Mapping changes in women's visual functions during the menstrual cycle: narrative review

Figueiredo, Bruna Gabrielli Damascena de; Rezende, Maria Thalita Cardoso; Santos, Natanael Antonio dos; Andrade, Michael Jackson Oliveira de

doi:10.1590/1516-3180.2020.0474.R2.03052021

Bruna Gabrielli Damascena de Figueiredo

Psychology Student, Neurosciences and Behavior Laboratory, Department of Psychology Perception, Universidade Federal da Paraiba (UFPB), João Pessoa (PB), Brazil.

http://orcid.org/0000-0003-4580-9199

Maria Thalita Cardoso Rezende

Psychology Student, Neurosciences and Behavior Laboratory, Department of Psychology Perception, Universidade Federal da Paraiba (UFPB), João Pessoa (PB), Brazil.

http://orcid.org/0000-0002-9406-7833

Natanael Antonio dos Santos

PhD. Full Professor, Neurosciences and Behavior Laboratory, Department of Psychology Perception, Universidade Federal da Paraiba (UFPB), João Pessoa (PB), Brazil.

http://orcid.org/0000-0001-7708-9929

Michael Jackson Oliveira de Andrade Address for correspondence: Michael Jackson Oliveira de Andrade Departamento de Psicologia, Universidade Estadual de Minas Gerais, Laboratório de Neurociências, Cronobiologia e Psicologia do Sono Divinópolis — Minas Gerais — Brasil CEP 35501-170 Tel. (+55 37) 3229-3590 E-mail: andrademjackson@gmail.com

PhD. Associate Professor, Laboratory of Neuroscience, Chronobiology and Sleep Psychology, Department of Psychology, Universidade do Estado de Minas Gerais (UEMG), Divinópolis (MG), Brazil.

http://orcid.org/0000-0002-2650-451X

Address for correspondence: Michael Jackson Oliveira de Andrade Departamento de Psicologia, Universidade Estadual de Minas Gerais, Laboratório de Neurociências, Cronobiologia e Psicologia do Sono Divinópolis — Minas Gerais — Brasil CEP 35501-170 Tel. (+55 37) 3229-3590 E-mail: andrademjackson@gmail.com

Authors’ contributions: Figueiredo BGD: investigation (equal), methodology (equal), writing-original draft (equal) and writing-review and editing (equal); Rezende MTC: funding acquisition (equal), investigation (equal), writing-original draft (equal) and writing-review and editing (equal); Santos NA: conceptualization (equal), formal analysis (equal) and writing-review and editing (equal); and Andrade MJO: conceptualization (equal), formal analysis (equal) and writing-review and editing (equal)

Conflicts of interest: None

Authors (year)	Country	Sample (phases of the cycle)	Method	Testing	Visual task	Stimuli	Results
Darlington, Ross, King & Smith (2001)²⁴24 Darlington CL, Ross A, King J, Smith PF. Menstrual cycle effects on postural stability but not optokinetic function. Neurosci Lett. 2001;307(3):147-50. PMID: 11438385; https://doi.org/10.1016/s0304-3940(01)01933-4. https://doi.org/10.1016/s0304-3940(01)01...	New Zealand	12 women aged 21.9 ± 4.0 years (menstrual, follicular, half-cycle and luteal phases)	P	NS	Eye movement	Oculogram and optokinetic (OKR)	There was no difference in eye movement speed
Apaydin, Akar, Akar, Zorlu & Ozer (2004)³⁴34 Apaydin KC, Akar Y, Akar ME, Zorlu GC, Ozer HO. Menstrual cycle-dependent changes in blue-on-yellow visual field analysis of young diabetic women with severe non-proliferative diabetic retinopathy. Clin Exp Ophthalmol. 2004;32(3):265-9. PMID: 15180838; https://doi.org/10.1111/j.1442-9071.2004.00814.x. https://doi.org/10.1111/j.1442-9071.2004...	Turkey	93 eyes of women in the follicular and luteal phases: 45 eyes of women with diabetes mellitus (34.9 ± 4.7 years) and 48 healthy controls (36.2 ± 5.2 years)	P	M (left eye recording)	Visual field	Humphrey Field Analyzer II (upper temporal, lower temporal, upper nasal and lower nasal)	There were no differences between women with and without diabetes. Women with diabetes had lower sensitivity in the visual field in the luteal phase
Eisner, Burke & Toomey (2004)²⁸28 Eisner A, Burke SN, Toomey MD. Visual sensitivity across the menstrual cycle. Vis Neurosci. 2004;21(4):513-31. PMID: 15579218; https://doi.org/10.1017/S0952523804214031. https://doi.org/10.1017/S095252380421403...	United States	4 women aged 21–29 years (menstrual, follicular and luteal phases)	P	M	Visual sensitivity	Temporal stimulus of 1.5 Hz square wave (wavelengths: 440, 460, 490, 510, 540, 580 and 640 nm)	No variation in visual sensitivity
Hausmann (2005)²³23 Hausmann M. Hemispheric asymmetry in spatial attention across the menstrual cycle. Neuropsychologia. 2005;43(11):1559-67. PMID: 16009238; https://doi.org/10.1016/j.neuropsychologia.2005.01.017. https://doi.org/10.1016/j.neuropsycholog...	New Zealand	24 women aged 33.93 ± 10.1 years (menstrual, follicular and luteal phases); 14 men aged 26.96 ± 6.19 years	P	NS	Spatial orientation	Line bisection task (17 horizontal lines)	Greater activation of spatial hemispheric asymmetry in the luteal phase
Giuffrè, Rosa & Fiorino (2007)³¹31 Giuffrè G, Di Rosa L, Fiorino F. Changes in colour discrimination during the menstrual cycle. Ophthalmologica. 2007;221(1):47-50. PMID: 17183201; https://doi.org/10.1159/000096522. https://doi.org/10.1159/000096522...	Italy	15 women aged 25 ± 4.0 years (3 evaluation phases: menstrual, ovulatory and luteal)	P	M (left-eye and right-eye recording)	Visual acuity, luminance contrast and color view	Vertical sine grids; Farnsworth-Munsell 100-hue test	There were no differences in visual acuity or luminance contrast; greater color vision in the ovulatory phase
Akara et al. (2013)¹⁸18 Akara Y, Yucel I, Akarb ME, Taskin O, Ozer HO. Menstrual cycle-dependent changes in visual field analysis of healthy women. Ophthalmologica. 2005;219(1):30-5. PMID: 15627825; https://doi.org/10.1159/000081780. https://doi.org/10.1159/000081780...	Turkey	59 eyes of women (follicular and luteal phases) 54 eyes of men	P	Monocular	Visual field	Humphrey Field Analyzer II (upper temporal, lower temporal, upper nasal and lower nasal); Ishiara's color test	Smaller auto-tinted perimeter in visual field sensitivity in the luteal phase
Kumar, Mufti & Kisan (2013)²¹21 Kumar S, Mufti M, Kisan R. Variation of reaction time in different phases of menstrual cycle. J Clin Diagn Res. 2013;7(8):1604-5. PMID: 24086851; https://doi.org/10.7860/JCDR/2013/6032.3236. https://doi.org/10.7860/JCDR/2013/6032.3...	India	30 women aged 21.33 ± 2.3 years (menstrual, follicular and luteal phases)	P	NS	Visual (TRV) and auditory (TRA) reaction time	Reaction time after the presentation of stimuli (green light; 4,000 Hz)	TRV and TRA were higher during the luteal phase and lower during the follicular phase
Danilenko & Sergeeva (2015)⁴³43 Danilenko K, Sergeeva UY. Immediate effect of blue-enhanced light on reproductive hormones in women. Neuro Endocrinol Lett. 2015;36(1):84-90. PMID: 25789589.	Russia	16 women aged 27.5 ± 1.9 years (follicular and mid-cycle phases)	P	NS	Visual sensitivity	Lumie SADlight with LEDs; light flashes of wavelengths: blue (480 nm) and red (651 nm)	Greater visual sensitivity at 480 nm during the follicular phase
Abdul et al. (2015)¹⁹19 Abdul Razzak R, Bagust J, Docherty S, et al. Menstrual phase influences gender differences in visual dependence: A study with a computerised Rod and Frame Test. Journal of Cognitive Psychology. 2015;27(1):80-8. https://doi.org/10.1080/20445911.2014.976227. https://doi.org/10.1080/20445911.2014.97...	United Kingdom	30 women in the follicular phase (19.72 ± 1.20 years); 24 women in the luteal phase; 30 men (20.16 ± 1.02 years)	P	Binocular	Spatial orientation	CRFT system (previous mechanical rod and frame test); line stimuli	Largest error in the spatial orientation of verticality for women in the luteal phase
Sudheer, Jagadeesan & Kammar (2016)³³33 Sudheer C, Jagadeesan S, Kammar KF. Auditory and visual reaction times during the menstrual cycle. National Journal of Physiology, Pharmacy and Pharmacology. 2017;7(3):297-300. https://doi.org/10.5455/njppp.2017.7.0926813112016. https://doi.org/10.5455/njppp.2017.7.092...	India	50 women aged 20-25 years (3 phases of evaluation: menstrual, ovulatory, and luteal)	P	NS	Visual (TRV) and auditory (TRA) reaction time	Reaction time after presentation of stimuli (flash/sound)	TRV and TRA were higher during the menstrual phase and lower during the luteal phase
Sy et al. (2016)¹¹11 Sy JL, Tomarken AJ, Patel V, Blake R. The time course of binocular rivalry during the phases of the menstrual cycle. J Vis. 2016;16(15):22. PMID: 28006072; https://doi.org/10.1167/16.15.22. https://doi.org/10.1167/16.15.22...	United States	16 women; mean age 22 years (follicular and luteal phases)	P	M (left/right eye recording)	Binocularity	Psychophysics toolbox; circular sinusoidal grid stimuli (4.5 and 30%; 1.48 in diameter)	There was no significant difference in binocularity or temporal dynamics
Webb, Hibbard & O’Gorman (2018)²⁰20 Webb ALM, Hibbard PB, O’Gorman R. Natural variation in female reproductive hormones does not affect contrast sensitivity. R Soc Open Sci. 2018;5(2): 171566. PMID: 29515869; https://doi.org/10.1098/rsos.171566. https://doi.org/10.1098/rsos.171566...	United Kingdom	21 women aged 21.6 ± 3.8 years (menstrual, ovulatory and luteal phases); 14 women who used contraceptives; 14 men	P	NS	Luminance contrast	Stimuli were Gabor's sinusoidal grids with spatial frequencies of 1, 4 and 16 cpd	There was no difference in luminance contrast according to hormonal shifts

Authors (year)	Country	Sample (phases of the cycle)	Method	Testing	Visual task	Test and stimuli	Results
Yılmaz, Erkin, Mavioglu & Sungurtekin (1998)¹⁴14 Yilmaz H, Erkin EF, Mavioǧlu H, Sungurtekin Ü. Changes in pattern reversal evoked potentials during menstrual cycle. Int Ophthalmol. 1998;22(1):27-30. PMID: 10090445; https://doi.org/10.1023/a:1006165126702. https://doi.org/10.1023/a:1006165126702...	Turkey	30 women aged 29.6 ± 6.4 years (4 evaluation phases: menstrual, follicular, ovulatory and luteal)	N (VEP)	M (left/right eye recording)	Visual electrophysiology	Visual evoked potential (reverse pattern); P100 latency and visual range (Oz)	Higher mean P100 amplitude during the ovulatory phase
Krug et al. (2007)¹³13 Krug R, Pietrowsky R, Fehm HL, Born J. Selective influence of menstrual cycle on perception of stimuli with reproductive significance. Psychosom Med. 2000;56(5):410-7. PMID: 7809340; https://doi.org/10.1097/00006842-199409000-00005. https://doi.org/10.1097/00006842-1994090...	Germany	11 women (in the menstrual, ovulatory and luteal phases); mean age 25.3 years	N (VEP)	NS	Visual electrophysiology	Social stimuli (sexy man, baby, people, woman); N1, P2, P3, LPC, SW (700-900 ms), LPC	Greater LPC amplitude to stimulate sexy men in the ovulatory phase
Derntl et al. (2008)³⁵35 Derntl B, Windischberger C, Robinson S, et al. Facial emotion recognition and amygdala activation are associated with menstrual cycle phase. Psychoneuroendocrinology. 2008;33(8):1031-40. PMID: 18675521; https://doi.org/10.1016/j.psyneuen.2008.04.014. https://doi.org/10.1016/j.psyneuen.2008....	Austria	22 women aged 24.45 ± 3 years (11 in the follicular phase and 11 in the luteal phase)	N (fMRI)	NS	Emotion recognition	3T scanner for amygdala activation (T2 protocol); emotional discrimination task (Vienna Emotion Recognition Tasks (VERT-K)	Greater neural activation for all follicular phase emotions. In particular, negative facial expressions caused greater activation of the amygdala
Zhang, Zhou & Ye (2013)⁴¹41 Zhang W, Zhou R, Ye M. Menstrual cycle modulation of the late positive potential evoked by emotional faces. Percept Mot Skills. 2013;116(3):707-23. PMID: 24175446; https://doi.org/10.2466/22.27.PMS.116.3.707-723. https://doi.org/10.2466/22.27.PMS.116.3....	China	29 women (premenstrual, post-menstrual and ovulation phases); aged 20.6 ± 1.5 years	N (VEP)	NS	Visual electrophysiology	Visual evoked potential; visual latency and amplitude components N1, P2, N2 in Fz, Cz, Pz; P3, LPP in Pz, Oz	Late positive potential (LPP) evokes changes in the premenstrual phase for facial expressions: fear (110-130 ms, 150-190 ms and 300-500 ms), sadness (230-300 ms), and anger (750- 1,000 ms.); lower LPP amplitude in the premenstrual phase
Mareckova et al. (2014)²⁵25 Marečková K, Perrin JS, Khan IN, et al. Hormonal contraceptives, menstrual cycle and brain response to faces. Soc Cogn Affect Neurosci. 2014;9(2):191-200. PMID: 23175677; https://doi.org/10.1093/scan/nss128. https://doi.org/10.1093/scan/nss128...	United Kingdom	20 women (10 in the regular cycle and 10 who used oral contraceptives (menstrual, follicular, mid-cycle and luteal phases); aged 20.44 ± 2.69 years	N (fMRI)	NS	Recognition of emotions	T1-weighted images (T1W), magnetic transfer rate (MTR) and diffusion tensor image (DTI)	Higher level of blood oxygenation (BOLD) in the fusiform area during the mid-cycle phase
Lusk et al. (2015)³⁷37 Lusk BR, Carr AR, Ranson VA, Bryant RA, Felmingham KL. Early visual processing is enhanced in the midluteal phase of the menstrual cycle. Psychoneuroendocrinology. 2015;62:343-51. PMID: 26366674; https://doi.org/10.1016/j.psyneuen.2015.08.022. https://doi.org/10.1016/j.psyneuen.2015....	Australia	28 women in the follicular phase (23.54 ± 6.6 years); 29 women in the luteal phase (24.41 ± 7.1 years); 27 men	N (VEP)	B	Visual electrophysiology	Visual evoked potential; latency and visual range of P100, P300, N200, N300 and LPP	Early latency in the luteal phase (P1, N1). Early latency for unpleasant images in the menstrual phase in P3 and LPP

Authors (year)	Country	Sample (phases of the cycle)	Method	Testing	Visual task	Test / Stimuli	Results
Penton-Voak & Perrett (1999)³⁰30 Penton-Voak IS, Perrett DI, Castles DL, et al. Menstrual cycle alters face preference. Nature. 1999;399(6738):741-2. PMID: 10391238; https://doi.org/10.1038/21557. https://doi.org/10.1038/21557...	United Kingdom	139 women; mean age 20 years (menstrual, follicular and luteal phases)	B	NS	Facial attractiveness	Emotional attractiveness task (female and male face stimuli)	Women showed greater facial attractiveness as facial stimuli in the follicular phase
Penton-Voak et al. (1999)³⁰30 Penton-Voak IS, Perrett DI, Castles DL, et al. Menstrual cycle alters face preference. Nature. 1999;399(6738):741-2. PMID: 10391238; https://doi.org/10.1038/21557. https://doi.org/10.1038/21557...	United Kingdom and Japan	20 women; mean age 21 years (follicular phase and luteal phase)	B	NS	Facial attractiveness	Visual stimuli consisting of male faces	Greater attractiveness to male faces of Caucasians in the follicular phase
Roberts et al. (2004)⁴⁷47 Roberts SC, Havlicek J, Flegr J, et al. Female facial attractiveness increases during the fertile phase of the menstrual cycle. Proc Biol Sci. 2004;271Suppl 5(Suppl 5):S270-2. PMID: 15503991; https://doi.org/10.1098/rsbl.2004.0174. https://doi.org/10.1098/rsbl.2004.0174...	United Kingdom and Czech Republic	130 men; 131 women; mean age 25 years	B	NS	Facial attractiveness	Emotional attractiveness task (female face stimuli in the follicular and luteal phases)	Women showed greater facial attractiveness in the menstrual cycle, and higher in the periovulatory than in the luteal phase
Pearson & Lewis (2005)²⁶26 Pearson R, Lewis MB. Fear recognition across the menstrual cycle. Horm Behav. 2005;47(3):267-71. PMID: 15708754; https://doi.org/10.1016/j.yhbeh.2004.11.003. https://doi.org/10.1016/j.yhbeh.2004.11....	United Kingdom	50 women of mean age 20 years (12 in the menstrual phase; 13 in the preovulatory phase; 11 in the ovulatory phase; and 14 in the luteal phase)	B	NS	Emotion recognition	Emotion recognition task (Face Bank; Paul Ekman)	Greater accuracy of the fear face in the menstrual phase
Little, Jones, Burt & Perrett (2007)³⁶36 Little AC, Jones BC, Burt DM, Perrett DI. Preferences for symmetry in faces change across the menstrual cycle. Biol Psychol. 2007;76(3):209-16. PMID: 17919806; https://doi.org/10.1016/j.biopsycho.2007.08.003. https://doi.org/10.1016/j.biopsycho.2007...	United Kingdom	31 women aged 20-25 years (in the follicular and luteal phases)	B	NS	Facial attractiveness	Male and female facial stimuli in 2D symmetry	Greater facial attractiveness of symmetrical faces in the follicular phase
Roney & Simmons (2008)²⁷27 Roney JR, Simmons ZL. Women's estradiol predicts preference for facial cues of men's testosterone. Horm Behav. 2008;53(1):14-9. PMID: 17950291; https://doi.org/10.1016/j.yhbeh.2007.09.008. https://doi.org/10.1016/j.yhbeh.2007.09....	United States	43 women aged 18.36 ± 0.10 years (menstrual phases: follicular, mid-cycle and luteal phases)	B	NS	Facial attractiveness	Visual stimuli consisting of male faces	Greater facial attractiveness of more masculine features in the late follicular phase
Rubinow et al. (2007)¹⁷17 Rubinow DR, Smith MJ, Schenkel LA, Schmidt PJ, Dancer K. Facial emotion discrimination across the menstrual cycle in women with Premenstrual Dysphoric Disorder (PMDD) and controls. J Affect Disord. 2007;104(1-3):37-44. PMID: 17367867; https://doi.org/10.1016/j.jad.2007.01.031. https://doi.org/10.1016/j.jad.2007.01.03...	United States	28 women with PMDD (37.9 ± 5.0 years); 27 women without PMDD (33.5 ± 7.0); evaluated in both the follicular and the luteal phases	B	NS	Emotion recognition	Emotional discrimination task	Better discrimination of sad face in the luteal phase for PMDD. Women with PMDD differed significantly from women without PMDD in the luteal phase regarding sad faces
Derntl et al. (2008)³⁵35 Derntl B, Windischberger C, Robinson S, et al. Facial emotion recognition and amygdala activation are associated with menstrual cycle phase. Psychoneuroendocrinology. 2008;33(8):1031-40. PMID: 18675521; https://doi.org/10.1016/j.psyneuen.2008.04.014. https://doi.org/10.1016/j.psyneuen.2008....	Austria	32 women aged 23.84 ± 3 years (15 in the follicular phase and 17 in the luteal phase)	B	NS	Emotion recognition	Emotional discrimination task (Vienna Emotion Recognition Tasks, VERT-K)	Better performance in the follicular phase; greater confusion in discrimination of negative emotions (anger and disgust) in the luteal phase
Guapo et al. (2009)³²32 Guapo VG, Graeff FG, Zani ACT, et al. Effects of sex hormonal levels and phases of the menstrual cycle in the processing of emotional faces. Psychoneuroendocrinology. 2009;34(7):1087-94. PMID: 19297103; https://doi.org/10.1016/j.psyneuen.2009.02.007. https://doi.org/10.1016/j.psyneuen.2009....	Brazil	30 women aged 22.1 ± 2.9 years (11 women in the follicular phase; 9 women in the ovulatory phase; and 10 women in the luteal phase); 10 healthy men	B	NS	Emotion recognition	Prototypes of emotional facial stimuli	Recognition of negative emotions, such as sadness, anger and fear in the follicular phase
Konishi et al. (2009)²⁹29 Konishi K, Kumashiro M, Izumi H, Higuchi Y, Awa Y. Effects of the menstrual cycle on language and visual working memory: a pilot study. Ind Health. 2009;47(5):560-8. PMID: 19834266; https://doi.org/10.2486/indhealth.47.560. https://doi.org/10.2486/indhealth.47.560...	Japan	12 women in the menstrual, follicular and luteal phases; aged 22.4 ± 1.1 years	B	NS	Visuospatial memory	Visual memory task using the Baddely model	Higher mental load performance in the luteal phase.
Oberzaucher et al. (2012)⁴⁰40 Oberzaucher E, Katina S, Schmehl S, Holzleitner I, Grammer K. The myth of hidden ovulation: Shape and texture changes in the face during the menstrual cycle. Journal of Evolutionary Psychology. 2012;10(4):163-75. https://doi.org/10.1556/JEP.10.2012.4.1. https://doi.org/10.1556/JEP.10.2012.4.1...	Austria, Czech Republic and Slovakia	10 women and 15 men; aged 23.35 ± 3.1 years)	B	NS	Facial attractiveness	Female facial stimuli in the ovulatory and luteal phases	Greater facial attractiveness of female stimuli in the ovulatory phase. There was no difference regarding the other phases of the menstrual cycle
Puts et al. (2013)¹⁵15 Puts DA, Bailey DH, Cárdenas RA, et al. Women's attractiveness changes with estradiol and progesterone across the ovulatory cycle. Horm Behav. 2013;63(1):13-9. PMID: 23159480; https://doi.org/10.1016/j.yhbeh.2012.11.007. https://doi.org/10.1016/j.yhbeh.2012.11....	United States	202 women aged 19.6 ± 1.6 years (late follicular and middle luteal phases)	B	NS	Facial attractiveness	Visual stimuli consisting of male faces	Greater facial attractiveness of more masculine features in the late follicular phase (increased estradiol)
Lobmaier, Bobst & Probst (2016)³⁸38 Lobmaier JS, Bobst C, Probst F. Can women detect cues to ovulation in other women's faces? Biol Lett. 2016;12(1):20150638. PMID: 26814224; https://doi.org/10.1098/rsbl.2015.0638. https://doi.org/10.1098/rsbl.2015.0638...	Switzerland	60 women aged 25.16 ± 5.1 years (2 evaluation phases: ovulatory and luteal)	B	NS	Facial attractiveness	Facial stimuli prototypes	Higher rate of facial recognition during the ovulatory phase
Marcinkowska & Holzleitner (2020)³⁹39 Marcinkowska UM, Holzleitner IJ. Stability of women's facial shape throughout the menstrual cycle. Proc Biol Sci. 2020;287(1924):20192910. PMID: 32259474; https://doi.org/10.1098/rspb.2019.2910. https://doi.org/10.1098/rspb.2019.2910...	Poland	102 women aged 28.8 ± 4.6 years	B	NS	Facial attractiveness	Female facial stimuli in the ovulatory and luteal phases	Greater facial attractiveness of female stimuli in the ovulatory phase. There was no difference regarding facial symmetry and sexual dimorphism during the phases of the cycle

[1] Address for correspondence: Michael Jackson Oliveira de Andrade Departamento de Psicologia, Universidade Estadual de Minas Gerais, Laboratório de Neurociências, Cronobiologia e Psicologia do Sono Divinópolis — Minas Gerais — Brasil CEP 35501-170 Tel. (+55 37) 3229-3590 E-mail: andrademjackson@gmail.com

Brasil

Brasil

Mapping changes in women's visual functions during the menstrual cycle: narrative review

ABSTRACT

BACKGROUND:

OBJECTIVES:

DESIGN AND SETTING:

METHODS:

RESULTS:

CONCLUSIONS: