2019 Modulation of Visual Attention Assessed Using The Stroop Task During The Menstrual Cycle Comparison Between The Menstrual and Ovulation Phases

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Received: 12 February 2019 Revised: 1 August 2019 Accepted: 4 August 2019

DOI: 10.1002/col.22425

RESEARCH ARTICLE

Modulation of visual attention assessed using the Stroop task


during the menstrual cycle: Comparison between the menstrual
and ovulation phases

Mayuko Iriguchi1 | Hiroki Koda1 | Takamasa Koyama2 | Nobuo Masataka1

1
The Cognition and Learning section, the
Primate Research Institute, Kyoto Abstract
University, Inuyama, Japan Women might have changes in perception and cognition of colours according to
2
The Department of Psychology, Japan hormonal changes during the menstrual cycle. Colours are often associated with
Women's University, Kawasaki, Japan
specific emotional facial expressions, but how these two factors interact with each
Correspondence other and differ according to the cycle has remained unclear. We investigated atten-
Mayuko Iriguchi, Primate Research Institute, tional interference between colours and emotional facial expressions for women in
Kyoto University, Inuyama, Japan.
the menstrual compared to the ovulation phases by colour judgment based on
Email: iriguchi.mayuko.25m@kyoto-u.jp
the Stroop tasks. Participants identified the colours (either red, yellow, or blue) of
Funding information three types of face stimuli (happy, neutral, or sad) and corresponding scrambled
Japan Society for the Promotion of Science
(JSPS) and Ministry of Education, Culture,
face stimuli by pressing buttons, and we recorded participants' reaction times. The
Sports, Science and Technology (MEXT) results showed better performance in the menstrual phase than in the ovulation
KAKENHI, Grant/Award Numbers: phase. An interference effect was not observed. However, in the scrambled face
#18H03503, #4903, JP17H06380
stimuli task, only the reaction time for happy scrambled face shape and red did not
differ between the phases. Thus, participants might pay stronger attention to faces
with colours in the menstrual phase than in the ovulation phase but weaker atten-
tion to scrambled face shapes in the menstrual phase.

KEYWORDS
colour judgment, emotional facial expression, menstrual cycle, Stroop task

1 | INTRODUCTION behavior, such as more frequent attendance at social meet-


ings, use of cosmetics, and choices of products to enhance
1.1 | Female hormones, perception, and their appearance to attract men, although the subjects of
cognition these studies have been limited to only university students in
the United States and Europe.2,5,6 Regarding perceptual and
Women often experience various changes in perception,
cognitive functioning, women show differences in perfor-
cognition, and behavior caused by changes in female hor-
mance of visual processing of asymmetries,7 visual-spatial
mone levels during the menstrual cycle.1-4 This cycle typi-
tasks,8,9 and the Stroop task3 across the menstrual cycle. For
cally occurs over about 28 days, and ovulation occurs at example, performance in visual processing of asymmetries
about 14 days prior to the beginning of the next menstrua- and spatial pointing became better in the luteal phase with a
tion, although the length of one regular cycle depends on the higher hormone level,7,8 while performance in the Stroop
individual and health conditions.1 Regarding evolutionary task and spatial orientation task was better in the menstrual
aspects, women near the time of ovulation have higher phase with a lower hormone level than the mid-luteal
reproductive fertility, and they show changes in social phase.3,9 In addition, women were reported to have a lower

Color Res Appl. 2019;1–10. wileyonlinelibrary.com/journal/col © 2019 Wiley Periodicals, Inc. 1


2 IRIGUCHI ET AL.

threshold of olfactory perception near the time of ovulation,4 findings suggest that hormonal changes during the menstrual
but some studies found higher sensitivity in the ovulation cycle may influence specific perception, preferences, and
phase or no clear differences during the course of the men- social behavior regarding colours that may be related to fer-
strual cycle.10,11 These findings suggest that there is a rela- tility, while the effect of hormonal changes during the men-
tionship between the menstrual cycle and perceptual and strual cycle on attention measured using the Stroop task has
cognitive functions and that the sensitivities of various func- remained controversial.
tions show different tendencies during the course of the
cycle. There does not seem to be a consistent pattern among
1.3 | Social stimulus recognition: Emotional
the sensitivities reported thus far, and hormones may affect facial expressions
the sensitivities differently, particularly cognitive functions,
according to the different types of task.3 Women are likely to modulate their recognition of social
information, particularly facial expressions, according to the
menstrual cycle. At the time of ovulation, women are likely
1.2 | Colour perception and cognition to prefer masculine faces of men.24,25 Regarding emotional
Perception and cognition, particularly of colours, may also facial expressions, women are able to detect and remember
change during the menstrual cycle. Regarding social behavioral facial expressions better in the follicular phase than the luteal
aspects such as colour preference, a number of studies demon- phase,26,27 and women tend to perceive angry and sad faces
strated that women prefer warmer colours, especially red or more accurately in the follicular phase than any other
pink, in the ovulatory phase at peak fertility and wear clothes phases.28 However, several studies reported different results,
with these colours, and this might be part of women's strategy for example, results showing that women have difficulties in
to enhance their reproduction by making themselves look more perceiving or remembering expressions such as disgust, sad-
attractive to men.12-14 Regarding perception, women using hor- ness, and fear in the follicular phase, while sensitivity to
monal contraceptives showed more errors in the ability of col- these facial expressions increases in the luteal phase.29-31
our perception than women who did not use hormonal Other studies also reported that women showed no differ-
contraceptives,15 and women perform better in a colour dis- ence in preference for masculine faces of men during
crimination task at ovulation than at the beginning of the men- ovulation,32 and they showed a delayed response when
strual phase (day 1-3) and end of the cycle (day 26-32).16 In matching a stimulus of emotional facial expression to one of
addition, visual perception of short-wavelength (bluish) colours the choices regarding it according to their memory during
could be affected by hormonal changes, and the visual field the follicular phase.30 Thus, during the menstrual cycle,
threshold sensitivity for perceiving these colours seems to female hormones could affect facial preference and percep-
decline in the luteal phase.17,18 Our previous study also demon- tion of emotional facial expressions, but these influences still
strated that postmenopausal women had relatively slower reac- seem to be controversial.
tion times to blue stimuli than premenopausal women in colour
judgment in the Stroop task.19
1.4 | Social information, emotion and colour
In order to examine attentional judgment of coloured
stimuli in women during the menstrual cycle, the colour- Attention and recognition of social information, including
word Stroop task is often used. This task was originally emotion and facial expressions, are often examined, and the
designed to examine interference when a participant looked Stroop task, particularly the form of it called the emotional
at a stimulus consisting of two different types of information Stroop task, is used as one of the experimental methods for
(eg, colour words and colours), and attentional perception such examinations. Several studies used this task to examine
was compared between a congruent condition (colour words emotional interference using emotional words such as war
tinted with the same colours as the words' meanings) and an and abuse and showed that participants who have high anxi-
incongruent condition (colour words tinted with different ety sensitivity tend to respond to words related to anxiety
colours from their meanings).20 Regarding performance in more than to any other words.33-35
attentional judgment of women during the menstrual cycle, Emotional facial expressions or emotional words might
using the colour-word Stroop task, Hatta and Nagaya dem- often be associated with specific colours (eg, a happy face
onstrated that times to complete the Stroop task in the men- with yellow or a sad face with blue),36-38 although the stud-
strual phase (with lower hormonal levels) were significantly ies that found such an association mainly focused on univer-
shorter than the times in the luteal phase (with higher hor- sity students as participants, and the association with
monal levels).3 However, several studies found no clear dif- different background factors such as age, gender, and culture
ference in performance in the Stroop task according to might be unclear. However, interaction between emotional
hormonal changes during the menstrual cycle.21-23 These facial expressions and colours in the Stroop task has not
IRIGUCHI ET AL. 3

been well examined. Eschenbeck et al used pictorial facial had regular menstrual cycles and recorded each starting date
images (happy and threatening) and four colours (red, blue, of menstruation (mean with SD of menstrual cycle: 29.73
yellow, and green) in the Stroop task for school children, ± 2.82 days) without taking contraceptive or hormonal med-
and the results showed that children with higher levels of icine. After receiving consent to participation, we asked all
anxiety had higher errors when they judged colours of participants about their menstrual cycle history for the past
threatening stimuli.39 However, how attention to and judg- several months. Based on these records, we calculated the
ment of colours are interfered with by emotional facial next starting date of a menstrual period and the approximate
expressions remains unknown, and in particular, how date of ovulation, which is about 14 days before the next
women give attention to and judge colours of the emotional starting date of a menstrual period. Each participant joined
facial stimuli according to hormonal changes during the the experiments twice, namely, on a date within 4 days from
menstrual cycle has not been reported. the beginning of a menstrual period and on a date within
As a number of previous studies suggest, women may have 3 days from the estimated date of ovulation. According to
some modulations of perception and cognition according to participants' menstrual cycle, some participants participated
colour and social information. However, the interaction in the first experiment at the beginning of a menstrual period
between colour and social information, such as emotional and in the second experiment during the ovulation period,
facial expressions, and the association between this interaction and others participated in the opposite order, and thus, the
and women's menstrual cycle have remained unclear. In order order of experiments was counterbalanced for participants.
to examine the interaction between colour and emotional facial After the experiments, particularly at the time of ovulation,
expressions of women during the menstrual cycle, we applied we asked all participants to inform us of the next start date
the Stroop task, which is the same task we previously used to of the menstrual period in order to confirm the estimated
examine the association between colour and emotional facial ovulation date. Of 26 participants, 15 participated in experi-
expression according to menopausal status.19 In the present ments earlier or later than the first 4 days from the start
experiment, we predicted that task performance of participants of the menstrual period or more than 3 days earlier or later
would decline when they were in the menstrual phase, with than the calculated time of ovulation, so we excluded the
lower hormonal levels, compared to when they were in the data of these participants from the analysis. The remaining
ovulation phase, with higher levels. We also hypothesized that, 11 participants participated in the experiments twice: on
when judging colours, participants' responses could be inter- dates within the first 4 days from the start of the menstrual
fered with by emotional facial expressions, particularly when period and on the calculated ovulation dates without a shift
these colours and emotional facial expressions were incongru- of more than 3 days from the estimated ovulation time, and
ent and that the responses could also differ between the men- we carried out the analysis using the data of these 11 partici-
strual phase and ovulation phase. pants (age: 22.00 ± 1.67 years, range: 20-24 years, men-
This study is a part of the doctoral thesis of one of the strual cycle: 30.55 ± 2.50 days). All participants were
authors, Mayuko Iriguchi, and participants in this study also Japanese, and they had no cognitive disorder tested by the
participated in another study, which has been submitted for Raven Coloured Progressive Matrices or colour blindness
publication. tested by the Ishihara Color Vision Test.

2 | MATERIALS AND METHODS 2.3 | Visual stimuli


We used simple cartoon depictions of faces as social stimuli
2.1 | Ethics
and scrambled faces as nonsocial stimuli. These face stimuli
We carried out all experiments in accordance with the Guide- had three types of emotional expressions: happy, neutral, or
lines for Research in Human Participants, issued by the Human sad, and each type of face was scrambled to produce the
Research Ethics Committee of Primate Research Institute, three types of scrambled face stimuli (Figure 1). Each stimu-
Kyoto University, and the experimental protocol was approved lus was shown with one of three colours: red, yellow, or blue
by the Committee (Permit No.2017-05). Before the experi- (Table 1). All stimuli were converted to a size fitted to
ments, we obtained a signed consent form from all participants. 250 × 250 pixels, and these stimuli were approximately
4 cm in diameter and 50 cm away from the participant.
2.2 | Participants
2.4 | Apparatus
Twenty-six female university undergraduate and postgradu-
ate students (mean with SD of ages: 21.62 ± 1.499 years, We used a table computer with a custom-made program
range: 20-24 years) participated in the experiments, and they written with OpenSesame software ver. 3.1.6 (Mathôt,
4 IRIGUCHI ET AL.

angle connecting the center of the screen and participant's


eye position was approximately 30 . In a single trial, first, a
fixation dot of an 8-pixel radius appeared at the center of the
screen on a gray background (Table 1, Figure 2). After a ran-
dom interval of 0.5 to 1.5 seconds, the fixation dot dis-
appeared, and one of either a happy, neutral, or sad stimulus
appeared at the center of the screen. The stimulus dis-
appeared either when participants pressed a button or auto-
matically after a 15-second interval if participants did not
press any button. When the stimulus appeared, participants
judged the colour (either red, yellow, or blue) of the stimulus
by pressing one of the three buttons of the keypad, which cor-
responded with the colour, using their right hand. The posi-
tions of buttons were counterbalanced for each participant.
After participants responded, the next trial was automatically
started. The study included an initial practice session, followed
by two experimental tasks. Each task consisted of 81 trials, in
which three types of stimuli, happy, neutral, and sad, appeared
randomly in any one of three colours—red, yellow, or blue—
nine times for each (three stimulus types × three
colours × nine times). Each participant performed both the
face stimuli task and scrambled face stimuli task for a total of
FIGURE 1 Types of stimuli: emotional face expressions 162 trials (81 trials × 2 tasks). We recorded all the reaction
included happy, neutral, and sad (left), and scrambled stimuli contained times of the keypad presses during the experiments.
their scrambled elements (right)

2.6 | Analysis
T A B L E 1 Colours of stimuli and background by Yxy (CIE,
Reaction times were analyzed by a repeated-measurements
cd/m2), measured by a chromatic photometer (Konica Minolta,
CS-100A)
design based on linear mixed models in SPSS ver. 25. Prior
to fitting the model, we used the reaction times with correct
Colour Y x y answers and those within the range of two times the SDs
Red 18.1 0.556 0.361 (2SD) and excluded the outlier data beyond these ranges
Yellow 73.0 0.432 0.488 (about 6.3% of all the data). We set the repeated conditions
Blue 21.5 0.202 0.243 of participants (menstrual phase or ovulation phase), the
Background 55.5 0.312 0.356 stimulus type (happy, neutral, or sad), and the colour (red,
yellow, or blue) with their interaction effect terms (con-
dition × stimulus type × colour) as the fixed main effect
2010-2016) in Microsoft Surface Pro 2 for all tasks in the terms, and participant ID was a random-effect term. When
experiments and a USB keypad that was connected to the we observed a significant interaction effect, as a post hoc
tablet. Participants pressed one of the buttons on the keypad comparison, we computed the 95% confidence intervals of
to indicate their judgment of the stimulus colours, and their the estimated marginal means between two comparison
response times were recorded on the keypad. levels for each level of the other condition and examined
whether the two levels differed significantly.

2.5 | Procedure
3 | RESULTS
In the experiments, participants sat in front of the Surface
screen (resolution: 1920 × 1080 pixels) and the keypad on a We found a statistically significant difference in reaction
desk in an experimental room illuminated with daylight and time in the face stimuli task between participants in the men-
standard fluorescent lights with a colour temperature of strual phase and ovulation phase (F1, 1651.063 = 11.725,
4200 K (Hotalux Ltd., Tokyo, Japan). The screen was P = .001, partial η2 = 0.062; Figure 3). Participants were
approximately 50 cm away from the participant, and the likely to respond to the stimuli faster in the menstrual phase
IRIGUCHI ET AL. 5

FIGURE 2 Procedure of experiment: a fixation dot appeared at the center of the screen on a gray background. After a 0.5 to 1.5-second
interval, the fixation dot disappeared, and one of either a happy, neutral, or sad stimulus appeared with either red, yellow, or blue colour. Then,
participants judged the colour of the stimulus by pressing one of the three buttons of the keypad

than in the ovulation phase. However, no interaction effects and those for scrambled face stimuli task were 96.7% and
were found between conditions, stimuli types, and colours. 96.9% in the menstrual phase and ovulation phase, respectively.
A similar pattern appeared in the scrambled face stim- Women were thus likely to have relatively high accuracy rates
uli task, namely, participants were likely to respond to in both phases and both tasks.
stimuli faster in the menstrual phase than the ovulation
phase (F1, 1641.106 = 14.335, P < .001, partial η2 = 0.063;
Figure 4). However, in the scrambled face stimuli task, we 4 | DISCUSSION
also found interaction effects between conditions of par-
ticipants and stimuli types (F2, 1641.097 = 4.488, P = .011, The results showed different patterns of the reaction times
partial η2 = 0.038) and between conditions and colours between the menstrual phase and ovulation phase. Partici-
(F2, 1641.056 = 3.383, P = .034, partial η2 = 0.031). Reaction pants tended to respond to stimuli faster when they were in
times of participants to a happy scrambled face did not differ the menstrual period than when they were near the ovulation
between the menstrual and ovulation phases, while those to period, in both face stimuli and scrambled face stimuli tasks.
neutral and sad scrambled faces became faster in the menstrual These results were contrary to our prediction that perfor-
phase than in the ovulation phase (Figure 5). Likewise, reac- mance would be better during ovulation than during men-
tion times to red did not largely differ between the phases, but struation. Moreover, in disagreement with our hypothesis, in
those to yellow and blue showed differences between the men- the face stimuli task, an interaction between emotional facial
strual phase and ovulation phase (Figure 5). expressions (happy, neutral, or sad) and colours (red, yellow,
The accuracy rates for face stimuli task were 97.5% and or blue) was not observed in either the menstrual or ovula-
95.8% in the menstrual phase and ovulation phase, respectively, tion phase. Thus, participants were not likely to experience
6 IRIGUCHI ET AL.

FIGURE 3 Average reaction time (ms) in the face stimuli task with the SE for participants in menstrual phase (left) and ovulation phase
(right) according to stimulus colour and type. Graph (A) shows reaction times to happy face, graph (B) shows those to neutral face, and graph
(C) shows those to sad face. In these graphs, bars indicate the colour of each stimulus: white bar for red, gray bar for yellow, and black-dotted bar
for blue

interference by emotional facial expressions when they space relations, particularly related to three-dimensional
judged stimulus colours. tasks, in the menstrual phase, with low hormone level, than
Our findings showed that participants tended to perform in the late follicular or midluteal phase, when the hormone
better regarding colour judgment in the Stroop task during level is increased.9,40 Performance in the colour-word Stroop
the menstrual phase than during the ovulation phase, and this task reported by Hatta and Nagaya demonstrated that women
pattern seemed to occur both in the face and scrambled face performed better in the menstrual phase than in the midluteal
stimuli tasks. Thus, unlike our initial prediction, it may not phase, suggesting that the menstrual phase with low hor-
be straightforward to argue that women's performance would mone level might influence better performance, particularly
simply decline in the menstrual phase according to the low in tasks related to attention.3 Hormonal changes during the
level of hormones, while the performance would be better in menstrual cycle may modulate perceptual and cognitive
the ovulation phase according to the higher hormonal levels. functions of women, but such modulation might appear in
Similarly, several studies reported better task performance different manners according to the types of task.
when the hormonal level was lower in the menstrual or fol- Some studies also reported that emotional facial expres-
licular phase than when the hormonal level was higher in the sions could be associated with specific colours, and thus, we
ovulation or luteal phase. For instance, women had better are likely to imagine facial expressions with particular col-
performance in spatial tasks such as mental rotations and ours. For instance, participants were more likely to relate a
IRIGUCHI ET AL. 7

FIGURE 4 Average reaction time (ms) in the scrambled face stimuli task with the SE for participants in the menstrual phase (left) and
ovulation phase (right) according to stimulus colour and type. Graph (A) shows reaction times to happy scrambled shape, graph (B) shows those to
neutral scrambled shape, and graph (C) shows those to sad scrambled shape. In these graphs, bars indicate the colour of each stimulus: white bar for
red, gray bar for yellow, and black-dotted bar for blue

happy face with colours such as yellow, a sad face with blue, differ between the menstrual and ovulation phases
and an angry face with red.36-38 Sutton and Altarriba examined (Figure 5). One possible explanation for these phenomena is
160 emotional words with both positive and negative mean- that participants might not have strong attention for nonso-
ings, and interestingly, the majority of participants tended to cial stimuli with colours in the menstrual phase, so reaction
associate colours with specific emotional words.38 Children times did not differ largely between the phases, while they
aged 7 to 8 years old also seemed to categorize specific col- might have stronger attention for social stimuli, including
ours into either happy or unhappy emotions, although gender facial expressions, together with colours in the menstrual
differences in categorization were observed.41 phase than in the ovulation phase. Our findings demon-
However, in this study, interference by emotional facial strated no interference with colour judgment by emotional
expressions in colour judgment was not observed, and this facial expressions, that is, the Stroop effect, but suggested
could imply that the association between colours and emo- possible tendencies for participants' attention to vary
tional facial expressions was not strong enough to affect per- according to the menstrual cycle phase and possibly
ceptual and attentional levels. In the scrambled face stimuli according to whether the stimulus type was socially mean-
task, on the other hand, interaction effects between the men- ingful or meaningless.
strual cycle phase and stimulus shape and between the phase The present study includes several limitations to be con-
and colour were found, and only the participants' reaction sidered. First, the number of participants for whom analyz-
times to a happy scrambled face and those to red did not able data were obtained was 11 of 26 participants, which
8 IRIGUCHI ET AL.

FIGURE 5 Average reaction time (ms) in the menstrual and ovulation phases in the face stimuli task and scrambled stimuli task, compared
only by stimulus type and colour. Graph (A) shows average reaction times in the face stimuli task by stimulus type, and graph (B) shows those by
colour. Graph (C) shows average reaction times in the scrambled face stimuli task by stimulus type, and graph (D) shows those by colour

was not large enough to reach robust conclusions. The age participants' next start date of the menstrual period. How-
range of participants was also relatively narrow. Thus, our ever, the menstrual cycle, ovulation, and hormonal level
results showed possible trends regarding colour judgment in could vary according to the participant, and thus, measure-
the Stroop task for women during the menstrual cycle, and a ment of the hormonal level would be necessary in order to
larger number and age range of participants would be neces- more accurately confirm hormonal conditions. Third, in this
sary to obtain more concrete conclusions in further studies. study, we focused on the interaction between colour and
Second, participants' menstrual cycle history was based on emotional facial expression in attentional behavior by colour
their own records, and we calculated estimated ovulation judgment in the Stroop task according to the menstrual
dates according to these records and confirmed that the cycle, and association between a chromatic mechanism and
experiment dates near the estimated ovulation were appro- hormonal changes was not examined. Several studies men-
priate or not by calculation of the date 14 days prior to tioned a possible association between sensitivity to short-
IRIGUCHI ET AL. 9

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Mayuko Iriguchi is a doctoral student at the Primate
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information. Evol Hum Behav. 2014;35(1):9-16.
Research Institute, Kyoto University, Japan. She is inter-
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Kyoto University. His research interest is in the evolution
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Psychol. 2015;159:108-115. Psychology at Japan Women's University, Tokyo, Japan.
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anxiety sensitivity, bodily expectations, and cultural beliefs on mates to humans and evolution of the family and
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Nobuo Masataka is a professor in the Cognition and
during an emotional Stroop task. Int J Psychophysiol. 2007;63(3):
Learning section at the Primate Research Institute, Kyoto
221-231.
[36] Takahashi F, Kawabata Y. The association between colors and University. His recent research covers colour preference
emotions for emotional words and facial expressions. Color Res and aesthetic perceptual judgment of music in children
Appl. 2018;43(2):247-257. with autism.
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bias and anxiety in primary school children: a modified emotional
attention assessed using the Stroop task during the
Stroop colour-naming task using pictorial facial expressions.
Psychol Sci. 2004;46(4):451-465.
menstrual cycle: Comparison between the menstrual
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