More unintended consequences

Fond memories, by Raimundo de Madrazo y Garreta (1841-1920). The hormonal state of pregnancy causes women to have a lower capacity for multitasking and remembering future activities. What happens when oral contraceptives maintain this hormonal state for years and years?

In my last post I reviewed the literature on oral contraceptives and behavior. Women invest more in sexual attractiveness near the time of ovulation, putting on more makeup and sending out other visual, behavioral, and olfactory cues. Oral contraceptives seem to suppress this desire to be attractive.

Parallel to these attitudinal and behavioral changes over the menstrual cycle, we also find cyclical changes to certain brain regions:

[...] a large sample of 55 women was scanned three times along their menstrual cycle in concisely defined time windows of hormonal changes. Accordingly this is the first study using a large enough sample size to assess menstrual cycle dependent changes in human brain structure with sufficient power. Results confirm a significant estradiol-dependent pre-ovulatory increase in gray matter volumes of the bilateral hippocampus, but also show a significant, progesterone-dependent increase in gray matter volumes of the right basal ganglia after ovulation. No other areas were affect by hormonal changes along the menstrual cycle. These hormone driven menstrual cycle changes in human brain structure are small, but may be the underlying cause of menstrual cycle dependent changes in cognition and emotion. (Pletzer et al. 2018).

The same research team earlier reported differences in brain structure between oral contraceptive (OC) users and non-users. OC users were closer to men in their brain structure:

Men had larger hippocampi, parahippocampal and fusiform gyri, amygdalae and basal ganglia than women. Women showed larger gray matter volumes in the prefrontal cortex, pre- and postcentral gyri. These sex-dependent effects were modulated by menstrual cycle phases and hormonal contraceptives. We found larger volumes in the right fusiform/parahippocampal gyrus during early follicular compared to mid-luteal cycle phase. Women using hormonal contraceptives showed significantly larger prefrontal cortices, pre- and postcentral gyri, parahippocampal and fusiform gyri and temporal regions, compared to women not using contraceptives. (Pletzer et al. 2010).

This study was criticized because it made no distinction between progestin-only OCs and combined progestin/estradiol OCs. The results were quite different when another research team repeated this study with participants who used only the second type of pill. OC users now had less, not more, brain volume, particularly in certain regions of the cerebral cortex: 

In 90 women, (44 OC users, 46 naturally-cycling women), we compared the cortical thickness of brain regions that participate in the salience network and the default mode network, as well as the volume of subcortical regions in these networks. We found that OC use was associated with significantly lower cortical thickness measurements in the lateral orbitofrontal cortex and the posterior cingulate cortex. These regions are believed to be important for responding to rewards and evaluating internal states/incoming stimuli, respectively. (Petersen et al. 2015 - h/t to Wanda!)

These differing results may reflect the different types of OCs in use. Because progestin, like progesterone, has anti-estrogenic effects, long-term use would tend to masculinize a woman's brain; there is consequently more gray matter in the parahippocampal and fusiform gyri, which are likewise bigger in men than in women. In contrast, when women prevent conception by taking a mix of progestin and estradiol, which more closely mimics the hormonal state of pregnancy, certain regions of their cerebral cortex will tend to atrophy.

Momnesia?

This atrophy may have an evolutionary cause. Keep in mind that a pregnant woman has to cope with a different pattern of cognitive demands: 

Pregnant women often have difficulty with multi-tasking and remembering future activities; however, they show improvement in memory for faces and recognition of emotional changes, particularly in men. They tend to have an increased sensitivity to odors, many of which are perceived as unpleasant. Perceptions of taste alter throughout pregnancy, with cravings for sweet foods in the second trimester and for salt in the third; sour tends to be preferred throughout the pregnancy. (Stadtlander 2013)

In general, the overall cognitive load is lower during pregnancy, so it makes sense that a pregnant woman’s body would allocate more resources to her developing child and fewer to her brain. The brain is, after all, the costliest organ of the human body, and it can probably cope with being a lower priority over the short term. Problems develop only if the hormonal state of pregnancy is artificially maintained for years and years.

References

Petersen, N., A. Touroutoglou, J.M. Andreano, and L. Cahill. (2015).Oral contraceptive pill use is associated with localized decreases in cortical thickness. Human Brain Mapping 36(7): 2644-2654. 

https://dx.doi.org/10.1002%2Fhbm.22797

Pletzer, B., T. Harris, and E. Hidalgo-Lopez. (2018). Subcortical structural changes along the menstrual cycle: beyond the hippocampus. Scientific Reports 8: 16042 https://dx.doi.org/10.1038%2Fs41598-018-34247-4

Pletzer, B., M. Kronbichler, M. Aichhorn, J. Bergmann, G. Ladurner, and H.H. Kerschbaum. (2010). Menstrual cycle and hormonal contraceptive use modulate human brain structure. Brain Research 1348: 55-62.

https://dx.doi.org/10.1016/j.brainres.2010.06.019

Stadtlander, L. (2013).  Memory and perceptual changes during pregnancy. International Journal of Childbirth Education 28(2): 49-53.

Unintended consequences

Oral contraceptives suppress not only ovulation but also concurrent behavioral and attitudinal changes, including the desire to look more attractive. Has "the pill" changed our culture?

The oral contraceptive pill prevents pregnancy by suppressing ovulation—in short, by fooling a woman's body into thinking it is already pregnant. In addition to medical side effects, "the pill" also seems to modify behavior and attitude, often subtly. Whereas women are more likely to initiate sexual behavior at ovulation, this effect is suppressed in women on the pill (Adams et al. 1978). The latter also prefer men whose faces are less masculine (Little et al. 2002) and lighter-skinned (Frost 1994).

Among non-pill-users, ovulation coincides with greater use of cosmetics and increased time spent putting on cosmetics (Guéguen 2012). This behavioral effect seems to be likewise suppressed by pill use:

We photographed a sample of women (N = 36) who self-reported whether or not they use the contraceptive pill, as well as their cosmetic habits. A separate sample of participants (N = 143) rated how much makeup these target women appeared to be wearing. We found that women not using the contraceptive pill (i.e., naturally cycling women) reported spending more time applying cosmetics for an outing than did women who use the contraceptive pill. We also found that the faces of these naturally cycling women were rated as wearing more cosmetics than the faces of the women using the contraceptive pill. (Batres et al. 2018)

These findings are consistent with the results of a study on professional lap dancers. The participants made $335 in tips per 5 hour shift during ovulation, but only $260 per shift during the luteal phase and $185 per shift during menstruation. Lap dancers on contraceptive pills showed no change in earnings over the menstrual cycle (Miller et al. 2007). It's unclear what sort of visual or behavioral cues were suppressed by pill use:

[...] our study did not identify the precise proximal mechanisms that influence tip earnings. These might include the previously documented shifts in body scent, facial attractiveness, soft-tissue body symmetry, waist-to-hip ratio, and verbal creativity and fluency—or they might include shifts in other phenotypic cues that have not yet been studied. We can, however, exclude some possible mediators based on previous exotic dancer research. Tip earnings are unlikely to be influenced by cycle shifts in stage-dance moves, clothing, or initial conversational content because these cues just do not vary much for professional dancers (Miller et al. 2007)

Do women naturally have a more attractive physical appearance at ovulation?

Discussion

The past half-century has seen a trend toward androgyny among women. This trend is usually attributed to feminism and pop culture, but perhaps the latter have in turn been influenced by something else.

Today, "the pill" is used by approximately 100 million women worldwide, particularly in developed countries. Has this widespread use played a role in changing our cultural and ideological environment? 

I'm not suggesting that women look less feminine today simply because more of them are on the pill and thus are hormonally altered. Rather, if a larger proportion of women are in that kind of hormonal state, it will be easier for anti-feminine fashions and ideologies to achieve a critical mass and take off among all women, including those not on the pill.

References

Adams, D.B., A.R. Gold, and A.D. Burt. (1978). Rise in female-initiated sexual activity at ovulation and its suppression by oral contraceptives. New England Journal of Medicine 299: 1145-1150.

https://doi.org/10.1056/NEJM197811232992101  

Batres, C., A. Porcheron, G. Kaminski, S. Courrèges, F. Morizot, and R. Russell. (2018). Evidence that the hormonal contraceptive pill is associated with cosmetic habits? Frontiers in Psychology 9: 1459

https://doi.org/10.3389/fpsyg.2018.01459

Frost, P. (1994b). 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 79(1): 507-14.

https://doi.org/10.2466/pms.1994.79.1.507.

Guéguen, N. (2012). Makeup and menstrual cycle: near ovulation, women use more cosmetics. The Psychological Record 62: 541-548. 

https://doi.org/10.1007/BF03395819

Little, A.C., B.C. Jones, I.S. Penton-Voak, D.M. Burt, and D.I. Perrett. (2002). 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. 269: 1095-1100. 

https://doi.org/10.1098/rspb.2002.1984

Miller, G., J.M. Tybur, and B.D. Jordan. (2007). Ovulatory cycle effects on tip earnings by lap dancers: economic evidence for human estrus? Evolution and Human Behavior 28: 375-381. https://doi.org/10.1016/j.evolhumbehav.2007.06.002

Skin color and the menstrual cycle

 

The female torso visibly reddens towards the end of the menstrual cycle. Do men unconsciously pick up on this visual cue? (Figure from Edwards and Duntley, 1949)

 

Women vary in skin color over the menstrual cycle. From mid-cycle on, their skin steadily reddens because of an increase in blood flow that peaks in the day or two preceding menstruation.This cyclical “blushing” mainly affects the torso:

[…] these cyclic variations in blood flow were observed over the entire trunk and at least the upper parts of the limbs. There is suggestive evidence that the face and the hands and feet may share in these changes. (Edwards and Duntley, 1949)

Facial skin, especially around the eyes, shows a similar cyclical change, according to two questionnaire surveys: 

[…] about half the women questioned had some increase in skin pigmentation, which was noted in every case in the latter days of the menstrual cycle and in some cases during menstruation also. The others showed no skin changes whatsoever.

[…] The site most commonly showing pigmentation changes was the skin around the eyes. Next most frequently affected were the areola of the nipple and the perioral skin. The forehead, axilla, and abdomen were affected in less than one-third of the "positive" subjects. (McGuiness, 1961) 

In answer to the questionnaire, 18 women (62%) consistently noticed darkening of the peri-ocular skin towards the end of the menstrual cycle, i.e. immediately prior to the onset of menstruation; of these, three also noticed darkening of the nipple areolae, two the forehead skin and one the peri-oral skin. (Snell and Turner, 1966)

Snell and Turner (1966) confirmed these observations by measuring the percentage of light reflected by facial skin, although the cyclical variation was rather small. Unlike the torso, the face doesn’t redden towards the end of the cycle. Instead, it becomes browner through increased melanocyte activity:

The results from the skin reflectance readings did not show any great changes. The readings obtained from the cheek and lower eyelid indicated that the melanin content of the skin in these regions tended to rise in the later part of the cycle in many of the women. 

[…] The melanocytes of the anterior abdominal wall skin over the linea alba showed no changing pattern of activity at different phases of the menstrual cycle.

[…] It was concluded that a proportion of normal women, especially dark-skinned brunettes, have darkening of the facial skin during the later days of the menstrual cycle and this mainly involves the peri-ocular skin. (Snell and Turner, 1966) 

Does this cyclical variation provide men with a means to assess female fertility? An unconscious means, to be sure. Pierre van den Berghe thought so, but I ignored his gentle prodding and avoided the subject, all the more so because a search of the ethnographic literature failed to turn up any awareness in any human society of this cyclical change. In contrast, many societies have been keenly aware that women are fairer-skinned and men darker-skinned, often to the point of making this sex difference an artistic convention (van den Berghe and Frost, 1986; Frost, 1988; Tegner, 1992).

One research team has tried to find out whether men pick up on this cyclical variation:

Here, in an initial pilot study, we test the hypothesis that changes in female facial skin coloration across the menstrual cycle could be one of the signals that men have adapted to in order to assess female fertility. Spectrophotometric measurements of the facial skin color of normally ovulating Caucasian women (aged 24–29 years) were collected in the late follicular and midluteal phase of their menstrual cycle. Facial images were also taken in both sessions and judged for attractiveness and health by a panel of German men (aged 16–37 years). In line with Roberts et al. (2004), our results show that men perceive women in the late follicular phase to be significantly more attractive and healthier than those in the midluteal phase. However, we did not detect any significant differences in objective measurements of skin color between the two phases. (Samson et al., 2011)

This study suffers from a few flaws. The authors measured skin reflectance on the forehead and the cheeks, yet these body sites are less involved in darkening and lightening of female skin over the menstrual cycle. It would have been better to measure skin reflectance around the eyes (although premenstrual peri-ocular darkening might have likewise been absent in the fair-skinned German participants). Better yet, this study should have focused not on the face but on the torso, since that body region is the one most affected by this cyclical variation. We should also keep in mind that men unconsciously use two different aspects of female pigmentation for gender recognition. One is the lighter skin of a woman’s face. The other is the higher contrast between facial skin color and eye/lip color (Russell, 2009; Russell, 2010; Porcheron et al., 2013; see also Dupuis-Roy et al., 2009). This contrast effect might be weakened by the premenstrual darkening of skin around a woman’s eyes.

A more recent study has corroborated that men prefer faces of ovulating women to those of premenstrual women (Bobst and Lobmaier, 2012). It concludes that subtle changes in face shape are responsible, although changes in skin color cannot be ruled out. In fact, if men can respond to such subtle changes in face shape, they should also be able to respond to changes in facial color that are no less subtle.

It may be worthwhile to take another look through the ethnographic literature. One of my wonderful commenters has pointed me to an article by a sociologist of Zambian origin, Mwizenge S. Tembo:

It is [with] the frequent circulation of the hormones, the increased flow of blood during ovulation, and especially during pregnancy that women in Sub-Saharan Africa may acquire a characteristic mild to quite remarkable red-orangeish glow to their skin. In fact an obvious tell-tell sign of being pregnant among married women and also among young girls who may have had sex out of wed lock, even when the pregnancy is not even physically visible, is the characteristic lightening of the skin-tone whether the woman is light or very dark. Among the Tumbuka, Chewa, Nsenga, and Ngoni people of Eastern Zambia, several terms are used to describe the state of being pregnant. “Ali ndi pakati” means that “the woman is in between”. Because the majority of women in African societies prior to modern medicine had very high deaths and faced danger during the birthing process, the woman was said to be literally “between life and death” or “living with uncertainty”. “Ali ndi mimba” means “the woman has a stomach” referring to the obvious bulging stomach of a pregnant woman. The most relevant term to this discussion is “ali ndi pathupi” which means “the woman has a body” (Salaun, 1969; Price, 1970) which refers to the characteristic light skin tone or the visible obvious glow the woman assumes when she gets pregnant. 

This light reddish skin is considered desirable by African men and may serve an adaptive purpose: “Among many other possible explanations, the most compelling may be that the lighter skin, even among the darkest of indigenous Africans, may have been a normal and natural biological marker and signal that the woman was very fertile.” Tembo is a fan of evolutionary psychology and may be indirectly echoing a meme that began with me and Pierre van den Berghe. Nonetheless, there may indeed be more awareness of this menstrual change in skin color than I had thought, particularly in settings where most variation in skin color is intra-ethnic.

Conclusion

When all is said and done, this research topic may still be ‘a bridge too far.’ Admittedly, a researcher should have little trouble finding out whether the premenstrual darkening of the eye area is a sexual turnoff for men. I’m sure it is—many women certainly seem to think so. But how would one determine whether this male response is hardwired or not? By measuring it as a function of testosterone levels? Finally, would such a hardwired mental algorithm shed light on other feelings towards skin color?

It might be more interesting to investigate how men respond to the premenstrual reddening of the female torso region. Recruitment of female participants would nonetheless be much more difficult, as would be the task of getting approval from the research ethics committee. There’s also the little matter that this premenstrual ‘blushing’ is visible only in light-skinned women. Conversely, premenstrual darkening of the eye area is visible mainly in darker-skinned women. 

References

Bobst, C., and J.S. Lobmaier. (2012). Men's preference for the ovulating female is triggered by subtle face shape differences, Hormones and Behavior, 62, 413-417.

http://www.ncbi.nlm.nih.gov/pubmed/22846725

Dupuis-Roy, N., I. Fortin, D. Fiset, and F. Gosselin. (2009). Uncovering gender discrimination cues in a realistic setting, Journal of Vision, 9(2), 10, 1–8.

http://journalofvision.org/9/2/10/

Edwards, E.A. and S.Q. Duntley. (1949), Cutaneous vascular changes in women in reference to the menstrual cycle and ovariectomy, American Journal of Obstetrics and Gynecology, 57, 501-509.

Frost, P. (1988). Human skin color: a possible relationship between its sexual dimorphism and its social perception, Perspectives in Biology and Medicine, 32, 38-58.

McGuiness, B.W. (1961). Skin pigmentation and the menstrual cycle, British Medical Journal, 2, 563.

http://europepmc.org/articles/PMC1969464?pdf=render

Porcheron, A., E. Mauger, and R. Russell (2013). Aspects of facial contrast decrease with age and are cues for age perception. PLoS ONE 8(3): e57985

http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0057985

Russell, R. (2010). Why cosmetics work. In Adams, R., Ambady, N., Nakayama, K., & Shimojo, S. (eds.) The Science of Social Vision. New York: Oxford.

http://public.gettysburg.edu/~rrussell/Russell_SocialVision_cosmetics_chapter.pdf

Russell, R. ( 2009). A sex difference in facial contrast and its exaggeration by cosmetics, Perception, 38, 1211-1219

http://public.gettysburg.edu/~rrussell/Russell_2009.pdf

Samson, N., B. Fink, and P. Matts. (2011). Does a woman’s skin color indicate her fertility level? Preliminary findings, Swiss Journal of Psychology/Schweizerische Zeitschrift für Psychologie/Revue Suisse de Psychologie, 70(4), 99-202.

http://psycnet.apa.org/journals/sjp/70/4/199/

Snell, R.S. and R. Turner. (1966). Skin pigmentation in relation to the menstrual cycle, Journal of Investigative Dermatology, 47, 147-155.

http://www.nature.com/jid/journal/v47/n2/full/jid1966119a.html

Tegner, E. (1992). Sex differences in skin pigmentation illustrated in art, The American Journal of Dermatopathology, 14, 283-287.

http://journals.lww.com/amjdermatopathology/Abstract/1992/06000/Sex_Differences_in_Skin_Pigmentation_Illustrated.16.aspx

Tembo, M.S. (2010). The Rediscovery of the Beautiful Woman in African Societies. Eurocentric Destruction of Indigenous Conceptions: the Secret Rediscovery of the Beautiful Woman in African Societies.

http://people.bridgewater.edu/~mtembo/menu/articles/AfricanBeautyRevisedMarch162010.pdf
 

van den Berghe, P. L. and P. Frost. (1986), Skin color preference, sexual dimorphism, and sexual selection: A case of gene-culture co-evolution? Ethnic and Racial Studies, 9, 87-113.

http://www.tandfonline.com/doi/abs/10.1080/01419870.1986.9993516

Vargas-Guadarrama, L. (1971). Pigmentation cutanée et cycle menstruel, Paris, Université Paris VII, Thèse de doctorat.

Female brains and male skin tone

It is well known that women feel attracted to certain visual, auditory, and olfactory characteristics of men. This attraction seems to be hormonally regulated, as suggested by psychosexual studies of women at different phases of the menstrual cycle. In general, women are more strongly attracted to male characteristics during the estrogen-dominant phase of their cycle (first two-thirds) than during the progesterone-dominant phase (last third).

This cyclical change has been most recently shown by Rupp et al. (2009). MRI scans were used to measure how female brains process pictures of male faces that morphing software had either masculinized or feminized. The subjects were tested on days 10-12 and days 19-23 of the menstrual cycle. Measurements were taken of their levels of estradiol, progesterone, free testosterone, and total testosterone. The subjects also filled out questionnaires about their psychosexual profile (propensity for short-term sexual encounters, for sexual excitation, for sexual inhibition, etc.).

During the first time window (days 10-12), five brain regions showed a stronger neural response to masculinized faces than to feminized faces. No brain region showed the reverse pattern. During the second time window (days 19-23), only one region responded more to masculinized faces than to feminized faces. For both windows, some regions showed significant correlations between neural activation and hormone level. Estradiol correlated positively with neural activation whereas progesterone correlated negatively. The correlations were negative or positive for free and total testosterone. In some brain regions, neural activation also correlated with psychosexual variables.

What was driving these neural responses? What facial feature was turning these women on? In response to an e-mail, the lead author, Heather Rupp, told me that the morphing software had varied the shape of the male faces and their skin tone. The masculinized faces were darker-skinned and the feminized faces lighter-skinned. Her results may thus dovetail with my own findings on female preferences with regard to male skin tone, i.e., my subjects more strongly preferred darker male faces during the estrogen-dominant phase of their menstrual cycle than during the progesterone-dominant phase (Frost 1994).

References

Frost P. (1994). 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, 79, 507-514.

Rupp, H.A., T.W. James, E.D. Ketterson, D.R. Sengelaub, E. Janssen, and J.R. Heiman. (2009). Neural activation in women in response to masculinized male faces: mediation by hormones and psychosexual factors. Evolution and Human Behavior, 30, 1-10.