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Purves D, Augustine GJ, Fitzpatrick D, et al., editors. Neuroscience. 2nd edition. Sunderland (MA): Sinauer Associates; 2001.

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Neuroscience. 2nd edition.

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Central Nervous System Dimorphisms Related to Reproductive Behaviors

As these examples show, the actions of sex steroids on neurons provide powerful mechanisms for the production of behavioral differences between females and males. In experimental animals at least, the consequences in the central nervous system are evident in sexually dimorphic circuits and behaviors ranging from the control of motor responses to aspects of cognition. This section briefly reviews examples that are specifically related to reproductive behavior; the following section considers sexual dimorphisms related to cognitive behavior.

A good example of sexual dimorphism related to motor control of a reproductive behavior is the difference in size of a nucleus in the lumbar segment of the rat spinal cord called the spinal nucleus of the bulbocavernosus. The motor neurons of this nucleus innervate two striated muscles of the perineum, the bulbocavernosus and ischiocavernosus (Figure 30.4A). In males, the bulbocavernosus and the ischiocavernosus attach to the penis and play a role in both urination and copulation. In females, the bulbocavernosus and the ischiocavernosus are much smaller and attach to the base of the clitoris; they are used to constrict the opening of the vagina. Marc Breedlove and his colleagues first showed that the spinal nucleus containing the motor neurons that innervate the bulbocavernosus is much smaller in female rats compared to males (Figure 30.4B,Figure 30.4C). They next demonstrated that the development of this dimorphism in the spinal cord depends on the maintenance of target muscles by circulating androgens. Since developing males have high levels of circulating sex steroids whereas females do not, these muscles largely degenerate in developing female rats, leaving the motor neurons to atrophy in the absence of trophic support (see Chapter 23).

Figure 30.4. The number of spinal motor neurons related to the perineal muscles is different in female and male rodents.

Figure 30.4

The number of spinal motor neurons related to the perineal muscles is different in female and male rodents. (A) Diagram of the perineal region of a male rat. (B) A histological cross section through the fifth lumbar segment of the male. Arrows indicate (more...)

In humans, the spinal cord structure that corresponds to the spinal nucleus of the bulbocavernosus in rats is called Onuf's nucleus, which consists of two cell groups in the sacral cord (a dorsal-medial and a ventral-lateral group). Although the dorsal-medial group is not sexually dimorphic, human females have fewer neurons in the ventral-lateral group than males (Figure 30.4D). In contrast to rodents, the female perineal muscles in humans remain relatively large throughout life, but are nonetheless smaller than in the male. The difference in nuclear size in humans, like rats, presumably reflects the difference in the number of muscle fibers the motor neurons must innervate.

A variety of reproductive behaviors in both non-human primates and humans are governed by the hypothalamus, including mating, priming, and parenting behaviors (Figure 30.5). In rhesus monkeys, electrophysiological recordings from hypothalamic neurons during sexual activity show that neurons of the medial preoptic area of the anterior hypothalamus fire during different components of the sexual act. Such recordings have been carried out on male monkeys sitting in a flexible restraining chair that allows the male to gain access to a receptive female by pressing a bar, which brings the female close enough to allow mounting by the male. In this way, the responses of hypothalamic neurons can be correlated with “desire” (number of bar presses) and mating behavior (contact, mounting, intromission, thrusting). Neurons in the medial preoptic area of the male hypothalamus fire rapidly before sexual behavior but decrease their activity upon contact with the female and mating (Figure 30.6). In contrast, neurons in the dorsal anterior hypothalamus begin firing at the onset of mating and continue to fire vigorously during intercourse. Although these studies do not speak to sexual dimorphism, they provide direct evidence that the anterior hypothalamus helps to regulate aspects of sexual behavior.

Figure 30.5. Organization of the components of the hypothalamus involved in regulating sexual functions.

Figure 30.5

Organization of the components of the hypothalamus involved in regulating sexual functions. (A) The human hypothalamus, illustrating the location of the anterior hypothalamic area and other nuclei in which sexual dimorphisms have been observed in either (more...)

Figure 30.6. Many neurons in the primate hypothalamus are actively associated with sexual behavior.

Figure 30.6

Many neurons in the primate hypothalamus are actively associated with sexual behavior. This example shows a histogram of neuronal activity recorded in the medial preoptic area in a male monkey exposed to a receptive female (see text). The firing rate (more...)

These and other studies of rodents and non-human primates have stimulated a variety of observations in the human hypthalamus. The most thoroughly documented examples of sexually dimorphic hypothalamic nuclei in humans have been described by Laura Allen and Roger Gorski at the University of California at Los Angeles and supported by Dick Swaab and his colleagues at the Netherlands Institute for Brain Research. There are four cell groupings within the anterior hypothalamus of humans, collectively called the interstitial nuclei of the anterior hypothalamus (INAH; the nuclei are numbered 1–4 from dorsolateral to ventromedial) (Figure 30.7). The original studies by Allen and Gorski reported that nuclei 1–3 of the INAH can be more than twice as large in males as they are in females. These studies were extended by William Byne who reported, along with Swaab and colleagues, that only INAH-3 is consistantly sexually dimorphic in adults. INAH-1 and INAH-2 change in size over time, which may account for differences between the findings of various investigators. INAH-1 is the same size in females and males up until 2–4 years of age; it then becomes larger in males until approximately 50 years of age, when it decreases in size in both sexes. Although generally larger in males, INAH-2 is larger in females of childbearing age than in prepubescent and postmenopausal females. Such changes in nuclear size with age suggest that in humans, as in rodents, these hypothalamic dimorphisms may be related to levels of circulating sex steroids.

Figure 30.7. Sexual dimorphisms in the interstitial nuclei of the human anterior hypothalamus (INAH).

Figure 30.7

Sexual dimorphisms in the interstitial nuclei of the human anterior hypothalamus (INAH). (A) Diagrammatic coronal section through the anterior hypothalamus. The four interstitial nuclei of the anterior hypothalamus (red) are indicated by the numbers 1–4. (more...)

One aspect of human reproduction in which these nuclei have been implicated is the choice of a sexual partner. In addition to heterosexual behavior, some people express sexual interest in both females and males (bisexuality), and some only in members of their own phenotypic sex (homosexuality). Still other people are interested the opposite sex but have a gender identity that is at odds with their phenotypic sex (transgenderism). Based on experimental work in animals and evidence that relatively simple sexual behaviors are influenced by brain dimorphisms, explaining these more complex behaviors in the same general way has been an attractive possibility. To investigate this issue, Simon LeVay, then working at the Salk Institute, compared the INAH nuclei of heterosexual males and homosexual males. LeVay first confirmed Allen and Gorski's findings that the INAH nuclei are sexually dimorphic. He went on to discover that INAH-3 is more than twice as large in male heterosexuals as in male homosexuals (Figure 30.8A). LeVay suggested that this difference is related to sexual orientation.

Figure 30.8. Brain dimorphisms in heterosexual and homosexual human males.

Figure 30.8

Brain dimorphisms in heterosexual and homosexual human males. (A) Micrographs showing difference in INAH-3 between heterosexual and homosexual males. Arrowheads outline the nucleus. (B) The suprachiasmatic nucleus may also differ between homosexual and (more...)

Other researchers have also concluded that dimorphisms of the hypothalamic nuclei are related to sexual orientation and gender identity. Swaab and Michel Hofman examined the suprachiasmatic nucleus of the hypothalamus, which lies just above the optic chiasm in both rodents and humans and generates circadian rhythms (see Figure 30.5A and Chapter 28). This nucleus is also involved in reproductive behavior. In examining the suprachiasmatic nuclei of females, heterosexual males, and homosexual males, Swaab and Hofman found the volume of the suprachiasmatic nucleus to be almost twice as large in male homosexuals compared to male heterosexuals (Figure 30.8B). There was no difference, however, between the size of the suprachiasmatic nucleus in females and heterosexual males. Like LeVay, they suggested that the difference in nuclear size between homosexual and heterosexual men might be related to sexual orientation. This same group has also reported a dimorphism that may be related to gender identity. In comparing male-to-female transgendered individuals to heterosexual males, they found that another hypothalamic structure, the bed nucleus of the stria terminalis, is smaller in transgendered males, being closer in size to that of females.

Taken together, this evidence suggests a plausible explanation of the continuum of human sexuality: Small differences in the relevant brain structures generate significant differences in sexual identity and behavior. In analogy to the rodent, these brain dimorphisms are probably established by the early influence of hormones acting on the brain nuclei that mediate various aspects of sexuality. For instance, low levels of circulating androgens in a male early in life could lead to a relatively “feminine” brain in genotypic males, whereas high levels of circulating androgens in females could lead to a relatively “masculine” brain in genotypic females.

As attractive as this hypothesis may be (and it should be emphasized that it remains unproven), the development of sexuality in humans is probably a good deal more complicated than this scenario implies. Although LeVay's findings support the idea that homosexuality is related to “feminization” of the male brain (recall that INAH-3 in gay males is smaller than in straight males), Swaab and Hofman's data on the size of the suprachiasmatic nucleus undermine the interpretation that the male homosexual's brain is simply “feminized” by a lack of androgens early in development. Whereas they found a difference in the volume of the suprachiasmatic nucleus between homosexual and heterosexual males, in contrast to LeVay they found no difference in the volume of the nucleus between females and heterosexual males. In addition, the development of the INAH-1 dimorphism occurs between 2 and 4 years of age—long after the first testosterone surge in human males. These discrepancies suggest that the development of sexually dimorphic nuclei in humans does not depend solely on early hormone levels. Even adult neural circuits have some plasticity (see next section and Chapter 25), leaving open the possibility that behavior, experience, and changes in circulating hormone levels generate dimorphisms at later stages. In accord with this suggestion, Breedlove and colleagues have reported that the posterodorsal nucleus of the medial amygdala has a greater volume in male rats than in female, but that castration of adult males and androgen treatment of adult females reverses this effect. Thus, the question of whether we are simply born “that way” with respect to sexuality remains difficult to answer with any great confidence. Like most developmental events, a combination of intrinsic and extrinsic factors are probably involved.

Despite these uncertainties, work over the last decade has placed human sexuality on a much firmer biological footing. This is a welcome advance over the not-too-distant past when unusual sexual behavior was commonly explained in social, Freudian, or, worse yet, moralistic terms.

By agreement with the publisher, this book is accessible by the search feature, but cannot be browsed.

Copyright © 2001, Sinauer Associates, Inc.
Bookshelf ID: NBK10994

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