The influence of steroid sex hormones on the cognitive and emotional processing of visual stimuli in humans

Frontiers in Neuroendocrinology

Volumn 34, Issue 4, 2013, Pages 315-328

  Little, Anthony C ^a  

^a UNIVERSITY OF STIRLING   (United Kingdom)

Author keywords

Attractiveness; Menopause; Menstrual cycle; Oral contraception; Puberty; Recognition; Steroid sex hormones; Vision; Visual processing; Visual spatial

Indexed keywords

ESTRADIOL; ESTROGEN; GESTAGEN; GONADOTROPIN; ORAL CONTRACEPTIVE AGENT; PROGESTERONE; SEX HORMONE; TESTOSTERONE;

ASPERGER SYNDROME; ASSOCIATION; AUTISM; COGNITION; CONGENITAL ADRENAL HYPERPLASIA; EMOTION; FACIAL EXPRESSION; HEMISPHERIC DOMINANCE; HORMONAL CONTRACEPTION; HORMONE SUBSTITUTION; HUMAN; LIBIDO; MASCULINITY; MATE CHOICE; MENOPAUSE; MENSTRUAL CYCLE; MOTIVATION; PHYSICAL ATTRACTIVENESS; POSTMENOPAUSE; PREGNANCY; PRIORITY JOURNAL; PUBERTY; RECOGNITION; REVIEW; SEX DIFFERENCE; SEXUAL ORIENTATION; TURNER SYNDROME; VISUAL MEMORY; VISUAL STIMULATION;

ATTRACTIVENESS; MENOPAUSE; MENSTRUAL CYCLE; ORAL CONTRACEPTION; PUBERTY; RECOGNITION; STEROID SEX HORMONES; VISION; VISUAL PROCESSING; VISUAL-SPATIAL;

ANIMALS; COGNITION; EMOTIONS; GONADAL STEROID HORMONES; HUMANS; PHOTIC STIMULATION; SEXUAL BEHAVIOR; SEXUAL MATURATION;

EID: 84884586678     PISSN: 00913022     EISSN: 10956808     Source Type: Journal    
DOI: 10.1016/j.yfrne.2013.07.009     Document Type: Review

References (179)

1. Ahmed E.I., Zehr J.L., et al. Pubertal hormones modulate the addition of new cells to sexually dimorphic brain regions. Nature Neuroscience 2008, 11(9):995-997.
2. Aleman A., Bronk E., et al. A single administration of testosterone improves visuospatial ability in young women. Psychoneuroendocrinology 2004, 29(5):612-617.
3. Alexander G.M., Charles N. Sex differences in adults' relative visual interest in female and male faces, toys, and play styles. Archives of Sexual Behavior 2009, 38(3):434-441.
4. Alexander G.M., Sherwin B.B., et al. Testosterone and sexual-behavior in oral-contraceptive users and nonusers - a prospective-study. Hormones and Behavior 1990, 24(3):388-402.
5. Alvergne A., Lummaa V. Does the contraceptive pill alter mate choice in humans?. Trends in Ecology & Evolution 2010, 25(3):171-179.
6. Arnold A.P. The organizational-activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues. Hormones and Behavior 2009, 55(5):570-578.
7. Auyeung B., Knickmeyer R., et al. Effects of fetal testosterone on visuospatial ability. Archives of Sexual Behavior 2012, 41(3):571-581.
8. Bancroft J. The endocrinology of sexual arousal. Journal of Endocrinology 2005, 186:411-427.
9. Baron-Cohen S., Knickmeyer R.C., et al. Sex differences in the brain: implications for explaining autism. Science 2005, 310(5749):819-823.
10. Bayer U., Erdmann G. The influence of sex hormones on functional cerebral asymmetries in postmenopausal women. Brain and Cognition 2008, 67(2):140-149.
11. Benagiano, G., Bastianelli, C., et al., 2006. Contraception today. In: Creatsas, G., Mastorakos, G., Chrousos, G.P. (Eds.), Women's Health and Disease: Gynecologic, Endocrine, and Reproductive Issues, vol. 1092, pp. 1-32.
12. Berenbaum S.A. Effects of early androgens on sex-typed activities and interests in adolescents with congenital adrenal hyperplasia. Hormones and Behavior 1999, 35(1):102-110.
13. Berenbaum S.A., Beltz A.M. Sexual differentiation of human behavior: effects of prenatal and pubertal organizational hormones. Frontiers in Neuroendocrinology 2011, 32(2):183-200.
14. Berenbaum S.A., Bryk K.L.K., et al. Early androgen effects on spatial and mechanical abilities: evidence from congenital adrenal hyperplasia. Behavioral Neuroscience 2012, 126(1):86-96.
15. Bialy M., Nikolaev-Diak A., et al. Blockade of androgen receptor in the medial amygdala inhibits noncontact erections in male rats. Physiology & Behavior 2011, 103(3-4):295-301.
16. Bibawi D., Cherry B., et al. Fluctuations of perceptual asymmetry across time in women and men - effects related to the menstrual-cycle. Neuropsychologia 1995, 33(1):131-138.
17. Bos P.A., Hermans E.J., et al. The neural mechanisms by which testosterone acts on interpersonal trust. NeuroImage 2012, 61(3):730-737.
18. Bourne V.J. Lateralised processing of positive facial emotion: sex differences in strength of hemispheric dominance. Neuropsychologia 2005, 43(6):953-956.
19. Bourne V.J., Gray D.L. Hormone exposure and functional lateralisation: examining the contributions of prenatal and later life hormonal exposure. Psychoneuroendocrinology 2009, 34(8):1214-1221.
20. Brown W.M., Hines M., et al. Masculinized finger length patterns in human males and females with congenital adrenal hyperplasia. Hormones and Behavior 2002, 42(4):380-386.
21. Buchanan C.M., Eccles J.S., et al. Are adolescents the victims of raging hormones - evidence for activational effects of hormones on moods and behavior at adolescence. Psychological Bulletin 1992, 111(1):62-107.
22. Cardenas R.A., Harris L.J. Do women's preferences for symmetry change across the menstrual cycle?. Evolution and Human Behavior 2007, 28(2):96-105.
23. Cavior N., Lombardi D.A. Developmental aspects of judgment of physical attractiveness in children. Developmental Psychology 1973, 8(1):67-71.
24. Cherrier M.M., Asthana S., et al. Testosterone supplementation improves spatial and verbal memory in healthy older men. Neurology 2001, 57(1):80-88.
25. Chiazze L., Brayer F.T., et al. Length and variability of human menstrual cycle. Journal of the American Medical Association 1968, 203(6). 377-&.
26. Cicinelli E., De Tommaso M., et al. Oral contraceptive therapy modulates hemispheric asymmetry in spatial attention. Contraception 2011, 84(6):634-636.
27. Choleris E., Clipperton-Allen A.E., et al. Neuroendocrinology of social information processing in rats and mice. Frontiers in Neuroendocrinology 2009, 30(4):442-459.
28. Collaer M.L., Hines M. Human behavioral sex-differences - a role for gonadal-hormones during early development. Psychological Bulletin 1995, 118(1):55-107.
29. Collaer M.L., Reimers S., et al. Visuospatial performance on an Internet line judgment task and potential hormonal markers: sex, sexual orientation, and 2D:4D. Archives of Sexual Behavior 2007, 36(2):177-192.
30. Connellan J., Baron-Cohen S., et al. Sex differences in human neonatal social perception. Infant Behavior & Development 2000, 23(1):113-118.
31. Connolly J.M., Slaughter V., et al. The development of preferences for specific body shapes. Journal of Sex Research 2004, 41(1):5-15.
32. Conway C.A., Jones B.C., et al. Salience of emotional displays of danger and contagion in faces is enhanced when progesterone levels are raised. Hormones and Behavior 2007, 51(2):202-206.
33. Cross J.F., Cross J. Age, sex, race, and the perception of facial beauty. Developmental Psychology 1971, 5(3):433-439.
34. Danel D., Pawlowski B. Attractiveness of men's faces in relation to women's phase of menstrual cycle. Collegium Antropologicum 2006, 30(2):285-289.
35. DeBruine L.M., Jones B.C., et al. Women's attractiveness judgments of self-resembling faces change across the menstrual cycle. Hormones and Behavior 2005, 47(4):379-383.
36. Derntl B., Kryspin-Exner I., et al. Emotion recognition accuracy in healthy young females is associated with cycle phase. Hormones and Behavior 2008, 53(1):90-95.
37. Derntl B., Windischberger C., et al. Facial emotion recognition and amygdala activation are associated with menstrual cycle phase. Psychoneuroendocrinology 2008, 33(8):1031-1040.
38. Dion K. Young children's stereotyping of facial attractiveness. Developmental Psychology 1973, 9(2):183-188.
39. Eisenegger C., Haushofer J., et al. The role of testosterone in social interaction. Trends in Cognitive Sciences 2011, 15(6):263-271.
40. El-Hage G., Eden J.A., et al. A double-blind, randomized, placebo-controlled trial of the effect of testosterone cream on the sexual motivation of menopausal hysterectomized women with hypoactive sexual desire disorder. Climacteric 2007, 10(4):335-343.
41. Epting L.K., Overman W.H. Sex-sensitive tasks in men and women: a search for performance fluctuations across the menstrual cycle. Behavioral Neuroscience 1998, 112(6):1304-1317.
42. Falter C.M., Arroyo M., et al. Testosterone: activation or organization of spatial cognition?. Biological Psychology 2006, 73(2):132-140.
43. Feinberg D.R., Jones B.C., et al. Menstrual cycle, trait estrogen level, and masculinity preferences in the human voice. Hormones and Behavior 2006, 49(2):215-222.
44. Feinberg D.R., DeBruine L.M., et al. Correlated preferences for men's facial and vocal masculinity. Evolution and Human Behavior 2008, 29(4):233-241.
45. Fessler D.M.T. Reproductive immunosuppression and diet - an evolutionary perspective on pregnancy sickness and meat consumption. Current Anthropology 2002, 43(1):19-61.
46. Flaxman S.M., Sherman P.W. Morning sickness: a mechanism for protecting mother and embryo. Quarterly Review of Biology 2000, 75(2):113-148.
47. Frost P. Preference for darker faces in photographs at different phases of the menstrual cycle: preliminary assessment of evidence for a hormonal relationship. Perceptual and Motor Skills 1994, 79:507-514.
48. Frye C.A. Estrus-associated decrements in a water maze task are limited to acquisition. Physiology & Behavior 1995, 57(1):5-14.
49. Frye C.A. An overview of oral contraceptives - mechanism of action and clinical use. Neurology 2006, 66(6):S29-S36.
50. Galea L.A.M., Ormerod B.K., et al. Spatial working memory and hippocampal size across pregnancy in rats. Hormones and Behavior 2000, 37(1):86-95.
51. Gangestad S.W., Thornhill R. Human oestrus. Proceedings of the Royal Society B - Biological Sciences 2008, 275(1638):991-1000.
52. Gangestad S.W., Simpson J.A., et al. Women's preferences for male behavioral displays change across the menstrual cycle. Psychological Science 2004, 15(3):203-207.
53. Gangestad S.W., Garver-Apgar C.E., et al. Changes in women's mate preferences across the cycle. Journal of Personality and Social Psychology 2007, 92(1):151-163.
54. Gauthier I., Tarr M.J. Becoming a "greeble" expert: exploring mechanisms for face recognition. Vision Research 1997, 37(12):1673-1682.
55. Gilbert, S.F., 2000. Developmental Biology. Sinauer, USA.
56. Goldstein J.M., Jerram M., et al. Hormonal cycle modulates arousal circuitry in women using functional magnetic resonance imaging. Journal of Neuroscience 2005, 25(40):9309-9316.
57. Gomez-Gil E., Canizares S., et al. Androgen treatment effects on memory in female-to-male transsexuals. Psychoneuroendocrinology 2009, 34(1):110-117.
58. Gordon H.W., Lee P.A. No difference in cognitive performance between phases of the menstrual-cycle. Psychoneuroendocrinology 1993, 18(7):521-531.
59. Gordon H.W., Corbin E.D., et al. Changes in specialized cognitive function following changes in hormone levels. Cortex 1986, 22(3):399-415.
60. Gould E., Woolley C.S., et al. Gonadal-steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. Journal of Neuroscience 1990, 10(4):1286-1291.
61. Goy R.W., McEwen B.S. Sexual differentiation of the brain 1980, MIT Press, Cambridge.
62. Griksiene R., Ruksenas O. Effects of hormonal contraceptives on mental rotation and verbal fluency. Psychoneuroendocrinology 2011, 36(8):1239-1248.
63. Guapo V.G., Graeff F.G., et al. Effects of sex hormonal levels and phases of the menstrual cycle in the processing of emotional faces. Psychoneuroendocrinology 2009, 34(7):1087-1094.
64. Gur R.C., Sara R., et al. A method for obtaining 3-dimensional facial expressions and its standardization for use in neurocognitive studies. Journal of Neuroscience Methods 2002, 115(2):137-143.
65. Gur R.C., Schroeder L., et al. Brain activation during facial emotion processing. NeuroImage 2002, 16(3):651-662.
66. Halari R., Hines M., et al. Sex differences and individual differences in cognitive performance and their relationship to endogenous gonadal hormones and gonadotropins. Behavioral Neuroscience 2005, 119(1):104-117.
67. Hampson E. Estrogen-related variations in human spatial and articulatory-motor skills. Psychoneuroendocrinology 1990, 15(2):97-111.
68. Hampson E. Variations in sex-related cognitive-abilities across the menstrual-cycle. Brain and Cognition 1990, 14(1):26-43.
69. Hampson E., Kimura D. Reciprocal effects of hormonal fluctuations on human motor and perceptual-spatial skills. Behavioral Neuroscience 1988, 102(3):456-459.
70. Harris C.R. Menstrual cycle and facial preferences reconsidered. Sex Roles 2011, 64(9-10):669-681.
71. Haselton M.G., Miller G.F. Women's fertility across the cycle increases the short-term attractiveness of creative intelligence compared to wealth. Human Nature 2006, 17:50-73.
72. Hatta T., Nagaya K. Menstrual cycle phase effects on memory and stroop task performance. Archives of Sexual Behavior 2009, 38(5):821-827.
73. Hausmann M., Gunturkun O. Cerebral asymmetries after the menopause. Journal of Psychophysiology 1995, 9(3):276-277.
74. Hausmann M., Gunturkun O. Steroid fluctuations modify functional cerebral asymmetries: the hypothesis of progesterone-mediated interhemispheric decoupling. Neuropsychologia 2000, 38(10):1362-1374.
75. Hausmann M., Slabbekoorn D., et al. Sex hormones affect spatial abilities during the menstrual cycle. Behavioral Neuroscience 2000, 114(6):1245-1250.
76. Hausmann M., Becker C., et al. Functional cerebral asymmetries during the menstrual cycle: a cross-sectional and longitudinal analysis. Neuropsychologia 2002, 40(7):808-816.
77. Hawkes K., O'Connell J.F., et al. Grandmothering, menopause, and the evolution of human life histories. Proceedings of the National Academy of Sciences of the United States of America 1998, 95(3):1336-1339.
78. Heil M., Kavsek M., et al. Mental rotation in female fraternal twins: evidence for intra-uterine hormone transfer?. Biological Psychology 2011, 86(1):90-93.
79. Heister G., Landis T., et al. Shift of functional cerebral asymmetry during the menstrual-cycle. Neuropsychologia 1989, 27(6):871-880.
80. Hines M., Fane B.A., et al. Spatial abilities following prenatal androgen abnormality: targeting and mental rotations performance in individuals with congenital adrenal hyperplasia. Psychoneuroendocrinology 2003, 28(8):1010-1026.
81. Hlinak Z. Social recognition in ovariectomized and estradiol-treated female rats. Hormones and Behavior 1993, 27(2):159-166.
82. Hollander A., Hausmann M., et al. Sex hormonal modulation of hemispheric asymmetries in the attentional blink. Journal of the International Neuropsychological Society 2005, 11(3):263-272.
83. Imperatomcginley J., Pichardo M., et al. Cognitive-abilities in androgen-insensitive subjects - comparison with control males and females from the same kindred. Clinical Endocrinology 1991, 34(5):341-347.
84. Janowsky J.S., Oviatt S.K., et al. Testosterone influences spatial cognition in older men. Behavioral Neuroscience 1994, 108(2):325-332.
85. Jasnow A.M., Schulkin J., et al. Estrogen facilitates fear conditioning and increases corticotropin-releasing hormone mRNA expression in the central amygdala in female mice. Hormones and Behavior 2006, 49(2):197-205.
86. Johnston V.S., Hagel R., et al. Male facial attractiveness: evidence for a hormone-mediated adaptive design. Evolution and Human Behavior 2001, 22:251-267.
87. Jones B.C., Little A.C., et al. Commitment to relationships and preferences for femininity and apparent health in faces are strongest on days of the menstrual cycle when progesterone level is high. Hormones and Behavior 2005, 48(3):283-290.
88. Jones B.C., Perrett D.I., et al. Menstrual cycle, pregnancy and oral contraceptive use alter attraction to apparent health in faces. Proceedings of the Royal Society B - Biological Sciences 2005, 272(1561):347-354.
89. Jones B.C., DeBruine L.M., et al. Effects of menstrual cycle phase on face preferences. Archives of Sexual Behavior 2008, 37(1):78-84.
90. Jones B.C., Vukovic J., et al. Circum-menopausal changes in women's preferences for sexually dimorphic shape cues in peer-aged faces. Biological Psychology 2011, 87(3):453-455.
91. Kanwisher N., McDermott J., et al. The fusiform face area: a module in human extrastriate cortex specialized for face perception. Journal of Neuroscience 1997, 17(11):4302-4311.
92. Keenan P.A., Ezzat W.H., et al. Prefrontal cortex as the site of estrogen's effect on cognition. Psychoneuroendocrinology 2001, 26(6):577-590.
93. Kimura D. Sex, sexual orientation and sex hormones influence human cognitive function. Current Opinion in Neurobiology 1996, 6(2):259-263.
94. Kinsley C.H., Lambert K.G. The maternal brain. Scientific American 2006, 294(1):72-79.
95. Koehler N., Rhodes G., et al. Are human female preferences for symmetrical male faces enhanced when conception is likely?. Animal Behaviour 2002, 64:233-238.
96. Koehler N., Rhodes G., et al. Do cyclic changes in women's face preferences target cues to long-term health?. Social Cognition 2006, 24(5):641-656.
97. Lacreuse A., Verreault M., et al. Fluctuations in spatial recognition memory across the menstrual cycle in female rhesus monkeys. Psychoneuroendocrinology 2001, 26(6):623-639.
98. Lacreuse A., Martin-Malivel J., et al. Effects of the menstrual cycle on looking preferences for faces in female rhesus monkeys. Animal Cognition 2007, 10(2):105-115.
99. Lacreuse A., King H.M., et al. Testosterone may increase selective attention to threat in young male macaques. Hormones and Behavior 2010, 58(5):854-863.
100. Laeng B., Falkenberg L. Women's pupillary responses to sexually significant others during the hormonal cycle. Hormones and Behavior 2007, 52(4):520-530.
101. Langlois J.H., Kalakanis L., et al. Maxims or myths of beauty? A meta-analytic and theoretical review. Psychological Bulletin 2000, 126:390-423.
102. Lauritzen C., Klopper A. Estrogens and androgens. Endocrinology of Pregnancy 1983, 73-90. Harper & Row, Philadelphia. F. Fuchs, A. Klopper (Eds.).
103. Leow M.C., Davis G. An index of prenatal steroid exposure predicts adult face perception skills. Psychonomic Bulletin & Review 2012, 19(6):1094-1100.
104. Little A.C., Jones B.C. Variation in facial masculinity and symmetry preferences across the menstrual cycle is moderated by relationship context. Psychoneuroendocrinology 2012, 37(7):999-1008.
105. Little A.C., Jones B.C., et al. Partnership status and the temporal context of relationships influence human female preferences for sexual dimorphism in male face shape. Proceedings of the Royal Society B - Biological Sciences 2002, 269:1095-1100.
106. Little A.C., Jones B.C., et al. Preferences for masculinity in male bodies change across the menstrual cycle. Hormones and Behavior 2007, 51(5):633-639.
107. Little A.C., Jones B.C., et al. Preferences for symmetry in faces change across the menstrual cycle. Biological Psychology 2007, 76(3):209-216.
108. Little A.C., Jones B.C., et al. Preferences for variation in masculinity in real male faces change across the menstrual cycle: women prefer more masculine faces when they are more fertile. Personality and Individual Differences 2008, 45(6):478-482.
109. Little A.C., Saxton T.K., et al. Women's preferences for masculinity in male faces are highest during reproductive age range and lower around puberty and post-menopause. Psychoneuroendocrinology 2010, 35(6):912-920.
110. Little A.C., Jones B.C., et al. Facial attractiveness: evolutionary based research. Philosophical Transactions of the Royal Society B - Biological Sciences 2011, 366(1571):1638-1659.
111. Little, A.C., Burriss, R.P., et al., 2013. Oral contraceptive use in women changes preferences for male facial masculinity and is associated with partner facial masculinity. Psychoneuroendocrinology 38, 1777-1785.
112. Lord L.D., Bond J., et al. Rapid steroid influences on visually guided sexual behavior in male goldfish. Hormones and Behavior 2009, 56(5):519-526.
113. Lutchmaya S., Baron-Cohen S. Human sex differences in social and non-social looking preferences, at 12 months of age. Infant Behavior & Development 2002, 25(3):319-325.
114. Lutchmaya S., Baron-Cohen S., et al. Foetal testosterone and eye contact in 12-month-old human infants. Infant Behavior & Development 2002, 25(3):327-335.
115. Lutchmaya S., Baron-Cohen S., et al. 2nd to 4th digit ratios, fetal testosterone and estradiol. Early Human Development 2004, 77(1-2):23-28.
116. Macrae C.N., Alnwick K.A., et al. Person perception across the menstrual cycle: hormonal influences on social-cognitive functioning. Psychological Science 2002, 13(6):532-536.
117. Malouf M.A., Migeon C.J., et al. Cognitive outcome in adult women affected by congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Hormone Research 2006, 65(3):142-150.
118. Manning J.T., Scutt D., et al. The ratio of 2nd to 4th digit length: a predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Human Reproduction 1998, 13(11):3000-3004.
119. Manning J.T., Baron-Cohen S., et al. The 2nd to 4th digit ratio and autism. Developmental Medicine and Child Neurology 2001, 43(3):160-164.
120. Marecková, K., Perrin, J.S., et al., in press. Hormonal contraceptives, menstrual cycle and brain response to faces. Social Cognitive & Affective Neuroscience, http://dx.doi.org/10.1093/scan/nss128.
121. McCourt M.E., Mark V.W., et al. The effects of gender, menstrual phase and practice on the perceived location of the midsagittal plane. Neuropsychologia 1997, 35(5):717-724.
122. McEwen B.S., Alves S.E., et al. Ovarian steroids and the brain: implications for cognition and aging. Neurology 1997, 48(5):S8-S15.
123. Moffat S.D., Zonderman A.B., et al. Longitudinal assessment of serum free testosterone concentration predicts memory performance and cognitive status in elderly men. Journal of Clinical Endocrinology & Metabolism 2002, 87(11):5001-5007.
124. Moore D.S., Johnson S.P. Mental rotation in human infants: a sex difference. Psychological Science 2008, 19(11):1063-1066.
125. Nijhuis-van der Sanden M.W.G., Eling P., et al. A review of neuropsychological and motor studies in Turner Syndrome. Neuroscience and Biobehavioral Reviews 2003, 27(4):329-338.
126. Oinonen K.A., Mamanian D. Facial symmetry detection ability changes across the menstrual cycle. Biological Psychology 2007, 75(2):136-145.
127. Pauerstein C.J., Eddy C.A., et al. Temporal relationships of estrogen, progesterone, and luteinizing-hormone levels to ovulation in women and infrahuman primates. American Journal of Obstetrics and Gynecology 1978, 130(8):876-886.
128. Pawłowski B., Jasienska G. Women's preferences for sexual dimorphism in height depend on menstrual cycle phase and expected duration of relationship. Biological Psychology 2005, 70:38-43.
129. Pearson R., Lewis M.B. Fear recognition across the menstrual cycle. Hormones and Behavior 2005, 47(3):267-271.
130. Pearson R.M., Lightman S.L., et al. Emotional sensitivity for motherhood: late pregnancy is associated with enhanced accuracy to encode emotional faces. Hormones and Behavior 2009, 56(5):557-563.
131. Penton-Voak I.S., Perrett D.I., et al. Menstrual cycle alters face preference. Nature 1999, 399:741-742.
132. Peters M., Simmons L.W., et al. Preferences across the menstrual cycle for masculinity and symmetry in photographs of male faces and bodies. Plos One 2009, 4(1):e4138.
133. Peterson R.E. Corticosteriods and corticotropins. Endocrinology of Pregnancy 1983, 112-143. Harper & Row, Philadelphia. F. Fuchs, A. Klopper (Eds.).
134. Phillips K., Silverman I. Differences in the relationship of menstrual cycle phase to spatial performance on two- and three-dimensional tasks. Hormones and Behavior 1997, 32(3):167-175.
135. Puts D.A. Mating context and menstrual phase affect women's preferences for male voice pitch. Evolution and Human Behavior 2005, 26(5):388-397.
136. Puts D.A. Cyclic variation in women's preferences for masculine traits - potential hormonal causes. Human Nature - An Interdisciplinary Biosocial Perspective 2006, 17(1):114-127.
137. Puts D.A., McDaniel M.A., et al. Spatial ability and prenatal androgens: meta-analyses of congenital adrenal hyperplasia and digit ratio (2D:4D) studies. Archives of Sexual Behavior 2008, 37(1):100-111.
138. Puts D.A., Cardenas R.A., et al. Salivary testosterone does not predict mental rotation performance in men or women. Hormones and Behavior 2010, 58(2):282-289.
139. Quinn P.C., Liben L.S. A sex difference in mental rotation in young infants. Psychological Science 2008, 19(11):1067-1070.
140. Rhodes G. The evolutionary psychology of facial beauty. Annual Review of Psychology 2006, 57:199-226.
141. Rikowski A., Grammer K. Human body odour, symmetry and attractiveness. Proceedings of the Royal Society B - Biological Sciences 1999, 266:869-874.
142. Riley A., Riley E. Controlled studies on women presenting with sexual drive disorder: I. Endocrine status. Journal of Sex and Marital Therapy 2000, 26(3):269-283.
143. Rivera R., Yacobson I., et al. The mechanism of action of hormonal contraceptives and intrauterine contraceptive devices. American Journal of Obstetrics and Gynecology 1999, 181(5):1263-1269.
144. Roberts J.E., Bell M.A. Sex differences on a mental rotation task: variations in electroencephalogram hemispheric activation between children and college students. Developmental Neuropsychology 2000, 17(2):199-223.
145. Roberts S.C., Gosling L.M., et al. MHC-correlated odour preferences in humans and the use of oral contraceptives. Proceedings of the Royal Society B - Biological Sciences 2008, 275(1652):2715-2722.
146. Roney J.R., Simmons Z.L. Women's estradiol predicts preference for facial cues of men's testosterone. Hormones and Behavior 2008, 53(1):14-19.
147. Roney J.R., Simmons Z.L., et al. Changes in estradiol predict within-women shifts in attraction to facial cues of men's testosterone. Psychoneuroendocrinology 2011, 36(5):742-749.
148. Roof R.L., Havens M.D. Testosterone improves maze performance and induces development of a male hippocampus in females. Brain Research 1992, 572(1-2):310-313.
149. Roos A., Lochner C., et al. Selective attention to fearful faces during pregnancy. Progress in Neuro-Psychopharmacology & Biological Psychiatry 2012, 37(1):76-80.
150. Rosen M.L., Lopez H.H. Menstrual cycle shifts in attentional bias for courtship language. Evolution and Human Behavior 2009, 30(2):131-140.
151. Ross J.L., Stefanatos G.A., et al. Persistent cognitive deficits in adult women with Turner syndrome. Neurology 2002, 58(2):218-225.
152. Ross J., Roeltgen D., et al. Cognition and the sex chromosomes: studies in Turner syndrome. Hormone Research 2006, 65(1):47-56.
153. Rubinow D.R., Schmidt P.J., et al. Estrogen-serotonin interactions: implications for affective regulation. Biological Psychiatry 1998, 44(9):839-850.
154. Rupp H.A., Wallen K. Sex differences in response to visual sexual stimuli: a review. Archives of Sexual Behavior 2008, 37(2):206-218.
155. Rupp H.A., James T.W., et al. Neural activation in the orbitofrontal cortex in response to male faces increases during the follicular phase. Hormones and Behavior 2009, 56(1):66-72.
156. Rupp H.A., James T.W., et al. Neural activation in women in response to masculinized male faces: mediation by hormones and psychosexual factors. Evolution and Human Behavior 2009, 30(1):1-10.
157. Saxton T.K., Debruine L.M., et al. Face and voice attractiveness judgments change during adolescence. Evolution and Human Behavior 2009, 30(6):398-408.
158. Scarbrough P.S., Johnston V.S. Individual differences in women's facial preferences as a function of digit ratio and mental rotation ability. Evolution and Human Behavior 2005, 26(6):509-526.
159. Schoening S., Engelien A., et al. Functional anatomy of visuo-spatial working memory during mental rotation is influenced by sex, menstrual cycle, and sex steroid hormones. Neuropsychologia 2007, 45(14):3203-3214.
160. Sear R., Mace R., et al. Maternal grandmothers improve nutritional status and survival of children in rural Gambia. Proceedings of the Royal Society of London Series B - Biological Sciences 2000, 267(1453):1641-1647.
161. Shanley D.P., Sear R., et al. Testing evolutionary theories of menopause. Proceedings of the Royal Society B - Biological Sciences 2007, 274:2943-2949.
162. Sharp K., Brindle P.M., et al. Memory loss during pregnancy. British Journal of Obstetrics and Gynaecology 1993, 100(3):209-215.
163. Thornhill R., Gangestad S.W. Facial sexual dimorphism, developmental stability, and susceptibility to disease in men and women. Evolution and Human Behavior 2006, 27(2):131-144.
164. van Honk J., Tuiten A., et al. A single administration of testosterone induces cardiac accelerative responses to angry faces in healthy young women. Behavioral Neuroscience 2001, 115(1):238-242.
165. van Honka J., Schutter D.J., et al. Testosterone administration impairs cognitive empathy in women depending on second-to-fourth digit ratio. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(8):3448-3452.
166. Van Strien J.W., Weber R.F.A., et al. Higher free testosterone level is associated with faster visual processing and more flanker interference in older men. Psychoneuroendocrinology 2009, 34(4):546-554.
167. Vangoozen S.H.M., Cohenkettenis P.T., et al. Gender differences in behavior - activating effects of cross-sex hormones. Psychoneuroendocrinology 1995, 20(4):343-363.
168. VanGoozen S.H.M., Wiegant V.M., et al. Psychoendocrinological assessment of the menstrual cycle: the relationship between hormones, sexuality, and mood. Archives of Sexual Behavior 1997, 26(4):359-382.
169. Vanston C.M., Watson N.V. Selective and persistent effect of foetal sex on cognition in pregnant women. Neuroreport 2005, 16(7):779-782.
170. Voracek M., Dressler S.G. Lack of correlation between digit ratio (2D:4D) and Baron-Cohen's "Reading the Mind in the Eyes" test, empathy, systemising, and autism-spectrum quotients in a general population sample. Personality and Individual Differences 2006, 41(8):1481-1491.
171. Voyer D., Voyer S., et al. Magnitude of sex-differences in spatial abilities - a metaanalysis and consideration of critical variables. Psychological Bulletin 1995, 117(2):250-270.
172. Vukovic J., Jones B.C., et al. Circum-menopausal effects on women's judgements of facial attractiveness. Biology Letters 2009, 5(1):62-64.
173. Wang X.T., Johnston V.S. Changes in cognitive and emotional processing with reproductive status. Brain Behavior and Evolution 1993, 42(1):39-47.
174. Wedekind C., Seebeck T., Bettens F., Paepke A.J. MHC-dependent mate preferences in humans. Proceedings of the Royal Society B - Biological Sciences 1995, 260:245-249.
175. Welling L.L.M., Jones B.C., et al. Raised salivary testosterone in women is associated with increased attraction to masculine faces. Hormones and Behavior 2007, 52(2):156-161.
176. Welling L.L.M., Jones B.C., et al. Men report stronger attraction to femininity in women's faces when their testosterone levels are high. Hormones and Behavior 2008, 54(5):703-708.
177. Wilcox A.J., Dunson D.B., et al. Likelihood of conception with a single act of intercourse: providing benchmark rates for assessment of post-coital contraceptives. Contraception 2001, 63(4):211-215.
178. Wirth M.M., Schultheiss O.C. Basal testosterone moderates responses to anger faces in humans. Physiology & Behavior 2007, 90(2-3):496-505.
179. Zhu X., Wang X., et al. Brain activation evoked by erotic films varies with different menstrual phases: an fMRI study. Behavioural Brain Research 2010, 206(2):279-285.