higher scores than Controls on the self- (SPIN) and hetero- (BSPS) assessment social anxiety symptom scales, higher current (LSRDS) and lifetime (LSRDS) functional impairment, as well as higher frequency of depressed mood and anhedonia over two weeks (PHQ-2). 3.1. Facial emotion recognition The MANOVA for the intensity required for recognition showed significant differences for interaction (F3227 = 2.139; p = 0.050), but not for group (F3227 = 1.922; p = 0.078) and gender (F3227 = 1.337; p = 0.242). Therefore, a MANOVA was separately performed for gender. Women with SAD required less emotional intensity to recognize fear (F1146 = 10.210; p = 0.002), happiness (F1146 = 10.130; p = 0.002) and sadness (F1146 = 4.611; p = 0.033) (Fig. 1), but no dif-
Fig. 2. Mean number of frames advanced by men (intensity of emotion) to respond to each emotion. *Significant difference (MANOVA; p < 0.05).
ferences were found in males (Fig. 2). There were no significant effects for group (F3227 = 1.242; p = 0.286), gender (F3227 = 0.870; p = 0.517), and interaction (F3227 = 0.839; p = 0.541) for judgment accuracy or group (F3227 = 1.306; p = 0.256), gender (F3227 = 0.468; p = 0.831), and interaction (F3227 = 0.677; p = 0.669) for time spent to perform the task. The gender of the stimulus presented in the task also did not affect performance in terms of accuracy, time, and intensity required for recognition. Additionally, no statistical differences between the groups were found when the emotions were divided in two blocks according to their valence (positive and negative facial expressions), either in the time spent or emotional intensity. There were no differences for time spent (t = 0.235; p = 0.815), accuracy (t = 0.942; p = 0.351) or emotional intensity (t = 1.210; p = 0.233) when we compared SAD patients with or without depression. No correlations were found between the variables of the facial emotion recognition task and the clinical and subjective measures of social anxiety or depression. Finally, the results have shown that the recognition of facial emotion is unaffected by the gender of the stimulus. 4. Discussion This study was designed to investigate the recognition of facial expressions of emotion in patients with SAD and healthy controls, aiming to overcome the limitations of previous studies. As far as we know, this is the first study addressing the processing of facial affect in SAD patients with a large non-clinical, treatment-naïve sample with no current comorbities. The adoption of these parameters for the composition of the sample is important because recent studies suggest that treatments such as antidepressants can significantly reduce the response of the amygdala to faces of fear
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(Murphy et al., 2009) and could cause disinhibition in people with SAD that would eventually affect their ability to interact with other people (Valença et al., 2005). The performance of the patients in terms of the total time spent to assess the emotional task was similar to that of healthy controls. However, significant differences between the two groups were found regarding the emotional intensity required for judgment, represented by the number of frames advanced. The patients required lower emotional intensity to attain the same accuracy levels found in controls for the recognition of fear, sadness and happiness, with no differences for the other emotions. This effect was unrelated to previous depression episodes or depression symptoms scores. However, in an additional analysis to check the influence of gender on the recognition, we observed that this difference was significant only for the group of women. This finding is not unusual since several studies suggest that women with other disorders such as schizophrenia also perform better on tasks of recognition of facial expressions (Scholten et al., 2005). In the vast literature on the differentiated behavior of female and male subjects, it has been proposed that in selective attention tasks, female subjects’ processing entails more detailed elaboration of information than males (Meyers-Levy and Tybout, 1989; Meyers-Levy and Maheswaran, 1991 apud Güntekin and Basßar, 2007), and female subjects are more efficient in recognizing faces and facial expressions (Thayer and Johnsen, 2000; Cellerino et al., 2004 apud Güntekin and Basßar, 2007). By taking this trend in account, we could speculate that women with SAD have exacerbated this characteristic. The negative or contrasting findings of previous studies related to recognition biases for specific emotions by men or women with SAD may be due to the small sample size in many studies, which reduces the statistical power for this type of analysis. Several studies suggest that individuals with SAD show a bias for the recognition of negative expressions. However, in addition to differences related to the recognition of these expressions, this study found greater sensitivity to recognize positive emotions (happiness). A happy face is not just a learned stimulus; it is an emotion-laden social instrument to communicate friendly social alliance and a powerful social reward for showing assurance and acceptance and inviting collaboration (Oatley and Jenkins, 1996 apud Juth et al., 2005). Based on these data it is possible to conclude that the increased sensitivity demonstrated by women with SAD to recognize expressions of happiness could be associated with hypervigilance to detect signs of approval in facial expressions due to the desire for social acceptance, as a way to counterbalance the hypervigilance for negative expressions and the anxiety stemming from this bias. However, as suggested by Philippot and Douilliez (2005), recognition sensitivity could be unrelated to emotional valence and depend more on the individual’s personal concern about being judged, which could act as a signal to focus attention on his performance. The expression of fear is usually recognized as indicative of imminent threat, and the recognition of this expression was probably an advantage for the survival of the individual. Fear involves a withdrawal tendency (Davidson et al., 1990), but learning can attenuate, increase, or even replace this tendency with one of approach. The greater sensitivity for the recognition of fearful expressions could thus be attributed to the tendency of individuals with SAD to regard social or performance situations as threatening because of their excessive fear of humiliation or embarrassment in such situations. This increased sensitivity for the recognition of faces displaying fear may be an important factor in the maintenance of SAD, since the recognition of potential threat would lead the individual to decrease the frequency of social interactions due to regarding these as constant sources of threat. It is also important to emphasize that this hypervigilance to detect signs of threat or
approval in facial expressions may exacerbate the difficulty that people with SAD have to develop social skills (Levitan and Nardi, 2008). Different authors have proposed cognitive models to explain the way that people with social anxiety interact with their social environment. Clark and Wells (1995) state that people with social phobia, in the face of the situations they fear, tend to turn their attention toward themselves, making little use of available resources to monitor external stimuli as facial expressions of emotion, for example. Conversely, cognitive models of generalized social anxiety postulate an increase in the attention dedicated by the individuals to potentially threatening information (Mogg and Bradley, 1998; Mathews and Mackintosh, 1998). Thus, the social cues that are interpreted as critical and hostile can contribute to the maintenance of pathological levels of social anxiety (Leber et al., 2009). In addition to the happy and fearful faces, sadness was also recognized with less intensity, this gives further support to the hypothesis that SAD is related to a negative bias for the recognition of facial emotions. A possible explanation is that fearful and sad faces may be more easily recognized because they most closely represent the individual’s personal situational emotional state (Gilboa-Schechtman et al., 2008). Apparently, the emotional congruence between the stimulus and the beholder triggers related perceptual codes in memory, which facilitate the encoding of emotionally-congruent information (Bower, 1981; Niedenthal et al., 1997 apud Gilboa-Schechtman et al., 2008). Consistent with previous studies, our results suggest again that people with SAD and healthy controls differ in terms of their ability to recognize facial expressions of emotion. This difference is expressed in people with SAD by an apparent hypervigilance to fearful, sad, and happy faces, which would act as indicators of social threat and social reinforcement, in agreement with the disorder’s phenotype. In this study, no group differences were found related to the recognition of faces of disgust, anger or surprise. Although our work had a number of methodological strengths as compared to previous investigations, some limitations should be highlighted that could account for the discordant findings, especially in what concerns the expression of disgust, whose recognition seems to be most frequently reported as affected in SAD (e.g. Montagne et al., 2006). First, there were no time restraints and the stimuli remained on the screen until the volunteer provided a response The influence of the presentation time has been recognized as one of the factors that affect the recognition of facial expressions, since individuals with SAD submitted to brief expositions (500 ms) of facial expressions of emotion were shown to be more reactive to angry expressions, which did not occur when the presentation time of the stimuli was increased to 1250 ms (Mogg et al., 2004). Other studies also suggest that the processing of emotional stimuli is related to initial assessments of facial expressions (Simonian et al., 2001; Gilboa-Schechtman et al., 2005). Thus, with no time restraints for judgment, differences occurring at an early processing level (implicit processes) could be masked. Moreover, recent research shows evidence that the facial affect processing in social anxiety is influenced by experimental social threat conditions (Leber et al., 2009). Other limitations of our study were the non-acquisition of any other measures of anxiety other than social anxiety – which would be useful to investigate possible correlations with performance – and the adoption of static stimuli. Since emotional expressions are dynamic by nature, questions have been raised about the ecological adequacy of this stimulus design that was used in most of the studies to date (Sato and Yoshikawa, 2007 apud Johnston et al., 2008). Recent evidence suggests that emotional stimuli
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presented dynamically are recognized with greater accuracy as compared to static stimuli (Weyers et al., 2006 apud Johnston et al., 2008). Also, there is increasing evidence on the specialization of brain systems that are preferentially activated by biological movement, including the movement of facial features (Peuskens et al., 2005 apud Johnston et al., 2008). Despite these limitations, our findings suggest that SAD subjects are hypersensitive to threat-related and approval-related facial expressions. Future investigations to increase our knowledge in the field will benefit from the controlled inclusion of SAD patients in treatment, so that the potential effects of medication and psychotherapy – known to lead to symptom improvement – on the recognition of facial expressions of emotion can be evaluated. In addition, the neural basis of impaired processing of facial emotion could be explored using functional neuroimaging techniques, which would further our comprehension about the mechanisms of this disabling disorder. 5. Role of funding source K. Arrais, C. Trzesniak, M.C. Ferrari and J. Machado-de-Sousa are recipients of grants from the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Brazil). A.W. Zuardi (1C), S.R. Loureiro (1B), A.E. Nardi (1A) and J.A. Crippa (1C) are recipients of Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) productivity awards. This research was supported in part by a Fundação de Apoio ao Ensino, Pesquisa e Assistência do Hospital das Clínicas da Faculdade de Medicina de Ribeirão Preto da Universidade de São Paulo (FAEPA, Brazil) grant. Those funding had no further role in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication. 6. Contributors Crippa, Hallak, Loureiro and Machado-de-Sousa designed the study. Machado-de-Sousa, Trzesniak, Santos Filho, Ferrari and Osório were responsible for data collection. Arrais, Hallak, Crippa and Zuardi conducted the data analysis and interpretation of data. Arrais, Machado-de-Sousa, Zuardi, Hallak and Crippa managed the literature searches and wrote the initial drafts of the manuscript. Zuardi, Nardi and Hetem performed a critical revision of the manuscript for important intellectual content. All authors contributed to the final drafts of the manuscript and have approved the final version for publication. Conflict of interest statement The authors have no conflict of interest related to the topic of this trial. The grant for this research was provided by the Brazilian Council for Scientific and Technological Development (CNPq) and INCT Translational Medicine (CNPq). Acknowledgments The authors are grateful to Mrs. Sandra Bernardo for technical assistance and to Mr. Cássio dos Reis for help in statistical analysis. References Anderson IM, Del-Ben CM, Mckie S, Richardson P, Williams SR, Elliott R, et al. Citalopram modulation of neuronal responses to aversive face emotions: a functional MRI study. Neuroreport 2007;18(13):1351–5. Arnone D, Horder J, Cowen PJ, Harmer CJ. Early effects of mirtazapine on emotional processing. Psychopharmacology 2009;203:685–91. Beck AT. Cognitive therapy and the emotional disorders. New York: International Universities Press; 1976.
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