Social Neuroscience
ISSN: 1747-0919 (Print) 1747-0927 (Online) Journal homepage: http://www.tandfonline.com/loi/psns20
The mediation effect of menstrual phase on
negative emotion processing: Evidence from N2
Haiyan Wu, Chunping Chen, Dazhi Cheng, Suyong Yang, Ruiwang Huang,
Stephanie Cacioppo & Yue-Jia Luo
To cite this article: Haiyan Wu, Chunping Chen, Dazhi Cheng, Suyong Yang, Ruiwang Huang,
Stephanie Cacioppo & Yue-Jia Luo (2014) The mediation effect of menstrual phase on
negative emotion processing: Evidence from N2, Social Neuroscience, 9:3, 278-288, DOI:
10.1080/17470919.2014.886617
To link to this article: http://dx.doi.org/10.1080/17470919.2014.886617
Published online: 03 Mar 2014.
Submit your article to this journal
Article views: 159
View related articles
View Crossmark data
Citing articles: 3 View citing articles
Full Terms & Conditions of access and use can be found at
http://www.tandfonline.com/action/journalInformation?journalCode=psns20
Download by: [Institute of Psychology ]
Date: 30 November 2015, At: 00:28
SOCIAL NEUROSCIENCE, 2014
Vol. 9, No. 3, 278–288, http://dx.doi.org/10.1080/17470919.2014.886617
The mediation effect of menstrual phase on negative
emotion processing: Evidence from N2
Haiyan Wu1, Chunping Chen2, Dazhi Cheng3, Suyong Yang4, Ruiwang Huang5,
Stephanie Cacioppo6, and Yue-Jia Luo7
Downloaded by [Institute of Psychology ] at 00:28 30 November 2015
1
Key Laboratory of Behavioral Science, Institute of Psychology, Chinese Academy of Sciences,
Beijing, China
2
Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences,
Beijing, China
3
State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University,
Beijing, China
4
Key Laboratory of Exercise and Health Sciences of Ministry of Education, Shanghai University
of Sport, Shanghai, China
5
Center for Studies of Psychological Application, Guangdong Key Laboratory of Mental Health
and Cognitive Science, School of Psychology, South China Normal University, Guangzhou,
China
6
High Performance Electrical Neuroimaging Laboratory, University of Chicago, Chicago, USA
7
Institute of Affective and Social Neuroscience, Shenzhen University, Shenzhen, Guangdong,
China
Numerous studies have shown a ‘negativity bias’ in emotion processing and effect of menstrual phase on emotion
processing. Most of these results, however, did not match the arousal of different types of stimuli. The present study
examined the time course of negative emotion processing across different menstrual phases (e.g., late luteal/premenstrual phase and follicular phase) when the arousal level of negative and neutral stimuli was equal. Following
previous studies, an oddball paradigm was utilized in present study. Participants viewed neutral and negative (highly
(HN) and moderately negative (MN)) stimuli with matched arousal and were asked to make deviant vs. standard
judgments. The behavioral results showed a higher accuracy for HN stimuli than neutral stimuli, and the other
comparisons were not significant. The major event-related potential (ERP) finding was that N2 amplitude was larger
for MN than neutral in the late luteal phase, whereas such difference was absent during the follicular phase. Moreover,
The N2 for HN stimuli was larger in late luteal phase than in follicular phase. Therefore, female may be with higher
sensitivity to MN stimuli during late luteal phase than during follicular phase when the arousal of stimuli was well
controlled. These results provide additional insight to premenstrual affective syndrome and affective disorder.
Keywords: Menstrual phase; Negative emotion; ERP.
Correspondence should be addressed to: Yue-Jia Luo, Institute of Affective and Social Neuroscience, Shenzhen University, Nanhai Ave
3688, Nanshan District, Shenzhen, Guangdong, China. E-mail: luoyj@bnu.edu.cn
We acknowledge Dr Jiajin Yuan giving valuable suggestions on our revision. And, the author also wants to thank Dr Qingqing Qu for her
suggestions on the manuscript. This research was supported by the 973 Program [2014CB744603], the foundation of National Key Lab of
Human Factors Engneering [HF2012-K-03], National Basic Research Program of China [2011CB711000], NSFC [91132704], and the
Fundamental Research Funds for the Central Universities [2012YBXS01].
Haiyan Wu and Chunping Chen contribute equally to the work.
This article was originally published with errors. This version has been corrected. Please see Corrigendum http://dx.doi.org/10.1080/
17470919.2014.903103
© 2014 Taylor & Francis
Downloaded by [Institute of Psychology ] at 00:28 30 November 2015
MENSTRUAL PHASE AND NEGATIVE EMOTION
Numerous behavioral studies indicate a ‘negativity
bias’ in emotion processing such that people show
faster and more prominent responses to negative
than nonnegative stimulus or events (Hansen &
Hansen, 1988; Mogg & Bradley, 1998; Mogg et al.,
2000; Peeters & Czapinski, 1990; Taylor, 1991;
Wentura, Rothermund, & Bak, 2000). A growing
body of event-related potential (ERP) studies also
supports such negativity bias (Carretié, Iglesias, &
Garcı́a, 1997; Carretié, Mercado, Tapia, & Hinojosa,
2001; Huang & Luo, 2006; Ito, Larsen, Smith, &
Cacioppo, 1998; Smith, Cacioppo, Larsen, &
Chartrand, 2003; Stewart et al., 2010; Yuan et al.,
2007), with larger amplitude late positive brain potentials for negative as compared with positive stimuli,
even though both were equally arousing (e.g., Ito
et al., 1998). All in all these results provide support
for ‘the hypothesis that the negativity bias in affective
processing occurs as early as the initial categorization
into valence classes’ (Ito et al., 1998, p. 887).
Interestingly, behavioral and brain research on
negative affects and gender differences also shows a
greater sensitivity to negative information in women
as compared with men (Campanella et al., 2004;
Fujita, Diener, & Sandvik, 1991; Hall & Matsumoto,
2004; Hamann, 2005; Ladavas, Umiltà, & Ricci-Bitti,
1980; Rotter & Rotter, 1988). Specifically, women are
faster and better in identifying negative emotions than
men (Li, Yuan, & Lin, 2008; Montagne, Kessels,
Frigerio, de Haan, & Perrett, 2005; Smith et al.,
2003). Based on these findings and previous studies
on menstrual cycle and emotions and cognition
(Dietrich et al., 2001; Hatta & Nagaya, 2009; Maki
& Resnick, 2001; Scher, Pionk, & Purcell, 1981;
Weis, Hausmann, Stoffers, & Sturm, 2011), one may
assume that the gender difference observed in the
processing of negative emotions is governed (or at
least modulated) by sex hormones.
Regarding the association between menstrual cycle
and negative emotion, previous behavioral studies
have shown that the processing of negative emotions
may be affected by the menstrual cycle. For instance,
in an emotional expressions recognition study, women
were significantly more accurate in fear expression
recognition at the preovulatory surge (highest estrogen
levels) than during their menstruation period (Pearson
& Lewis, 2005). Another emotion recognition study
also demonstrated a menstrual phase effect such that
follicular group showed higher accuracy in facial
emotion recognition than luteal group (Derntl,
Kryspin-Exner, Fernbach, Moser, & Habel, 2008).
Similarly, in an emotional face identification task,
women in early follicular phase showed significantly
higher accuracy in identifying anger, sad, and fear
279
emotion than women in luteal phase (Guapo et al.,
2009). Nevertheless, study indicated that women with
premenstrual dysphoric disorder (PMDD) showed
stronger physiologic response to aversive stimulus
during the luteal compared to follicular phase
(Epperson et al., 2007).
Neuroimaging studies have identified similar results
during different phases of the menstrual cycle. For
instance, in women, the follicular phase has been associated with a greater amygdala activity (Derntl,
Windischberger, et al., 2008) in response to both negative and positive stimuli compared to neutral stimulus.
As an important neural network underlying social emotion processing, the orbitofrontal cortex (OFC) activation was modulated across the menstrual cycle as well
(Protopopescu et al., 2005). Specifically, compared with
neutral stimuli, OFC to negative or positive stimuli
showed greater responses during premenstrual phase in
medial regions, whereas greater response during the
postmenstrual phase in lateral regions. However, brain
image study also showed that hippocampus and amygdala activity to emotional stimuli was stronger during
mid-luteal phase, which may due to the higher levels of
progesterone (Andreano & Cahill, 2010). Goldstein
et al. (2005) found that amygdala, OFC and anterior
cingulate cortex (ACC) activity was stronger in
response to negative stimuli processing during the
early follicular phase than late follicular phase. Other
studies confirmed the mediation effect of menstrual
cycle on negative emotion processing and suggested
that the hormonal variation during menstrual cycle
might modulate the HPA activity, which regulates the
emotion arousal responses (Goldstein, Jerram, Abbs,
Whitfield-Gabrieli, & Makris, 2010). These results
reveal the difference of negative emotion-related behavioral or brain response during different menstrual cycle
phases. However, most of these functional magnetic
resonance imaging (fMRI) studies did not match the
arousal of different types of stimuli (Amin, Epperson,
Constable, & Canli, 2006; Andreano & Cahill, 2010;
Derntl, Windischberger, et al., 2008; Pearson & Lewis,
2005), which means the result could be attribute to the
arousal difference between negative and neutral stimulus but not the valence effect. According to the dimension theory of emotion, arousal is another different
emotion dimension, which needs to be controlled in
valence-related studies (Lang, 1995; Lawton, Kleban,
Rajagopal, & Dean, 1992; Lewis, Critchley, Rotshtein,
& Dolan, 2007). Thus, we cannot infer whether the
menstrual cycle regulate the response to emotional
valence or arousal. ERP result may provide further
time course information for the interaction between
menstrual cycle and negative emotion processing since
previous studies have demonstrated that the valence
Downloaded by [Institute of Psychology ] at 00:28 30 November 2015
280
WU ET AL.
effect modulated early ERPs (usually before 300 ms),
while the arousal effects observed for later components
(Codispoti, Ferrari, & Bradley, 2007; Olofsson, Nordin,
Sequeira, & Polich, 2008).
ERP studies have identified ERP components
modulated by the valence of emotion (Carretié et al.,
2001; Carretié, Hinojosa, Martín-Loeches, Mercado,
& Tapia, 2004; Huang & Luo, 2006) and provided
considerable evidence for gender difference in negative emotion processing. For instance, data from ERP
study which controlled the arousal level showed the
valence effect on N2 and P3 (Li et al., 2008; Yuan
et al., 2007, 2009; Yuan, Yang, Chen, Meng, & Li,
2010). Specifically, the N2 was largest under the
extremely negative condition compared with moderately negative (MN) and neutral stimuli. The valence
effect on N2 was considered as more attentional
resource allocation to negative stimuli in the early
phase (Yuan et al., 2007). Further valence effect was
found in subsequent P3 component, which indicated
that negative stimuli were associated with smaller P3
in implicit emotion task. That is, the smaller P3
reflects the inhibition process under negative condition in implicit emotion task (Yuan et al., 2007).
Overall, such two ERP components may provide us
more information about the modulation effect of menstrual cycle on negative emotion processing.
From the evolutionary point of view, women during
their follicular phase are with higher reproduction
ability and may with higher sensitivity to social–
emotion information for mating behavior (Derntl,
Windischberger, et al., 2008; Macrae, Alnwick, Milne,
& Schloerscheidt, 2002; Pearson & Lewis, 2005).
Previous studies on premenstrual syndrome, however,
suggest that the sensitivity to negative emotions may
exist before the menstrual phase (Miller & Miller,
2001; Rubinow & Schmidt, 2006; Woods, Most, &
Dery, 1982). Thus, there is a real need to understand
whether women have a higher sensitivity to negative
emotions in follicular phase or in late luteal phase/
premenstrual phase. This question is of critical importance as it might help to shed light on clinical premenstrual behaviors. The menstrual cycle phase is
correlated with the suicide behavior (Baca-Garcia,
Sanchez-Gonzalez, Gonzalez Diaz-Corralero, Garcia,
& de Leon, 1998; Saunders & Hawton, 2006). For
example, an investigation showed that 65% of the
suicide behavior occurs in pre- or during menstrual
phase (Baca-Garcia et al., 1998).
To test whether women process negative emotions
differently as a function of their menstrual phases
(when the affective arousal was controlled), we utilized ERP technique and a standard/deviant categorization task following previous studies (Li et al.,
2008; Yuan et al., 2007). We expected a larger frontal
N2 and smaller P3 component to more negative trials
and hypothesized that the menstrual effect on negative
emotion link to the N2 or P3 amplitude shift with the
menstrual cycle. Furthermore, to address the possibility of difference between highly negative (HN) and
MN information processing during different menstrual
cycle phases, we utilized HN, MN, and neutral stimulus and examine the effect of menstrual phases on
brain potential response.
METHODS
Participants
Sixteen right-handed healthy female students (mean
age = 22.4, SD = 4.8) participated in present study
and finished the ERP recordings in both the phases.
No participant was using oral contraceptives or psychoactive medication. To control the cycle individual
difference, participants finished an inquiry to make
sure all of them were with normal menstrual cycle
(i.e., the mean cycle days was 28 ± 2 days) in the last
two years before formal recruited. Each woman was
tested once during the late luteal phase/premenstrual
phase (days 2–3 before the onset of menses: M = 2.54
days, SD = 0.78) and once during the follicular phase
(days 6–10 after the onset of menses: M = 8.62 days,
SD = 1.85). To avoid the test–retest effect, half of the
participants performed the first ERP test in their luteal
phase and the other half in the follicular phase.
All participants were recruited through public
advertisement and with no history of neurological,
psychiatric illness and denied hormone using. All
procedures were approved by the institutional review
boards (IRBs) of Institute of Psychology, Chinese
Academy of Sciences. Participants signed the
informed consent before the experiment and were
paid after the study.
Stimuli and the control of stimuli
arousal
One neutral natural scene of cup was selected as the
frequent standard stimuli, which with 70% presentation
possibility. The deviants in the modified oddball task
totally consist of 60 black-and-white photographs,
which were selected from the Chinese Affective
Picture System (CAPS). In CAPS, each material was
evaluated by more than 500 hundred Chinese subjects
and provide the rating sores including valence, arousal
and dominance etc., on a nine-point scale.10 HN, 10
MENSTRUAL PHASE AND NEGATIVE EMOTION
TABLE 1
The emotional valence and arousal of experiment materials
(Mean ± SD)
Phase
Downloaded by [Institute of Psychology ] at 00:28 30 November 2015
Valence Late luteal phase
Follicular phase
Arousal Late luteal phase
Follicular phase
HN
2.11 ± 0.41
2.23 ± 0.47
5.23 ± 0.42
5.45 ± 0.42
MN
3.57
3.60
5.29
5.47
±
±
±
±
0.52
0.57
0.39
0.39
Neutral
5.34
5.39
5.59
5.39
±
±
±
±
0.73
0.80
0.35
0.36
MN, and 10 neutral pictures were used as deviant stimuli in the task of late luteal phase/premenstrual phase
and 30 pictures (10 HN, 10 MH, and 10 Neutral) were
used in the follicular phase.
To confirm the controlling of arousal dimension,
we conducted one-way ANOVA to the arousal rating
of pictures in three conditions (HN, MN, and Neutral)
during late luteal and follicular phases, respectively.
The main effect of arousal was not significant in the
late luteal phase (p = .19) and follicular phase
(p = .70). In the other hand, the ANOVA on valence
rating confirmed the valence manipulation such that a
significant emotion valence main effect was found in
the late luteal phase (p < .001) and follicular phase as
well (p < .001). Specifically, HN pictures were more
negative than MN pictures, and MN pictures were
more negative than neutral pictures (see Table 1). To
test the material matching in two menstrual cycles, the
ANOVA on emotion valence of pictures showed the
phase effect was not significant, F (1, 29) = 0.57,
p = .45. Also, the emotional arousal of pictures
between two phases was not significant either, F (1,
29) = 1.28, p = .26. Overall, the valence factor was
quantified by higher negative valence in HN than MN,
and also significant higher negative for MN than
neutral pictures. Importantly, the controlling of
valence was quantified by no significant difference
among HN, MN, and neutral pictures (See Table 1).
Affective assessment
To exclude the impact of mood disorder such as premenstrual mood disorders, each participant was
required to fill out questionnaires in both first and
second experiment. Questionnaires included Profile
of Mood States (POMS), the Positive and Negative
Affect Schedule (PANAS; Watson, Clark, & Tellegen,
1988), Beck Depression Inventory (BDI), and State
Anxiety Inventory (SAI). All subjects entering the
final data analysis showed no significant difference
in all these scores between first and second experiments. For all the 16 subjects, the t-test showed there
281
was no significant difference between the two cycle
phases in POMS (t (15) = 0.91, p = .37), the PANAS
(t (15) = 0.58, p = .57), BDI (t (15) = 0.73, P = .48),
and SAI (t (15) = 0.19, p = .85).
Procedure
Subjects were asked to perform the experiment twice,
and the first time ERP experiment between subjects
was counterbalanced based on their menstrual cycle.
That is, half subjects were first participated before the
onset of menses and half subjects were after the onset
of menses. The experimental procedure was identical
between first and second experiment, and using different materials. The experimental program was performed on the computer and presented by E-prime. In
each trial, a 300 ms fixation first presented, and then a
blank screen was displayed as interval, lasting randomly between 500 and 1000 ms. The stimuli were
then presented 1000 ms as standard or deviant stimuli.
Participants should make a key press that presses the
‘F’ to the standard stimulus and press ‘J’ to deviant
stimuli in this duration. The intertrial interval is
1000 ms.
Before the formal experiment, a 10 min practice
was performed to make subjects familiar with the task.
There were six blocks with 100 trials in each and
entire experiment takes about 30 min. Thus, there
were 420 standard trials and 180 deviant trials (i.e.,
60 HN, 60 MN, and 60 neutral stimulus).
EEG recording and data analysis
Participants sat on a chair in a dark room with their
head restrained in a chin rest. Raw electroencephalographic (EEG) data were collected at 500 Hz
sample rate, referenced to left mastoid, using 64channel Neuroscan Synamps (Neuroscan Inc.,
Herndon, VA). The continuous data were digitized
with a bandpass of 0.05–100 Hz, and the electrode
impedances were keep lower than 5 kΩ. Vertical
electrooculograms (EOGs) were recorded supraand infra-orbitally at the left eye. Horizontal EOG
was recorded as the left versus right orbital rim.
EEGs were re-referenced to the average of the left
and right mastoids and filtered with a low pass of
30 Hz off-line. Epochs were made beginning 200
ms prior to stimulus onset and continuing for
1000 ms. Trials exceeding ±80 μV epoch data
should pass through a computerized artifact
Downloaded by [Institute of Psychology ] at 00:28 30 November 2015
282
WU ET AL.
detection algorithm and trials with out of range
data (were excluded from further analysis. Three
subjects were excluded due to serious eyeblinks,
eye movements, or other artifacts. Trials of four
conditions (HN, MN, neutral stimulus, and standard
stimuli) were averaged, respectively, and then
using—200 ms to 0 ms baseline to perform a baseline correction.
Studies of ERP response to negative emotion were
well documented (Campanella et al., 2002; Li et al.,
2008; Yuan et al., 2007), and we thus will mainly
focus on N2 and P3 components based on existing
study (see Figures 1 and 2). The latency and amplitude of N2 (150–300 ms) were analyzed on peak
value in electrodes of F3, FZ, F4, FC3, FCz, FC4,
C3, Cz, and C4. And the amplitude of P3 (300–500
ms) were analyzed on mean amplitude values in electrodes of C3, Cz, C4, CP3, CPz, CP4, P3, Pz, and P4.
In the statistical analysis, a repeated measure ANOVA
was conducted with valence (three levels: HN vs. MN
vs. neutral), Electrode and cycle phase (luteal vs.
follicular) as within-subject factors. The degrees of
freedom of the F-ratio were corrected by using
Greenhouse–Geisser method when the sphericity was
violated.
RESULTS
Behavioral performance
Overview, the accuracy was extremely high for both
late luteal and follicular phase (98.2% for late luteal
phase and 99% for follicular phase, respectively). The
ANOVA with valence (HN vs. MN vs. neutral) and
phase (luteal vs. follicular) as within-subject factor on
response accuracy showed a significant main effect of
valence, F (2, 17) = 4.498, p < .05 and ηp2 = .273. The
pairwise comparison showed that the accuracy of HN
(M = .994, SE = .003) was significantly higher than
neutral stimulus (M = .974, SE = .004), p < .05.
Neither the comparison between HN and MN nor
between MN and neutral was significant. After
excluded incorrect trials, the ANOVA in RTs revealed
no significant main effect or interaction (see Table 2).
ERP results
The grand average ERPs for four conditions (HN vs.
MN vs. neutral vs. standard) are shown in Figure 1
(during late luteal/premenstrual phase) and Figure 2
Figure 1. The grand average ERPs at Fz, FCz, Cz, CPz, and Pz for females during luteal phase.
Note: During late luteal phase, the N2 amplitude increased with the intense of valence, such that HN stimuli evoked largest N2
and neutral stimuli evoked smallest N2. Moreover, the difference between MN and neutral stimuli was significant, i.e. p < .05.
Downloaded by [Institute of Psychology ] at 00:28 30 November 2015
MENSTRUAL PHASE AND NEGATIVE EMOTION
283
Figure 2. The grand average ERPs at Fz, FCz, Cz, CPz, and Pz for females during follicular phase.
Note: During follicular phase, HN stimuli evoked largest N2. However, the difference between MN and neutral stimuli was not
significant.
TABLE 2
The response accuracy and response time results in two phases (Mean ± SD)
Phase
Accuracy
RT (ms)
Late Luteal
Follicular
Late Luteal
Follicular
HN
0.99
0.99
488.16
478.52
±
±
±
±
(during follicular phase). Notably, the accepted trial
numbers for each condition indicated nonsignificant
(ps > .29) difference across conditions and phases. We
will mainly report the oddball effect and the amplitude
differences among three types of deviant pictures in
two phases.
Standard vs. deviant
To examine the oddball effect, we compared the
ERPs of deviant stimulus (1/3 HN + 1/3 MN +1/3
Neutral) with standard stimuli. The repeat measure
ANOVA with frequency (deviant vs. standard) and
phase as within-subject factors on N2 amplitude
revealed a significant main effect of Frequency,
MN
0.01
0.00
17.16
43.76
0.98 ± 0.01
0.99 ± 0.00
482.16 ± 16.38
473.95 ± 47.78
Neutral
0.97
0.98
492.88
484.26
±
±
±
±
0.01
0.01
15.68
43.47
F (1,12) = 76.87, p < .001, ηp2 = .865, showing that
deviant stimulus (M = –10.10 μV, SE = 1.24) elicited
larger N2 amplitude than standard stimuli s (M =
–3.55 μV, SE = .74).
Regarding the P3 component, the ANOVA result
showed a main effect of frequency, F (1,12) = 8.12,
p < .05, and ηp2 = .40, indicating the P3 for deviant
stimulus (M = 11.73 μV, SE = .74) was larger than
standard stimuli (M = 9.70 μV, SE = .77).
N2
The three-way (valence × electrode × phase)
ANOVA on N2 amplitude showed a significant main
effect of electrode, F (3,33) = 59.46, P < .001,
Downloaded by [Institute of Psychology ] at 00:28 30 November 2015
284
WU ET AL.
ηp2 = .83, and significant interaction of valence × electrode, F (5, 65) = 6.71, p < .001, ηp2 = .32. Moreover,
the three-way interaction (valence × electrode × phase)
was also significant, F (5,62) = 4.86, p = .001,
ηp2 = 0.29. The pairwise comparison for the electrode
main effect showed that FCz was with largest N2
(M = −13.30 μV, SE = 1.52) than the other electrodes
(ps < .05), indicating the dominant fronto–central distribution of N2 in the middle site. The further analyses
on the valence × electrode × phase interaction
revealed that MN pictures elicited larger N2 in the
frontal electrodes (Fz, F3, and F4) than neutral pictures, ps < .05. The post hoc analysis also revealed
phase cycle difference in left fronto–central electrodes
(C3, FC3) in HN pictures that the HN picture elicited
larger N2 in the late luteal phase than follicular phase,
ps < 0.05. No other significant main effects or interactions were found for N2 amplitudes and nor were
the main effects or interactions for N2 latency.
P3
The three-way (valence × electrode × phase)
ANOVA on P3 amplitude revealed a significant main
effect of Electrode, F (3,37) = 11.58,p < .01,
ηp2 = .49), indicating that the P3 was larger at centro-parietal sites (Pz, P4, CP4, P3, CP3, CPz) than
central electrodes(C3, C4), ps< .05.
Concerning P3 amplitude was suggested to be
modulated by depression (Campanella et al.,
2012), we also conducted the three-way (valence × electrode × phase) ANOVA with BDI score as covariance.
The result revealed a main effect of electrode, F
(3,37) = 6.35, p < .01, ηp2 = .37, indicating nonsignificant BDI modulation effect on P3 amplitude.
Furthermore, we also did a multivariate linear regression analysis as suggested by Campanella et al. (2012).
Specifically, we did the regression analysis on P3
amplitude and P3 latency, respectively, with PHASE
and BDI score as independent variables. However, no
predictor was found for P3 latency (ps > 0.79) or P3
amplitude (ps > 0.211).
DISCUSSION
As stated above, ERP studies have identified ERP
components modulated by emotion valence (Carretié
et al., 2001, 2004; Huang & Luo, 2006). For instance,
studies with implicit task (Carretié et al., 2001) or
explicit affective judgment task (Huang & Luo,
2006) indicated that the P200 was larger for negative
stimuli than positive stimuli (i.e., negative bias).
Furthermore, P300 also showed affective valence
effect in a study with controlled middle level arousal
pictures. More specifically, the P300 differed among
valence categories (negative, neutral, and positive) at
frontal sites but not parietal area (Conroy & Polich,
2007). In addition, ERP studies on negative stimuli
processing with affective arousal controlled also confirmed the valence effect on N2 and P3 (Li et al.,
2008; Yuan et al., 2007, 2009, 2010). More specifically, in the oddball paradigm, N2 was largest in the
extremely negative facial expression and smallest in
the neutral condition, which may indicate the attention
to significant stimuli for living (Yuan et al., 2007).
The further study on gender difference in negative
emotion also observed significant difference between
HN and neutral stimuli across N2 and P3 such that
indicated both male and female are sensitive to HN
stimuli. More importantly, only female showed susceptibility to lesser salience negative stimuli because
only female showed MN vs. neutral difference across
N2 and P3 (Li et al., 2008; Yuan et al., 2009).
However, whether such sensitivity on MN stimuli
was modulated by menstrual cycle was still unclear.
The present study investigated the menstrual cycle
effect on negative emotion processing, especially for
stimulus that matched arousal. Following previous
studies (Li et al., 2008; Yuan et al., 2007), an oddball
paradigm was utilized. In consistent with previous
study that showed no gender effect or valence effect
on RTs (Li et al., 2008), the analyses of RTs revealed
no valence or phase effect. However, the behavioral
results of present study indicated a higher accuracy for
HN stimulus than neutral stimulus. This may due to
the negative bias that the automatic attention to HN,
and thus the response accuracy was higher. Our result
was also in line with previous reports showed relatively better performance for negative stimuli than
neutral stimuli (Kensinger & Corkin, 2003; Murty
et al., 2009).
Regarding the ERP results, basically, the N2 and
P3 showed an oddball effect that larger N2 and P3
was found in deviant stimuli than standard stimuli.
Moreover, the analysis showed no phase related effect
in deviant vs. standard comparison demonstrated that
the oddball effect was not affected by the cycle phase.
The larger N2 and P3 amplitude to deviant stimuli
was congruent with previous studies showed such
enhanced N2 or P3 to novel stimuli (Campanella
et al., 2004; Langeslag, Franken, & Van Strien,
2008; Nagy, Potts, & Loveland, 2003), which was
interpreted as an increased orienting of attention or
significance to novel stimuli. Since the valence difference between deviant vs. standard stimuli, our result
could not simply attribute to the oddball effect.
However, compared with a prior study showed gender
Downloaded by [Institute of Psychology ] at 00:28 30 November 2015
MENSTRUAL PHASE AND NEGATIVE EMOTION
different that females showed larger P3 to rare stimuli
than males (Yuan et al., 2010), our result showed a
stable enhanced N2 and P3 to deviant stimuli for
females in both late luteal and follicular phase.
On the other hand, the brain potential responses to
negative emotion were modulated by the menstrual
cycle. The major finding of our study is that MN
stimuli demonstrated larger N2 amplitudes compared
to neutral stimuli in the late luteal phase (Figure 1).
Such difference indicated that females could differentiate MN and neutral information in the time interval of 150–300 ms in the premenstrual phase. In this
phase, the N2 amplitude was largest for HN stimuli
and smallest for neutral stimuli, which was consistent
with previous evidence have suggested that N2 is
sensitive to negative facial expressions and may
reflect the early attention processing to emotional or
significant stimuli (Campanella et al., 2002; Herrmann
et al., 2002). Considering numerous prior studies utilized oddball paradigm interpreted the N2 as orienting
attention to salient stimuli (Campanella et al., 2004;
Muller-Gass, Stelmack, & Campbell, 2006; Nagy
et al., 2003), such larger N2 to MN stimuli suggested
more attention to MN stimuli than neutral stimuli in
the late luteal phase.
However, such MN vs. neutral N2 difference was
absent in the follicular phase (Figure 2). For previous
study focus on gender difference indicated that only
female showed MN vs. neutral N2 difference and
confirmed the females’ susceptibility to MN emotion
but not HN stimuli(Li et al., 2008; Yuan et al., 2009),
our result may provide further evidence for female’s
ability to differentiate less salient negative stimuli and
indicated such female advantage in MN emotion may
also vary across the menstrual cycle.
Importantly, our finding showed that the N2 for
HN condition varied across menstrual cycle. More
specifically, HN stimuli elicited larger N2 in left
fronto–central electrodes during the late luteal phase
than follicular phase. This may indicate that women in
premenstrual phase showed enhanced sensitivity to
HN stimuli than during follicular phase. Similarly,
there is some evidence to suggest that the perception
processing (Smith et al., 2003) or social-cognitive
function varies across the menstrual cycle (Macrae
et al., 2002). Previous studies have suggested
enhanced negative emotional processing in PMDD
(Protopopescu et al., 2008) and higher stress vulnerability during the premenstrual phase (Ossewaarde
et al., 2010). Extending these findings, the present
results revealed the cycle-dependent effect on negative emotion processing in normal subjects. Our findings show women during late luteal/premenstrual
phase may with higher sensitivity to negative stimuli
285
(both moderately and HN stimuli), such sensitivity
may provide new insight to the research on PMDD
and menstrual cycle-depended stress vulnerability.
Furthermore, our result showed that females are
more sensitive to negative emotion in luteal phase
was inconsistent the evolutionary view and evidence
showed that females were with better performance in
emotion recognition or increase amygdala activity to
negative stimulus during follicular phase (Derntl,
Kryspin-Exner, et al., 2008; Derntl, Windischberger,
et al., 2008). One possible reason, as we stated, is that
we controlled arousal dimension of the negative emotion in the present study. That is, the previous results
may attribute the higher arousal of negative emotion
and the N2 in our finding seems sensitive to valence
effect.
Although the N2 results showed interactions
between the different types of picture and the phase
of menstrual cycle, we failed to find the effect of
valence or phase in P3. Alternatively, we just find a
consistent topography distribution of P3 that larger P3
occurred at posterior sites. Considering previous study
indicated that the valence affect frontal P3 but not
parietal P3 when arousal was controlled (Conroy &
Polich, 2007), the no valence effect may because we
analyzed posterior P3. It is also possible that the
individual difference and relative small subject sample
make the P3 result did not reach significant.
However, we must acknowledge certain limitations
of the present study. The major limitation was the
sample size (N = 16) is relatively small. Such small
sample size may help us to explain the absence of P3
effect. For instance, the P3 amplitude and latency
cannot be predicted by the BDI score in present
study, which failed to repeat the pilot study
(Campanella et al., 2012). And, another limitation is
that the hormone levels were not measured in present
study, which makes our inference about hormone
levels and negative emotion processing difficult.
Furthermore, although we tried to control the affective
state of the subjects by BDI, SAI, and PANAS scales,
the absence of the trait anxiety measurement may
affect the conclusion given that the influence of
Toronto Alexithymia Scale (TAS) on N2 in a previous
study (Campanella et al., 2012).
Overall, our result further confirmed the negative
bias across menstrual cycle that females were with
higher accuracy to HN stimuli than neutral stimuli.
Moreover, N2, a ERP component reflects early attention processing, indicated a valence effect that the N2
amplitude enlarge along with the intense of negative
emotion in the late luteal phase. However, the N2
difference between MN and neutral stimuli was not
significant and the larger N2 for HN in follicular
286
WU ET AL.
phase than late luteal phase may together indicated
that females were with higher sensitivity to negative
emotion during luteal phase than during follicular
phase when arousal was well controlled. Considering
the gender difference in emotion processing and the
affective disorder (Miller & Miller, 2001), our result
may provide new insights on issues such as premenstrual symptoms, individual differences in
emotion processing, and affective disorder.
Downloaded by [Institute of Psychology ] at 00:28 30 November 2015
Original manuscript received 5 August 2013
Revised manuscript accepted 18 January 2014
First published online 3 March 2014
REFERENCES
Amin, Z., Epperson, C. N., Constable, R. T., & Canli, T.
(2006). Effects of estrogen variation on neural correlates
of emotional response inhibition. NeuroImage, 32(1),
457–464. doi:10.1016/j.neuroimage.2006.03.013
Andreano, J. M., & Cahill, L. (2010). Menstrual cycle
modulation of medial temporal activity evoked by negative emotion. NeuroImage, 53(4), 1286–1293.
doi:10.1016/j.neuroimage.2010.07.011
Baca-García, E., González, A., Gonzalez Diaz-Corralero, P.,
García, I., & de Leon, J. (1998). Menstrual cycle and
profiles of suicidal behaviour. Acta Psychiatrica
Scandinavica, 97(1), 32–35. doi:10.1111/j.16000447.1998.tb09959.x
Campanella, S., Falbo, L., Rossignol, M., Grynberg, D.,
Balconi, M., Verbanck, P., & Maurage, P. (2012). Sex
differences on emotional processing are modulated by
subclinical levels of alexithymia and depression: A preliminary assessment using event-related potentials.
Psychiatry Research, 197(1–2), 145–153.
Campanella, S., Gaspard, C., Debatisse, D., Bruyer, R.,
Crommelinck, M., & Guerit, J. M. (2002). Discrimination
of emotional facial expressions in a visual oddball task: An
ERP study. Biological Psychology, 59(3), 171–186.
doi:10.1016/S0301-0511(02)00005-4
Campanella, S., Rossignol, M., Mejias, S., Joassin, F.,
Maurage, P., Debatisse, D., . . . Guérit J. M. (2004).
Human gender differences in an emotional visual oddball
task: An event-related potentials study. Neuroscience
Letters, 367(1), 14–18. doi:10.1016/j.neulet.2004.05.097
Carretié, L., Hinojosa, J. A., Martín-Loeches, M., Mercado,
F., & Tapia, M. (2004). Automatic attention to emotional
stimuli: Neural correlates. Human Brain Mapping, 22(4),
290–299. doi:10.1002/hbm.20037
Carretié, L., Iglesias, J., & Garcı́a, T. (1997). A study on the
emotional processing of visual stimuli through eventrelated potentials. Brain and Cognition, 34(2),
207–217. doi:10.1006/brcg.1997.0895
Carretié, L., Mercado, F., Tapia, M., & Hinojosa, J. A.
(2001). Emotion, attention, and the ‘negativity bias’,
studied through event-related potentials. International
Journal
of
Psychophysiology,
41(1),
75–85.
doi:10.1016/S0167-8760(00)00195-1
Codispoti, M., Ferrari, V., & Bradley, M. M. (2007).
Repetition and event-related potentials: Distinguishing
early and late processes in affective picture perception.
Journal of Cognitive Neuroscience, 19(4), 577–586.
doi:10.1162/jocn.2007.19.4.577
Conroy, M. A., & Polich, J. (2007). Affective valence and
P300 when stimulus arousal level is controlled.
Cognition & Emotion, 21(4), 891–901. doi:10.1080/
02699930600926752
Derntl, B., Kryspin-Exner, I., Fernbach, E., Moser, E., &
Habel, U. (2008). Emotion recognition accuracy in
healthy young females is associated with cycle phase.
Hormones and Behavior, 53(1), 90–95. doi:10.1016/j.
yhbeh.2007.09.006
Derntl, B., Windischberger, C., Robinson, S., Lamplmayr, E.,
Kryspin-Exner, I., Gur, R. C., . . . Habel U. (2008). Facial
emotion recognition and amygdala activation are associated
with menstrual cycle phase. Psychoneuroendocrinology, 33
(8), 1031–1040. doi:10.1016/j.psyneuen.2008.04.014
Dietrich, T., Krings, T., Neulen, J., Willmes, K., Erberich,
S., Thron, A., & Sturm, W. (2001). Effects of blood
estrogen level on cortical activation patterns during cognitive activation as measured by functional MRI.
NeuroImage,
13(3),
425–432.
doi:10.1006/
nimg.2001.0703
Epperson, C. N., Pittman, B., Czarkowski, K. A., Stiklus, S.,
Krystal, J. H., & Grillon, C. (2007). Luteal-phase accentuation of acoustic startle response in women with premenstrual dysphoric disorder. Neuropsychopharmacology,
32(10), 2190–2198. doi:10.1038/sj.npp.1301351
Fujita, F., Diener, E., & Sandvik, E. (1991). Gender differences in negative affect and well-being: The case for
emotional intensity. Journal of Personality and Social
Psychology,
61(3), 427–434. doi:10.1037/00223514.61.3.427
Goldstein, J. M., Jerram, M., Abbs, B., Whitfield-Gabrieli,
S., & Makris, N. (2010). Sex differences in stress
response circuitry activation dependent on female hormonal cycle. Journal of Neuroscience, 30, 431–438.
doi:10.1523/JNEUROSCI.3021-09.2010
Goldstein, J. M., Jerram, M., Poldrack, R., Ahern, T., Kennedy,
D. N., Seidman, L. J., & Makris, N. (2005). Hormonal
cycle modulates arousal circuitry in women using functional magnetic resonance imaging. Journal of
Neuroscience,
25,
9309–9316.
doi:10.1523/
JNEUROSCI.2239-05.2005
Guapo, V. G., Graeff, F. G., Tagliati Zani, A. C., 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
processing of emotional faces. Psychoneuroendocrinology,
34(7), 1087–1094. doi:10.1016/j.psyneuen.2009.02.007
Hall, J. A., & Matsumoto, D. (2004). Gender differences in
judgments of multiple emotions from facial expressions.
Emotion, 4(2), 201–206. doi:10.1037/1528-3542.4.2.201
Hamann, S. (2005). Sex differences in the responses of the
human amygdala. The Neuroscientist, 11(4), 288–293.
doi:10.1177/1073858404271981
Hansen, C. H., & Hansen, R. D. (1988). Finding the face in
the crowd: An anger superiority effect. Journal of
Personality and Social Psychology, 54(6), 917–924.
doi:10.1037/0022-3514.54.6.917
Hatta, T., & Nagaya, K. (2009). Menstrual cycle phase
effects on memory and stroop task performance.
Downloaded by [Institute of Psychology ] at 00:28 30 November 2015
MENSTRUAL PHASE AND NEGATIVE EMOTION
Archives of Sexual Behavior, 38(5), 821–827.
doi:10.1007/s10508-008-9445-7
Herrmann, M. J., Aranda, D., Ellgring, H., Mueller, T. J.,
Strik, W. K., Heidrich, A., & Fallgatter, A. J. (2002).
Face-specific event-related potential in humans is independent from facial expression. International Journal of
Psychophysiology, 45(3), 241–244. doi:10.1016/S01678760(02)00033-8
Huang, Y. X., & Luo, Y. J. (2006). Temporal course of
emotional negativity bias: An ERP study. Neuroscience
Letters, 398(1–2), 91–96.
Ito, T. A., Larsen, J. T., Smith, N. K., & Cacioppo, J. T.
(1998). Negative information weighs more heavily on
the brain: The negativity bias in evaluative categorizations. Journal of Personality and Social Psychology,
75(4), 887–900. doi:10.1037/0022-3514.75.4.887
Kensinger, E. A., & Corkin, S. (2003). Memory enhancement for emotional words: Are emotional words more
vividly remembered than neutral words? Memory &
Cognition, 31(8), 1169–1180. doi:10.3758/BF03195800
Ladavas, E., Umiltà, C., & Ricci-Bitti, P. E. (1980).
Evidence for sex differences in right-hemisphere dominance for emotions. Neuropsychologia, 18(3), 361–366.
doi:10.1016/0028-3932(80)90132-3
Lang, P. J. (1995). The emotion probe: Studies of motivation
and attention. American Psychologist, 50(5), 372–385.
doi:10.1037/0003-066X.50.5.372
Langeslag, S. J. E., Franken, I. H. A., & Van Strien, J. W.
(2008). Dissociating love-related attention from taskrelated attention: An event-related potential oddball
study. Neuroscience Letters, 431(3), 236–240.
doi:10.1016/j.neulet.2007.11.044
Lawton, M. P., Kleban, M. H., Rajagopal, D., & Dean, J.
(1992). Dimensions of affective experience in three age
groups. Psychology and Aging, 7(2), 171–184.
doi:10.1037/0882-7974.7.2.171
Lewis, P. A., Critchley, H. D., Rotshtein, P., & Dolan, R. J.
(2007). Neural correlates of processing valence and arousal in affective words. Cerebral Cortex, 17(3), 742–748.
doi:10.1093/cercor/bhk024
Li, H., Yuan, J., & Lin, C. (2008). The neural mechanism
underlying the female advantage in identifying negative
emotions: An event-related potential study. NeuroImage,
40(4), 1921–1929. doi:10.1016/j.neuroimage.2008.01.033
Macrae, C. N., Alnwick, K. A., Milne, A. B., &
Schloerscheidt, A. M. (2002). Person perception across
the menstrual cycle: Hormonal influences on socialcognitive functioning. Psychological Science, 13(6),
532–536. doi:10.1111/1467-9280.00493
Maki, P. M., & Resnick, S. M. (2001). Effects of estrogen
on patterns of brain activity at rest and during cognitive
activity: A review of neuroimaging studies. NeuroImage,
14(4), 789–801. doi:10.1006/nimg.2001.0887
Miller, M. N., & Miller, B. E. (2001). Premenstrual exacerbations of mood disorders. Psychopharmacology
Bulletin, 35(3), 135–149.
Mogg, K., & Bradley, B. P. (1998). A cognitive-motivational
analysis of anxiety. Behaviour Research and Therapy,
36(9), 809–848. doi:10.1016/S0005-7967(98)00063-1
Mogg, K., McNamara, J., Powys, M., Rawlinson, H.,
Seiffer, A., & Bradley, B. P. (2000). Selective attention
to threat: A test of two cognitive models of anxiety.
Cognition & Emotion, 14(3), 375–399. doi:10.1080/
026999300378888
287
Montagne, B., Kessels, R. P. C., Frigerio, E., de Haan, E. H.
F., & Perrett, D. I. (2005). Sex differences in the perception of affective facial expressions: Do men really lack
emotional sensitivity? Cognitive Processing, 6(2), 136–
141. doi:10.1007/s10339-005-0050-6
Muller-Gass, A., Stelmack, R. M., & Campbell, K. B.
(2006). The effect of visual task difficulty and attentional
direction on the detection of acoustic change as indexed
by the Mismatch Negativity. Brain Research, 1078,
112–130. doi:10.1016/j.brainres.2005.12.125
Murty, V. P., Sambataro, F., Das, S., Tan, H. Y., Callicott, J. H.,
Goldberg, T. E., . . . Mattay, V. S. (2009). Age-related alterations in simple declarative memory and the effect of negative
stimulus valence. Journal of Cognitive Neuroscience,
21(10), 1920–1933. doi:10.1162/jocn.2009.21130
Nagy, E., Potts, G. F., & Loveland, K. A. (2003). Sexrelated ERP differences in deviance detection.
International Journal of Psychophysiology, 48(3),
285–292. doi:10.1016/S0167-8760(03)00042-4
Olofsson, J. K., Nordin, S., Sequeira, H., & Polich, J.
(2008). Affective picture processing: An integrative
review of ERP findings. Biological Psychology, 77(3),
247–265. doi:10.1016/j.biopsycho.2007.11.006
Ossewaarde, L., Hermans, E. J., van Wingen, G. A.,
Kooijman, S. C., Johansson, I. M., Bäckström, T., &
Fernández, G. (2010). Neural mechanisms underlying
changes in stress-sensitivity across the menstrual cycle.
Psychoneuroendocrinology, 35(1), 47–55. doi:10.1016/j.
psyneuen.2009.08.011
Pearson, R., & Lewis, M. B. (2005). Fear recognition across
the menstrual cycle. Hormones and Behavior, 47,
267–271. doi:10.1016/j.yhbeh.2004.11.003
Peeters, G., & Czapinski, J. (1990). Positive-negative asymmetry in evaluations: The distinction between affective and
informational negativity effects. European Review of Social
Psychology, 1(1), 33–60. doi:10.1080/14792779108401856
Protopopescu, X., Pan, H., Altemus, M., Tuescher, O.,
Polanecsky, M., McEwen, B., . . . Stern E. (2005).
Orbitofrontal cortex activity related to emotional processing changes across the menstrual cycle. Proceedings of
the National Academy of Sciences of the United States of
America,
102(44),
16060–16065.
doi:10.1073/
pnas.0502818102
Protopopescu, X., Tuescher, O., Pan, H., Epstein, J., Root,
J., Chang, L., . . . Silbersweig, D. (2008). Toward a
functional neuroanatomy of premenstrual dysphoric disorder. Journal of Affective Disorders, 108(1–2), 87–94.
Rotter, N. G., & Rotter, G. S. (1988). Sex-differences in the
encoding and decoding of negative facial emotions.
Journal of Nonverbal Behavior, 12(2), 139–148.
doi:10.1007/BF00986931
Rubinow, D. R., & Schmidt, P. J. (2006). Gonadal steroid
regulation of mood: The lessons of premenstrual syndrome. Frontiers in Neuroendocrinology, 27(2),
210–216. doi:10.1016/j.yfrne.2006.02.003
Saunders, K. E., & Hawton, K. (2006). Suicidal behaviour
and the menstrual cycle. Psychological Medicine, 36(7),
901–912. doi:10.1017/S0033291706007392
Scher, D., Pionk, M., & Purcell, D. G. (1981). Visual
sensitivity fluctuations during the menstrual-cycle under
dark and light adaptation. Bulletin of the Psychonomic
Society, 18(3), 159–160. doi:10.3758/BF03333591
Schöning, S., Engelien, A., Kugel, H., Schäfer, S., Schiffbauer,
H., Zwitserlood, P., . . . Konrad, C. (2007). Functional
Downloaded by [Institute of Psychology ] at 00:28 30 November 2015
288
WU ET AL.
anatomy of visuo-spatial working memory during mental
rotation is influenced by sex, menstrual cycle, and sex
steroid hormones. Neuropsychologia, 45(14), 3203–3214.
doi:10.1016/j.neuropsychologia.2007. 06.011
Smith, N. K., Cacioppo, J. T., Larsen, J. T., & Chartrand,
T. L. (2003). May I have your attention, please:
Electrocortical responses to positive and negative stimuli. Neuropsychologia, 41(2), 171–183. doi:10.1016/
S0028-3932(02)00147-1
Stewart, J. L., Silton, R. L., Sass, S. M., Fisher, J. E., Edgar,
J. C., Heller, W., & Miller, G. A. (2010). Attentional bias
to negative emotion as a function of approach and withdrawal anger styles: An ERP investigation. International
Journal of Psychophysiology, 76(1), 9–18. doi:10.1016/j.
ijpsycho.2010.01.008
Taylor, S. E. (1991). Asymmetrical effects of positive and
negative events: The mobilization-minimization hypothesis. Psychological Bulletin, 110(1), 67–85. doi:10.1037/
0033-2909.110.1.67
Watson, D., Clark, L. A., & Tellegen, A. (1988).
Development and validation of brief measures of positive
and negative affect: The PANAS scales. Journal of
Personality and Social Psychology, 54(6), 1063–1070.
doi:10.1037/0022-3514.54.6.1063
Weis, S., Hausmann, M., Stoffers, B., & Sturm, W. (2011).
Dynamic changes in functional cerebral connectivity of
spatial cognition during the menstrual cycle. Human
Brain Mapping, 32(10), 1544–1556. doi:10.1002/
hbm.21126
Wentura, D., Rothermund, K., & Bak, P. (2000). Automatic
vigilance: The attention-grabbing power of approachand avoidance-related social information. Journal of
Personality and Social Psychology, 78(6), 1024–1037.
doi:10.1037/0022-3514.78.6.1024
Woods, N. F., Most, A., & Dery, G. K. (1982). Prevalence of
perimenstrual symptoms. American Journal of Public
Health, 72(11), 1257–1264. doi:10.2105/AJPH.72.11.1257
Yuan, J. J., Luo, Y. J., Yan, J. H., Meng, X. X., Yu, F. Q., &
Li, H. (2009). Neural Correlates of the females’ susceptibility to negative emotions: An insight into genderrelated prevalence of affective disturbances. Human
Brain Mapping, 30(11), 3676–3686. doi:10.1002/
hbm.20796
Yuan, J. J., Yang, J. M., Chen, J., Meng, X. X., & Li, H.
(2010). Enhanced sensitivity to rare, emotion-irrelevant stimuli in females: Neural correlates.
Neuroscience, 169(4), 1758–1767. doi:10.1016/j.
neuroscience.2010.06.024
Yuan, J. J., Zhang, Q. L., Chen, A. T., Li, H., Wang, Q. H.,
Zhuang, Z. C. X., & Jia, S. (2007). Are we sensitive to
valence differences in emotionally negative stimuli?
Electrophysiological evidence from an ERP study.
Neuropsychologia, 45(12), 2764–2771. doi:10.1016/j.
neuropsychologia.2007.04.018