SITES OF HORMONAL ACTION: A. Motivational Mechanisms; 4. A Male sex motivational mechanism

4. A male sex motivational mechanism; organized perinatally by androgen and activated in adulthood by androgen.

As mentioned in the introduction, the existence of a male sex motivational mechanism remains controversial. Although it was suggested by Beach many years ago under the name of a "sexual arousal mechanism" (Beach, 1.956), its existence has been doubted in recent years by many authors, including its original proponent (Beach, 1976b).

The following type s of evidence indicate the existence of a male sex motivational mechanism, and will be considered here in some detail:; (1) the distinction between motivating stimuli and releasing and directing stimuli for male sexual behavior; (2) the temporal coincidence of several motor patterns, including mounting, spinal reflexes, and ultrasound; and (3) the effects of androgen upon all of.these.

Motivating stimuli of male sexual behavior may be distinguished from the releasing and directing stimuli of specific motor patterns. The releasing stimuli of the spinal reflexes of male sexual behavior are tactile stimuli which release particular motor patterns of thrusting, erection, intromission, ejaculation, and kick-off (Hart, 1978; Sachs, 1978). The releasing stimuli of mounting behavior presumably involve exteroceptive stimuli which ensure that the male mounts only appropriately shaped objects and from the proper orientation. Ultrasound, still another motor pattern, may not require any releasing stimuli.

The motivating stimuli for male sex are primarily olfactory, including vomeronasal. Female odors greatly facilitate the mounting by male hamsters (Darby et aI, 1975; Macrides et aI, 1977) and voles (Stehn et aI, 1976). Destruction of olfactory inputs can abolish copulatory behavior in the male hamster (Murphy and Schneider, 1970), mouse (Rowe and Edwards, 1972; Cooper, 1978), and the inexperienced male rat (Wilhelmsson and Larsson, 1973; Thor and Flannelly, 1977). At least part of the deficit may be due to involvement of the vomeronasal system and its projections to the cortico-medial amygdala {Powers and Winans, 1975; Harris and Sachs, 1975). Bulbectomy does not always abolish male sexual behavior, however; male gerbils continue to mate after bulbectomy (Cheal and Domesick, 1979), and sexually experienced male rats are less disrupted than naive males. This suggests that sensory systems other than olfaction may provide motivating stimuli, and that conditioning may occur, at least in the rat. Unlike the female sex motivational mechanism, the male mechanism apparently does. not receive motivating stimuli from genital tactile stimulation (Carlsson and Larsson, 1964; Adler and Bermant, 1966); instead, such stimuli are limited to releasing and directing role for the spinal reflexes of male sex.

The distinction between motivating stimuli and releasing/directing stimuli parallels a distinction that has long been made between a "sexual arousal mechanism" and an "intromission and ejaculating mechanism" (Beach, 1956). The former corresponds to what I am calling the male sex motivational mechanism and is activated by motivating stimuli. The latter corresponds to the motor patterns that I am calling the spinal male reflexes and are activated by releasing and directing stimuli.

When the male sex motivational mechanism has been activated, there are at least three types of motor patterns simultaneously activated: mounting, male sex spinal reflexes, and ultrasound vocalization. I have reviewed the effects of olfactory motivating stimuli upon mount1ng above. The male spinal reflexes of sex follow the temporal patterning of excitation and inhibition of sexual behavior that is shown by mounting (Sachs and Garinello, 1978), and although relevant data have not yet been obtained in muroid rodents, there are exteroceptive motivating stimuli for the male sex spinal reflexes in other mammals (Hart, 1967a). Finally, there are data suggesting the ultrasound vocalization of male sexual arousal is activated by the same motivating stimuli that act upon mounting. Ultrasound in the male hamster may be obtained in response to an anesthetized female (Floody and Pfaff, 1977b) ,in the sexually experienced male mouse ultrasound may be obtained in response to female urine (Dizinno et a1, 1918), and in the rat it may be obtained in response to female odors, especially those of estrous females (Geyer and Barfield, 1978). The data. on ultrasounds are sometimes difficult to interpret, because there is some indication that muroid rodents may use more than one type of ultrasound vocalization. There may be a long pulse vocalization which is a motor pattern of submission and sexual arousal, and a short pulse that may be used for echolocation either in conjunction with locomotion or as a motor pattern of exploration/marking (Adams, submitted for publication). During courtship the male rat shifts from 50 khz ultrasound which may be exploratory to 22 khz that is probably a motor pattern of the male sex motivational system at the peak of sexual arousal (Geyer and Barfield, 1978).

The effect of androgen upon male sex may be interpreted as the activation of a motivational mechanism for male sexual behavior (figure 1, site 4). Castration, after a lapse of time, causes the disappearance of normal male mounting behavior, and androgen administration restores normal levels of responding in the rat (Beach and Holz-Tucker, 1949) and hamster (Clemens, 1974). Castration also greatly reduces ultrasound vocalization by male mice in response to female odors and androgen administration restores normal responding (Dizinno and Whitney, 1977). Females can be made to show male sexual behavior if injected with androgen as an adult, especially if they have been subjected to androgen at the age of sexual differentiation either due to male littermates in the womb or else due to experimental injections (Clemens, 1974).

The hypothetical male sex motivational mechanism may be located in the medial preoptic hypothalamus which is apparently the site of the facilitating effects of androgen on male sexual behavior. Preoptic lesions abolish mounting behavior in normal male rats (Heimer and Larsson, 1966; Singer, 1968). Testosterone is specifically taken cells of the preoptic hypothalamus, and implantation of testosterone in this region can induce male sexual behavior in the rat (Davidson, 1966). In the rat, electrical stimulation of the medial preoptic area produces mounting (Malsbury, 1971) and lesions of the medial forebrain bundle can abolish mounting (Hitt et al, 1970), perhaps because they interrupt fibers projecting from the preoptic to lower nervous centers.

A clear distinction between the female and male sex motivational mechanisms can be made On the basis of brain lesion data. Lesions that abolish male sexual behaviors are anterior to those that abolish female sexual behaviors (Singer, 1968; Dörner. et a1, 1969).

The effects of neural structures in the brain upon mounting and the various spinally-organized sexual reflexes may be due to disinhibition, i.e. the removal of a normal tonic inhibition of spinally- organized reflexes (Beach, 1967a). Thus, for example, spinal reflexes evoked by genital stimulation are more easily evoked in an animal after cutting of the spinal cord to remove brain influences (Hart, 1968). This might also explain why lesions of the diencephalic/mesencephalic junction (that would be expected to disrupt descending influences from the preoptic hypothalamus) appear to disinhibit male mounting behavior (Heimer and Larsson, 1964).

The neural substrate of male sexual behavior is organized early in life by circulating androgen. If a male is castrated in the first few days of life, it fails to show complete male sexual behavior when given androgen as an adult, although even by this age there is some effect of androgen from the embryonic testes (Beach, 1976b). Injection of androgen into a young genetic female rat will organize her male sexual motivational mechanism so that she shows not only mounting behavior as an adult (Sachs et a1, 1973; Gray et a1, 1976) but also male patterns of ultrasound as well (Pollak and Sachs, 1975). Similar data have also been obtained from the hamster (Crossley and Swanson, 1968), but in the mouse, perinatal androgen does not increase the occurrence of adult mounting (Edwards and Burge, 1971). In the mouse, as well as the rat, male sexual behavior may be obtained in otherwise normal adult females by the injection of testosterone, which may be dependent upon previous androgenic stimulation from male littermates in the womb (Clemens, 1974). The perinatal effects of androgen are apparently exerted upon hypothalamic neurons (Nadler, 1968), presumably those which form the male sex motivational mechanism in adulthood. A low level of male sexual behavior is normal among females in many species without additional administration of androgen (Beach, 1968).

References A-B

References C-H

References J-P

References Q-Z

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