Hormones and Behavior 63 (2013) 97–104

Contents lists available at SciVerse ScienceDirect

Hormones and Behavior

j ourna l homepage: www.e lsev ie r .com/ locate /yhbeh

Association of menstrual cycle phase with the core components of empathy

Birgit Derntl a,b,c,⁎, Ramona L. Hack a, Ilse Kryspin-Exner a, Ute Habel b,c

a Institute for Clinical, Biological and Differential Psychology, Faculty of Psychology, University of Vienna, Vienna, Austriab Department of Psychiatry, Psychotherapy and Psychosomatics, RWTH Aachen University, Aachen, Germanyc Jülich Aachen Research Alliance, Translational Brain Medicine, Germany

⁎ Corresponding author at: Department of Psychiatry, PsyRWTH Aachen University, Pauwelssstrasse 30, D-52074 Aa

E-mail address: bderntl@ukaachen.de (B. Derntl).

0018-506X/$ – see front matter © 2012 Elsevier Inc. Allhttp://dx.doi.org/10.1016/j.yhbeh.2012.10.009

a b s t r a c t

a r t i c l e i n f o

Article history:Received 25 January 2012Revised 17 October 2012Accepted 18 October 2012Available online 23 October 2012

Keywords:EmpathyEmotion recognitionPerspective takingAffective responsivenessMenstrual cycleProgesteroneEstrogenSocial interaction

Evidence has accumulated that emotion recognition performance varies with menstrual cycle phase. However,according to some empathy models, facial affect recognition constitutes only one component of empathicbehavior, besides emotional perspective taking and affective responsiveness. It remains unclear whethermenstrual cycle phase and thus estradiol and progesterone levels are also associated with the two otherempathy constructs.Therefore, we investigated 40 healthy right-handed females, 20 during their follicular phase and 20 duringtheir midluteal phase and compared their performance in three tasks tapping the empathic components aswell as self-report data. Salivary hormone levels were obtained and correlated with performance parameters.Subjects were matched for age and education and did not differ in neuropsychological function. Analysis ofempathy performance revealed a significant effect of phase in emotion recognition, showing higher accuracyin the follicular group. Regarding affective responsiveness, we observed a significant difference in reactiontimes, with faster responses for sad and angry stimuli in the midluteal group. No significant group differenceemerged for emotional perspective taking. Furthermore, significant correlations between progesterone levelsand emotion recognition accuracy and affective responsiveness emerged only in the luteal group. However,groups did not differ in self-reported empathy.Our results indicate that menstrual cycle phase and thus ovarian hormone concentration are differentiallyrelated to empathic behavior, particularly emotion recognition and responsiveness to negative situations,with progesterone covarying with both in the luteal phase.

© 2012 Elsevier Inc. All rights reserved.

Introduction

Behavioral evidence documents that sex hormone concentrationaffects cognition, emotion and nonverbal behavior, thus a broad spec-trum of human behavior, across the whole lifespan starting within thefirst trimester of pregnancy (for reviews see Boulware et al., 2011;Hines, 2010; Vincent and Tracey, 2010). Concerning emotional abili-ties in females, previous studies mostly focused on the impact ofmenstrual cycle phase on facial emotion processing: Pearson andLewis (2005) reported a significant positive association of estrogenlevels with fear recognition, with highest accuracy during the preovu-latory phase when estrogen levels are high. Conway et al. (2007)demonstrated that progesterone levels in healthy female subjectsare related to intensity ratings of disgusted and fearful but nothappy faces. Thus, the authors assume that elevated progesterone levelsare associated with increased sensitivity to facial cues carrying sources ofthreat or contagion. Our preceding findings (Derntl et al., 2008a,b)showed a significant difference in emotion recognition performance

chotherapy and Psychosomatics,chen, Germany.

rights reserved.

across the menstrual cycle, with higher accuracy during the follicularphase which was further supported by a significant negative correlationof progesterone levels with recognition accuracy. Notably, analysis oferror tendencies strongly corroborated results by Conway et al.(2007) aswe observed statistically significant higher recognition errorsfor anger and disgust during the luteal phase, thus further supportingthe assumption that raised progesterone levels bias behavioral tenden-cies towards threatening stimuli with the possible aim of protectionfrom any source of threat or danger (e.g., illness). Moreover, Guapo etal. (2009) reported a significant difference in the identification ofanger and sadness between females at three different stages of themenstrual cycle, again with better performance during the follicularphase. Authors also observed a significantly negative correlation be-tween estrogen levels and recognition performance for angry malefaces, while no significant association between progesterone and per-formance was mentioned. Thus, previous research showed that perfor-mance in facial affect recognition is modulated by menstrual cyclephase. However, studies investigating a broader spectrum of emotionalabilities such as empathy are missing.

Empathy, the ability to infer and share another's internal emotion-al states, is a multidimensional phenomenon. Due to the complexityof the construct, empathy has various definitions (e.g., Preston and

Table 1Demographic information showing mean values and standard deviation in parenthe-ses. Groups differed significantly in their progesterone and estradiol levels (p-valuesin bold) as expected but had similar age and years of education.

Early follicularn=20

Midlutealn=17

p-Value

Age (years) 25.1 (3.3) 26.0 (3.3) .39Education (years) 18.3 (2.2) 18.4 (1.7) .81Estradiol (pg/ml) 2.6 (1.3) 3.7 (1.2) .02Progesterone (pg/ml) 61.1 (17.9) 221.5 (109.9) b .001

98 B. Derntl et al. / Hormones and Behavior 63 (2013) 97–104

de Waal, 2002; Singer and Lamm, 2009; Walter, 2012), but mostmodels differentiate between cognitive and affective empathy. Cogni-tive empathy refers to the ability to understand the feelings of others.It is very closely related to theory of mind (ToM), i.e. the ability torepresent and understand the mental states of others in general.Mentalizing about affective states of others is also called affectivetheory of mind—which is more or less synonymous with cognitiveempathy. Affective empathy refers to an affective response that is elic-ited by the perceived, imagined, or inferred affective state of anotherperson, which has also been called affect sharing or affective respon-siveness. In their comprehensive model, Decety and Jackson (2004)postulate that at least three core components of empathy can bederived: (1) recognition of emotions in oneself and others via facialexpressions, speech or behavior, (2) an affective component. i.e. theability to experience similar emotions as others while being consciousthat this is the simulation of the emotional feeling and it is not one'sown emotion (affective responsiveness), and (3) a cognitive compo-nent, i.e. to take the perspective of another person, though the distinc-tion between self and other remains intact (emotional perspectivetaking).

As shown above several studies investigated emotion recognitionacross the menstrual cycle and observed significant group differences,but no such study exists for emotional perspective taking or affectiveresponsiveness.

Hence, we examined whether menstrual cycle phase and sexhormone levels (estradiol and progesterone) are associated with thethree core components of empathy by comparing females duringthe early follicular phase with females during the midluteal phase oftheir menstrual cycle. Our aim was to analyze whether menstrualcycle phase is significantly related to empathy performance, thus higherorder emotional abilities. According to previous results (Derntl et al.,2008a,b; Guapo et al., 2009; Pearson and Lewis, 2005) we hypothesizedthat females during their follicular phase show better emotion recogni-tion performance due to a probably higher social sensitivity even in theearly follicular phase (Guapo et al., 2009; Macrae et al., 2002). More-over, we expected a significant menstrual phase group effect on theother two components, again with better performance of femalesduring the follicular phase.

Materials and methods

Sample

Forty right-handed healthy females aged 19–34 years (mean age25.3 years, SD=3.4) participated in the study. When contacted,female participants were asked about their menstrual cycle phaseand cycle duration and were then assigned a testing date. Onlyfemales who reported regular cycle duration (range: 25–35 days,M=29.0, SD=1.8) were included. Twenty females were in theirearly follicular phase (days 2–5 of menstrual cycle; low estradioland progesterone levels; FO), and the other 20 were in their midlutealphase (days 18–25 of menstrual cycle; high estradiol and progester-one levels, LU).

Participants were recruited by advertisements at the University ofVienna and the Medical University of Vienna, Austria. The female par-ticipants were screened for history of any psychiatric or mental disor-der by using the German version of the structured interview of DSMIV (SCID; Wittchen et al., 1997). Written informed consent wasobtained from all subjects prior to the examination.

Saliva samples

To obtain actual estradiol and progesterone levels saliva sampleswere collected on the day of testing. Saliva samples have beenshown to have great potential for studying ovarian hormone levelsas a reliable, feasible and non-invasive method (e.g., Gandara et al.,

2007). Due to the circadian secretion pattern of steroid hormonesall samples were collected between 10 am and 12 am. Furthermore,to exclude external hormone influences only females without oralcontraceptives or any hormone treatment were included. Beforewe started obtaining saliva samples we asked participants to washout their mouth with water. In order to obtain more representativemeasures, we collected saliva samples for each hormone every halfhour, thus we collected three samples per hormone in total (multiplesampling). For data analysis, the values were then averaged acrossthe three samples for each participant and these mean values wereused for further analyses. Participants were instructed to fill a smallplastic vial with at least 1.5 ml saliva (max. 3 ml) using a straw tostimulate saliva flow. Participants' collection vials were sealed aftereach collection and frozen immediately in accordance with previousresearch on sample storage (see Gröschl, 2008).

Saliva samples were analyzed by the European Institute for SalivaryAnalysis (Swiss Health Med, Aying, Germany) using an enzyme-linkedimmunoassay method from DRG (DRG Marburg, Germany; SalivaryEstradiol ELISA SLV-4188 and DRG Salivary Progesterone ELISASLV-2931). Analytical sensitivities (confidence interval 95%) were0.4 pg/ml (Estradiol) and 3.9 pg/ml (Progesterone). For estradiol,intra- and interassay coefficients were 3.8% and 2.6% respectively. ForProgesterone, intra- and interassay coefficients were 7.7% and 5.3%,respectively.

For details on hormone concentration and sociodemographic datasee Table 1.

Material

Emotion recognition

We used the Vienna Emotion Recognition Task—Shortversion(VERT-K) that consisted of 36 facial expressions of five basic emotions(anger, disgust, fear, happiness, and sadness) as well as neutralexpressions taken from a validated stimulus set (Gur et al., 2002).The instruction was to recognize the emotion depicted and a forced-choice answering format with all emotions and neutral was listedon the right side of the screen. The stimuli were balanced with respectto gender, age, intensity, valence, and brightness. All actors were Cau-casians and appeared only once. Facial expressions were presentedmaximally for 5 s and manual response triggered the next stimulus.Scores were calculated as the percent of items judged correctly andreaction times were assessed. The emotion recognition task isdescribed in more detail elsewhere (Derntl et al., 2008a) and hasbeen used in several studies of our group (e.g., Derntl et al., 2008a,2009, 2011; Seidel et al., 2010a,b).

Emotional perspective taking

Participants viewed 60 pictures each presented for 4 s depictingscenes showing two Caucasians involved in social interaction therebyportraying five basic emotions and neutral scenes (10 stimuli per

99B. Derntl et al. / Hormones and Behavior 63 (2013) 97–104

condition). The face of one person was masked and participants wereasked to infer the corresponding emotional expression of the maskedface that would fit the emotional situation. Responses were made byselecting between two different emotional facial expressions or aneutral expression presented after each scene. Facial alternativeswere taken from the same stimulus set described above. One optionwas correct and the other was selected at random from all otherchoices. Again, scores were calculated as percent of items judged cor-rectly and reaction times were assessed.

Affective responsiveness

We presented 150 short written sentences describing real-life sit-uations, which induced basic emotions (the same emotions asdescribed above), and situations that were emotionally neutral (25stimuli per condition). Participants were asked to imagine how theywould feel if they were experiencing those situations. Stimuli werepresented for 4 s and response format was the same as for emotionalperspective taking. Response format was kept maximally similaracross tasks allowing comparisons between tasks, i.e. differencescould be traced back to different task requirements not to differentresponse formats. Similar to both other tasks, percent correct andreaction times were calculated and used for data analysis.

Prior to the study, the stimuli of the emotional perspective takingand the affective responsiveness tasks were rated by 30 healthyadults and only those stimuli correctly identified by over 70% of thesample were included in the main study. Additionally, the emotionalperspective taking and affective responsiveness tasks have been usedin clinical studies (e.g., Derntl et al., 2009; Seidel et al., 2010a,b) andneuroimaging studies (Derntl et al., 2010, 2012).

To control for order effects, the tasks were presented in count-erbalanced order. Regarding behavioral performance, no gender differ-ences for the three tasks were observed in our previous studies.

Empathy questionnaires and neurocognitive tests

Three questionnaires measuring cognitive and affective empa-thy were administered: the Questionnaire Measure of EmotionalEmpathy (QMEE, Mehrabian and Epstein, 1972), the GermanQuestionnaire for Assessment of Empathy, Prosociality andAggression (FEPAA, Lukesch, 2006) and the German version ofthe Interpersonal Reactivity Index (IRI, Davis, 1983; Germanversion: Saarbrückener Persönlichkeitsfragebogen, SPF, Paulus,2009). In a previous study on gender differences in empathic abil-ities, we observed a significant effect for the SPF only, with femalesdescribing themselves as more empathic than males (Derntl et al.,2010), thereby supporting existing literature (e.g., Rueckert andNaybar, 2008). However, for both other self-report measures(QMEE, FEPAA), no significant gender difference emerged.

Moreover, to assess neuropsychological functioning, all partici-pants completed tests tapping crystallized verbal intelligence(Mehrfachwahl-Wortschatz-Test, MWT-B, Lehrl, 1996) and executivefunctions (Trail-Making-Test, TMT-A/-B, Reitan, 1956).

Data analysis

Statistical analyses were performed using SPSS 17.0 and level of sig-nificance was set at p=.05. Mean percent correct and reaction timeswere analyzed for each empathy task using repeated-measuresANOVAs with emotion as within-subject factor and group (FO vs. LU)as between-subject factors. For significant effects partial-eta squaresare listed as estimates of effect size. In cases of violations of sphericity,statistical tests involving the emotion factor employed Greenhouse–Geisser correction. All post hoc results were Bonferroni corrected.

Group differences in the empathy questionnaires and theneurocognitive tests were assessed using two sample t-tests. For

significant differences Cohen's d are listed as estimates of effectsize.

Pearson correlations (two-tailed) between accuracy measures ofthe empathy paradigms and self-report measures (SPF empathyscore, FEPAA empathy score, and QMEE) were computed.

Since progesterone levels were not normally distributed as testedwith the Kolmogorov–Smirnov test (FO group: p=.04, LU group: p=.32), we transformed the values taking the square root, which is anadequate tool to apply to right skewed data (Bortz, 1999). Thetransformed progesterone values then were normally distributed(FO group: p=.24, LU group: p=.50) and thus were entered intofurther analyses. Pearson correlations (two-tailed) were calculated toinvestigate the association of female sex hormone levels with empathicperformance and self-reportmeasures for each group separately. To ad-just for significant inter-hormonal correlations additional partial corre-lationswere calculated, controlling for estradiol/progesterone influenceon the correlations between performance and hormone levels, respec-tively. Moreover, estradiol/progesterone ratio was calculated and en-tered in the correlation analyses.

Results

Three females during their luteal phase were excluded since theirprogesterone and estradiol levels were out of range for luteal phase.Hence, final analysis was performed for 20 follicular and 17 lutealfemales.

Females of the two groups (FO vs. LU) did not differ in their age(t(35)=−0.87, p=.39), and education (t(35)=−0.25, p=.808),nor in the duration of their menses (t(35)=1.04, p=.31). However,FO and LU differed in their estradiol (t(35)=−2.36, p=.02) andprogesterone levels (t(35)=−6.72, pb .001), with higher values inthe LU group, thus indicating that their hormonal profiles differedsignificantly.

Empathy tasks

Emotion recognitionFor accuracy, the repeated measures ANOVA revealed a significant

emotion effect (F(3.80,133.11)=12.73, pb .001, part eta sq=.27) anda significant group effect (F(1,35)=4.33, p=.04, part-eta sq=.11),with higher accuracy in the FO group. However, no significantemotion-by-group interaction (F(3.80,133.11)=1.68, p=.16) oc-curred. Post hoc analysis of the significant emotion effect indicatedthat happy expressions were recognized significantly better thansad, disgust, and fear (all pb .001), and neutral expressions (p=.02)but no difference emerged to angry faces (p=.08).

For reaction times, analysis revealed a significant emotion effect(F(2.11,69.72)=10.09, pb .001, partial eta sq.=.23), but no significantgroup effect (F(1,35)=1.02, p=.32) and no significant emotion-by-group interaction (F(2.11,69.72)=0.53, p=.60). Post hoc analysis ofthe significant emotion effect demonstrated fastest reaction times forhappy faces (happy vs. sad: p=.01, happy vs. anger: p=.002, happyvs. fear/disgust: pb .001; happy vs. neutral: p=.04) followed by neu-tral, anger, disgust, sadness, and fear.

Emotional perspective takingAnalysis of accuracy revealed a significant emotion effect (F(3.74,

131.09)=23.24, pb .001, part-eta sq=.40), but no significant groupeffect (F(1,35)=2.11, p=.16), nor a significant emotion-by-groupinteraction (F(3.74, 131.09)=0.47, p=.75). Post hoc analysis of thesignificant emotion effect showed highest accuracy for happy condi-tions (happy vs. disgust/sad/anger/fear: pb .001; happy vs. neutral:p=.01) followed by neutral, sadness, anger, disgust and fearconditions.

Analysis of reaction times revealed a significant emotion effect(F(5,175)=20.05, pb .001, partial eta sq.=.36), no group effect

100 B. Derntl et al. / Hormones and Behavior 63 (2013) 97–104

(F(1,35)=2.07, p=.16) and no significant emotion-by-group interac-tion (F(5,175)=0.98, p=.43). Post hoc analysis of the significant emo-tion effect yielded fastest times for happy conditions (happy vs. anger/disgust/fear/neutral/sad: pb .001) followed by neutral, anger, sadness,disgust, and fear conditions.

Affective responsivenessFor accuracy, repeated measures analysis demonstrated a signifi-

cant emotion effect (F(3.55, 124.14)=35.23, pb .001, part-eta sq=.50), but no significant group effect (F(1,35)=0.28, p=.60) and nosignificant emotion-by-group interaction (F(3.55, 124.14)=0.76, p=.54). Post hoc analysis of the significant emotion effect demonstratedbest performance again for happy conditions (happy vs. anger/disgust/fear/sad: pb .001; happy vs. neutral: p=.01), followed by neutral, fear,disgust, sadness, and anger conditions.

Analysis of reaction times showed a significant emotion effect(F(3.66,128.08)=30.30, pb .001, partial eta sq.=.46), no significantgroup effect (F(1,35)=2.58, p=.12), but a significant emotion-by-group interaction (F(3.66,128.08)=7.94, pb .001, partial eta sq.=.19). Post hoc analysis of the significant emotion effect yielded fastesttimes for happy conditions (happy vs. anger/disgust/fear/sad:pb .001; happy vs. neutral: p=.02) followed by neutral, sadness,disgust, fear, and anger. Disentangling the significant emotion-by-group interaction, post hoc analyses revealed significant group differ-ences for reaction times to sad (p=.01) and angry stimuli (p=.01),always showing faster responses in females during the luteal phase,while no group differences emerged for the other comparisons(fear: p=.06, disgust: p=.53, happy: p=.68; neutral: p=.67).

Fig. 1 illustrates performance parameters (accuracy and reactiontimes) for the three empathy tasks for both groups and Table 2 listsmeans and p-values of the various ANOVAs (for the main effect ofphase).

Fig. 1. Recognition accuracy (a) and reaction times (b) with standard error of mean for then=17 females, LU). Data analysis yielded a significant group effect for emotion recognitionlicular phase marked with an asterisk. Moreover, analysis of reaction times for affective reangry stimuli (p=.02).

Empathy questionnaires and neurocognitive tests

Regarding the self-report measures of empathy, analysis of group ef-fects revealed no differences for any of the self-report measures (QMEE:t(35)=1.16, p=.26; SPF (fantasy: t(35)=0.66, p=.51; perspectivetaking: t(35)=0.30, p=.77; empathic concern: t(35)=−1.24, p=.22; personal distress: t(35)=−0.11, p=.91; empathy: t(35)=−0.74,p=.46); FEPAA: t(35)=−0.23, p=.82).

Moreover, regarding neurocognitive performance, groups did notdiffer in verbal crystallized intelligence (t(35)=0.32, p=.75), nor in ex-ecutive functions (TMT-A, t(35)=0.70, p=.49; TMT-B, t(35)=−0.96,p=.34).

Mean values of the questionnaire data and neurocognitive testsare given in Table 3.

Correlation analyses

Results of the correlation analyses between hormone levels andperformance in empathy tasks (total percent correct and mean reac-tion times) are listed in Table 4. Correlation analyses for FO revealedno significant association between hormone levels (estradiol orprogesterone) and behavioral performance (all p>.13). For LU, a sig-nificant negative correlation between progesterone levels and emo-tion recognition accuracy (r=−0.51, p=.04) and a significantpositive correlation between progesterone levels and affective re-sponsiveness accuracy (r=0.49, p=.05) emerged.

As estradiol and progesterone concentrations are often correlated,we conducted additional partial correlations to control for estradiolinfluence on the significant progesterone correlations in the LUgroup. For emotion recognition, partial correlation with progesteroneand emotion recognition performance controlling for estradiol revealeda marginally significant association (r=−0.49, p=.05), while the

separate empathy tasks for both groups (early follicular: n=20 females, FO; midluteal:accuracy (p=0.01), revealing better performance of the females during their early fol-sponsiveness revealed significantly faster responses of LU group for sad (p=.02) and

Table 2Mean values for accuracy (% correct) and reaction times (in seconds) of the threeempathy paradigms for each group and p-values as indicated by the repeated measuresANOVA (main effect group). Groups only differed in emotion recognition accuracy(marked with bold p-value).

Early follicularn=20

Midlutealn=17

p-value

Emotion recognition (%) 84.9% (6.5) 79.2% (3.9) .04Emotion recognition (rt) 3.4 s (0.8) 3.5 s (0.7) .32Emotional perspective taking (%) 88.2% (4.5) 85.4% (7.1) .16Emotional perspective taking (rt) 1.3 s (0.2) 1.2 s (0.2) .16Affective responsiveness (%) 90.7% (3.9) 91.2% (2.6) .60Affective responsiveness (rt) 1.0 s (0.2) 1.0 s (0.1) .12

Table 3Neurocognitive and self-report data showing mean values and standard deviation inparentheses. Groups showed similar neurocognitive performance and similar self-reports in empathy questionnaires.

Early follicularn=20

Midlutealn=17

p-Value

MWT-B (raw score) 28.2 (3.6) 27.7 (3.1) .75TMT-A (s) 19.3 (5.6) 18.2 (5.9) .49TMT-B (s) 34.8 (7.8) 38.3 (14.3) .34SPF empathy 46.0 (6.3) 47.5 (5.7) .46SPF fantasy 15.6 (3.4) 15.2 (2.8) .91SPF distress 10.8 (3.1) 9.9 (2.3) .32SPF perspective taking 15.4 (2.6) 15.8 (2.9) .68SPF empathic concern 15.3 (2.4) 16.4 (2.2) .12

QMEE 16.6 (4.2) 15.2 (2.7) .26FEPAA empathy 21.7 (3.4) 21.9 (2.6) .82

Note: MWT-B=Mehrfachwahl-Wortschatz-Test-B measures verbal intelligence, TMT-A =Trail-Making-Test A measures information processing speed, and TMT-B =Trail-Making-Test B measures cognitive flexibility; SPF = SaarbrückenerPersönlichkeitsfragebogen (German version of the Interpersonal Reactivity Index),QMEE = Questionnaire Measure for Emotional Empathy; FEPAA = German Ques-tionnaire for Assessment of Empathy, Prosociality and Aggression.

101B. Derntl et al. / Hormones and Behavior 63 (2013) 97–104

correlation for affective responsiveness and progesterone (controlledfor estradiol) remained similar (r=0.50, p=.05).

However, additional corollary analyses with the estradiol/progesterone ratio and performance parameters (% correct andreaction times for the three tasks) revealed no significant associa-tion between performance and hormone data neither for FO (allp> .13) nor for LU (p=.18).

The significant correlations are depicted in Fig. 2.Correlation analyses between self-report measures and task per-

formance showed a significant positive association between emotionrecognition accuracy and QMEE scores (r=0.38, p=.02), while noother correlation reached significance (all p>.11).

Table 4Results of the correlational analyses (two-tailed) between hormone concentration (estradio(% correct and reaction time, rt) for the three empathy tasks separately for each group (FO

ER % EPT %

Estradiol FO r=0.17,p=.48

r=0.24,p=.31

LU r=−0.30,p=.24

r=−0.36,p=.15

Progesterone FO r=−0.33,p=.16

r=0.19,p=.36

LU r=−0.51,p=.04

r=−0.29,p=.27

E:P ratio FO r=0.26,p=.27

r=0.01,p=.96

LU r=−0.08,p=.76

r=−0.32,p=.21

Note: ER = emotion recognition, EPT = emotional perspective taking, AR = affective resp

Discussion

In this study we demonstrated a significant association of menstrualcycle phase and ovarian hormone levels with specific components ofempathic behavior. More precisely, we observed significantly higheremotion recognition accuracy in females during their early follicularphase (FO group) compared to females during the midluteal phase (LUgroup), thereby supporting previous results (Derntl et al., 2008a,b) andpartly in accordance with existing literature (Guapo et al., 2009;Pearson and Lewis, 2005). Regarding reaction times, data analysisrevealed that females in the LU group showed faster responses thanthe other group in affective responsiveness to negative stimuli, specifi-cally sad and angry situations. Notably, emotion recognition perfor-mance showed a significant negative correlation with progesteronelevels, indicating better performance during phases of lower progester-one levels, however only in the LU group. Also in the LU group, proges-terone levels were positively associated with accuracy in the affectiveresponsiveness task, pointing to better performance with higher proges-terone levels. Against our expectations, we did not observe any groupdifference for emotional perspective taking or self-report empathy.

Taken together, these results suggest a variation in emotion recog-nition accuracy across the menstrual cycle but only a weaker or evenno association with the two other empathy components.

Besides the reported results for empathic abilities, females onlydiffered in their estradiol and progesterone levels, but showed similarneuropsychological performance and demographic variables.

Pearson and Lewis (2005) demonstrated that the ability tocorrectly recognize fearful faces varies across the menstrual cycle: fe-males during the preovulatory phase (highest estrogen level) showedthe highest accuracy for fear. In contrast, Guapo et al. (2009) ob-served significantly higher recognition accuracy for sad and angryfaces in early follicular females compared to midluteal females;females during the ovulatory phase demonstrated better fear recogni-tion than males. Moreover, a significant association of estrogen levelswith anger recognition, particularly male anger recognition, emerged.Hence, our results only partly support previous findings and differ-ences might be due to several methodological issues: 1) Pearsonand Lewis (2005) only indirectly inferred hormone levels via cyclephase without obtaining hormone samples, thus only a rough estima-tion of a hormone association was possible, 2) while we and Guapo etal. (2009) compared females during the early follicular phase andmidluteal phase, Pearson and Lewis measured females during variousstages of the menstrual cycle (menstruation, pre-ovulation, ovulation,and luteal), thus hormonal profiles of the follicular groups are different,3) similar to our study, Pearson and Lewis aswell as Guapo et al. (2009)relied on an explicit emotion recognition paradigm, however, bothstudies included surprised faces instead of neutral expressions aspresented in our study, and 4) Guapo and colleagues presented faces

l, transformed progesterone, estradiol:progesterone ratio) and performance parameters= follicular group; LU = luteal group). Significant correlations are marked in bold.

AR % ER rt EPT rt AR rt

r=−0.13,p=.59

r=0.35,p=.13

r=−0.28,p=.23

r=−0.01,p=.68

r=−0.20,p=.44

r=0.02,p=.93

r=0.16,p=.53

r=−0.25,p=.34

r=0.09,p=.72

r=−0.24,p=.30

r=−0.09,p=.71

r=0.14,p=.55

r=0.49,p=.05

r=0.44,p=.08

r=0.02,p=.95

r=−0.16,p=.54

r=−0.19,p=.43

r=0.37,p=.13

r=−0.01,p=.96

r=−0.27,p=.25

r=−0.33,p=.18

r=−0.20,p=.44

r=0.07,p=.79

r=0.12,p=.65

onsiveness.

Fig. 2. Correlation analyses revealed significant results for the LU group only: (a) for emotion recognition, a significant negative association between transformed progesteronelevels (pg/mL) and accuracy (r=−0.51, p=.04) occurred. (b) A marginally significant positive correlation between transformed progesterone levels and accuracy in affectiveresponsiveness (r=0.49, p=.05) emerged.

102 B. Derntl et al. / Hormones and Behavior 63 (2013) 97–104

only for 0.5 s and their emotional faces varied in intensities (from 10%to 100%), however, in the end only a total correct score was used foranalysis, thus it remains unclear how intensity levels influenced results.

It seems noteworthy that we were able to replicate previous find-ings from our group, where we also showed better emotion recogni-tion performance in females during the follicular phase compared tothe luteal phase for the third time (Derntl et al., 2008a,b), in a newand independent female sample. However, we were not able to repli-cate the significant correlation of progesterone levels with recogni-tion accuracy in both menstrual cycle groups. Nevertheless, takenour results and those from previous studies, variations in recognitionaccuracy across the menstrual cycle seem to be a reliable effect,though the underlying causality is less clear.

Results from Macrae et al. (2002) point out that females are moreinterested in social signals and interactions during the follicular phasewhen they are fertile and in better mood than during the luteal phase.Accordingly, they might also tend to exert more attention on emo-tional expressions as a basis for more successful interaction and gen-erally higher social competence which might already be observable inthe first days of the follicular phase as suggested by our results andresults from Guapo et al. (2009). Moreover, in a prior fMRI study(Derntl et al., 2008b), we showed that amygdala activation variesaccording to the menstrual cycle phase, with stronger activation dur-ing emotion recognition in the follicular phase. Hence, besides differ-ences in social interaction and mood states, differences in the neuralcorrelates might also underlie this finding.

Regarding affective responsiveness, we did not observe any groupdifferences for accuracy. However, we noted a significant differencefor reaction times, with faster responses to angry and sad stimuli inthe LU group compared to the FO group. Hence, despite similar accura-cy, females during the second half of the menstrual cycle demonstratefaster responsiveness and reactivity to certain emotionally negativestimuli. In our affective responsiveness task we asked females to putthemselves in a certain situation and then tell us how they wouldfeel. Hence, this is the only self-centered emotional task in our study.Thus, our findings may support results showing that females duringthe luteal phase are more reactive to social stress (Kirschbaum et al.,1999) and experience more intrusive recollections about negativeevents than females during the follicular phase (Ferree and Cahill,2009). Moreover, studies of daily moods reported higher negativemoods and depression scores during the luteal phase compared tothe follicular phase (Allen et al., 2009; Reed et al., 2008) which mighttrigger a mood-congruent bias as seen in females suffering from pre-menstrual dysphoric disorder (PMDD, Rubinow et al., 2007) or morefrequently reported in depressed patients (for review see Bourke etal., 2010) and in subjects at high-risk for depression (Watters andWilliams, 2011). However, we did not observe any difference in accu-racy nor a general facilitation effect or mood-congruent bias in emotionprocessing irrespective of the task requirements, i.e. better recognitionof or faster reaction times to angry/sad faces in the other tasks. Hence,we speculate that this faster responsiveness in the LU group might beemotion-dependent and specific to self-centered tasks where females

103B. Derntl et al. / Hormones and Behavior 63 (2013) 97–104

are asked about their mood or emotional states. Alternatively, anddespite unaffected reaction times in both other empathy tasks andneuropsychological tests (e.g. TMT), females of the FO group mightstruggle with a finer distinction between internal emotional states,reflected in the slower responses to sad and angry stimuli in the affec-tive responsiveness task. Thus, while females during the first half oftheir menstrual cycle are very sensitive to external emotional cues theymight show some difficulties in differentiating specific internal emotions.

To further evaluate these hypotheses, data from larger samples atvarious stages of the menstrual cycle are needed. Moreover, answer-ing formats presenting all emotions simultaneously would be favor-able, enabling a thorough error analysis and thereby may help toshed light on the underlying processes.

For emotional perspective taking, we did not observe any differ-ence across the menstrual cycle phase nor any correlation withhormone concentration and performance parameters (% correct andreaction times). While previous studies addressed the impact oftestosterone or oxytocin administration on cognitive empathy, morespecifically the ability to infer emotional states from the eye region(testosterone: Van Honk et al., 2011; oxytocin: Domes et al., 2007)or measured (neural) responses of synchronous vs. intrusive mothers(Atzil et al., 2011), this is the first study exploring the association ofestradiol and progesterone concentration with emotional perspectivetaking. Although we expected better performance of females duringthe first half of the menstrual cycle due to their suggested highersensitivity for social signals, emotional perspective taking does notseem to be associated with menstrual cycle phase or hormone con-centration to the same extent as e.g., emotion recognition. This lackof a significant hormonal association with perspective taking mightbe due to several reasons 1) we used a simple task design, particularlythe response format with only two choices given might not be sensi-tive enough to detect differences, 2) we did not investigate femalesduring their periovulatory phase where they are most fertile andmost interested in social signals (cf. Macrae et al., 2002), thuspreventing us to thoroughly investigate the impact of menstrualcycle phase on and the association of estradiol (unopposed by proges-terone) with this competency.

Notably, comparable to previous findings from our lab (Derntl etal., 2008a,b) we did not see a significant association of estrogen levelswith performance in empathy related tasks but instead our resultsagain show a significant correlation of progesterone with empathiccompetencies, i.e. facial affect recognition and affective responsive-ness, however only in the LU group. Accordingly, Conway et al.(2007) showed that females during their luteal phase with raisedprogesterone levels judged fearful and disgusted faces with avertedgaze as more intense than expressions with direct gaze, indicatingthat progesterone levels maymodulate emotional behavior. It has fre-quently been reported that mood is more negative during the lutealphase and we speculate that high progesterone levels might be linkedto a reduced sensitivity to certain social signals coming from others,such as emotional expressions, whereas mood-congruent or distressoriented stimuli concerning the self elicit increased responsivity(Kirschbaum et al., 1999).

Regarding the influence of progesterone on neural activation dur-ing emotion processing, van Wingen et al. (2008) showed that asingle dose of progesterone during the early follicular phase led toan increase in amygdala reactivity to threatening faces. Furthermore,in the same study authors report that progesterone increased func-tional coupling of the amygdala with the medial prefrontal cortex(mPFC), indicating that progesterone influences the communicationbetween the amygdala and mPFC, hence, two key regions regardingemotion processing and empathy. However for emotional memory,decreased amygdala activity during the memorization of happy andneutral faces after a single dose of progesterone was observed (vanWingen et al., 2007). Moreover, Derntl et al. (2008b) report decreasedamygdala activation during emotion recognition in females during

the luteal phase compared to the follicular phase. Taken togetherthese data suggest that the influence of progesterone on amygdalareactivity is task- and probably dose-dependent (for review see vanWingen et al., 2011). Multiple studies indicate that progesteroneand the progesterone derivative allopregnanolone have significantmodulatory effects upon neurotransmitter systems involved in theregulation of affect and behavior such as serotonin and noradrenalin(e.g. Bethea et al., 1998; Epperson et al., 1999). Interestingly regard-ing negative mood, allopregnanolone seems to exert a paradoxicaleffect mediated via the GABA-A receptor probably causing higher ex-citability of some brain regions (e.g., Bäckström et al., 2011). Since wedid not assess neural activation or experimentally administer proges-terone, we can only speculate about the underlying associations. Fu-ture neuroimaging studies that explore how progesterone affectsthe neural correlates of a broader spectrum of social–emotional abil-ities are mandatory to further highlight the impact of menstrual cyclephase and sex hormone concentration on the neural basis of emotion-al behavior.

While this study provides new insight into the relation of menstrualcycle phase and thus ovarian hormones with emotional competencies,i.e. empathic behavior, several methodological constraints have to beconsidered: besides the small sample we did not examine empathicabilities in a longitudinal approach investigating females at variousstages during the menstrual cycle to analyze intra-individual differ-ences. However, groups are well matched for various neuropsycholog-ical parameters and were carefully screened as well as selected, hencewe are convinced that the results presented in this manuscript are rep-resentative. Future studies exploring behavioral and neural correlatesof empathic abilities and emotional competencies should includefemales during the periovulatory phase where conception risk is highto better characterize any association of cycle phase and ovarian hor-mones with emotional behavior.

We did not examine women using hormone contraceptives, sincethis external hormone intake might alter emotion processing. How-ever, investigating the effect and alterations of oral contraceptiveson neural activation and emotional performance would be of high in-terest, as the number of females taking oral contraceptives is steadilyrising and short- as well as long-term effects on neural activation andperformance are still unclear (Kurshan and Neill Epperson, 2006).Recently, Pletzer et al. (2010) reported a significant correlation ofthe volume of the parahippocampal gyrus with duration of oral con-traceptive intake. Hence, investigating the effect and alterations oforal contraceptives on cognitive and social–emotional competenciesas well as the underlying neural correlates is of high interest.

Due to the fact that we only investigated females, interaction ofgender and hormone levels and their association with empathicbehavior were not examined. However, investigation of hormonal in-fluences has important implications for the understanding of gender-specific emotional functioning, thus probably helps to further charac-terize previously reported gender differences in the neural correlatesof empathic abilities (e.g., Derntl et al., 2010; Li et al., 2008;Schulte-Rüther et al., 2008).

Conclusions

We conclude that menstrual cycle phase and progesterone con-centration are only associated with specific components of empathyand not a broader spectrum of emotional competencies. Despitesignificantly reduced emotion recognition accuracy, we observed nogroup difference for perspective taking but faster affective respon-siveness to negative stimuli, i.e. angry and sad situations, during theluteal phase. Moreover, emotion recognition accuracy correlatedwith progesterone levels in the LU group, indicating better perfor-mance in females with lower progesterone levels. And, progesteronelevels were also positively associated with affective responsiveness,suggesting better performance with higher progesterone levels in

104 B. Derntl et al. / Hormones and Behavior 63 (2013) 97–104

the LU group. Thus, our findings suggest the possibility that elevatedprogesterone levels facilitate responsivity to distressing situationsconcerning the self i.e. internal emotions, while inhibiting facial affectrecognition, thus emotional expressions from others i.e. externalemotions. Summarizing, our data underline that emotion recognitionperformance is better during the first phase of the menstrual cycleand females during the luteal phase may be faster in responsivenessto negative emotions, but no group difference was observed for emo-tional perspective taking.

Acknowledgments

BD and UH were supported by the German Research Foundation(DFG, IRTG 1328, KFO 112, Ha3202/7-2). BD, IKE and UH were alsosupported by the Austrian Science Fund (FWF P23533). UH wasfurther supported by the Interdisciplinary Centre for ClinicalResearch (IZKF) within the Faculty of Medicine at the RWTH AachenUniversity (TV N70, VV N68-j), the Federal Ministry of Educationand Research (BMBF: FKZ 01GW0751) as well as the HelmholtzAlliance (016W0751). None of these funding institutions had afurther role in study design; the collection, analysis and interpreta-tion of data; in the writing of the report; and in the decision tosubmit the paper for publication.

References

Allen, S.S., Allen, A.M., Pomerleau, C.S., 2009. Influence of phase-related variability inpremenstrual symptomatology, mood, smoking withdrawal, and smoking behaviorduring ad libitum smoking, on smoking cessation outcome. Addict. Behav. 34,107–111.

Atzil, S., Hendler, T., Feldman, R., 2011. Specifying the neurobiological basis of humanattachment: brain, hormones, and behavior in synchronous and intrusive mothers.Neuropsychopharmacology 36, 2603–2615.

Bäckström, T., Haage, D., Löfgren, M., Johansson, I.M., Strämberg, J., Nyberg, S., Andréen,L., Ossewaarde, L., vanWingen, G.A., Turkmen, S., Bengtsson, S.K., 2011. Paradoxicaleffects of GABA-A modulators may explain sex steroid induced negative moodsymptoms in some persons. Neuroscience 191, 46–54.

Bethea, C.L., Pecins-Thompson, M., Schutzer, W.E., Gundlah, C., Lu, Z.N., 1998. Ovariansteroids and serotonin neural function. Mol. Neurobiol. 18, 87–123.

Bortz, J., 1999. Statistik für Sozialwissenschafter. Springer, Berlin.Boulware, M.I., Kent, B.A., Frick, K.M., 2011. The impact of age-related ovarian hormone

loss on cognitive and neural function. Curr. Top. Behav. Neurosci. http://dx.doi.org/10.1007/7854_2011_122.

Bourke, C., Douglas, K., Porter, R., 2010. Processing of facial emotion expression inmajor depression: a review. Aust. N. Z. J. Psychiatry 44, 681–696.

Conway, C.A., Jones, B.C., DeBruine, L.M., Welling, L.L.M., Law Smith, M.J., Perrett, D.I.,Sharp, M.A., Al-Dujaili, E.A.S., 2007. Salience of emotional displays of danger andcontagion in faces is enhanced when progesterone levels are raised. Horm.Behav. 51, 202–206.

Davis, M.H., 1983. The effects of dispositional empathy on emotional reactions andhelping: a multidimensional approach. J. Pers. 51, 167–184.

Decety, J., Jackson, P.L., 2004. The functional architecture of human empathy. Behav.Cogn. Neurosci. Rev. 3, 71–100.

Derntl, B., Kryspin-Exner, I., Fernbach, E., Moser, E., Habel, U., 2008a. Emotion recognitionaccuracy in healthy young females is associated with cycle phase. Horm. Behav. 53,90–95.

Derntl, B., Windischberger, C., Robinson, S., Lamplmayr, E., Kryspin-Exner, I., Gur, R.C.,Moser, E., Habel, U., 2008b. Facial emotion recognition and amygdala activation areassociated with menstrual cycle phase. Psychoneuroendocrinology 33, 1031–1040.

Derntl, B., Finkelmeyer, A., Toygar, T.K., Hülsmann, A., Schneider, F., Falkenberg, D.I.,Habel, U., 2009. Generalized deficit in all core components of empathy in schizo-phrenia. Schizophr. Res. 108, 197–206.

Derntl, B., Finkelmeyer, A., Eickhoff, S., Kellermann, T., Falkenberg, D.I., Schneider, F.,Habel, U., 2010. Multidimensional assessment of empathic abilities: neural corre-lates and gender differences. Psychoneuroendocrinology 35, 67–82.

Derntl, B., Seidel, E.-M., Eickhoff, S.B., Kellermann, T., Gur, R.C., Schneider, F., Habel, U.,2011. Neural correlates of social approach and withdrawal in patients with majordepression. Soc. Neurosci. http://dx.doi.org/10.1080/17470919.2011.579800.

Derntl, B., Finkelmeyer, A., Voss, B., Eickhoff, S.B., Kellermann, T., Schneider, F., Habel,U., 2012. Neural correlates of the core facets of empathy in schizophrenia.Schizophr. Res. 136, 70–81.

Domes, G., Heinrichs, M., Michel, A., Berger, C., Herpertz, S.C., 2007. Oxytocin improves"mind-reading" in humans. Biol. Psychiatry 61, 731–733.

Epperson, C.N., Wisner, K.L., Yamamoto, B., 1999. Gonadal steroids in the treatment ofmood disorders. Psychosom. Med. 61, 676–697.

Ferree, N.K., Cahill, L., 2009. Post-event spontaneous intrusive recollections andstrength of memory for emotional events in men and women. Conscious.Cogn. 18, 126–134.

Gandara, B.K., Leresche, L., Mancl, L., 2007. Patterns of salivary estradiol and progesteroneacross the menstrual cycle. Ann. N. Y. Acad. Sci. 1098, 446–450.

Gröschl, M., 2008. Current status of salivary hormones analysis. Clin. Chem. 54,1759–1769.

Guapo, V.G., Graeff, F.G., Zani, A.C.T., Labate, C.M., dos Reis, R.M., Del-Ben, C.M., 2009.Effects of sex hormonal levels and phases of the menstrual cycle in the processingof emotional faces. Psychoneuroendocrinology 34, 1087–1094.

Gur, R.C., Radim, S., Hagendoorn, M., Marom, O., Hughett, P., Macy, L., Turner, T., Bajcsy, R.,Posner, A., Gur, R.E., 2002. A method for obtaining 3-dimensional facial expressionsand its standardization for use in neurocognitive studies. J. Neurosci. Methods 115,137–143.

Hines, M., 2010. Sex-related variation in human behavior and the brain. Trends Cogn.Sci. 14, 448–456.

Kirschbaum, C., Kudielka, B.M., Gaab, J., Schommer, N.C., Hellhammer, D.H., 1999.Impact of gender, menstrual cycle phase, and oral contraceptives on the activityof the hypothalamus–pituitary–adrenal axis. Psychosom Med. 61, 154–162.

Kurshan, N., Neill Epperson, C., 2006. Oral contraceptives and mood in women withand without premenstrual dysphoria: a theoretical model. Arch. Womens Ment.Health 9, 1–14.

Lehrl, S., 1996. Der MWT- ein Intelligenztest für die ärztliche Praxis. Prax. Neurol.Psychiatr. 7, 488–491.

Li, H., Yuan, J., Lin, C., 2008. The neural mechanism underlying the female advantage inidentifying negative emotions: an event-related potential study. NeuroImage 40,1921–1929.

Lukesch, H., 2006. FEPAA. Fragebogen zur Erfassung von Empathie, Prosozialität,Aggressionsbereitschaft und aggressivem Verhalten. Beltz, Göttingen.

Macrae, C.N., Alnwick, K.A., Milne, A.B., Schloerscheidt, A.M., 2002. Person perceptionacross the menstrual cycle: hormonal influences on social-cognitive functioning.Psychol. Sci. 13, 532–536.

Mehrabian, A., Epstein, N., 1972. A measure of emotional empathy. J Pers. 40, 525–543.Paulus, C., 2009. Der Saarbrückener Persönlichkeitsfragebogen SPF (IRI) zur Messung

von Empathie: Psychometrische Evaluation der deutschen Version des Interper-sonal Reactivity Index. http://psydok.sulb.uni-saarland.de/volltexte/2009/2363/.

Pearson, R., Lewis, M.B., 2005. Fear recognition across the menstrual cycle. Horm.Behav. 47, 267–271.

Pletzer, B., Kronbichler, M., Aichhorn, M., Bergmann, J., Ladurner, G., Kerschbaum, H.H.,2010. Menstrual cycle and hormonal contraceptive use modulate human brainstructure. Brain Res. 1348, 55–62.

Preston, S.D., de Waal, F.B., 2002. Empathy: its ultimate and proximate bases. Behav.Brain Sci. 25, 1–71.

Reed, S.C., Levin, F.R., Evans, S.M., 2008. Changes in mood, cognitive performance andappetite in the late luteal and follicular phases of the menstrual cycle in womenwith and without PMDD (premenstrual dysphoric disorder). Horm. Behav. 54,185–193.

Reitan, R.M., 1956. Trail Making Test: Manual for Administration, Scoring and Interpre-tation. Indianapolis.

Rubinow, D.R., Smith, M.J., Schenkel, L.A., Schmidt, P.J., Dancer, K., 2007. Facial emotiondiscrimination across the menstrual cycle in women with premenstrual dysphoricdisorder (PMDD) and controls. J. Affect. Disord. 104, 37–44.

Rueckert, L., Naybar, N., 2008. Gender differences in empathy: the role of the righthemisphere. Brain Cogn. 67, 162–167.

Schulte-Rüther, M., Markowitsch, H.J., Shah, N.J., Fink, G.R., Piefke, M., 2008. Genderdifferences in brain networks supporting empathy. NeuroImage 42, 393–403.

Seidel, E.-M., Habel, U., Finkelmeyer, A., Schneider, F., Gur, R.C., Derntl, B., 2010a.Implicit and explicit behavioral tendencies inmale and female depression. PsychiatryRes. 177, 124–130.

Seidel, E.-M., Habel, U., Kirschner, M., Gur, R.C., Derntl, B., 2010b. The impact of facialemotional expressions on behavioral tendencies in women and men. J. Exp. Psychol.Hum. Percept. Perform. 36, 500–507.

Singer, T., Lamm, C., 2009. The social neuroscience of empathy. Ann. N. Y. Acad. Sci.1156, 81–96.

van Honk, J., Schutter, D.J., Bos, P.A., Kruijt, A.-W., Lentjes, E.G., Baron-Cohen, S., 2011.Testosterone administration impairs cognitive empathy in women depending onsecond-to-fourth digit ratio. Proc. Natl. Acad. Sci. U. S. A. 108, 3448–3452.

van Wingen, G., van Broekhoven, F., Verkes, R.J., Peteresson, K.M., Bäckström, T.,Buitellaar, J., Fernandez, G., 2007. How progesterone impairs memory for biologicallysalient stimuli in healthy young women. J. Neurosci. 27, 11416–11423.

Van Wingen, G., van Broekhoven, F., Verkes, R.J., Petersson, K.M., Bäckström, T.,Buitelaar, J.K., Fernandez, G., 2008. Progesterone selectively increases amygdalareactivity in women. Mol. Psychiatry 13, 325–333.

Van Wingen, G.A., Ossewaarede, L., Bäckström, T., Hermans, E.J., Fernández, G., 2011.Gonadal hormone regulation of the emotion circuitry in humans. Neuroscience191, 38–45.

Vincent, K., Tracey, I., 2010. Sex hormones and pain: the evidence from functionalimaging. Curr. Pain Headache Rep. 14, 396–403.

Walter, H., 2012. Social cognitive neuroscience of empathy: concepts, circuits, andgenes. Emot. Rev. 4, 9–17.

Watters, A.J., Williams, L.M., 2011. Negative biases and risk for depression; integratingself-report and emotion task markers. Depress. Anxiety 28, 703–718.

Wittchen, H.-U., Zaudig, M., Fydrich, T., 1997. Strukturiertes Klinisches Interview fürDSM-IV. Hogrefe, Göttingen.