Hens and roosters are different. Cows and bulls are different. Men and women are different. Even girls and boys are different. Humans, like many animals, are sexually dimorphic (di, “two”; morph, “type”) in the size and shape of their bodies, their physiology, and for our purposes, their behavior. The behavior of boys and girls differs in many ways. Girls generally excel in verbal abilities relative to boys; boys are nearly twice as likely as girls to suffer from dyslexia (reading difficulties) and stuttering and nearly 4 times more likely to suffer from autism. Boys are generally better than girls at tasks that require visuospatial abilities. Girls engage in nurturing behaviors more frequently than boys. More than 90% of all anorexia nervosa cases involve young women. Young men are twice as likely as young women to suffer from schizophrenia. Boys are much more aggressive and generally engage in more rough-and-tumble play than girls (Berenbaum, Martin, Hanish, Briggs, & Fabes, 2008). Many sex differences, such as the difference in aggressiveness, persist throughout adulthood. For example, there are many more men than women serving prison sentences for violent behavior. The hormonal differences between men and women may account for adult sex differences that develop during puberty, but what accounts for behavioral sex differences among children prior to puberty and activation of their gonads? Hormonal secretions from the developing gonads determine whether the individual develops in a male or female manner. The mammalian embryonic testes produce androgens, as well as peptide hormones, that steer the development of the body, central nervous system, and subsequent behavior in a male direction. The embryonic ovaries of mammals are virtually quiescent and do not secrete high concentrations of hormones. In the presence of ovaries, or in the complete absence of any gonads, morphological, neural, and, later, behavioral development follows a female pathway.
Sex differences in appearance are often more pronounced in nonhuman animals than in humans. Male birds particularly, for example roosters, tend to have physical features that differ from the females and also differ significantly in size. [Image: John Cudworth, https://goo.gl/oopnqM, CC BY-NC 2.0, https://goo.gl/VnKlK8]
Gonadal steroid hormones have organizational (or programming) effects upon brain and behavior (Phoenix, Goy, Gerall, & Young, 1959). The organizing effects of steroid hormones are relatively constrained to the early stages of development. An asymmetry exists in the effects of testes and ovaries on the organization of behavior in mammals. Hormone exposure early in life has organizational effects on subsequent rodent behavior; early steroid hormone treatment causes relatively irreversible and permanent masculinization of rodent behavior (mating and aggressive). These early hormone effects can be contrasted with the reversible behavioral influences of steroid hormones provided in adulthood, which are called activational effects. The activational effects of hormones on adult behavior are temporary and may wane soon after the hormone is metabolized. Thus, typical male behavior requires exposure to androgens during gestation (in humans) or immediately after birth (in rodents) to somewhat masculinize the brain and also requires androgens during or after puberty to activate these neural circuits. Typical female behavior requires a lack of exposure to androgens early in life which leads to feminization of the brain and also requires estrogens to activate these neural circuits in adulthood. But this simple dichotomy, which works well with animals with very distinct sexual dimorphism in behavior, has many caveats when applied to people.
If you walk through any major toy store, then you will likely observe a couple of aisles filled with pink boxes and the complete absence of pink packaging of toys in adjacent aisles. Remarkably, you will also see a strong self-segregation of boys and girls in these aisles. It is rare to see boys in the “pink” aisles and vice versa. The toy manufacturers are often accused of making toys that are gender biased, but it seems more likely that boys and girls enjoy playing with specific types and colors of toys. Indeed, toy manufacturers would immediately double their sales if they could sell toys to both sexes. Boys generally prefer toys such as trucks and balls and girls generally prefer toys such as dolls. Although it is doubtful that there are genes that encode preferences for toy cars and trucks on the Y chromosome, it is possible that hormones might shape the development of a child’s brain to prefer certain types of toys or styles of play behavior. It is reasonable to believe that children learn which types of toys and which styles of play are appropriate to their gender. How can we understand and separate the contribution of physiological mechanisms from learning to understand sex differences in human behaviors? To untangle these issues, animal models are often used. Unlike the situation in humans, where sex differences are usually only a matter of degree (often slight), in some animals, members of only one sex may display a particular behavior. As noted, often only male songbirds sing. Studies of such strongly sex-biased behaviors are particularly valuable for understanding the interaction among behavior, hormones, and the nervous system.
A study of vervet monkeys calls into question the primacy of learning in the establishment of toy preferences (Alexander & Hines, 2002). Female vervet monkeys preferred girl-typical toys, such as dolls or cooking pots, whereas male vervet monkeys preferred boy-typical toys, such as cars or balls. There were no sex differences in preference for gender-neutral toys, such as picture books or stuffed animals. Presumably, monkeys have no prior concept of “boy” or “girl” toys. Young rhesus monkeys also show similar toy preferences.
If you think back to the toys and clothing you played with and wore in your youth, do you think they were more a result of your hormonal activity or the choices that society and your parents made for you? [Image: CC0 Public Domain, https://goo.gl/m25gce]
What then underlies the sex difference in toy preference? It is possible that certain attributes of toys (or objects) appeal to either boys or girls. Toys that appeal to boys or male vervet or rhesus monkeys, in this case, a ball or toy car, are objects that can be moved actively through space, toys that can be incorporated into active, rough and tumble play. The appeal of toys that girls or female vervet monkeys prefer appears to be based on color. Pink and red (the colors of the doll and pot) may provoke attention to infants.
Society may reinforce such stereotypical responses to gender-typical toys. The sex differences in toy preferences emerge by 12 or 24 months of age and seem fixed by 36 months of age, but are sex differences in toy preference present during the first year of life? It is difficult to ask pre-verbal infants what they prefer, but in studies where the investigators examined the amount of time that babies looked at different toys, eye-tracking data indicate that infants as young as 3 months showed sex differences in toy preferences; girls preferred dolls, whereas boys preferred trucks. Another result that suggests, but does not prove, that hormones are involved in toy preferences is the observation that girls diagnosed with congenital adrenal hyperplasia (CAH), whose adrenal glands produce varying amounts of androgens early in life, played with masculine toys more often than girls without CAH. Further, a dose-response relationship between the extent of the disorder (i.e., degree of fetal androgen exposure) and degree of masculinization of play behavior was observed. Are the sex differences in toy preferences or play activity, for example, the inevitable consequences of the differential endocrine environments of boys and girls, or are these differences imposed by cultural practices and beliefs? Are these differences the result of receiving gender-specific toys from an early age, or are these differences some combination of endocrine and cultural factors? Again, these are difficult questions to unravel in people.
Even when behavioral sex differences appear early in development, there seems to be some question regarding the influences of societal expectations. One example is the pattern of human play behavior during which males are more physical; this pattern is seen in a number of other species including nonhuman primates, rats, and dogs. Is the difference in the frequency of rough-and-tumble play between boys and girls due to biological factors associated with being male or female, or is it due to cultural expectations and learning? If there is a combination of biological and cultural influences mediating the frequency of rough-and-tumble play, then what proportion of the variation between the sexes is due to biological factors and what proportion is due to social influences? Importantly, is it appropriate to talk about “normal” sex differences when these traits virtually always arrange themselves along a continuum rather than in discrete categories?
Sex differences are common in humans and in nonhuman animals. Because males and females differ in the ratio of androgenic and estrogenic steroid hormone concentrations, behavioral endocrinologists have been particularly interested in the extent to which behavioral sex differences are mediated by hormones. The process of becoming female or male is called sexual differentiation. The primary step in sexual differentiation occurs at fertilization. In mammals, the ovum (which always contains an X chromosome) can be fertilized by a sperm bearing either a Y or an X chromosome; this process is called sex determination. The chromosomal sex of homogametic mammals (XX) is female; the chromosomal sex of heterogametic mammals (XY) is male. Chromosomal sex determines gonadal sex. Virtually all subsequent sexual differentiation is typically the result of differential exposure to gonadal steroid hormones. Thus, gonadal sex determines hormonal sex, which regulates morphological sex. Morphological differences in the central nervous system, as well as in some effector organs, such as muscles, lead to behavioral sex differences. The process of sexual differentiation is complicated, and the potential for errors is present. Perinatal exposure to androgens is the most common cause of anomalous sexual differentiation among females. The source of androgen may be internal (e.g., secreted by the adrenal glands) or external (e.g., exposure to environmental estrogens). Turner syndrome results when the second X chromosome is missing or damaged; these individuals possess dysgenic ovaries and are not exposed to steroid hormones until puberty. Interestingly, women with Turner syndrome often have impaired spatial memory.
Female mammals are considered the “neutral” sex; additional physiological steps are required for male differentiation, and more steps bring more possibilities for errors in differentiation. Some examples of male anomalous sexual differentiation include 5α-reductase deficiency (in which XY individuals are born with ambiguous genitalia because of a lack of dihydrotestosterone and are reared as females, but masculinization occurs during puberty) and androgen insensitivity syndrome or TFM (in which XY individuals lack receptors for androgens and develop as females). By studying individuals who do not neatly fall into the dichotic boxes of female or male and for whom the process of sexual differentiation is atypical, behavioral endocrinologists glean hints about the process of typical sexual differentiation.
We may ultimately want to know how hormones mediate sex differences in the human brain and behavior (to the extent to which these differences occur). To understand the mechanisms underlying sex differences in the brain and behavior, we return to the birdsong example. Birds provide the best evidence that behavioral sex differences are the result of hormonally induced structural changes in the brain (Goodson, Saldanha, Hahn, & Soma, 2005). In contrast to mammals, in which structural differences in neural tissues have not been directly linked to behavior, structural differences in avian brains have been directly linked to a sexually behavior: birdsong.
Several brain regions in songbirds display significant sex differences in size. Two major brain circuit pathways, (1) the song production motor pathway and (2) the auditory transmission pathway, have been implicated in the learning and production of birdsong. Some parts of the song production pathway of male zebra finches are 3 to 6 times larger than those of female conspecifics. The larger size of these brain areas reflects that neurons in these nuclei are larger, more numerous, and farther apart. Although castration of adult male birds reduces singing, it does not reduce the size of the brain nuclei controlling song production. Similarly, androgen treatment of adult female zebra finches does not induce changes either in singing or in the size of the song control regions. Thus, activational effects of steroid hormones do not account for the sex differences in singing behavior or brain nucleus size in zebra finches. The sex differences in these structures are organized or programmed in the egg by estradiol (masculinizes) or the lack of steroids (feminizes).
Taken together, estrogens appear to be necessary to activate the neural machinery underlying the song system in birds. The testes of birds primarily produce androgens, which enter the circulation. The androgens enter neurons containing aromatase, which converts them to estrogens. Indeed, the brain is the primary source of estrogens, which activate masculine behaviors in many bird species.
Figure 2: The sexually dimorphic nuclei of the preoptic area (SDN-POA) Gonadal steroid hormones have organizing effects upon brain and behavior. The organizing effects of steroid hormones are relatively constrained to the early stages of development. Exposure to testosterone (which is converted to estradiol) or estradiol causes masculinization of the brain. These are cross-sections through the brains of rats that show a male (left), a female (center), and a female treated with testosterone as a newborn (right). Note that the SDN-POA (the dark cell bodies) of the male are substantially larger than those of the untreated female but are equal in size to those of the testosterone-treated female. The extent that these sex differences in brain structure account for sex differences in behavior remain unspecified in mammals. OC = optic chiasm; SCN = suprachiasmatic nucleus; V = third ventricle.
Sex differences in human brain size have been reported for years. More recently, sex differences in specific brain structures have been discovered (Figure 2). Sex differences in a number of cognitive functions have also been reported. Females are generally more sensitive to auditory information, whereas males are more sensitive to visual information. Females are also typically more sensitive than males to taste and olfactory input. Women display less lateralization of cognitive functions than men. On average, females generally excel in verbal, perceptual, and fine motor skills, whereas males outperform females on quantitative and visuospatial tasks, including map reading and direction finding. Although reliable sex differences can be documented, these differences in ability are slight. It is important to note that there is more variation within each sex than between the sexes for most cognitive abilities (Figure 3).
Figure 3: The average sex differences in human performance often reflect significant overlap between the sexes There are often greater differences in performance between individuals of the same sex (for example, between Steve and Rick in the figure) than between individuals of the opposite sex (for example, between Steve and Jane in the figure)
Hormones & Behavior by Randy J. Nelson is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License. Permissions beyond the scope of this license may be available in our Licensing Agreement.
