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Subtypes of anhedonia and facial electromyography response to negative affective pictures in non-psychiatric adults a

a

a

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L.S. Kadison , K.A. Ragsdale , J.C. Mitchell , J.E. Cassisi & J.S. a

Bedwell a

Psychology Department, University of Central Florida, 4111 Pictor Lane, Orlando, FL, USA Published online: 04 Sep 2014.

Click for updates To cite this article: L.S. Kadison, K.A. Ragsdale, J.C. Mitchell, J.E. Cassisi & J.S. Bedwell (2015) Subtypes of anhedonia and facial electromyography response to negative affective pictures in nonpsychiatric adults, Cognitive Neuropsychiatry, 20:1, 31-40, DOI: 10.1080/13546805.2014.955172 To link to this article: http://dx.doi.org/10.1080/13546805.2014.955172

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Cognitive Neuropsychiatry, 2015 Vol. 20, No. 1, 31–40, http://dx.doi.org/10.1080/13546805.2014.955172

Subtypes of anhedonia and facial electromyography response to negative affective pictures in non-psychiatric adults L.S. Kadison, K.A. Ragsdale, J.C. Mitchell, J.E. Cassisi and J.S. Bedwell* Psychology Department, University of Central Florida, 4111 Pictor Lane, Orlando, FL, USA

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(Received 23 May 2013; accepted 8 August 2014) Introduction. Flat/constricted affect and anhedonia are symptoms found in several psychiatric disorders such as depression and schizophrenia. However, there are very few studies on the relationships between specific anhedonia subtypes and objectively assessed flat affect, and it appears that none of the existing studies examined potential moderation by sex. Methods. Forty-seven undergraduate students (60% male) completed self-report questionnaires assessing three subtypes of anhedonia – non-social consummatory (CON) and anticipatory (ANT) anhedonia, and overall social anhedonia. Participants viewed 15 pictures (5 neutral and 10 negative) from the International Affective Picture System, whereas facial muscle reaction was recorded using electromyography (EMG). Results. Male participants reporting a greater level of overall social or non-social CON anhedonia showed a greater EMG activity increase in the corrugator supercilii muscle to negative (vs. neutral) pictures. In females, the relationship was only found with social anhedonia and was opposite in direction, as increased social anhedonia related to less EMG activity change in the corrugator muscle. Conclusions. The relationship between anhedonia and flat affect varied as a function of sex and anhedonia subtype. These findings may help explain discrepancies in the sparse existing literature examining this relationship in psychiatric populations and have implications for assessment and treatment of these symptoms across psychiatric disorders. Keywords: anhedonia; facial; emotion; expression; electromyography

Anhedonia refers to a deficit in the experience of pleasure and is often broken down into two distinct subtypes: consummatory (CON) and anticipatory (ANT). CON anhedonia refers to a decreased capacity for pleasure in the moment (e.g., the enjoyment of the smell of freshly cut grass), whereas ANT anhedonia specifies diminished pleasure when thinking about an upcoming event (e.g., deriving pleasure from the anticipation of a favourite meal). Anhedonia can also be defined based on the type of stimulus, such as social or nonsocial. Social anhedonia is a lessened experience of pleasure from various types of interpersonal interactions (discernible from social anxiety; Brown, Silvia, Germeys, & Kwapil, 2007). Non-social anhedonia refers to a deficit in the experience of pleasure in response to a stimulus or situation that is not primarily related to interpersonal interactions. Anhedonia is considered a core symptom of several psychiatric disorders including schizophrenia-spectrum, depressive and bipolar disorders (American Psychiatric Association,

*Corresponding author. Email: [email protected] © 2014 Taylor & Francis

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2013); however, specific subtypes appear to be more prevalent within certain disorders. For example, several studies have shown that schizophrenia and depression are associated with intact CON pleasure but deficient ANT pleasure (Heerey & Gold, 2007; Horan, Blanchard, Clark, & Green, 2008; Horan, Wynn, Kring, Simons, & Green, 2010; although see Strauss, Wilbur, Warren, August, & Gold, 2011; depression: see review by Dichter, 2010). Further, social anhedonia is particularly predictive of later development of schizophrenia (Gooding, Tallent, & Matts, 2005; Kwapil, 1998). Additionally, males tend to report more social and non-social anhedonia than females in both clinical and non-clinical samples (Fonseca-Pedrero, Lemos-Giraldez, Muniz, Garcia-Cueto, & Campillo-Alvarez, 2008; Miettunen & Jaaskelainen, 2010). Diminished facial expressivity in response to emotional stimuli is another core symptom of many psychiatric disorders and is a subtype of what is often referred to as constricted or flattened affect. Whereas flat affect may appear to be a manifestation of anhedonia, it is not the same construct. Anhedonia is an internal emotional experience, whereas flattened affect is outward expression. Further, anhedonia is defined as diminished positive emotion, unlike flat affect, which is diminished positive and negative emotion expression. Facial electromyography (EMG) is an objective measure of facial emotional expression with good psychometric properties (Fridlund & Cacioppo, 1986; Lee, Shackman, Jackson, & Davidson, 2009). EMG can differentiate negatively and positively valenced emotional reactions by measuring activity in the corrugator supercilii and zygomatic major facial muscle groups, respectively (Cacioppo, Berntson, Larsen, Poehlmann, & Ito, 2000). Research using facial EMG has consistently reported diminished expressivity in response to emotional stimuli in a subset of individuals with schizophrenia (see review by Kring & Moran, 2008) and depression (Greden, Genero, Price, Feinberg, & Levine, 1986). Further, sex differences have been reported, as females display greater facial EMG signals in response to unpleasant pictures than males (Dimberg & Lundquist, 1990; Huang & Hu, 2009; Lundqvist, 1995). Research examining relationships between anhedonia and flattened affect in schizophrenia have produced mixed results. One study with individuals with schizophrenia found that increased clinician-rated anhedonia was related to reduced inflection in speech – one form of flattened affect (Cohen, Alpert, Nienow, Dinzeo, & Docherty, 2008). However, another study found no relationship between clinician-rated anhedonia and the use of positive or negative emotional words in spoken narratives in a schizophrenia sample (Alpert, Rosenberg, Pouget, & Shaw, 2000). To gain further insight into the relationship of flattened affect and anhedonia, it is important to study these constructs in nonpsychiatric samples, which will allow the examination of the relationships without confounds often present in psychiatric disorders (e.g., medication effects, complex symptom interactions). Leung, Couture, Blanchard, Lin, and Llerena (2010) found that higher levels of social anhedonia were related to diminished facial expressivity in response to emotional film clips in a female non-psychiatric sample. However, an earlier study combining non-psychiatric males and females found that higher physical (i.e., primarily nonsocial) anhedonia was related to greater (rather than diminished) facial expressivity to both positive and negative stimuli (Fitzgibbons & Simons, 1992). Overall, this relationship has only been directly examined using objective markers of expressivity in a handful of studies, which vary in the type of sample examined, anhedonia assessed, and emotional expression assessed. The potential moderation of sex also needs to be examined in this relationship, as sex has been found to be a greater predictor of facial expressivity than anhedonia (Berenbaum, Snowhite, & Oltmanns, 1987).

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To address this gap in research, the current study examined the relationship between three self-reported anhedonia subtypes (i.e., overall social anhedonia, and non-social ANT and CON anhedonia) and facial affective expressivity to negatively valenced pictures in non-psychiatric males and females. This study further contributes to the existing literature by examining the potential moderation of sex on these relationships. A better understanding of this relationship informs assessment and treatment across populations presenting with these symptoms. For example, examining whether sex moderates this relationship will inform clinicians who are assessing and treating these symptoms to consider how the presentation and response to treatment may vary by sex. It was hypothesised that sex and social anhedonia will interact in relation to facial expressivity to negatively valenced pictures; however, given the mixed existing literature on this topic, examination of the simple effects will be exploratory. We expected moderation of sex based on findings of increased facial expressivity in females (Dimberg & Lundquist, 1990; Huang & Hu, 2009; Lundqvist, 1995) and greater selfreported anhedonia in males (Fonseca-Pedrero et al., 2008; Miettunen & Jaakelainen, 2010). In terms of non-social anhedonia, CON, rather than ANT, anhedonia was hypothesised to show a more robust relationship with EMG, as it reflects self-report of typical “in-the-moment” emotion, similar to the in-the-moment EMG assessment. In addition, social, rather than non-social, anhedonia was hypothesised to have a stronger relationship to the EMG response, as social anhedonia has shown stronger links to schizophrenia (Gooding et al., 2005; Kwapil, 1998) – a disorder that often includes flat affect.

Methods Participants Participants were enrolled in courses offered by a Psychology Department of a large university in the USA, using an online recruitment system that awarded course credit in return for participation. Participants were recruited as part of a larger study (Mitchell et al., under review), which included an online administration of the Schizotypal Personality Questionnaire (SPQ; Raine, 1991) and two validity scales. After excluding individuals based on the validity scales or incomplete responses, participants falling in the top and bottom twentieth percentile on the SPQ total score were invited to participate in the lab-based portion of this study. Forty-nine individuals participated in the lab-based study; however, two individuals were excluded from the data analysis due to invalid EMG data (as a result of artefact). Therefore, the final sample consisted of 47 participants (60% male). The average age of this sample was 20.37 (SD = 4.74), and the reported race was 66.1% Caucasian, 14.3% “Mixed/Other,” 10.7% Hispanic, 5.4% African American and 3.6% Asian. Although participants were initially recruited based on the online SPQ total scores being relatively high or low, the scores from a lab-based re-administration of the SPQ reflected a relatively normal, but wide, distribution. As the relationships between the SPQ and the EMG data (without considering anhedonia) have been previously reported for this sample (Mitchell et al., under review), the present study will focus on relationships between the self-reported anhedonia and the EMG, when covarying for the SPQ total score.

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Measures Temporal Experience of Pleasure Scale (TEPS) The TEPS is an 18-item self-report measure that provides subscales for CON and ANT pleasure and has been found to have good psychometric properties (Gard, Gard-Germans, Kring, & Oliver, 2006). The TEPS assesses CON and ANT pleasure in primarily nonsocial contexts. It is scored on a Likert scale ranging from very false for me (1) to very true for me (6), with lower scores indicating more anhedonia.

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Anticipatory and Consummatory Interpersonal Pleasure Scale (ACIPS) The ACIPS is a recently developed 17-item self-report measure designed to measure social and interpersonal pleasure (Gooding & Pflum, 2014a, 2014b). The ACIPS is scored on a 6-point Likert scale, with lower scores indicating more social anhedonia. As factor analysis on this measure does not support the use of separate ANT and CON subscales (Gooding & Pflum, 2014b), we used the total score in our analyses. Two studies have revealed that the ACIPS total score has high internal consistency along with good convergent and discriminant validity (Gooding & Pflum, 2014a, 2014b). Self-Assessment Manikin (SAM) The SAM (Lang, Bradley, & Cuthbert, 2008) was used during the lab-based phase to assess arousal and affective valence in response to affective pictures using the number keys 1–9 on a keyboard. Arousal is measured on a range from calm (1) to excited (9) in response to a figure which illustrates arousal level. Similarly, valence is measured on a scale from unpleasant (1) to pleasant (9) in response to a figure which illustrates valence. Affective Picture Electromyography Task (APET) Based on the published normative ratings using the SAM affective rating system, 5 neutral pictures and 10 negatively valenced pictures (containing images of threatening stimuli and others in distress) were selected from the International Affective Picture System (IAPS; Lang et al., 2008). Normative SAM ratings for the 15 pictures are presented in Table 1. Using E-Prime 2.0 (Psychology Software Tools), each picture was displayed for 8 seconds, immediately followed by the SAM ratings (unlimited time) and by an interstimulus interval that randomly varied between 30 and 40 seconds. Procedure The lab-based session consisted of informed consent, a re-administration of the SPQ (paper version) and administration of the TEPS, ACIPS and APET. During the APET, EMG signals over the corrugator supercilii and the zygomatic major muscle groups were recorded using MindWare Technologies Inc. (Gahanna, OH) and BioLab Acquisition software (Version 3.0; MindWare Technologies, 2010). Five cup-style Ag–AgCl facial electrodes (two measuring corrugator supercilii, two measuring zygomatic major and one ground electrode) were filled with saline conductive gel and placed on the participant using 4-mm adhesive discs. EMG signals were amplified at a gain of 2,000. Data processing and statistical analyses Offline data were subjected to a 30–200-Hz band pass filter to partially exclude movement and eye-blink artefact. The signal was then rectified to convert the

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Table 1. Normative ratings of IAPS pictures using the SAM. IAPS picture number/description Negative

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Neutral

9,413, 2,703, 9,075, 6,500, 3,168, 1,114, 1,525, 2,120, 6,260, 6,830, 7,000, 7,010, 7,175, 7,090, 7,080,

men being hanged crying children starving child knife to throat mutilated face open mouth edsnake attack dog close up of angry male face gun pointed at observer masked man with guns rolling pin wicker basket lamp book fork

Valence rating, M (SD) 1.76 1.91 1.29 2.73 1.56 4.03 3.09 3.34 2.44 2.82 5.00 4.94 4.87 5.19 5.27

(1.08) (1.26) (.64) (2.38) (1.06) (2.16) (1.72) (1.91) (1.54) (1.81) (.84) (1.07) (1.00) (1.46) (1.09)

Arousal rating, M (SD) 6.81 5.78 6.57 7.09 6.00 6.33 6.51 5.18 6.93 6.21 2.42 1.76 1.72 2.61 2.32

(2.09) (2.25) (2.39) (1.98) (2.46) (2.17) (2.25) (2.52) (1.93) (2.23) (1.79) (1.48) (1.26) (2.03) (1.84)

negative-to-positive range of values to absolute values. The peak amplitude of the EMG signal (measured in microvolts) during the 8 seconds following each stimulus was identified. We then calculated peak EMG amplitude change scores separately for each of the two muscle groups by subtracting the average peak amplitude during the neutral pictures from the average peak amplitude during the negatively valenced pictures. This peak EMG amplitude change score was used for all analyses. Each of the three scales of pleasure (ANT and CON TEPS and total ACIPS scores) was examined in separate 2 × 2 mixed analyses of covariance that examined the influence of sex, anhedonia and interaction in relation to the peak EMG amplitude change score, when covarying for the SPQ total score. In addition, 2 × 2 mixed multivariate analyses of covariances (MANCOVAs) were used to examine the relationship between each of the anhedonia subtypes and sex (and interaction) on the combination of the arousal and valence from the SAM ratings, when controlling for the SPQ score. Further exploratory analyses were conducted using partial correlations, which controlled for the SPQ score.

Results The descriptive statistics for all measures can be found in Table 2, and zero-order correlations can be found in Table 3. Anticipatory non-social pleasure (TEPS-ANT) and change in corrugator EMG response There was no main effect of sex, F(1, 42) = 1.79, p = .19, ή = .04, or TEPS-ANT, F(1, 42) = .001, p = .97, ή < .001, and no interaction between sex and TEPS-ANT, F(1, 42) = 1.97, p = .17, ή = .05.

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Table 2. Descriptive statistics by sex. Males (N = 28)

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1. 2. 3. 4. 5. 6. 7. 8. 9.

ACIPS total TEPS-CON TEPS-ANT* ZYGO CORR Arousal Valence SPQ total score Constrict Affect

Females (N = 19)

Mean

SD

Range

Mean

SD

Range

82.11 37.46 44.00 –.85 .96 2.77 –2.06 25.07 2.46

10.79 5.59 6.79 2.51 2.38 1.29 1.11 17.03 1.97

44–97 28–47 33–58 –8.1 to 3.92 –5.06 to 7.4 –.30 to 4.90 –4.3 to –.300 3–63 0–7

87.05 38.86 48.00 –.19 1.20 3.54 –2.62 21.95 1.63

7.01 5.75 4.4 1.21 3.90 1.69 1.15 16.18 1.67

72–99 23–47 41–59 –3.87 to 2.05 –6.96 to 10 –.30 to 5.60 –4.6 to –.60 2–58 0–6

ACIPS total = total score on the Anticipatory and Consummatory Interpersonal Pleasure Scale; TEPS-CON = total Consummatory score on the Temporal Experience of Pleasure Scale; TEPS-ANT = total Anticipatory score on the Temporal Experience of Pleasure Scale; ZYGO = peak amplitude of the zygomatic major EMG to negative minus neutral pictures; CORR = peak amplitude of the corrugator supercilii EMG to negative minus neutral pictures; Arousal = average SAM arousal rating to negative minus neutral pictures; Valence = average SAM valence rating to negative minus neutral pictures; SPQ = Schizotypal Personality Questionnaire; Constrict Affect = total score on Constricted Affect Subscale of the SPQ. *p < .05 between sexes.

Table 3. Zero-order correlations by sex; males (N = 28) are shown below the diagonal, and females (N = 19) are shown above the diagonal.

1. 2. 3. 4. 5. 6. 7. 8. 9.

ACIPS total TEPS-CON TEPS-ANT ZYGO CORR Arousal Valence SPQ total Constrict Affect

1.

2.

3.

4.

5.

6.

7.

8.

9.

— .53** .60** –.07 –.56** .17 .05 –.06 –.34

.38 — .49** –.15 –.47* .13 –.30 .13 –.14

.38 –.15 — –.11 –.38* .36 –.18 –.05 –.22

–.01 .04 .29 — .19 .24 .13 .06 –.08

.45* .40 .12 .17 — –.08 .07 –.22 .11

.38 .57* .22 .06 .29 — –.48** –.16 –.20

–.31 –.50* –.04 .15 –.43 –.76** — –.11 –.08

–.13 .14 .36 .29 .08 –.08 .19 — .59**

–.30 –.003 .15 .16 –.09 –.22 .37 .86** —

ACIPS total = total score on the Anticipatory and Consummatory Interpersonal Pleasure Scale; TEPS-CON = total Consummatory score on the Temporal Experience of Pleasure Scale; TEPS-ANT = total Anticipatory score on the Temporal Experience of Pleasure Scale; ZYGO = peak amplitude of the zygomatic major EMG to negative minus neutral pictures; CORR = peak amplitude of the corrugator supercilii EMG to negative minus neutral pictures; Arousal = average SAM arousal rating to negative minus neutral pictures; Valence = average SAM valence rating to negative minus neutral pictures; SPQ total = total score from Schizotypal Personality Questionnaire; and Constrict Affect = Constricted Affect Subscale of the SPQ. *p < .05; **p < .01.

Consummatory non-social pleasure (TEPS-CON) and change in corrugator EMG response There was a significant main effect of sex, F(1, 42) = 8.93, p = .005, η2 = .17, as females showed a greater change in corrugator EMG response. There was no main effect for TEPS-CON, F(1, 42) = .20, p = .66, η2 = .005. However, there was a significant interaction between sex and TEPS-CON, F(1, 42) = 9.21, p = .004, η2 = .18. After covarying for the SPQ total score, males showed a significant negative correlation

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between TEPS-CON and the corrugator EMG change (i.e., a greater level of CON non-social anhedonia related to a greater EMG change), r(25) = –.46, p = .02, whereas females showed no relationship, r(16) = .39, p = .11.

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ACIPS total score and change in corrugator EMG response There was a significant main effect of sex, F(1, 42) = 11.88, p = .001, η2 = .22, as females showed a greater change in corrugator EMG response. There was no main effect for ACIPS total score, F(1, 42) = 1.35, p = .25, η2 = .03. However, there was a significant interaction between sex and ACIPS total score, F(1, 42) = 12.30, p = .001, η2 = .23. After covarying for the SPQ total score, males showed a significant negative correlation between the ACIPS total score and the corrugator EMG change (i.e., a greater level of social anhedonia related to a greater EMG change), r(25) = –.59, p = .001 (see Figure 1), whereas females showed a significant positive relationship (i.e., a greater level of social anhedonia related to a weaker EMG change), r(16) = .47, p = .05 (see Figure 2). Anhedonia ratings and change in zygomatic EMG response (negative minus neutral pictures) Results revealed that there was no main effect of anhedonia or sex, and no interaction between sex and anhedonia for any of the three anhedonia subtypes (all ps > .50). Anhedonia ratings and subjective SAM ratings of pictures MANCOVAs revealed that, of the three anhedonia subtypes, only TEPS-CON showed a significant relationship with the two SAM ratings (arousal and valence), F(2, 41) = 5.12, p = .01, ή = .20, but there was no interaction between the TEPS-CON and sex in this relationship, F(2, 41) = 1.83, p = .17, ή = .08. Partial correlations of this main effect (controlling for SPQ) showed a positive relationship between the TEPS-CON and the arousal change, r(44) = .37, p = .01, and a negative relationship between the TEPS-CON

Figure 1. Scatterplot of EGM peak amplitude change in corrugator muscle in relation to the ACIPS total score in male participants.

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Figure 2. Scatterplot of EGM peak amplitude change in corrugator muscle in relation to the ACIPS total score in female participants.

and the valence change, r(44) = –.40, p = .01. Individuals with more CON non-social anhedonia (i.e., lower TEPS-CON score) showed less of an increase in arousal, but a greater decrease in valence (i.e., more unpleasant), to negative, compared with neutral, pictures.

Conclusions The hypothesis that sex and anhedonia would interact in relation to facial expressivity was supported. With regard to CON non-social anhedonia, increased anhedonia related to a greater EMG change in males, but no relationship was found for females. This result was consistent with a study with a non-psychiatric sample that also found an increased EMG change to negative pictures in relation to physical anhedonia, although that study did not explore moderation of sex (Fitzgibbons & Simons, 1992). The heightened negative response to negatively valenced stimuli in our male participants could relate to a potentiation of negative emotion seen in anhedonic conditions (e.g., depression), or suggest that negative expression is less blunted than positive, which has been reported in depression (Bylsma, Morris, & Rottenberg, 2008). Consistent with the EMG results, individuals with more CON non-social anhedonia showed a greater increase in self-reported negative valence to the negative pictures. Whereas this finding was limited to males with the EMG, the relationship with behavioural ratings was found across both sexes. Overall social anhedonia, as expected, showed the strongest relationships with the EMG response. Consistent with CON non-social anhedonia, greater social anhedonia related to a greater EMG response in males (see Figure 1). However, females showed a significant, albeit weaker, relationship in the opposite direction; more social anhedonia related to a weaker EMG change in females (see Figure 2). This is consistent with one study that examined non-psychiatric females, which also found that greater social anhedonia related to a weaker facial expressivity change (Leung et al., 2010). Social anhedonia did not relate to the behavioural ratings of the pictures within either sex.

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The current results inform both assessment and treatment of flat affect and anhedonia in psychiatric disorders, as the results highlight the importance of considering sex. For example, males presenting with high levels of negative affective facial expression may still be experiencing anhedonia, whereas this is less likely for females. These relationships appear to be particularly strong with social anhedonia. In terms of treatment, patients presenting with either extreme of facial expressivity may benefit from clinician feedback and self-monitoring. The findings of this study highlight the importance of considering sex in such a treatment, given the differential relationship with the experience of anhedonia. Further research is needed to clarify why the sexes differed in these relationships, as the current study cannot address the particular mechanisms involved. A limitation of this study was not including positively valenced stimuli, as the larger study was focused on reactions to negative stimuli. Thus, as expected, no relationships were found in the zygomatic EMG response (which measures positive expressions) for sex or anhedonia subtypes. Future research should examine these relationships in response to positively valenced stimuli to determine whether the zygomatic muscle group shows a similar pattern of relationships found in the present study. In closing, this study shows that sex and anhedonia interact in relation to facial expressivity. Social anhedonia in particular shows a strong relationship with facial expressivity and shows the most robust interaction with sex. These findings may help explain many discrepancies in the current research examining anhedonia and flat affect and have clinical implications for assessment and treatment of these symptoms across psychiatric disorders. Acknowledgements The authors would like to thank Ms Daniella S. Schlander and Mr Christopher Spencer for assistance with data collection and entry. In addition, the authors thank Drs Valerie Sims and Deborah C. Beidel for contributions with the design and interpretation of the data.

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Subtypes of anhedonia and facial electromyography response to negative affective pictures in non-psychiatric adults.

Flat/constricted affect and anhedonia are symptoms found in several psychiatric disorders such as depression and schizophrenia. However, there are ver...
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