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Frank A. Beach award. Homologies of animal and human sexual behaviors.

Theoretical models of animal and human sexual behavior have evolved from two very different literatures, yet they contain many common behavioral components that may reflect the action of similar neuroendocrine and neurochemical systems. The study of animal sexual behavior has been largely concerned with mechanisms that underlie the pattern of consummatory behaviors observed during copulation, behaviors that tend to be highly stereotyped, sexually differentiated, and species-specific. There are important species differences in the behavioral topography, endocrine control, and neural substrates of consummatory behaviors, which tend to be extreme when comparing animals and humans. Although this has led to an increased interest in comparative animal behavior, it has also helped to foster a general perception that animals and humans are fundamentally different. In contrast to consummatory behaviors, appetitive behaviors (which serve to bring animals and humans into contact with sexual incentives) are more flexible, less sexually differentiated, and less species-specific and span a variety of situations other than sexual interactions. Appetitive behaviors are thus viewed as "sexually specific" when they are displayed under sexual circumstances and reinforced by sexual incentives. Interestingly, an appetitive/consummatory dichotomy has emerged in the human literature which distinguishes measures of sexual desire or arousal from "performance" measures of masturbation or copulation. In fact, sexual desire, which reflects fantasy and behavioral excitement, has been further differentiated from sexual arousal, which reflects genital blood flow. The present analysis attempts to pull together these seemingly disparate literatures into a coherent theoretical framework that emphasizes similarities and differences in the structure of sexual behavior across rats and humans.

Animals↗

The selective D2 dopamine receptor antagonist eticlopride counteracts the ejaculatio praecox induced by the selective D2 dopamine agonist SND 919 in the rat.

The selective D2 antagonist eticlopride, at a dose (0.01 mg/kg, s.c.) that fails to modify the normal behavior of rats, significantly reversed all the behavioral effects exerted by the selective D2 agonist SND 919 (0.1 mg/kg, i.p.), namely, the stimulation of stretching-yawning, penile erection and sedation and the inhibition of grooming. In the copulatory test, eticlopride at the same dose did not affect animal sexual behavior but potently counteracted the reduction in mount and intromission frequency and latency to ejaculation induced by SND 919 at 0.1 mg/kg, a behavioral pattern which might possibly be proposed as an animal model for human ejaculatio praecox.

Animals↗

What can animal models tell us about human sexual response?

In all species, sexual behavior is directed by a complex interplay between steroid hormone actions in the brain that give rise to sexual arousability and experience with sexual reward that gives rise to expectations of competent sexual activity, including sexual arousal, desire, and performance. Sexual experience allows animals to form instrumental and Pavlovian associations that predict sexual outcome and thereby directs the strength of sexual responding. Although the study of animal sexual behavior by neuroendocrinologists has traditionally been concerned with mechanisms of copulatory responding, more recent use of conditioning and preference paradigms, and a focus on environmental circumstances and experience, has revealed behaviors and processes that resemble human sexual responses. In this paper, we review behavioral paradigms used with rodents and other species that are analogous or homologous to human sexual arousal, desire, reward, and inhibition. The extent to which these behavioral paradigms offer predictive validity and practicality as preclinical tools and models is discussed. Identification of common neurochemical and neuroanatomical substrates of sexual responding between animals and humans suggests that the evolution of sexual behavior has been highly conserved and indicates that animal models of human sexual response can be used successfully as preclinical tools.

Animals↗

The effects of repeated administration of MDMA on the expression of sexual behavior in the male rat.

3,4-Methylenedioxymethamphetamine (MDMA, "Ecstasy") is a potent neurotoxin which preferentially produces 5-HT nerve terminal degeneration in the CNS in both rodents and primates. Timely research on the behavioral effects of acute and long term treatment of MDMA is critical due to the neuropathological effects of MDMA and its abuse liability. Presently, there are no published reports that have systematically examined the effects of acute or chronic treatment of MDMA on animal sexual behavior. Accordingly, the effects of repeated systemic administration of MDMA on a variety of parameters of male sexual behavior in sexually vigorous male rats were studied. Treatment consisted of subcutaneous injections of MDMA (40 mg/kg) or saline (1 ml/kg) every 12 hours for 4 consecutive days. In addition, neurochemical assessments of brain 5-HT and 5-HIAA depletion following repeated MDMA treatment were also conducted using reverse phase liquid chromatography. The results of this study revealed that repeated systemic administration of MDMA to sexually vigorous male rats produced a transient disruption of the expression of male copulatory behavior. In addition, in MDMA-treated males that did display copulatory behavior, both the ejaculation latency and postejaculatory interval were dramatically lengthened when compared to saline injected controls. Surprisingly, one week after the first behavioral test, copulatory behavior in MDMA treated rats appeared unaffected despite a marked depletion of 5-HT and 5-HIAA content in the striatum, and hippocampus.

3,4-Methylenedioxyamphetamine↗

Sexual behavior of farm animals.

The field of sexual behavior of domestic farm animals is discussed with emphasis on studies of cattle, sheep and goats. Descriptions are provided of behaviors related to the attractivity, proceptivity and receptivity of females, as well as environmental and physiological factors influencing both male and female sexual behavior. The organizational and activational actions of steroid hormones on behavior are also reviewed.

Journal Article↗

Medical differentials with potential behavioral manifestations.

Boundaries between behavioral conditions and medical differentials are likely to blur more rather than less as we learn more about genomic, cellular, and subcellular effects on common conditions. These changes should lead to better treatment but may also require a paradigm shift in how we view behavioral conditions and the mechanisms that contribute to them.

Aggression↗

Preclinical models of sexual desire: conceptual and behavioral analyses.

The epidemiology, etiology and proposed treatments for the sexual desire disorders are briefly reviewed before turning to an analysis of preclinical models. We suggest that the concept of sexual desire in the human is equivalent to sexual motivation as employed in the scientific literature. Many animal tests for sexual motivation have been described over the years. Most of them are based on the evaluation of the rate or speed of performing learned operant responses. These are not ideal measures for inferring the intensity of sexual motivation. We present a test for sexual incentive motivation, which has been used in male and female rats. No learning is involved, and the test is rather insensitive to variations in ambulatory activity and it does not employ rate measures. A procedure that recently has attracted much attention, paced-mating behavior in the female, does not seem to be as useful as could be expected. In fact, it does not appear to be superior to tests for sexual receptivity (lordosis). The lack of established, clinically efficient treatments for sexual desire disorders makes it difficult to evaluate if any model has predictive validity. However, the model proposed here may be isomorphic and homologous to the human condition.

Animals↗

Molecular biology tools for dissecting sexual behavior.

The tools of molecular biology have just begun to demonstrate the role of genes in controlling sexual behavior and how hormones can influence sexual and reproductive motivation by controlling gene expression. In this review article the use of the new term "molecular sexology" is proposed to indicate the growing evidence that molecular biology techniques can be a useful tool not only to understand the genetic bases of the animal (and soon human) sexual behavior, but also in order to provide the rationale of the use of advanced therapeutic approaches, such as gene transfer, to the symptoms and diseases of sexuality.

Animals↗

Chlordecone (Kepone) on the night of proestrus inhibits female sexual behavior in CDF-344 rats.

The effect of the estrogen-like chlorinated pesticide chlordecone (Kepone) on sexual behavior was examined in proestrous rats following treatment with 25, 50, or 75 mg/kg chlordecone. In most animals, sexual behavior, both receptivity and proceptivity, was reduced within 60 min following the higher dosage of chlordecone. Reduced sexual receptivity occurred more slowly with 50 mg/kg chlordecone (usually within 180 min) and no reduction was seen following 25 mg/kg chlordecone. The reduced sexual behavior after chlordecone treatment preceded the onset of marked chlordecone-induced tremor. A group of rats treated with 75 mg/kg chlordecone was euthanized at the time that behavioral inhibition began to develop. The content of serotonin, norepinephrine, and their principal metabolites was determined by high-performance liquid chromatography of extracts of brain tissue of these animals. In hypothalamus, increases in serotonin (5-HT) and 5-hydroxyindoleacetic acid (5-HIAA) content, and a decrease in the level of norepinephrine (NE), were detected in chlordecone-treated rats relative to matched controls which received vehicle. The content of 5-HT was also increased in preoptic area of chlordecone-treated females. The content of the catecholamine metabolite, 3,4-dihydroxy-phenylacetic acid, was unaffected by chlordecone in either part of brain. These are the first observations of the parallel effects of chlordecone on receptive and proceptive behaviors, and on neurochemistry, in female rats; the results demonstrate short-latency effects of the pesticide treatment on the CNS events that mediate female reproductive behavior. Results of previous studies had led to the suggestion that chlordecone's inhibition of sexual behaviors resulted from its interaction with the intracellular estrogen receptor. However, the rapidity of the inhibition during the period of ongoing sexual behavior makes it unlikely that the inhibition is mediated by the pesticide's action at the intracellular estrogen receptor. Because of the importance of sexual behaviors to reproductive fitness, the current results indicate that nonsteroidal, behavioral mechanisms could contribute to chlordecone's neuroreproductive toxicity.

Analysis of Variance↗

Animals models for the development of human sexuality: a critical evaluation.

Biological explanations of human homosexuality build upon a theoretical framework developed from the study of animals, especially that of rodents. Researchers have constructed a physiological model to explain the origin and development of "masculine" and "feminine" behavior. According to this model hormones acting at critical stages in early development organize cells in key areas of the brain. After puberty these hormonally organized brain regions are purportedly capable of activation by post-pubertally produced circulating hormones. This model of sexual development, called the organizational-activational (O/A) model, has framed research on sexual behavior in animals and animal-based account of human behavior for more than 30 years. However, evidence from a variety of sources has slowly accumulated, requiring modification after modification of the original premise. Continuing to use the organizational-activational model now interferes with the acquisition of new knowledge. I sketch the outlines of an alternative bio-social program for research on the development of sexual behavior in animals.

Adolescent↗

Hormones and history: the evolution and development of primate female sexuality.

Sexual behavior is required for reproduction in internally fertilizing species but poses significant social and physical risks. Females in many nonprimate species have evolved physical and behavioral mechanisms restricting sexual behavior to when females are fertile. The same hormones producing female fertility also control these mechanisms, assuring that sex only occurs when reproduction is possible. In contrast to nonprimate mammals, hormones do not regulate the capacity to engage in sex in female anthropoid primates, uncoupling fertility and the physical capacity to mate. Instead, in primates, sexual motivation has become the primary coordinator between sexual behavior and fertility. This dependence upon psychological mechanisms to coordinate physiology with behavior is possibly unique to primates, including humans, and allows a variety of nonphysiological influences, particularly social context, to regulate sexual behavior. The independence between hormonal state and sexual behavior allows sex to be used for social purposes. This complex regulation of primate sexuality develops during adolescence, where female monkeys show both hormonally influenced sexual motivation and socially modulated sexual behavior. We present findings from rhesus monkeys illustrating how social context and hormonal state interact to modulate adolescent and adult sexuality. It is argued that this flexibility in sexual behavior, combined with a tight regulation of sexual motivational systems by reproductive hormones, allows sexual behavior to be used for nonreproductive purposes while still assuring its occurrence during periods of female fertility. The evolutionary pressures that produced such flexibility in sexual behavior remain puzzling, but may reflect the importance of sexuality to primate social attraction and cohesion.

Adolescent↗

Age-related changes in plasma oestrogen concentration, behavioural responsiveness to oestrogen, and reproductive success in female gray-tailed voles, Microtus canicaudus.

Age-related increases in the incidence of vaginal cornification were associated with increases in the reproductive success of female gray-tailed voles previously isolated from males. The pregnancy rate of females first paired with males at 30-50 days of age was significantly lower than that of females first paired at 90-120 or 150-200 days of age. The improvement was due to increases in propensities to display receptive behaviours and decreases in the incidence of sterile matings. Although plasma oestrogen concentrations increased with age and were higher in receptive than unreceptive females, plasma oestrogen values alone did not account completely for differences in receptive behaviours amongst females of different ages. Females ovariectomized at 30-50 days of age rarely displayed receptive behaviours when treated with large doses of oestradiol benzoate, whereas nearly all females similarly treated were receptive if ovariectomies were performed between 150 and 200 days of age. The receptivity rate of females ovariectomized between 90 and 150 days was intermediate between the rates of the other two groups.

Animals↗