Neural activation in women in response to masculinized male faces: mediation by hormones and psychosexual factors

Abstract

Women's preference for masculine faces varies with hormonal state, sociosexuality, and relationship status, but the underlying mechanisms are poorly understood. We hypothesized that hormones and psychosexual factors (sociosexuality, sexual inhibition/excitation) mediate the perception and evaluation of male faces thereby influencing women's preferences. We used functional magnetic resonance imaging to measure brain activity in 12 women as they evaluated pictures of male faces (half 30% masculinized, half 30% feminized). Participants were heterosexual women, age 23–28 years, who were not in a committed relationship and not using hormonal contraception. Women were tested during both the follicular and luteal phase of their menstrual cycle. We found five brain regions related to face and risk processing that responded more to the masculinized than to the feminized faces, including the superior temporal gyrus, precentral gyrus, posterior cingulate cortex, inferior parietal lobule, and anterior cingulate cortex. Increased activation in the anterior cingulate cortex, specifically, may indicate that women perceive masculinized faces to be both more risky and more attractive. We did not see any areas that were more strongly activated by feminized faces. Levels of activation were influenced by hormonal and psychosexual factors. The patterns of hormonally and psychosexually mediated neural activation observed may offer insight into the cognitive processes underlying women's partner preferences.

Introduction

Mate choice is a complex decision with high potential risks for women. Because male traits generally thought to predict good condition and even genetic quality often coincide with less desirable characteristics, women must balance potentially disparate mating priorities (Gangestad & Simpson, 2000, Jones et al., 2008). For example, although men characterized by more masculine testosterone-linked traits (Penton-Voak & Chen, 2004) may be socially dominant (Boothroyd, Jones, Burt, & Perrett, 2007) and physically healthy (Rhodes et al., 2003, Thornhill & Gangestad, 2006), they are also less likely to invest in offspring (Fleming et al., 2002, Roney et al., 2006) and to enter into a partnered relationship (Booth & Dabbs, 1993, Van Anders & Watson, 2006). Facial, morphological, and behavioral cues of masculinity have been previously proposed to be salient cues of risk and reward for women in their assessment of men as potential sexual partners (Miller & Todd, 1998). Although the computation of the relative risks and rewards of a potential mate would be expected to be the product of conscious and unconscious cognitive processing of stimuli in the brain, the neural processes associated with women's evaluations of men during women's sexual decision making and how those processes may relate to preferences for more or less masculine men are not known.

Preferences for facial masculinity fluctuate across the menstrual cycle in parallel with changes in hypothesized reproductive priorities (Gangestad et al., 2004, Gangestad et al., 2007; Penton-Voak & Perrett, 2000). Around the time of ovulation, when conception is likely, women may be more responsive to cues that predict male genetic quality, specifically, traits indicating increased androgens, leading to a preference for traits that are not favored during other phases (Gangestad et al., 2004, Jones et al., 2005, Pawlowski & Jasienska, 2005, Penton-Voak et al., 1999, Penton-Voak & Parrett, 2000). Evidence suggests a direct relationship between specific hormones, including estrogens, testosterone, and progesterone, and women's preferences for certain masculine traits (Roney & Simmons, 2008, Welling et al., 2007). For example, recent work demonstrates direct positive correlations between women's subjective evaluations of masculine men and their testosterone (Welling et al., 2007) and estradiol (Roney & Simmons, 2008). Furthermore, women using hormonal contraception do not demonstrate the same fluctuating patterns of attraction to masculine men as observed in normally cycling women (Penton-Voak et al., 1999). However, although the literature supports an association between hormonal state and women's preferences for more or less masculine men, little is known about how hormones mediate women's mate choice preferences.

We hypothesize that hormones mediate the perception and evaluation of male faces. If true, we would expect to see hormonal effects on neural activation in brain areas involved in face perception, the evaluation of facial attractiveness, and decision making, including the anterior cingulate, insula, amygdala, nucleus accumbens, medial prefrontal cortex, fusiform gyrus, and superior temporal gyrus (Allison et al., 2000, Harris et al., 2007, Haxby et al., 2000, Heekeren et al., 2008, Kranz & Ishai, 2006, O'Doherty et al., 2003, Palermo & Rhodes, 2007, Redcay, 2008, Stevens et al., 2005, Winston et al., 2007). We expect this network of brain regions to be influenced by both the masculinity of face stimuli and the phase of a woman's menstrual cycle at the time of testing based on extensive behavioral literature documenting women's increased preferences for masculine men during the follicular phase (reviewed in Jones et al., 2008). An understanding of women's neural responses to masculine men across the menstrual cycle will further our knowledge of the proximate mechanisms by which hormones alter the reward value and/or the perception of masculine faces.