Effects of Trimester and Fetal Sex on Face Recognition Memory and
Hemispheric Asymmetry in Pregnancy
Evrim Gülbetekin1, Mehmet Şimşek2
1Akdeniz University,Faculty of Letters,
Depart-ment of Psychology, Antalya
2Akdeniz University,Medical Faculty,
Depart-ment of Gynecology and Obstetrics, Antalya Corresponding Author: Evrim Gülbetekin, Akdeniz University, Faculty of Letters, Depart-ment of Psychology, Antalya, Turkey Phone: +90-242-3103278 Fax: +90-0242 3102287 E-mail: evrimg@akdeniz.edu.tr Date of receipt: 03 November 2016 Date of acceptance: 16 January 2017
ABSTRACT
Background: Although hemispheric asymmetries (HA) in face perception during menstrual cycle
have been studied, there is no study about HA in face perception during pregnancy. The aim of this study was to find out if face perception changes during pregnancy and to test the effects of trimester and fetal sex on HA and face recognition memory.
Methods: In the first experiment, we investigated HA of pregnant women (n=31) in a
face-dis-crimination task by using visual half-field technique and compared their performance with non-preg-nant (n=34) women who were in menstruation phase. Additionally, face recognition memory was tested. In the second experiment, we tested the effects of trimester and fetus sex on face perception of pregnant women (n=49).
Results: Pregnant and non-pregnant participants showed right hemispheric dominance (RHD) in
face discrimination F(1, 63) = 8.17, p = .006, np2 = .11; however, pregnant women (n = 31, M = 6.16,
SD = 1.43) recognized more facial stimuli than non-pregnant women (n = 34, M = 5.24, SD = 1.77) F(1, 63) = 22,78, p = .001, n2 = .27. A RHD was observed in all trimesters F(1, 43) = 9.81, p = .003, np2 =
.19. However, we found a trimester-fetus sex interaction in LVF/RH (left visual field/right hemisphere) performance F (2, 43) = 5.07, p = .01, n2 = .19. The performance in LVF/RH condition improved from
the first trimester to the second trimester in pregnant women who had male fetus (p = .02) while it remained steady in pregnant women who had female fetus. Subjects in the third trimester recognized more stimuli than the subjects in the first trimester (p = .02).
Conclusions: Right hemispheric pattern for face-discrimination is stable while the performance
is affected by the trimester and fetal sex in pregnancy. Face recognition memory seems to be increased from the first trimester to the third trimester. The findings were discussed in the context of the cognitive effects of increasing hormone levels during pregnancy.
Keywords: Pregnancy, hemispheric asymmetry, face discrimination, face recognition memory,
visual-half field.
ÖZET
Hamilelikte Trimesterin ve Fetal Cinsiyetin Yüz Tanıma Belleği ve Hemisferik Asimetri Üzerindeki Etkisi
Amaç: Menstrüasyon döneminde yüz algısına ilişkin hemisferik asimetriler (HA) çalışılmış
ol-makla birlikte, hamilelik dönemindeki yüz algısına ilişkin HA ile ilgili hiçbir çalışma bulunmamaktadır. Bu nedenle, bu çalışmada hamilelik boyunca değişen yüz algısının ve trimester ile fetal cinsiyetin HA ve yüz tanıma belleği üzerindeki etkilerinin araştırılması amaçlanmıştır.
Yöntem: İlk deneyde bir yüz ayırt etme görevinde görsel yarı-alan tekniği kullanılarak hamile
kadınlardaki (n=31) HA araştırılmış ve bu katılımcıların performansları, hamile olmayan ve menstru-asyon döneminde bulunan kadınlarla (n=34) karşılaştırılmıştır. Ayrıca, yüz tanıma belleği test edilm-iştir. İkinci deneyde hamile kadınların (n=49) yüz algısında trimesterin ve fetüs cinsiyetinin etkileri test edilmiştir.
Bulgular: Hamile olan ve olmayan kadınlar yüz ayırt etmede bir sağ hemisfer baskınlığı (SAHB)
göstermiş (F(1, 63) = 8.17, p = .006, np2 = .11); bununla birlikte, hamile kadınlar (n = 31, M = 6.16, SD
= 1.43), yüz ayırt etme görevinde görmüş oldukları yüz uyarıcılarını hamile olmayan kadınlara (n = 34, M = 5.24, SD = 1.77) kıyasla daha yüksek oranda doğru olarak hatırlamıştır F(1, 63) = 22,78, p = .001, n2 = .27. Tüm trimesterlerde sağ hemisfer performansının daha yüksek olduğu gözlenmiştir (F(1,
43) = 9.81, p = .003, np2 = .19). Ayrıca, SOGA/SAH (sol görsel alan/sağ hemisfer) performansında
tri-mester-fetüs cinsiyeti etkileşimi gözlenmiştir F (2, 43) = 5.07, p = .01, n2 = .19. Erkek fetüse sahip olan
kadınlarda SOGA/SAH koşulundaki performans birinci trimesterdan ikinci trimestere doğru artış gös-termiş; kız fetusü olanlarda performans sabit kalmıştır. Genel olarak, üçüncü trimesterdeki katılımcılar, birinci trimesterdaki katılımcılardan daha fazla uyarıcı hatırlamıştır (p = .02).
Sonuçlar: Hamilelik boyunca yüz ayırt etmede sağ hemisfer örüntüsü sabit kalmakla birlikte,
performans trimester ve fetal cinsiyet tarafından etkilenmektedir. Yüz tanıma belleği ilk trimesterdan üçüncü trimestere doğru artış göstermektedir. Bulgular hamilelikte artan hormon düzeylerinin bilişsel etkileri bağlamında tartışılmıştır.
Anahtar sözcükler: Hamilelik, hemisferik asimetri, yüz ayırt etme, yüz tanıma belleği, görsel
INTRODUCTION
It has been known for literally hundreds of years that the two si-des of the human brain are different in their processing abilities and preferences.1 The structural and functional differences between the
two hemispheres are called hemispheric asymmetry. Although left he-misphere is specialized for language function and right hehe-misphere is specialized for spatial processing and face recognition, sex differences have been observed in some of those lateralized cognitive functions3.
Although not all lateralization studies have shown gender effect, “the pattern of a more symmetrical lateralization in females, but a more pronounced asymmetry in males pervades in many studies”.2 Thus,
hormonal differences may be one of the possible factors affecting he-mispheric asymmetries. There are some studies focusing on the link of hemispheric asymmetry and hormonal levels. By using half-visual field presentation techniques, Hausmann and Güntürkün have shown that performance of young women in the right (face discrimination, figural comparison) and the left hemisphere tasks (lexical decision) had chan-ged during the menstrual cycle whereas, the lateralization patterns for post-menopausal women were identical to those of young men.2
Young women showed less hemispheric asymmetry in their perfor-mance when they were tested in midluteal phase (when progesterone level was relatively high) and showed more asymmetrical performan-ce in menstrual phase (when progesterone level was low). According to progesterone-mediated interhemispheric decoupling hypothesis progesterone reduces cortico-cortical transmission resulting functi-onal hemispheric decoupling and a temporal reduction in functifuncti-onal asymmetry. 2 Hausmann and his colleagues have also found a strong
relationship among the levels of progesterone and functional cerebral asymmetries (FCAs) by using visual half field technique in various cog-nitive tasks.4 On the other hand, Compton and his colleagues found
no significant correlation between progesterone levels and interhe-mispheric communication. 5 Recent studies have shown that estradiol
had also influence on functional cerebral asymmetries.6-8 Dietrich and
colleagues showed that the estrogen level increases the size, but not the pattern of cortical activation during the performance of cognitive tasks such as verbal and mental rotation.9
Being one of the lateralized cognitive functions, face perception has been studied by means of a number of imaging techniques and right hemisphere dominance was observed even if a complex bilate-rally distributed network is responsible for such perception.10 Other
behavioral studies such as chimeric face studies11 and half-visual field
experiments12 have supported this right hemisphere specialization in
face perception.
Lateralization in face perception is also thought to be affected by hormonal fluctuations. Hausman and colleagues observed that estrogen, but not progesterone was correlated to the performance of both hemispheres in face discrimination task4. In another study it has
been shown that asymmetry pattern in face perception decreased li-nearly from a large right hemisphere superiority during menstruation to a small left hemisphere superiority during the premenstrual pha-se.13 However, Bibawi and colleagues found that face processing is
less likely to show phase-related effects indicating a right hemispheric dominance.14
Interestingly, right hemisphere lateralization is more apparent in men than it is in women15 On the other hand, face perception studies
indicate that women especially in emotion perception tasks, have su-perior face recognition ability than men.16-20 Women’s advantage over
men in memory for faces is particularly marked for female faces and is typically smaller for male faces.21 In an fMRI study it was found that
women recognized more female than male faces and they showed
higher activity to female than male faces in individually defined regi-ons of fusiform face area (FFA) and inferior occipital gyri.22 Infant
fa-ces elicit sex differenfa-ces in behavior and brain responses that appear dependent on sex hormones.10 Some studies have shown that babies’
faces took the attention more than adult faces did. 23,24 For infant faces,
Kringelbach and colleagues found a peak in activity first in medial or-bitofrontal cortex and then in the right FFA.25
Hormones also affect the recognition of emotions: it changes cyc-lically in women and negative correlation was found between recogni-tion of negative emorecogni-tions and both estrogen and progesterone levels.
26,27 Mareckova and colleagues found stronger neural responses to
fa-ces in the right FFA in women taking oral contraceptives (vs freely cyc-ling women) and during mid-cycle (vs menstruation) in both groups.28
It seems that neural responses to faces in the right FFA get higher when the levels of progesterone and estrogen increase. Consistently, it was suggested that increases in progesterone levels during the luteal pha-se of menstrual cycle were associated with increapha-sed accuracy in de-coding facial expressions and increased attention to social stimuli.29
Conway and colleagues found that non-pregnant women were more sensitive to facial cues signaling nearby contagion and physical threat when progesterone level was raised concluding that elevating proges-terone prepares the body for pregnancy.30
Pregnancy is a special period of a woman’s life during which va-rious hormonal changes (estradiol, progesterone, 17-hydroxyproges-terone, and 11-deoxycortisol, cortisol and androstenedione) peak31.
These hormonal changes do not only prepare the woman to share her body with a developing embryo, but also prepare the body including brain towards being a mother. It was shown that brain plasticity oc-curs during pregnancy.32-36 The neurological effects of pregnancy also
include areas that regulate learning, memory and areas involved the control of fear and anxiety.37 A large amount of data shows that
preg-nancy affects memory and attention in women.36,38-40,42-46 Anderson
and Rutherford pointed out the pregnancy-induced advantage in re-cognition memory and social re-cognition.39 They interpreted the
preg-nancy-induced memory decline in some cognitive tasks and enhanced social cognition as a protective function of pregnancy.39
There are also pregnancy studies focusing on face perception. The comparison of early and late pregnancy shows that participants had higher accuracy scores to encode negative emotions such as sadness during late pregnancy.47 Similarly, Roos and colleagues found that
pregnant women showed altered attentional responses to fearful fa-ces, in comparison to controls and attention to fear was significantly associated with increased levels of estrogen and progesterone at tri-mester 2, and decreased levels of cortisol at tritri-mester 3 of pregnan-cy.48 In another study, Roos and colleagues measured neural activity of
prefrontal cortex (PFC) of pregnant women for fearful faces by using near-infrared spectroscopy (NIRS).49 They found that the activation
was most pronounced at trimester 2, compared to the other trimes-ters. PFC activation was significantly associated with increased levels of cortisol and testosterone in pregnancy.49
The sex of the fetus may have an additional hormonal effect on pregnant women’s cognition. It has been shown that maternal serum HCG (MSHCG) is higher when the fetus is a female than when it is a male as early as week 3 post-fertilization.50 Additionally, the
concent-ration of anti-Müllerian hormone (AMH) changes according to the fetal sex. AMH is known to be one of the two classic hormones deter-mining sex differentiation in the developing fetus. Immediately after the testis becomes morphologically recognizable (at around day 40 after conception in humans) it starts to secrete AMH, which, in concert with testosterone, ensures male development of the secondary sex
characteristics. In contrast, the female fetus does not secrete these two hormones and develops femaleness according to the classical pa-radigm.51 Consistently, a recent study showed that pregnant women
with male fetuses performed better than mothers with female fetuses on the Computation Span (arithmetic working memory), Listening Span (verbal working memory ) and the Shephard Metzler Mental Ro-tation Task (Spatial visualization/spatial working memory).52
In the light of the presented literature, we conducted two experi-ments: In the first experiment, we aimed to examine face perception in pregnancy where we can indirectly observe the effects of hormo-nes such as progesterone and estradiol by comparing pregnant wo-men in the third trimester and non-pregnant wowo-men. We investigated hemispheric asymmetries in pregnant women in a face discrimination task which is known as a typical right hemisphere task53 and
compa-red their performance with young women who were not pregnant and in menstruation phase of their cycle when the progesterone and estrogen levels were expected to be low. Our hypothesis was that he-mispheric specialization pattern of face processing in pregnant and non-pregnant women would be different due to the hormonal chan-ges occurring in pregnancy. Additionally, we hypothesized that face recognition performance of pregnant women would be higher due to the increasing hormone levels. In the second experiment, we aimed to test the effects of trimester and sex of fetus on hemispheric asymmetry pattern in face discrimination and face recognition performance. Our hypothesis was that hemispheric specialization pattern in face proces-sing and face recognition performance of pregnant women would be affected by the trimester and fetus sex due to being exposed to diffe-rent hormone levels.
METHODS Participants
Sixty-five women subjects participated the study, 31 of whom visited the Gynecology and Obstetrics Polyclinic of Akdeniz Univer-sity Medical Faculty Hospital. All pregnant subjects were in the third trimester of their pregnancy. The other 34 women were undergradu-ate students in Akdeniz University who had regular menstrual cycle. Women who had 28-32 days menstrual cycle were assumed to have regular cycle. Non-pregnant women did not use any oral contracepti-ves and none of the subjects had any
hor-monal, neurological and psychiatric treat-ment. None of the subjects had any head injury, neurological or psychiatric diagnosis. The age of pregnant women ranged 19-39 (M = 27.48, SD = 4.78 years) and the age of non-pregnant women ranged 19-25 (M = 20.8, SD = 1.8 years). Prior to the expe-rimental sessions, subjects were informed about the general procedure and a questi-onnaire about their general health (psycho-logical, neurological symptoms etc.) was filled. Pregnant women filled an additional questionnaire about their pregnancy-rela-ted symptoms. The gestation weeks of the pregnant women ranged 24-38 (M = 30.16, SD = 4.82 weeks). Non-pregnant women were tested during their menstruation pha-se between the 1st and the 5th days of their cycle. Edinburgh Handedness Inventory was used to determine participants’ hand
use.4 The asymmetry-index (LQ) was calculated as (R-L / R+L) / 100.
The subjects whose asymmetry index were +60 and above included in
the experiment as right hand users. The subjects had normal or corre-cted visual acuity. All participants completed and signed an informed consent form while their anonymity was strictly guaranteed. Experi-mental procedure was approved by the Ethical Committee of Akdeniz University Faculty of Medicine.
Materials and Procedures
Facial Stimuli. Nine facial photographs (3 men’s, 3 women’s and 3 babies’ faces) were used. The photographs were black and white and only facial features and hair were included. In half of the trials, one element of the face (the eye, nose, or mouth) was erased.
Procedure
Subjects were seated in an adjustable chair and their heads were fixed by a chin rest approximately 40 cm from the screen in order to maintain viewing distance.
Face discrimination task
E-Prime 2 software was used for stimulus presentation and data acquisition. Subjects were instructed to fix their heads in the chin rest and focus on the fixation point on the computer screen. After present-ing the fixation point for 2seconds, a face stimulus was shown in one of the visual fields for 120 msec. After the first stimulus disappeared, the second stimulus was presented in the same visual field for 120 msec. The stimuli subtended a visual angle of 10.13° horizontal by 12.17° vertical and each stimulus positioned 13.40° from the fixation point.
After the presentation of the two stimuli, subjects were asked if the two photographs were identical or not. In half of the trials (36), the photographs were identical; whereas, in the other half of the trials (36) the photographs were changed by erasing one element of the facial re-gions such as eye, nose or mouth. Participants were told to press “1” on the keyboard if the faces were identical and to press “2” if any part of the face was erased. Participants’ evaluation time and responses were recorded. Figure 1 shows a left visual field /right hemisphere stimulus presentation as an example to the procedure. The stimuli were pre-sented in a randomized order and the order of the stimulus position (left-visual half field (LVF) / right visual half field (RVF)) was also ran-domized. Participants were tested by using both the left and the right hands. The order of the hand use was counterbalanced between sub-jects. One session consisted of 72 trials.
At the end of the experimental session, 18 facial photographs were presented on paper. Nine of the face photographs were the
Figure 1. Face discrimination task procedure. A LVF/RH presentation is represented. In half of
the trials (a), the photographs were identical; in the other half of the trials (b) the photographs were changed by erasing one element of the facial regions such as eye, nose or mouth.
original faces which were presented in the experiment. The other nine photographs were new faces. The original and the new faces were pre-sented in a mixed fashion. The subjects were required to choose the faces that they had seen in the experimental session. The numbers of the correct and incorrect answers were recorded in order to measure the face recognition memory of the subjects. We calculated the “fa-cial recognition memory score” by subtracting the number of incorrect stimuli from the number of the correct stimuli.
RESULTS
Facial Discrimination Task: Correct Response Ratio
We calculated the ratio of correct responses to total responses. In order to determine the effects of the subject type and visual half field/hemisphere on subjects’ correct response ratio, 2 x 2 (Subject type [menstruation, pregnant] × Visual half field/hemisphere [RVF/ LH and LVF/RH]) repeated measures ANOVA was conducted. Data analyses were carried out with subject type as between subject fac-tor and visual half field/hemisphere as a within subject facfac-tor. Within subject factor results indicated a significant main effect of visual half field/hemisphere, F(1, 63) = 8.17, p = .006, np2 = .11 (Figure 2).; but no
significant interaction effect of subject type and VHF/hemisphere was found (Table 1a).
We observed that, correct response ratio in LVF/RH condition is higher than the correct response ratio in RVF/LH conditions (Table 1b). Therefore, subjects in both menstruation and pregnancy groups showed a right hemispheric advantage in face discrimination task.
(Table 1a, 1b)
Facial Discrimination Task: Response Time
In order to determine the effects of subject type and visual half field/hemisphere on subjects’ response time (the medians of the re-action times), 2 x 2 (Subject type [mens, pregnant] × Visual half field/ hemisphere [RVF/LH and LVF/RH]) repeated measures ANOVA was conducted. Data analyses were carried out with subject type as be-tween subject factor and visual half field/hemisphere as a within sub-ject factor. Within subsub-ject factor results indicated no significant main effect of visual half field/hemisphere, and no significant interaction effect of subject type and VHF/hemisphere.
Face Recognition Memory
We presented 18 facial photographs at the end of the experi-mental session and calculated the “facial recognition memory score” by subtracting the number of incorrectly recognized stimuli from the number of correct stimuli. We conducted one-way ANOVA in order to compare the memory score of each group. The one-way ANOVA showed that the difference in memory scores of menstruation group (n = 34, M = 5.24, SD = 1.77) and pregnant group (n = 31, M = 6.16, SD = 1.43) was statistically significant F(1, 63) = 22,78, p = .001, n2 =
.27 (Table 2a). Pregnant women recognized more facial stimuli than non-pregnant women. Descriptive statistics are presented in Table 2b, Figure 4.
EXPERIMENT II METHODS Participants
Forty-nine pregnant women participated the study who visit-ed the Gynecology and Obstetrics Polyclinic of Akdeniz Universi-ty Medical FaculUniversi-ty Hospital. Of those 16 were in the first trimester
Figure 2. Means of correct response ratios in RVF/LH and LVF/RH
conditions of pregnant women and women at menstrual phase. Both groups showed right hemisphere dominance in face discrimination task.
Table 1a. Results of Repeated Measures ANOVA for Correct Response
Ratio in Face Discrimination Task
Source Sum of Squares df Mean Square F p n2 Between (Subject type) .015 1 .015 .673 .415 .011
Error 1.409 63 .022
Within (VHF/H) .084 1 .084 8.17 .006 .115 Subject type X VHF/H .003 1 .003 .285 .596 .04
Error .645 63 .01
Table 1b. Means and Standard Deviations for Correct Response Ratio
in Face Discrimination Task
RVF/Left Hemisphere LVF/Right Hemisphere
Subject Type M SD M SD
Pregnant .77 .13 .81 .07
Menstruation .74 .16 .80 .13
Figure 3. Facial recognition memory score (means of correct -
incorre-ct facial stimuli) of pregnant women and women at menstrual phase. Pregnant women recognized more facial stimuli than women at mens-trual phase.
(M = 10.06, SD = .58 weeks), 16 were in the second trimester (M = 19, SD = .59 weeks) and other 17 were in the third trimester (M = 31.4, SD = 1.09 weeks) of their pregnancy. The age of pregnant women ranged 19-38 [the first trimester (M = 27.6, SD = 1.55 years), the second tri-mester (M = 28.63, SD = 1.32 years), the third tritri-mester (M = 26.76, SD = 1.31 years)]. Education levels (p > .05) and age of the subjects (p >.05) did not differ among three groups. Twenty-five of the subjects had male fetuses and 24 of the subjects had female fetuses. Education levels (p > .05) and the age of the subjects (p > .05) did not differ be-tween these two groups. Prior to the experimental sessions, subjects were informed about the general procedure and a questionnaire about their general health (psychological, neurological symptoms etc.) and an additional questionnaire about their pregnancy-related symptoms were filled. Edinburgh Handedness Inventory was used to determine participants’ hand use.54 The asymmetry-index (LQ) was calculated as
(R-L / R+L) / 100. The subjects whose asymmetry index were +60 and above included in the experiment as right hand users. The subjects had normal or corrected visual acuity. All participants gave written in-formed consent. Experimental procedure was approved by the Ethical Committee of Akdeniz University’s Faculty of Medicine.
Materials and Procedures
The same stimuli and experimental procedure in the first experi-ment were used. An additional information, the sex of the fetus, was recorded. It was determined by ultrasound imaging techniques. The sex of the fetus was confirmed after the delivery.
RESULTS
Hemispheric Asymmetry in Facial Discrimination Task: Cor-rect Response Ratio
We calculated the ratio of correct responses to total responses. In order to determine the effects of trimester, fetus sex and visual half field/hemisphere on subjects’ correct response ratio, 3 × 2 × 2 (Trimes-ter [1, 2, 3] × Fetus sex [male, female] ×Visual half field/hemisphere [RVF/LH and LVF/RH]) repeated measures ANOVA was conducted. Data analyses were carried out with trimester and fetus sex as be-tween subject factor and visual half field/hemisphere as a within sub-ject factor. Within subsub-ject factor results indicated a significant main effect of visual half field/hemisphere, F(1, 43) = 9.81, p = .003, np2 =
.19 (Table 3a, Figure 5); but no significant interaction effect of trimester and VHF/hemisphere was found. We found neither interaction effect of fetus sex and VHF/hemisphere nor interaction effect of trimester, fetus sex and VHF/hemisphere.
We observed that, correct response ratio in LVF/RH condition is higher than the correct response ratio in RVF/LH conditions (Table 3b). Therefore, subjects in all trimester groups and both subject groups ha-ving female and male fetuses showed the same right hemispheric pat-tern in face discrimination.
Hemispheric Asymmetry in Facial Discrimination Task: Res-ponse Time
In order to determine the effects of trimester and fetus sex and visual half field/hemisphere on subjects’ response time (the medians of the reaction times), 3 × 2 × 2 (Trimester [1, 2, 3] × Fetus sex [male, female] ×Visual half field/hemisphere [RVF/LH and LVF/RH]) re-peated measures ANOVA was conducted. Data analyses were carried out with trimester and fetus sex as between subject factor and visual half field/hemisphere as a within subject factor. Within subject factor results indicated no significant main effect of visual half field/hemi-sphere, and no significant interaction effect of trimester, fetus sex and VHF/hemisphere.
Effects of Trimester and Sex of Fetus on each Hemispheric Condition (RVF/LH and LVF/RH)
We aimed to find out if trimester and fetus sex have any effect
Table 2a. One-Way ANOVA Results for Facial Recognition According
to Subject Type
Source SquaresSum of df SquareMean F p
Between 60.15 1 60.15 22.78 .001
Within 166.31 63 2.64
Sum 226.46
Table 2b. Means and Standard Deviations of Facial Recognition
Memory
Baby Faces Female Faces Male Faces Total
Subject Type M SD M SD M SD M SD
Pregnant 2.63 .55 2.38 .66 2.09 .73 7.16 1.42 Menstruation 2.32 .77 1.44 .89 1.50 .66 5.23 .31
Figure 4. Number of stimuli (baby faces, female and male faces) those
are correctly recognized by pregnant women and women at menstrual phase.
Figure 5. A LVF/RH superiority pattern was observed in face
on the performance of RVF/LH and LVF/RH conditions. Therefore, we conducted multivariate ANOVA in order to see the effects of indepen-dent variables (trimester and fetus) on depenindepen-dent variables separately (correct response ratio of RVF/LH and LVF/RH conditions, response time of RVF/LH and LVF/RH conditions). MANOVA results indicated that the multivariate main effect of trimester and fetus sex on depen-dent variables were not significant. However, the results from this MANOVA demonstrated a significant multivariate effect for the inte-raction of fetus sex and trimester, F (8, 78) = 2.09, p < .05; Hotelling’s T = .43, partial n2 = .18.
Univariate results demonstrated a significant interaction effect of fetus sex and trimester for correct response ratio of LVF/RH, F (2, 43) = 5.07, p = .01, n2 = .19 and response time of LVF/RH, F (2, 43) = 3.78, p =
.03, n2 = .15. Additionally, univariate results demonstrated a significant
interaction effect of fetus sex and trimester for response time of RVF/ LH, F (2, 43) = 3.92, p = .03, n2 = .15. The results for correct response
ratio of RVF/LH was not significant.
Following the significant fetus sex x trimester interaction effect, we conducted two separate MANOVA for each fetus group in order to see the trimester effect on correct response ratio of LVF/RH, response time of LVF/RH and RVH/LH. Results from this MANOVA demonst-rated a significant multivariate effect for the trimester in male fetus group, F(8, 36) = 2.31, p = .01; Hotelling’s T = 3.07, partial n2 = .41, but not in female fetus group. The univariate results for women who had male fetus indicated a significant trimester effect on correct response ratio of LVF/RH, F (2, 22) = 5.02, p = .02, n2 = .31 (Figure 6). No significant effect was found for the response time of LVF/RH and RVH/LH. Post hoc Tukey HSD tests for correct response ratio of LVF/RH showed that the difference between the performance of subjects in trimester 1 (n = 9, M = .69, SD = .19) and trimester 2 (n = 7, M = .88, SD = .05) was statistically significant however no significant difference was found between the trimester 1 and trimester 3 (n = 9, M = .83, SD = .08) and also trimester 2 and 3.
Face Recognition Memory
We presented 18 facial photographs at the end of the experimental session and calculated “facial recognition memory score” by subtracting the number of incorrectly recognized stimuli from the number of correct stimuli as we did in the first experiment. We conducted one-way ANO-VA in order to compare the memory scores of each group. The one-way ANOVA showed that the difference among memory scores of subjects in trimester 1 (n = 16, M = 6.56, SD = 1.15), trimester 2 (n = 16, M = 6.81, SD = 1.17) and trimester 3 (n = 17, M = 7.72, SD = 1.66) was statistically significant F(2, 43) = 4.35, p = .02, n2 = .17 (Table 4a, 4b,
Fi-gure 7). Tukey Post-hoc comparison tests indicated that the memory scores of subjects in trimester 1 and the subjects in trimester 3 were different, p = .02. However, neither the difference between trimester 1 and trimester 2 nor the dif-ference between trimester 2 and 3 were statistically signifi-cant. Pregnant women in trimester 3 recognized more facial stimuli than the pregnant women in trimester 1. The main effect of fetus sex and the interaction effect of trimester and fetus sex were not significant.
DISCUSSION
In the first experiment, we compared the hemispheric asymmetry pattern of pregnant and non-pregnant women in a face discrimina-tion task. We observed that both pregnant women and the women at menstrual phase showed a right hemispheric advantage for cor-rect response ratio data. Our findings for women in menstruation is consistent with the other studies11,10,3,12 indicating right hemispheric
dominance in face perception during menstrual phase when the levels of estrogen and progesterone are relatively low. On the other hand, parallel with the progesterone-mediated interhemispheric decoupling hypothesis we were expecting that pregnant women might show less hemispheric asymmetry due to elevating levels of progesterone. How-ever, we observed that pregnant women had also right hemispheric bias in face discrimination. Our response ratio findings are consistent with the findings of Bibawi et al. showing that face processing is less likely to show phase-related effects indicating a right hemispheric dominance.14 Consistently, some emotional face perception
stud-ies47,48 in pregnancy indicated that levels of estrogen and progesterone Table 3a. Results of Repeated Measures ANOVA for Correct Response Ratio in
Face Discrimination Task
Source SquaresSum of df SquareMean F p n2
Between (Trimester) .020 2 .010 .24 .792 .011 (Fetus) .000 1 .000 .007 .935 .000 (Trim X Fetus) .270 2 .135 3.23 .05 .13 Error 1.799 43 0.42 1.17 Within (VHF/H) .072 1 .072 9.81 .003 .19 Fetus X VHF/H .000 1 .000 .049 .82 .001 Trim X VHF/H .012 2 .006 .812 .45 .036 Trim X Fetus X VHF/H .017 2 .009 1.17 .318 .052 Error .316 43 .007
Table 3b. Means and Standard Deviations for Correct Response Ratio in Face
Discrimination Task
RVF/Left
Hemisphere HemisphereLVF/Right
Subject Type N M SD M SD
Trimester 1 16 .75 .18 .77 .16
Trimester 2 16 .73 .21 .80 .20
Trimester 3 17 .76 .11 .83 .06
Figure 6. The LVF/RH performance of subjects who had male fetus
im-proved from the first trimester to the second trimester, whereas LVF/ RH performance of subjects who had female fetus remained steady.
were associated with higher performance in attention and encoding tasks. It seems that elevating levels of estrogen and progesterone in pregnancy do not change the hemispheric asymmetry pattern rather it may steam up the typical hemispheric dominancy pattern for face discrimination.
The second interesting finding of our first experiment was that pregnant women recognized more facial stimuli than women in men-struation phase did contrary to the general findings about decline of memory performance in pregnancy. Similarly, Anderson and Ruther-ford pointed out pregnancy-induced advantage in recognition memo-ry and social cognition.39 Roos and colleagues also showed that
preg-nant women’s attention to fearful faces was significantly associated with increased levels of estrogen, progesterone and cortisol in preg-nancy.48 Thus, we propose that estrogen and additionally
progester-one may be responsible for increase in facial memory scores during luteal phase and pregnancy and for decline of facial memory scores in menstruation phase. Because these two hormones are secreted in maximum levels during luteal phase and pregnancy, however it reach-es its minimum levels in menstruation phase.
We observed from the descriptive statistics that both pregnant and non-pregnant women recognized more baby faces than female and male adult faces. Studies about infant face perception indicated that baby faces took the attention more than adult faces did. 23,24 This
may be due to the anatomic structures that baby faces have such as large eyes, small chin and short face. These physical features may have stronger effects in memory and they may be easier to be recalled. Even if the baby faces activated the same brain regions as adult stimu-li did, Kringelbach and colleagues showed that infant faces elicited early activity in OFC that adult faces could not.25 It seems that the infant face is processed
in a somewhat specific way. Thus, one may expect that due to having a potential baby, pregnant women might be more sensitive to baby faces comparing to non-pregnant women. However, we observed that both groups recognized baby faces better than the other faces. Because all of the young women have a potential to have a baby, their brain may be hard-wired for being a mother before they have this expe-rience. We found that pregnant women significantly recognized more faces than women in menstruation did. In pregnancy, recognizing a man or a woman who is not trustworthy may be critical for both the survival of mother and her offspring. Additionally, recent findings indicated that gray matter volume in brain regions related to social cognition chang-es during pregnancy and 2 years post-pregnancy55. Probably these
changes improve woman’s ability to understand her baby’s needs. In the second experiment, we compared hemispheric asymmetry pattern in face perception and face recognition memory among tri-mesters and additionally we tested the effect of fetus sex. We observed the same left visual field/right hemispheric bias for correct response ratio in all trimesters. Additionally we found a significant fetus sex and trimester interaction effect on correct response ratio of LVF/RH. The correct response ratio of LVF/RH in women who had male fetus changed among trimesters while correct response ratio of LVF/RH in women who had female fetus remained steady. Correct response ratio of LVF/RH increased from trimester 1 to trimester 2 for mothers who had male fetus. Second trimester is a critical time point for sexual dif-ferentiation in genitals of fetus. Immediately after the testis becomes morphologically recognizable (at around day 40 after conception in humans) it starts to secrete AMH, which, in concert with testoster-one, ensures male development of the secondary sex characteris-tics.51 Increasing levels of AMH and testosterone might be responsible
for the improvement of right hemispheric performance of mothers with male fetus in the face discrimination task. Consistently, anoth-er study indicated that pregnant women with male fetus panoth-erformed better than mothers with female fetus did on the Shephard Metzler Mental Rotation Task, which also requires using right hemisphere.52
Neural responses to faces in the right FFA got higher when the levels of progesterone and estrogen increased.28 Similarly, PFC NIRS
activa-tion for faces was most pronounced at trimester 2 compared to other trimesters and it was associated with increased levels of cortisol and testosterone.49 Additionally, attention to faces was significantly
asso-ciated with increased levels of estrogen and progesterone at trimester 2.48 Overall, increasing hormone levels in trimester 2 seem to improve
right hemisphere’s performance on face processing.
Another result of the second experiment was that, pregnant wo-men in trimester 3 recognized more faces than pregnant wowo-men in trimester 1 did. It seems that face recognition memory got better with Table 4a. One-Way ANOVA Results for Facial Recognition According to Trimesters
Source SquaresSum of df Mean Squ-are F p
Between 12.01 2 6.007 4.193 .021
Within 65.904 46 1.43
Sum 77.918 48
Table 4b. Means and Standard Deviations of Facial Recognition Memory
Baby Faces Female Faces Male Faces Total
Subject Type M SD M SD M SD M SD Male Fetus Trimester 1 2.56 .53 2.44 .53 1.67 .50 6.33 1.22 Trimester 2 2.86 .38 1.29 .49 2 .82 6.14 1.07 Trimester 3 2.78 .67 2.78 .44 2.22 .83 7.78 1.56 Femala Fetus Trimester 1 2.86 .38 2.29 .49 2.14 .69 6.86 1.07 Trimester 2 2.56 .53 2.67 .50 2.11 .60 7.33 1 Trimester 3 2.63 .52 2.25 .71 2.50 .54 7.63 .92
Figure 7. Subjects in the third trimester recognized more facial stimuli
the increasing hormone levels in pregnancy. Second trimester is a cri-tical period of pregnancy for hormonal fluctuations: Cortisol increa-sed up to the second trimester and androstenedione increaincrea-sed by 80 percent by gestation week 12 then remained steady.31 AMH in
con-cert with testosterone goes on to be secreted in the second trimester from male fetuses. Therefore, additional hormonal effects from fetus occur since trimester 2. Other hormones such as cortisol, androstene-dione, DHEA-S may also mediate the functional asymmetries of face perception in pregnancy. Therefore, more detailed hormone measures should be taken into account in order to clarify the hormonal effects on hemispheric asymmetry pattern and face recognition memory in pregnancy.
One of the limitations of our study is, hormone levels were not measured in pregnant and non-pregnant women. We collected data according to the term of menstrual cycle and pregnancy. However, it seems that it is crucial to show the link between hormone levels and the performance. The second limitation is we did not have direct me-asurement of hemispheric activity. We measured the behavioral aspe-cts of hemispheric asymmetry such as the reaction time and the cor-rect response ratio by using visual half field presentation technique. It would be supportive to use a direct brain imaging technique for showing the hemispheric asymmetry pattern in face perception.
Overall, our study evidenced that the term of pregnancy is a specific timeframe for face perception in women. Progesterone and estrogen are thought to be the most probable hormones associated with the improvement in face perception. Additionally, AMH and tes-tosterone may be responsible hormones for the improvement of right hemispheric performance of mothers with male fetuses in the second trimester. It seems that all these hormones have influence on face per-ception during pregnancy; however, there is strong need for further research with hormonal measures to clearly understand how the hor-mones effect hemispheric asymmetries and face recognition memory in pregnancy.
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