The role of aromatization in androgen stimulation of gerbil scent marking

The androgen dependent scent marking behavior of male Mongolian gerbils (Meriones unguiculatus) can be stimulated after castration by either testosterone or estrogen, but not by dihydrotestosterone (DHT). To determine if DHT fails to evoke scent marking because it cannot be aromatized to form an estrogen, two other nonaromatizable androgens, 1α-methyltestosterone and 6α-fluorotestosterone, were studied. 6α-Fluorotestosterone and its propionate ester stimulated scent marking in castrated male gerbils as effectively as testosterone and its ester did. Hence, an androgen's aromatizability does not determine its ability to influence gerbil scent marking behavior.     

The hormonal control of scent marking and precopulatory behavior in male gray short-tailed opossums (Monodelphis domestica)

Little is known about the hormonal control of behavior in marsupials. In the present study, the effects of castration and of testosterone or estradiol replacement therapy on scent marking and precopulatory behavior in male gray short-tailed oppossums (Monodelphis domestica) were examined. It was found that castration resulted in decreases in chest and flank/hip marking displayed by male gray opossums. Testosterone but not estradiol stimulated chest marking in castrates. Males treated with either estradiol or testosterone displayed more flank/hip marking than control males. Highest levels of female aggression toward males were seen when the males had received testosterone treatment. These findings are discussed with respect to similarities and differences between marsupials and eutherians in the neural metabolism of testosterone and the hormonal control of scent marking behavior.     

Independent control of sexual and scent marking behaviors of male gerbils by cells in or near the medial preoptic area

This research studied the role of the medial preoptic area and adjacent cell populations in androgen control of scent marking and sexual behavior in male gerbils (Meriones unguiculatus). Experiment 1 replicated previous research showing that implants of testosterone propionate in or near the medial preoptic area reinstate marking behavior in castrates. Implant sites near the diagonal band of Broca or in the posterior part of the medial preoptic area, near the anterior hypothalamus, are more effective than other sites. Experiment 2 showed that medial preoptic area lesions permanently impair sexual behavior despite testosterone stimulation. Experiments 2–4 showed that lesions in or near the medial preoptic area can also disrupt scent marking; however, this behavior gradually recovered in many lesioned males, especially if they received testosterone. The data suggest that both scent marking and sexual behavior are controlled by androgens acting on cells in or near the medial preoptic area, but the cell populations involved in these two behaviors are probably not the same.     

Sexual behavior and scent marking in male gerbils: comparison of changes after castration and testosterone replacement

This study compared changes in sexual behavior of male gerbils with changes in scent-marking frequency following castration and exposure to various doses of testosterone. Castration eliminated sexual activity in male gerbils. Injections of testosterone propionate (75 μg twice weekly) prevented this decrease. Larger (600 μg) injections of testosterone propionate or implantation of Silastic capsules of testosterone reinstated mating behavior. Sexual behavior showed a different pattern of changes than scent marking. Sexual behavior was maintained more effectively than scent marking by hormone injections, but scent marking was reinstated more readily than sexual behavior by the tonic hormone levels produced by Silastic implants.     

Social parameters and urinary testosterone level in male chimpanzees (Pan troglodytes)

Studies investigating relationships between social parameters (such as dominance rank, rates of aggressive and sexual behaviors) and androgen (particularly, testosterone) levels in male primates have yielded inconsistent results. In the present study, we address the relationship between androgens, male dominance rank and rank-associated behaviors in two groups of captive chimpanzees, a species characterized by a pronounced dominance hierarchy between adult males. By combining behavioral observations with urinary testosterone (T) measurements, we found that the differences in T concentrations between males were small and not obviously related to their dominance rank. T levels were not related to the rates of initiated aggression and copulatory behavior, but a significant negative relationship between male T level and the rates of strong aggression received was apparent. Our findings, combined with those of others, suggest that any relationship between dominance rank and T depends upon the extent to which individual rank-associated behaviors (e.g. aggressive/sexual) are themselves related to T.     

Castration in Gambel's and Scaled Quail: ornate plumage and dominance persist, but courtship and threat behaviors do not

During the breeding season, testosterone in male birds is often linked to some secondary sexual ornaments, courtship behaviors, and intrasexual aggression. I examined the effect of castration on plumage expression in Gambel's Quail (Callipepla gambelii), a species in which males are highly ornate, and in Scaled Quail (C. squamata), an unornamented species. Using male pairs, each consisting of a castrate and a control, I also assessed whether castration affected (1) the behavior of males, (2) the mating decisions of females, or (3) the outcome of male-male competition. Castration did not alter the plumage of male Gambel's or Scaled Quail. In these species, and some other members of the avian order Galliformes, production of ornate plumage appears to be independent of testosterone. In contrast, castration reduced or eliminated courtship behaviors. Females almost never preferred castrated individuals. During male-male competition, castrates also exhibited lower rates of threat behaviors, which appear to be identical to those used during courtship. Castration did not, however, influence the outcome of male-male competition. Castrates of both species exhibited overt aggression (pecks, chases, displacement) and frequently won male contests. Such results suggest that certain types of aggressive behavior may be testosterone-independent. In both Gambel's and Scaled Quail, male body size correlated positively with dominant individuals.     

Regulation of Male Sexual Behavior by Progesterone Receptor, Sexual Experience, and Androgen

Recent studies have demonstrated that physiological doses of progesterone may facilitate the androgen-dependent display of male sexual behavior in laboratory rats and three species of lizard. We used mice with a targeted disruption of the progesterone receptor to investigate whether such interactions exist in male mice and whether they may be modified by sexual experience. We found that naive intact male progesterone receptor knockout (PRKO) mice exhibit reduced mount frequencies compared to wild-type (WT) mice. Also unlike WT mice, sexually experienced PRKO males show profound losses in many measures of sexual behavior following castration. In a second experiment, we tested whether male mice heterozygous for a null mutation at the progesterone receptor locus were responsive to testosterone and progesterone treatment. We found that heterozygous males showed a reduced response to testosterone. The data are consistent with experiments indicating that the progesterone receptor is able to facilitate male-typical sex behaviors in other species and suggest novel mechanisms underlying the interaction of androgens and experience.     

Factors influencing aggression toward females by male rats exposed to anabolic androgenic steroids during puberty

Previous results showed that male rats pubertally exposed to anabolic androgenic steroids (AAS) displayed aggression towards females in response to physical provocation. This experiment examined two factors that may modulate AAS-induced behavior towards females: olfactory cues and frustration. Gonadally intact males began one of three AAS treatments at puberty (D40): testosterone propionate (T), stanozolol (S), T+S, or vehicle control. To test for the relevance of olfactory cues in the elicitation of behavior toward females, a hidden neighbor paradigm was used. The proximal stimulus was an ovariectomized (OVX) female, estrogen plus progesterone (E+P) female, or an E+P female with tape-obstructed vagina (OBS). Distal olfactory cues from a hidden neighbor were delivered from a separate cage connected to the testing arena. The vaginally obstructed, sexually receptive female (OBS) was used to determine the effects of frustration on behavior by AAS males. Both sexual and aggressive behaviors were measured. The presence of distal olfactory cues had no effect on either sexual or aggressive behavior. In the presence of E+P and OBS females, all males displayed sex behaviors, not aggression. However, AAS males displayed significantly more aggression towards proximal OVX females than controls. AAS males mounted OBS females significantly more than controls, indicating a persistence of once rewarded behavior. These results suggest (1) proximal cues of the conspecific female are more salient than distal olfactory cues in determining behavior and (2) AAS males display frustration-induced persistence in response to vaginally obstructed receptive females.     

Neurobiological correlates premeditated (learned) aggression: seeking new experimental approaches]

Theoretical possibility of experimental modeling of learned (premediated) aggression developing in human after experience of aggression is considered. The sensory contact technique increases aggressiveness in male mice and allows aggressive type of behavior to be formed as a result of repeated experience of victories in daily agonistic confrontations. Some behavioral domains confirm the development of learned aggression in males similar to those in humans. The features are: repeated experience of aggression reinforced by victories; elements of learned behavior after period of confrontations; intent, measured by increase of the aggressive motivation prior agonistic confrontation; decreased emotionality estimated by parameters of open field behavior. Relevant stimuli provoke demonstration of aggression. This review summarized data on the influence of positive fighting experience in daily intermale confrontations on the behavior, neurochemistry and physiology of aggressive mice (winners). This sort of experience changes many characteristics in individual and social behaviors, these having been estimated in different tests and in varied situations. Some physiological parameters are also changed in the winners. Neurochemical data confirm the activation of brain dopaminergic systems and functional inhibition of serotonergic system in winners under influence of repeated experience of aggression. The expression of the neurochemical and behavioral changes observed in winners has been found dependent on the mouse strain and on the duration of their agonistic confrontations. Similarities in mechanisms of learned aggression in humans and mice are considered.     

Olfactory preferences, scent marking, and "proceptivity" in female hamsters

Two appetitive sexual behaviors of female hamsters, attraction to odors of males and vaginal scent marking, were investigated and the correlations of each to reproductive states were determined. Both estrous and diestrous females were more attracted to the odors of intact males than to the odors of females or castrated males; this differential attraction was more pronounced for estrous females. Lactating females, but not pregnant females, were also preferentially attracted to odors of intact males. Thus, odors alone provided sufficient information to allow sexual discrimination by females, and estrous, diestrous, and lactating females were preferentially attracted to odors of intact males whereas pregnant females were not. Reproductive condition had no influence on responses to odors of castrated males or diestrous females. Vaginal scent marking was strongly influenced by reproductive state: Marking frequency was low in estrous, pregnant, and early lactation females, but high in late lactation and diestrous females, suggesting a function of advertisement of approaching receptivity. Thus sexual preferences based on olfactory cues and vaginal scent-marking frequency differed in their relationships to reproductive conditions. It is suggested that in other species such relationships between appetitive sexual behaviors and reproductive condition will depend on the species social organization, ecological niche, and taxonomic group, and consequently that the concept of preceptive behaviors should be broadened to include all appetitive sexual behaviors of females, not just those that are correlated with the hormonal state characterizing estrus.     

Comparing the relative amount of testosterone required to restore sexual arousal, motivation, and performance in male rats

It is well established that male rat reproductive behaviors including sexual arousal, motivation, and performance are dependent on circulating levels of testosterone (T). The present study was designed to (1) compare the relative amount of T required to restore these different aspects of behavior in castrated rats, and (2) create an animal model for clinical populations with sexual impairments. Twenty-nine male Long–Evans rats were tested before and after castration for sexual performance (copulation), motivation (partner preference), and arousal (50 kHz ultrasonic vocalizations; measured together with scent marking). Sexual arousal was also inferred from copulation data. Rats were then assigned to one of four groups, and T was re-introduced via Silastic capsule implants varying in length and content: No T (empty capsules), Low T (2 mm capsules), Medium T (5 mm capsules), or High T (two 10 mm capsules). The highest dose was intended to restore physiological levels. Results indicate that High T is required for 50 kHz vocalizations, while Medium T was sufficient for the restoration of copulation, partner preference, and scent marking. These data suggest that sexual arousal may be most sensitive to reductions in testosterone. The role of T levels in measures of generalized and specific (sexual) arousal is discussed in the context of other reproductive behaviors. Furthermore, because the Low T group showed impairments across all behaviors during post-implant tests, we propose that these animals may provide a good animal model for studying clinical conditions marked by reduced motivation and arousal, including Hypoactive Sexual Desire Disorder.     

Paternal aggression in a biparental mouse: parallels with maternal aggression

Environmental and social factors have important effects on aggressive behaviors. We examined the effect of reproductive experience on aggression in a biparental species of mouse, Peromyscus californicus. Estrogens are important in mediating aggressive behavior so we also examined estrogen receptor expression and c-fos for insights into possible mechanisms of regulation. Parental males were significantly more aggressive than virgin males, but no significant differences in estrogen receptor alpha or beta expression were detected. Patterns of c-fos following aggression tests suggested possible parallels with maternal aggression. Parental males had more c-fos positive cells in the medial amygdala, and medial preoptic area relative to virgin males. The medial preoptic area is generally considered to be relatively less important for male-male aggression in rodents, but is known to have increased activity in the context of maternal aggression. We also demonstrated through habituation-dishabituation tests that parental males show exaggerated investigation responses to chemical cues from a male intruder, suggesting that heightened sensory responses may contribute to increased parental aggression. These data suggest that, in biparental species, reproductive experience leads to the onset of paternal aggression that may be analogous to maternal aggression.     

Scent marking by voles in response to predation risk: a field-laboratory validation

Predators use scent to locate their prey, and prey animals oftenalter their behavior in response to predation risk. I testedthe hypothesis that voles would decrease their frequency ofscent marking in response to predation risk. I conducted trialsin which prairie voles, Microtus ochrogaster, and woodland voles,M. pinetorum, were allowed to scent mark ceramic tiles placedin their runways in the field. The tiles were subjected to oneof three treatments: scented with odor from mink, Mustela vison(a rodent predator); rabbit, Oryctolagus cuniculus (a nonpredatormammal control); and no odor (control). No significant differenceswere found in the frequency of scent marking in response tothe three treatments for either species. To validate that volesdid not decrease their scent marking in response to predationrisk, I brought male prairie voles from the field site intothe laboratory and allowed them to scent mark white paper substratetreated with mink odor, rabbit odor, or no odor. No significantdifferences were found in the frequency of scent marks in responseto the three treatments. These results differ from what waspredicted based on laboratory studies with other species ofrodents that show avoidance, reproductive suppression, decreasedactivity, and reduced scent marking in response to odors ofpredators. Voles appear to scent mark different substrates andunder a wide variety of social and environmental situations,and this is not influenced by the presence of odor from a predator.     

Long-term effects of pubertal anabolic-androgenic steroid exposure on reproductive and aggressive behaviors in male rats

The current study examined acute and long-term effects of anabolic-androgenic steroid (AAS) exposure during puberty on copulation, vocalizations, scent marking, and intermale aggression, both with and without tail pinch, in intact male rats. Animals received 5 mg/kg of testosterone, nandrolone, stanozolol, or vehicle, beginning at puberty. After 5 weeks, behavior tests were performed while continuing AAS injections. AAS treatment was then discontinued. Behaviors were tested during 3-5 weeks, 9-11 weeks, and 15-17 weeks of withdrawal. During AAS administration, stanozolol males showed significant reductions in all behaviors compared with controls, except aggression with tail pinch. Nandrolone treatment significantly reduced vocalizations and scent marking, and testosterone had no significant effect on behavior. During withdrawal, behaviors in stanozolol males recovered to control levels at variable rates: aggression at 4 weeks; mounts, vocalizations, and scent marking at 9 weeks; and ejaculations at 15 weeks of withdrawal. Stanozolol males showed significantly higher levels of tail pinch-induced aggression during every withdrawal test. Nandrolone-treated males scent-marked at control levels by 9 weeks withdrawal but displayed significantly fewer vocalizations and significantly more tail pinch-induced aggression than controls for the entire study. Testosterone-treated males scent-marked significantly below controls at 3 weeks withdrawal and showed significantly more tail pinch-induced aggression at 5 weeks withdrawal. All three AAS significantly increased tail pinch-induced aggression compared with corresponding nontail pinch tests, even at study endpoint. These results suggest that alterations in androgen-dependent behaviors by pubertal AAS exposure can persist long after drug exposure, and some effects may even be permanent.     

Brain aromatase, 5 alpha-reductase,and 5 beta-reductase change seasonally in wild male song sparrows: relationship to aggressive and sexual behavior

In many species, territoriality is expressed only during the breeding season, when plasma testosterone (T) is elevated. In contrast, in song sparrows (Melospiza melodia morphna), males are highly territorial during the breeding (spring) and nonbreeding (autumn) seasons, but not during molt (late summer). In autumn, plasma sex steroids are basal, and castration has no effect on aggression. However, inhibition of aromatase reduces nonbreeding aggression, suggesting that neural steroid metabolism may regulate aggressive behavior. In wild male song sparrows, we examined the neural distribution of aromatase mRNA and seasonal changes in the activities of aromatase, 5 alpha-, and 5 beta-reductase, enzymes that convert T to 17 beta-estradiol, 5 alpha-dihydrotestosterone (5 alpha-DHT, a potent androgen), or 5 beta-DHT (an inactive metabolite), respectively. Enzyme activities were measured in the diencephalon, ventromedial telencephalon (vmTEL, which includes avian amygdala), caudomedial neostriatum (NCM), and the hippocampus of birds captured during spring, molt, or autumn. Aromatase and 5 beta-reductase changed seasonally in a region-specific manner. Aromatase in the diencephalon was higher in spring than in molt and autumn, similar to seasonal changes in male sexual behavior. Aromatase activity in the vmTEL was high in both spring and autumn but significantly reduced at molt, similar to seasonal changes in aggression. 5 beta-Reductase was not elevated during molt, suggesting that low aggression during molt is not a result of increased inactivation of androgens. These data highlight the relevance of neural steroid metabolism to the expression of natural behaviors by free-living animals.     

Increased aggression and activity level in 3- to 11-year-old girls with congenital adrenal hyperplasia (CAH)

Experimental research in a wide range of mammals has documented powerful influences of androgen during early development on brain systems and behaviors that show sex differences. Clinical research in humans suggests similar influences of early androgen concentrations on some behaviors, including childhood play behavior and adult sexual orientation. However, findings have been inconsistent for some other behaviors that show sex differences, including aggression and activity level in children. This inconsistency may reflect small sample sizes and assessment limitations. In the present study, we assessed aggression and activity level in 3- to 11-year-old children with CAH (38 girls, 29 boys) and in their unaffected siblings (25 girls, 21 boys) using a questionnaire that mothers completed to indicate current aggressive behavior and activity level in their children. Data supported the hypotheses that: (1) unaffected boys are more aggressive and active than unaffected girls; (2) girls with CAH are more aggressive and active than their unaffected sisters; and (3) boys with and without CAH are similar to one another in aggression and activity level. These data suggest that early androgens have a masculinizing effect on both aggressive behavior and activity level in girls.     

Female prairie voles do not choose males based on their frequency of scent marking

We conducted an experiment to test three alternative hypotheses for the function of frequency of scent marking in male prairie voles, MICROTUS OCHROGASTER: (1) sexual attraction (to advertise male quality for mating); (2) reproductive competition; and (3) self-advertisement or individual identity. In laboratory experiments, males deposited scent on all areas of a bare substrate, and more in an area next to a stimulus animal than other areas, regardless of the stimulus animal's sex. Females did not choose mates based on their frequency of scent marking and scent marking did not antagonize or stimulate aggression between males. The frequency of scent marking by males supports the individual identity hypothesis, and is less consistent with the sexual attraction or reproductive competition hypotheses. Mate choice is likely based on a complex suite of characters, but at least in prairie voles, the frequency of scent marking by males does not appear to be one of them.     

Are Androgens Related to Aggression in House Wrens?

Elevated circulating testosterone levels are hypothesized to allow male animals to direct resources into territorial and mating behaviors at the expense of reducing paternal care of offspring. For this hypothesis to apply, testosterone must facilitate territorial/mating behaviors and have antagonistic effects on paternal care, but this pattern has only been supported in some, not all, species. I tested whether androgens correlate with aggressive behaviors in male house wrens ( Troglodytes aedon), a double‐brooded species where paternal and aggressive behaviors overlap temporally. House wrens may therefore benefit from having a hormonal mechanism that allows males to rapidly change behavioral states. However, I found no evidence that androgens (testosterone and 5α‐dihydrotestosterone) relate to aggression in house wrens: Androgens did not increase in response to playback, and endogenous‐circulating androgens were not correlated with how aggressively males responded to those playbacks. Moreover, androgen levels were low during the pre‐breeding stage of the second brood, when many males establish new territories and attract new mates. This study adds to a growing body of the literature suggesting that the relationship between circulating androgens and aggressive behavior is more complex than originally thought.     

Anabolic androgenic steroids differentially affect social behaviors in adolescent and adult male Syrian hamsters

Anabolic androgenic steroids (AAS) are synthetic derivatives of testosterone used by over half a million adolescents in the United States for their tissue-building potency and performance-enhancing effects. AAS also affect behavior, including reports of heightened aggression and changes in sexual libido. The expression of sexual and aggressive behaviors is a function of complex interactions among hormones, social context, and the brain, which is extensively remodeled during adolescence. Thus, AAS may have different consequences on behavior during adolescence and adulthood. Using a rodent model, these studies directly compared the effects of AAS on the expression of male sexual and aggressive behaviors in adolescents and adults. Male Syrian hamsters were injected daily for 14 days with either vehicle or an AAS cocktail containing testosterone cypionate (2 mg/kg), nandrolone decanoate (2 mg/kg), and boldenone undecylenate (1 mg/kg), either during adolescence (27-41 days of age) or in adulthood (63-77 days of age). The day after the last injection, males were tested for either sexual behavior with a receptive female or agonistic behavior with a male intruder. Adolescent males treated with AAS showed significant increases in sexual and aggressive behaviors relative to vehicle-treated adolescents. In contrast, AAS-treated adults showed significantly lower levels of sexual behavior compared with vehicle-treated adults and did not show heightened aggression. Thus, adolescents, but not adults, displayed significantly higher behavioral responses to AAS, suggesting that the still-developing adolescent brain is more vulnerable than the adult brain to the adverse consequences of AAS on the nervous system and behavior.