Chapter 4: Neuroendocrinology of Sexual Behavior
in the Male
In the last chapter, we looked at the role of primarily estrogen
and progesterone in stimulating proceptive and receptive aspects of
female sex behavior.
In our consideration of male sex behavior, we will consider how
the primary androgen, testosterone, is secreted by the testes. And
then, further, the role of two metabolites of testosterone, estrogen
and 5a-dihydrotestosterone (DHT), to the control of sexual motivation
andcopulatory behavior in the adult male. We will then go on to
consider what brain regions play an important role in mediating the
various aspects of male copulation and the role of select
neuropeptides in stimulating this response.
How do we define male sex behavior?
Male sex behavior is defined as having two major components (similar to what we discussed in females): 1) precopulatory behaviors, and 2) copulatory behaviors. A related concept, that is important to our understanding of male sex behavior, is the role of sexual motivation, or sexual desire.
* precopulatory behaviors can range from a few seconds of sniffing odors secreted by a female to elaborate displays of courtship behaviors (that occur in a variety of fish and bird species)
* in rats, females secrete one class of odors that stimulate the male to investigate the anogenital region of the female (chemoinvestigation) and another class to stimulate the male to mount the female (copulation); during this period of precopulatory investigation, both males and female may emit ultrasonic vocalizations that augment each others' excitation as well as their own; so sniffing and chasing the female as well as producing ultrasonic vocalizations are the major precopulatory behaviors shown by a male rat
* the purpose of precopulatory behaviors is to stimulate sexual excitation in an individual and in his or her partner
* precopulatory behaviors are followed by copulatory behaviors; copulatory behaviors are categorized into three main groups:
* mounts: male mounts a sexually receptive female
* intromissions: following mounting, a male will show penile erection and insertion of the penis into the vagina
* after a series of mounts and intromissions, a male will show an ejaculation: explusion of a copulatory "plug" which is composed of secretions from the prostate, seminal vesicle, and coagulating gland plus sperm from the testes; the copulatory plug ensures that the sperm will pass into the uterus, increasing the likelihood that fertilization of ova will occur
* In rats, as is true of many other species, a male will display several mounts and intromissions before ejaculating. The male will mount a female, intromit, and then dismount after each intromission; the male will show a series of mounts with intromissions before ejaculating. Following ejaculation, there is a refractory period in which the male does not engage in sexual activity with the female (this period is called postejaculatory interval). After several ejaculations with a female, the male will stop mating; sexual satiety.
If we are interested in understanding how hormones can affect male
sex behavior, then we have to have an idea of how we can quantify
male copulation. There are several measurements that can be
quantified with respect to male copulation:
* measure the amount of time the male spends sniffing female's odors (chemoinvestigation)
* mount latency: amount of time it takes for a male to mount the female for the first time
* record the number of mounts shown by a male during a particular period of time
* record the number of intromissions as well as the length of time between each intromission (interintromission interval) and even the number of intromissions that precede an ejaculation
* ejaculation latency as well as the postejaculatory interval (which is the time from the occurrence of the ejaculation to the next mount); in animals that ejaculate multiple times, we can determine the number of ejaculations shown during a given mating test
Precopulatory and copulatory behaviors are clearly apparent when
watching males engage in sex behavior. Less clear, but equally
important, is the male's desire to engage in sexual activity.
* sexual motivation: can be defined as a male's inclination to seek out and approach a female for the purpose of mating
* sexual motivation differs from the ability to engage in a sexual act. Your book describes the example of a diabetic man whose penile erectile capacity is compromised due to damage to the innervation of erectile tissues of the penis; so the man cannot engage in sexual activity, but this is due to the fact that he cannot maintain an erection not because he is uninterested in sexual activity; so when an individual does not engage in sex, it becomes an issue of whether that individual is may not be interested in sex (low motivation) or simply unable to engage insex (physical disorder)
How can we study sexual motivation?
* some scientists have suggested that the latency to mount may provide an adequate measurement of sexual motivation (more motivation > faster mounting); however, others have argued that additional factors could influence the rate of mounting that would make this measure invalid: What kinds of factors could influence the rate of mounting? physical attributes of the male (if a male had an injured hindlimb, he would have a slow latency to mount but that really would not reflect sexual motivation, rather it would indicate a problem in his ability to catch the female); proceptive behavior shown by the female
* other tests have been designed to get at the sexual motivation of the male without possible confounding effects of motoric responses or that of the female
* for example, a male is placed on one side of an obstacle, electrified grid, and a female is placed on the other; after each mount or intromission, the male is returned to the other side of the obstacles; the amount of electrical current the male withstands to reach the female is taken as a measure of sexual motivation
* female is placed in a box at the end of a runway; how quickly the male runs down the runway to reach the female can be used as an indication of sexual motivation (assumption would be that different groups of males can show a similar rate of locomotion)
* a male may be required to press a bar or lever a certain number of times in order to gain access to a receptive female
Neuroendocrine Function in the Male
* In the male, neurons in the hypothalamus secrete GnRH into the median eminence, which stimulate the release of LH and FSH into general circulation.
* The release of GnRH and other steroids occurs in a pulsatile fashion; this is true in the female as well as in the male.
* LH will act at receptors in the Leydig cells of the testes to stimulate testosterone formation and secretion.
* Testosterone will act then upon androgen receptors (testosterone or dihydrotestosterone) and/or estrogen receptors (via aromatization to estrogen) in the adult male brain to stimulate components of male sex behavior.
* Testosterone is also important for the production of sperm; T plus FSH act upon receptors on Sertoli cells to stimulate spermatogenesis (formation of mature sperm from dividing germ cells in the seminiferous tubules).
There is considerable variation among vertebrate species in the
seasonal pattern of testosterone secretion and in the sensitivity of
the brain to the actions of testosterone.
* in seasonal breeders (hamsters, ferrets & sheep), mating occurs during a specific time of the year; during breeding season, levels of GnRH, LH and testosterone are high as well as the display of male sex behavior; when the animal passes out of the breeding season, there is a regression of the hypothalamic-pituitary-gonadal axis; so levels of GnRH, LH and testosterone decrease dramatically, testicular regression,and cessation of production of mature sperm (these changes reverse when breeding season again approaches)
* in season breeders, changes in photoperiod (relative duration of day and night) play a role in timing changes in hypothalamic-pituitary-gonadal axis; photoperioid interacts with length of gestation to influence the timing of breeding
* Ex. in male sheep, breeding occurs in the fall in response to shortening day length; in male ferrets, breeding occurs in the spring, when the days are growing longer; so breeding can occur in response to increasing or decreasing day length, the key difference is the length of gestation and its importance to survival of the offspring. In sheep, gestation lasts 5 months, so mating and fertilization occurs in the fall, so that the offspring (lambs) are born in the spring, when conditions are optimal for survival of the newborn. In ferrets, gestation lasts only 41 days and so mating can occur in the spring because the offspring will be born in the spring and will have the best chance for survival.
* there are species that are not seasonal breeders; rats and primates
In addition to controlling testosterone secretion, there is some
suggestion that photoperiod can affect the responsiveness of the
nervous system to circulating hormones.
* For example, castrated hamsters housed given them exogenous
testosterone while housing them under a short-day photoperiod or a
long-day photoperiod, you will find that the short-day photoperiod
has an inhibitory effect on male sex behavior, even though levels of
testosterone are the same between the two groups (normally, hamsters
are not sexually active under conditions of a short-photoperiod).
What is the role of testosterone, and its metabolites
estrogen and 5a-reductase, in stimulating male copulation?
We will focus our discussion initially on sex behavior in male
rats, and then discuss some differences between species.
In the male rat:
* developmentally: T is important for virilization of the Wolffian ducts, T > DHT is important for masculine development of external genitalia, and development of spinal nucleus of bulbocavernosus, T > E is important for masculinizing the brain (development of the SDN-POA)
* in the adult, it has been suggested that T > DHT is important
facilitating penile erections and intromissive capacity (E or
androgens from other sources may play a role under certain
circumstances); T > E is important for facilitating mating
behavior (display of mounts and intromissions); how can we tell?
Picture (flips/flops); study penile erections without a female;
latency to penile erection; study mating by measuring latency to
first intromission with a female Figure 4.1.
* in rats, if you give castrated males estrogen, the male will
show mounting and intromission, although full erectile function is
believed to require androgens; in other species, androgens must be
present for erections to occur; if you give castrated male's DHT, the
male will not show mounting or intromission, although the male is
capable of producing penile erections
* Does estrogen duplicate all of the behavioral effects of
testosterone? No, suggested that, in at least some species like
ferrets, T may be important in stimulating masculine sexual
motivation including partner preference. Figure 4.3.
* in male rats and hamsters, E is thought to stimulate mating and DHT (and E) stimulates erectile function
* in other species, lizard, mouse and guinea pig, DHT can stimulate mating
* in primates, neither E, nor DHT, nor their combination can duplicate the activational effects of T on masculine sexual performance
How do androgens and estrogens interact within the brain to
stimulate male sex behavior?
First, the MPOA is critical for the display of mounts,
intromissions and ejaculations, and for the ability of gonadal
steroids to stimulate the response.
* if you lesion MPOA, male loses ability to show these behaviors
* if you electrically stimulate MPOA, the occurrence of these behaviors are increased (facilitatory effect)
* if you castrate male rats, and then implant T or E into MPOA, male rats will show mounts and intromissions; ERs and ARs are present within MPOA; if you implant DHT into MPOA, no or little sex behavior will be shown
* [if you implant aromatiase inhibitor into MPOA of intact males, you will inhibit mounts and intromissions]
MPOA projects to neurons within midbrain and brainstem (not
midbrain central gray), and from there neurons project to spinal
cord; these are excitatory inputs and they lead to 2 major effects:
1) autonomic control of erections and ejaculations, 2) motor control
of mounting and pelvic thrusting; MPOA is important in controlling
Brain regions in the forebrain can facilitate or inhibit the
display of male sex behavior. Let's consider two brain regions that
can facilitate the display of male copulation.
The amygdala plays an important role in associative
processes that feed into emotional and behavioral circuits. When we
consider male sex behavior we can define it into two main types of
responses: appetitive responses and consummatory responses. This
distinction is true of other behaviors.
* refers to the more stereotypedresponses such as the display of mounts and intromissions; MPOA is critical for the display of these copulatory reflexes
* corticomedial amygdala (CMA) processes olfactory inputs > MPOA > midbrain/brainstem >SC (show schematic)
* in some species, like the hamster, chemosensory inputs are critical to the display of male sex behavior; if you block the detection of pheromones, you block male sex behavior; other species are less dependent upon chemosensory inputs (inputs may facilitate behavior but they are not required for behavior to occur)
* refers to processes that bring a male into direct contact with the female, and can include locomotor activity, chemoinvestigation or other types of learned responses (such as bar pressing to gain access to a female)
* in the amygdala, the basolateral nucleus (BLa) has been implicated in associative learning that feeds into motivational circuits
* BLa > NAcc (ventral striatum; linked to motivational responses) ventral pallidum brain regions involved in motor responses
* chapter describes the role of BLa in associating relationship between bar pressing to gain access to an estrous female; if you lesion BLa, the male will stop bar pressing to gain access to the estrous female, but if you place a female into his cage, he can readily mate with her;what is lost is the learned association between bar pressing and access to an estrous female
* similarly, lesions of NAcc have only minor effects on the display of copulation; one can dissociate motivational circuits from those involved in specific motoric responses such as mounting; but increased sexual motivation can enhance the rate of male copulation
Of interest, dopamine plays an important role in these
* dopamine cell groups implicated in male sex behavior: 1) neurons within ventral tegmental area (VTA) > nucleus accumbens (NAcc) > ventral pallidum > motor control areas of brain (imp. for motivation and reward; not specific to sex behavior); 2) incertohypothalamic dopamine neurons > MPOA (imp. for mounts, intromissions, and ejaculations; 3) substantia nigra > dorsal striatum (general locomotion)
* we can measure level of dopamine and/or its metabolites within extracellular space; it is believed that increased levels of extracellular dopamine indicates increased release of dopamine at synapses
* we can follow the release of dopamine in specific brain region during sex behavior
* in dorsal striatum, dopamine release increases significantly when male engages in sex behavior (link to locomotion associated with mating)
* in nucleus accumbens, dopamine increases first when a male is placed into chamber in which it has mated previously (anticipatory response), dopamine increases further when the male can see the female but not contact her, and then even more when he is able to mate with the female (link to responses not simply associated with mounts and intromissions; role in sexual motivation)