Sex difference and menstrual cycle effects on semantic priming and remembering Anlamsal hazırlama ve hatırlamada cinsiyet farkı ve menstural dönem etkileri

Purpose: It is known that women and men may have different performance in some cognitive tasks and different hemispheric specializations. However, results of the sex difference studies are not always consistent. Recent studies indicate that some cognitive abilities of women fluctuate throughout menstrual cycle. In this study, it is aimed to find out if men and women in ovulation and menstruation phases perform differently in semantic priming (SP) task and remembering task. Additionally, it is aimed to find out if there is any hemispheric specialization in SP. Methods: Seventy two women and 29 men undergraduate students participated to the study. Two pictures were presented successively to participants for SP. The first picture was presented for 100 msec on the leftside, right-side or the center of the screen according to the experimental condition by using visual half-field technique and the second picture was presented on the center. Participants were required to report if two pictures were related or unrelated. After the SP task, participants chose stimuli that they had rememberred from a list of the stimuli in the Özet Amaç: Kadınların ve erkeklerin bazı bilişsel işlemlerde ve hemisferik özelleşmelerde farklılık gösterdiği; buna karşın, cinsiyet farklılıklarına ilişkin çalışmaların her zaman çok tutarlı olmadığı bilinmektedir. Son dönemlerde yapılan çalışmalar, kadınlardaki bilişsel becerilerin menstural döneme bağlı olarak dalgalanma gösterebildiğine işaret etmiştir. Sunulan çalışmada erkeklerin ve farklı menstural dönemdeki kadınların (yumurtlama ve mensturasyon) anlamsal hazırlama (AH) ve hatırlama görevindeki peformansları yönünden farklılık gösterip göstermediğini incelemek amaçlanmıştır. Ayrıca AH görevinde cinsiyete özgü hemisferik özelleşme olup olmadığı incelenmiştir. Yöntem: Çalışmaya 72 kadın ve 29 erkek üniversite öğrencisi katılmıştır. AH görevi için katılımcılara arka arkaya iki resim gösterilmiştir. Görsel-yarı alan tekniği kullanılarak ve deney gruplarına uygun olarak ilk resim sol görsel alanda, sağ görsel alanda ya da merkezde100ms sunulmuş; katılımcılardan merkezde sunulan birinci resimle ikinci resmin ilişkili olup olmadığını belirtmeleri istenmiştir. AH görevinin ardından katılımcılara deneydeki uyarıcıların bir 1 Assistant Prof. Dr. Akdeniz University, Faculty of Letters, Department of Psychology, evrimg@akdeniz.edu.tr 2 Prof. Dr., Izmir University of Economics, Faculty of Arts and Sciences, Department of Psychology, hakan.cetinkaya@ieu.edu.tr 3 Associate Prof. Dr., Izmir University of Economics, Faculty of Arts and Sciences, Department of Psychology, seda.dural@ieu.edu.tr Gülbetekin, E., Çetinkaya, H., & Dural, S. (2015). Anlamsal hazırlamada ve hatırlamada cinsiyet farkı ve menstural dönem etkileri. International Journal of Human Sciences, 12(1), 743-760. doi: 10.14687/ijhs.v12i1.3197 744 experiment in one-minute period. Findings: Results indicated that all groups had shown SP and there was no hemispheric specialization. Men responded related pictures faster than women in ovulation period however, no difference was observed between men and women in menstruation phase. Similarly, men remembered more stimuli than the women in ovulation phase. But no difference was observed between the number of stimuli remembered by the men and women in menstruation phase. Discussion and Conclusion: Generally findings indicated that cognitive sex differences might change according to the menstrual phase of women and these cyclical changes should be considered in reviewing the results of sex difference studies or conducting new research. It was proposed that cyclical cognitive sex differences might be related to hormonal levels those fluctuate across the menstrual cycle. The findings were discussed in the context of the negative effects of increasing luteinizing hormone (LH) levels on attentional and executive functions in both ovulatory phase and Alzheimer’s disease.


Extended English Abstract
How semantic knowledge is represented in the human brain and in our cognitive system is one of the most intriguing and debated topics of contemporary neuropsychology (Laiacona, Barbarotto, & Capitani, 2006).Processing of semantic knowledge also became a frequently studied subject due to it's close relations to decision making, categorization and problem solving.Additionally, studying semantic knowledge seems to be critical to understand the mechanisms underlying diseases such as dementia and Alzheimer's disease in which there is big loss of understanting.
Semantic priming is one of the experimental methods for studying semantic knowledge."Priming" follows an encounter with a stimulus (a word, a face or other object) and constitutes unconscious alterations in our subsequent response to that stimulus or a related one.These behavioral changes can include increase of speeding response, increasing the accuracy of response, or biasing (Smith & Kosslyn, 2007).Semantic priming (SP) is remembering a target stimulus ('chair'), faster when it is preceeded by a related stimulus ('table '), than it is preceeded by an unrelated stimulus ('horse').Usually, words or pictures are used as prime or target stimuli in SP tasks and subjects are required to state if the two stimuli are related or which category the target stimulus is belong to.
In an SP study (Laisney et al., 2011), a picture and a word those belong to same category were presented to subjects and they were asked if the target stimulus was belong to a natural (animal) or artificial (object) category.They ( 2011) found an SP effect showing that the subjects responded faster for the same category stimuli.
On the other hand, some studies (Barbarotto et al., 2002;Bermeitinger et al., 2008;Laws, 2002) indicated that there was a sex difference in SP tasks.For instance, women had more positive priming effect than men in natural categories while men had priming effect in both natural and artificial categories (Bermeitinger et al., 2008).The data concern Alzheimer patients, aphasic patients and an unselected series of patients affected by herpetic encephalitis indicated disproportionate impairment of knowledge of biological items in males (See in Laicona et al., 2006).In another sex difference study, Gohier and colleagues (2013) found that male participants demonstrated significantly stronger priming effects in emotionally negative conditions, compared to females while female participants demonstrated significantly stronger priming effects in emotionally positive conditions.Some EP studies (Bermeitinger et al., 2008;Meyer & Federmeier, 2007) showed that right and left hemispheres might give different contributions to semantic priming.Meyer and Federmeier, (2007) proposed that left hemisphere focused on only one context-related meaning in SP task.In another study (Koivisto & Revonsuo, 2000) left hemisphere was found to be related to priming effects for both picture and word stimuli.However, there is also data (Koivisto & Laine, 1999) showing that both hemispheres contributed to sematic priming.
Ovulation occurs 12-14 days after the first day of menstruation.In this phase, progesterone decreases and estrogen increases for a limited short time.However, luteinizing hormone (LH) which was critical for ovulation peaks in this period.Casadesus and colleagues (2006) showed that Alzheimer's disease was correlated with high LH levels.Other studies (Bowen, Isley, & Atkinson, 2000;Short, Bowen, O'Brien, & Graff-Radford, 2001) also showed that Alzheimer's patients have LH levels two times more than the paired healthy sample.Research on women who are treated with LHRH (luteinizing hormone releasing hormone) analogs showed that objective (Sherwin & Tulandi, 1996) and subjective (Newton, Slota, Yuzpe, & Tummon, 1996;Kortepeter, Macmillan, & Ferrell, 1992) memory scores decrease.Green and colleagues (2000) also found that memory, attention and executive functions of men who treated with LH agonists due to prostate cancer impaired.
In light of the presented literature, we aimed to find out if men and women in different menstrual phases (low LH level menstruation phase; and high LH level ovulation phase) would have different performance in SP and remembering task.

Method Participants
Seventy five hetereosexual women and 29 heterosexual men who were right-handed undergratuate student in Ege University and Izmir University of Economics volunteered to participate the study.Their age ranged 18-26. Ediburg Handedness Inventory (Oldfields, 1971) was used to determine the hand use.Those who had +60 and above Laterality Quotient participated the experiment.
According to their self-report, participants had normal vision or corrected to normal vision.Women participants had regular menstrual cycle and they had no hormonal manipulation according to their self-report.

Apparatus and Materials
Fourty two related and unrelated visual stimulus pairs were used.In a preliminary study, we gave a 5-point Likert Scale to 45 undergratuate students to determine the degree of relationship between the pairs.The most related 10 and the most unrelated 10 stimulus pairs were selected for the original experimental presentation.The visual stumuli were black and white colored, they were equalized by their size, color and resolution.The size of the pictures was 291 x 335 pixel (wide x lenght).Microsoft VB 6.0 software was used for stimulus presentation and data acquisition.

Procedure
Prior to the experimental session, a meeting was appointed with women to have information about their menstrual cycle to arrange the next meeting.Edinburgh Handedness Inventory (Oldfield, 1971) was applied in order to determine the hand use and the subjects whose laterality quotient was above +60 (right hand users) voluteered the study.Women for the menstrual period were participated on one of the first 3 days of their bleeding while women for the ovulation period were participated 12-14 days after the first day of their bleeding.Participants filled the informed consent form.
Microsoft VB 6.0 software was used for stimulus presentation and data acquisition.Subjects were randomly assigned one of the experimental groups: left viusal field (LVF) group, right visual field (RVF) group and bilateral (BIVF) group.Subjects were instructed to fix their heads on the chin rest and focus on the fixation point (radius=0.84°)on the computer screen.After presenting the fixation point for 2s, a stimulus was shown in one of the visual fields (left, right or center) for 100 msec.The stimuli subtended a visual angle of 10.94° horizontal by 14.61° vertical and the center of each stimulus positioned 14.98° from the fixation point for the lateral presentations.For the bilateral presentation the stimulus was presented at the same position with the fixation point.After the presentation of the first stimulus, the second stimulus was presented in the center of the screen and the subject was asked if the first and the second picture were related or unrelated.
The related and unrelated stimulus pairs were presented in a mixed fashion.Subjects responded by using the keyboard (a and k).We recorded the correct response ratio and response time of the subjects.The first two trials were not considered due to the habituation process.Subjects' evaluation time and evaluation scores were recorded.
After the experimental session subjects were given a list including the names of the stimuli presented in the experiment.The subjects were asked to mark the names of the stimuli that they had seen in the experiment.

Semantic Priming Results
We compared the reaction time for related and unrelated stimuli to find out if SP effect occurred.
We conducted 3 (group) X 3 (visual field/hemisphere) two-way repeated measures ANOVA.The results of the analysis showed that reaction time for related and unrelated stimuli (F(1, 92=74.9,p<.05) and group X reaction time interaction were significant (F(2, 92)=3.01,p<.05).Visual field / hemisphere and the other interactions were not significant (p>.05).
The data was splitted in respect to group and repeated measures ANOVA was conducted.According to this analysis, we found a significant reaction time effect for men (F(1, 28)=35.11,p<.05); women in menstruation phase (F(1, 36)=15.34,p<.05) and women in ovulation phase (F(1, 34)=21.09,p<.05).Related stimuli were responded faster than than the unrelated stimuli in all of the groups indicating an SP effect.

Results for ResponseTime, Correct Response Rate and Number of Remembered Stimuli
We conducted 3 X 3 MANOVA in order to find out the effects of our independent variables group (men, menstruation, ovulation) and visual field /hemisphere (RVF, LVF and BVF) on the dependent variables response time, correct response rate and the number of rememberred stimuli.We found a significant group effect (Wilk's λ=0.93,F(12, 174)=2.04,p<.02, partial ε 2 =.12).However, we did not find any significant effects of visual field/hemisphere (p>.05) and interaction of group X visualfield/hemisphere (p>.05).
Following the main effect of group in ANOVA we conducted Bonferroni pairwise comparisions.There was significant difference between the number of stimuli remembered by the women in ovulationary phase (M=12.31,SD=2.82) and the number of stimuli remembered by men (M =14.03,SD =2.56) P=.03.On the other hand, no significant difference was found between the number of stimuli remembered by the women in menstruation phase (M =13.05,SD =2.14) and men (p>.05).We also did not observe significant difference between the number of stimuli remembered by the women in menstruation phase and the women in ovulation phase.(p>.05).
The results of Bonferroni pairwise comparison tests for the number of remembered unrelated stimuli indicated that there was significant difference between women in ovulation period (M =4.72, SD =1.78) and men (M =5.72, SD =1.85) p=.05 .On the other hand, no significant difference was found between men and women in menstruation phase (M = 4.97 SD =1.40) (p>.05) and women in ovulation phase and menstruation phase (p>.05).
The same pattern was also observed in the reaction time for related stimuli.Bonferroni pairwise comparison test showed that respose time of women in ovulation phase (M =13517.6,SD =4663.99)and men (M =11979.96,SD =3013.51)was significantly different p =.05.But, no significant difference was found between the response time of men and women in menstruation phase (M =12377.19,SD =4365.99)(p>.05) and response time of women in ovulation phase and women in menstruation phase (p>.05).

Discussion
Results of the presented study indicated that all groups had shown SP and there was no hemispheric specialization.Men responded related pictures faster than women in ovulation period however, no difference was observed between men and women in menstruation phase.Similarly, men rememberred more stimuli than the women in ovulation phase.But no difference was observed between the number of stimuli rememberred by the men and women in menstruation phase.
The most interesting finding of our study is changing sex difference in memory performance regarding to the menstrual cycle.We found that women in ovulation period remembered less stimuli than men did while, there was no significant difference between men and women in menstruation period.One of the explanations for this finding is, negative effect of LH on memory which is known to be secreted maximally in ovulation and not secreted in menstruation phase.Alzheimer studies (Bowen, Isley, & Atkinson, 2000;Short, Bowen, O'Brien, & Graff-Radford, 2001), showed that LH was secreted two times more than the matched population in patients with Alzheimer's diesease.Additionally, LH containing drugs have also negative effects on memory performance (Green et al., 2002;Newton, Slota, Yuzpe, & Tummon, 1996;Kortepeter, Macmillan, & Ferrell, 1992, Sherwin & Tulandi, 1996).Animal studies (e.g.Casadesus et al., 2006) support the relationship between LH levels and Alzheimer's diesease.They show that high LH levels diminish the memory performance (Berry, Tomidokoro, Ghiso, & Thornton, 2008).Thus, in our study we speculate that the poorer memory performance of women in ovulation phase might be correlated with the LH levels that was assumed to be highest in ovulatory phase of the menstrual cycle.
We collected data on the 12 th -14 th day of menstrual cycle from the women who had regular cycle to detect the ovulation period.However, if we had measured the hormone levels in the ovulation period, we would show a more precise relationship between memory performance and LH levels.Therefore, we suggest to measure hormone levels for the future studies.
Generally, our study indicated that sex difference in cognitive proceses such as SP and memory can be altered by the menstrual cycle of women.Our findings pointed out that menstrual phases of female subjects should be taken into account in evaluating and conducting cognitive sex difference studies.