ANALYSIS OF FACTORS INVOLVED IN THE AROUSAL, MAINTENANCE AND MANIFESTATION OF SEXUAL EXCITEMENT IN MALE ANIMALS1

Abstract

A review of numerous experiments dealing with the mating behavior of males of various vertebrate species has suggested a tentative interpretation of the physiological basis of sexual excitement and copulatory reactions. The interpretation is not offered as a completely satisfactory explanatory theory,--but has been formulated with the thought that it may indicate profitable lines of experimental approach to the important problems with which it deals. Sexual arousal leading to mating is regarded as a product of two independent variables. Males differ innately in their susceptibility to sexual arousal. Various stimulus objects differ in their capacity to elicit sexual excitement. The perfectly receptive female constitutes the maximally exciting stimulus object; but a highly excitable male may attempt to mate with less stimulating incentives. The appearance of copulatory reactions is thus seen as a joint function of the male's responsiveness and the incentive's excitatory value. In vertebrate species below the primates the motor patterns of copulation appear to be innately organized. Monkeys and apes give evidence of the inheritance of incompletely organized patterns which must be supplemented by experience. In many species the copulatory pattern is fully organized before puberty, and may be activated by prepubertal administration of hormones. In at least the majority of species the male's copulatory response constitutes a recombination of previously existing motor acts into a new sequence, with the addition of one novel element, --the ejaculatory reaction. The discrete acts comprising the pattern appear to depend upon the activity of centers in the brain stem and spinal cord. The sequential integration of the pattern is mediated by circuits lying below the cerebral cortex, probably in the midbrain; and these executive circuits are subject to afferent impulses from several sensory systems. Excitation of the neuromotor circuits by application of the proper combination of stimuli sometimes raises nervous activity to the threshold level, with the resultant activation of the copulatory response. In all mammals, and to some extent in submammalian vertebrates, the sexual arousal of the inexperienced male depends upon specific patterns of multisensory stimulation. There is no convincing indication that activation of any single sensory system is essential to the occurrence of mating. Conversely, it appears that several kinds of sensory data contribute to the critical pattern which evokes sexual excitement. Experimental evidence shows that the male's susceptibility to sexual arousal is in part a function of forebrain activity. The ease and rapidity with which copulatory reactions may be evoked are greatly reduced by removal of the cerebral cortex. Such findings suggest that the circuits for organization of the motor acts may be subject to facilitative impulses from higher brain centers. It has been proposed that the forebrain contains a Central Excitatory Mechanism contributing to the male's sexual responsiveness. This c.e.m. receives sensory impulses from several receptor systems; and is congenitally predisposed to react maximally to afferent stimulation conforming to a definite pattern (involving the sensory qualities of the receptive female). A centrally maintained tonus in the c.e.m. is augmented by such peripheral stimulation; and when activity within the mechanism reaches the threshold value efferent discharge is conveyed to the neuromotor circuits wherein the copulatory act is organized. Impulses from from the c.e.m. exert a facilitative effect upon the executive circuits, lowering the threshold of the latter to more direct stimulation from the peripheral receptors. The importance of such facilitation is so critical that if it is absent or markedly reduced (consequent to cortical injury) males of some species will not mate. The c.e.m. is thought to increase the “conditionability” of sexual responsiveness. The initial arousal of sexual excitement resulting in mating appears to depend upon the specific stimulus pattern comprising certain sensory qualities of the receptive female. Marked individual differences in sexual excitability may be detected in males of every species; and the inherited level of excitability may be extensively modified by experience. Repeated contact with nonreceptive animals, prolonged segregation, and various other types of experience tend to lower the male's responsiveness to the receptive female. In contrast, secondary stimuli which are originally nonsexual in nature tend to acquire a sexually exciting character when encountered in conjunction with other stimuli to which the male is innately responsive. Subsequently the secondary stimuli may be sufficiently exciting to elicit mating in the absence of many of the originally essential elements of the stimulus pattern. Testicular hormones are assumed to increase the excitability of the c.e.m., and to lower the thresholds of the integrative circuits wherein the masculine copulatory reactions are organized. In the absence of such hormones sexual responsiveness is low, but sluggish copulatory reactions may occasionally occur in response to intense stimulation. Normal amounts of androgen maintain excitability at average levels, permitting the appearance of mating behavior when the receptive female is encountered. If the androgen level is raised far above normal, sexual excitability is markedly increased with the result that the male executes copulatory attempts in response to stimuli normally inadequate to elicit sexual arousal. In addition to mechanisms responsible for organizing the masculine copulatory reactions, the male is endowed with a neuromotor system capable of mediating the mating pattern of the female of his species. These neuromotor circuits receive impulses from certain peripheral receptors, and are simultaneously subject to facilitation from the c.e.m. In the genetic male the threshold of the executive centers mediating feminine copulatory behavior is much higher than the threshold in circuits producing the masculine pattern. Furthermore the male is infrequently subjected to the stimulus pattern adequate to elicit feminine copulatory behavior. Accordingly the appearance of feminine reactions in the male occurs rarely in most species. The incidence of feminine behavior in the male may be increased by either of two methods. If estrogen is administered to the male two effects are produced. The excitability of the c.e.m. is increased (since this mechanism responds to either masculine or feminine hormones), and the threshold of the circuits mediating feminine behavior is lowered. Accordingly the application of the appropriate stimulus pattern may evoke feminine mating reactions. At the same time, because of heightened excitability in the c.e.m., there occurs an increase in the ease with which the masculine response may be elicited. The second method of increasing the feminine reactions in the male rests upon the fact that the central excitatory mechanism is connected with both effector circuits, --one of which produces masculine, and one feminine behavior. Intense activity can be built up within the c.e.m. if the androgen level is very high and maximally exciting stimuli are applied. If, under such conditions, execution of the masculine copulatory reaction is prevented, and if the stimuli which normally evoke the feminine response are brought to bear, the feminine response is elicited. Executive centers for masculine behavior cannot carry out their function because of limitations in the stimulus situation. Efferent discharge from the central mechanism is accordingly diverted into circuits producing feminine behavior, and excitation is so intense that the high threshold in these circuits is overcome. It is suggested that the current but Cartesian differentiation between the sexual behavior of lower animals and that of humans is based upon misconceptions as to the role of the so-called psychic factors in the reactions of the two groups. In actuality the difference is much less marked than is generally supposed, and derives from a purely quantitative variation in the relative importance of extraneous and originally nonsexual factors which are involved in the reproductive reactions of males of all vertebrate species. Future experimentation involving careful analysis of the importance of environmental and experiential factors in the sexual behavior of lower mammals will undoubtedly increase the applicability of results obtained with such subjects to the interpretation of human problems.