Adult Male Macaques Research Articles

Gonadotropin‐Releasing Hormone Antagonist (Cetrorelix) Therapy Fails to Protect Nonhuman Primates (Macaca arctoides) From Radiation‐Induced Spermatogenic Failure

Treatment of men of reproductive age with radiation or alkylating agents often produces prolonged azoospermia. We previously demonstrated that suppression of testosterone (T) with gonadotropin-releasing hormone (GnRH) analogs restored spermatogenesis following atrophy induced by radiation or chemotherapy in rats. This study tested whether GnRH antagonist therapy could reverse radiation-induced testicular injury in primates with a similar protocol. Adult male stump-tailed macaques were given either 6.7 Gy radiation to the testis alone, 6.7 Gy radiation combined with GnRH-antagonist treatment starting on the day of exposure, or daily injections of the GnRH antagonist Cetrorelix for 3 months alone and were monitored for 18 months. Cetrorelix alone produced a 20-40-week fully reversible suppression of serum T, but although spermatogenic recovery was incomplete, 40%-90% of tubules contained differentiating germ cells. Following radiation alone, testis volumes were reduced to approximately 28% and sperm counts to less than 1% of pretreatment values. A biopsy at 18 months after radiation showed that only 3.0% of seminiferous tubule cross sections had germ cells. In irradiated animals that received GnRH antagonist, testis volumes were reduced to 18% of pretreatment volume, and at 18 months, only 1.9% of seminiferous tubule cross sections contained germ cells. Inhibin B values were reduced to 10% and 3% of pretreatment levels in the radiation-only and the radiation plus GnRH antagonist groups, respectively. Species differences exist in the testicular response to radiation, GnRH antagonist therapy, or both, so that rescue protocols that were successful in rodents might not work in primates.

Increased aggressive behavior and decreased affiliative behavior in adult male monkeys after long-term consumption of diets rich in soy protein and isoflavones

Estrogen produced by aromatization of gonadal androgen has an important facilitative role in male-typical aggressive behavior that is mediated through its interaction with estrogen receptors (ER) in the brain. Isoflavones found in soybeans and soy-based dietary supplements bind ER and have dose- and tissue-dependent effects on estrogen-mediated responses. Yet, effects of isoflavone-rich diets on social and aggressive behavior have not been studied. We studied the effects of long-term (15 months) consumption of diets rich in soy isoflavones on spontaneous social behavior among adult male cynomolgus macaques ( Macaca fascicularis) ( n = 44) living in nine stable social groups. There were three experimental conditions which differed only by the source of dietary protein: casein and lactalbumin (no isoflavones), soy protein isolate containing 0.94 mg isoflavones/g protein, and soy protein isolate containing 1.88 mg isoflavones/g protein. In the monkeys fed the higher amount of isoflavones, frequencies of intense aggressive (67% higher) and submissive (203% higher) behavior were elevated relative to monkeys fed the control diet ( P's < 0.05). In addition, the proportion of time spent by these monkeys in physical contact with other monkeys was reduced by 68%, time spent in proximity to other monkeys was reduced 50%, and time spent alone was increased 30% ( P's < 0.02). There were no effects of treatment on serum testosterone or estradiol concentrations or the response of plasma testosterone to exogenous gonadotropin-releasing hormone (GnRH). The results indicate that long-term consumption of a diet rich in soy isoflavones can have marked influences on patterns of aggressive and social behavior.

The effects of substratum inclination on locomotor patterns in primates

To explore the change from the horizontal quadrupedal walking to the vertical climbing in primates, I designed an experiment on an inclined substratum. The subjects were an adult male Japanese macaque and a 2-year-old female white-handed gibbon. The animals moved on a substratum made of bamboo pipe (8 cm diameter). The inclination of the substratum was changed from 15 degrees to 65 degrees in 5-degree increments for the Japanese macaque and from 20 degrees to 70 degrees with 10-degree increments for the white-handed gibbon. I placed surface electrodes and telemetry transmitters on the subjects to record the activity of the long head of the triceps brachii and the long head of the biceps brachii muscles. The Japanese macaque utilized horizontal quadrupedal walking until the incline was 15 degrees. Vertical climbing began at an inclination of 55 degrees. The intermediate locomotor mode was observed between 20 degrees and 50 degrees. The white-handed gibbon changed the locomotor mode from horizontal quadrupedal walking to vertical climbing at 40 degrees. I believe that the difference observed in locomotor mode between these two species was mainly due to differences in the intermembral index. The white-handed gibbon had a large intermembral index, which meant she had longer forelimbs and could therefore change locomotor mode at a lower inclination of the substratum.

Central Nervous System Monoamine Correlates of Social Dominance in Cynomolgus Monkeys (Macaca fascicularis)

Social dominance is a fundamental component of both human and nonhuman primate sociality. However, its neurobiological correlates remain incompletely understood. We evaluated the association between dominance status and monoamine metabolite concentrations in cisternal cerebrospinal fluid (CSF) in adult male (n = 25) and female (n = 21) cynomolgus macaques (Macaca fascicularis) housed in unisexual social groups. Concentrations of the metabolites of dopamine (homovanillic acid [HVA]), norepinephrine (3-methoxy-4-hydroxyphenylglycol [MHPG]) and serotonin (5-hydroxyindoleacetic acid [5-HIAA]) were assayed. Dominant monkeys, both males and females, had significantly higher CSF HVA concentrations than did subordinates (p values < .05). Among males, but not females, dominants also had lower CSF 5-HIAA than subordinates (p < .05). The Dominance-HVA association observed here is consistent with recent speculation that social extraversion, a dominance-related personality trait in humans, may also reflect heightened central nervous system dopaminergic activity.

Craniometry of Adult Male Japanese Macaques from the Yakushima, Koshima and Kinkazan Islands

Craniometry of Adult Male Japanese Macaques from the Yakushima, Koshima and Kinkazan Islands

Anatomic relationships between aromatase and androgen receptor mRNA expression in the hypothalamus and amygdala of adult male cynomolgus monkeys.

This study mapped the regional locations of cells expressing cytochrome P450 aromatase (P450AROM) and androgen receptor (AR) mRNAs in the adult male macaque hypothalamus and amygdala by in situ hybridization histochemistry using monkey-specific cRNA probes. High densities of P450AROM and AR mRNA-containing neurons were observed in discrete hypothalamic areas involved in the regulation of gonadotropin secretion and reproductive behavior. P450AROM mRNA-containing neurons were most abundant in the medial preoptic nucleus, bed nucleus of the stria terminalis, and anterior hypothalamic area, whereas AR mRNA-containing neurons were most numerous in the ventromedial nucleus, arcuate nucleus, and tuberomamillary nucleus. Moderate to heavily labeled P450AROM mRNA-containing cells were present in the cortical and medial amygdaloid nuclei, which are known to have strong reciprocal inputs with the hypothalamus. Heavily labeled P450AROM mRNA-containing cells were found in the accessory basal amygdala nucleus, which projects to the cingulate cortex and hippocampus, areas that are important in the expression of emotional behaviors and memory processing. In contrast to P450AROM, the highest density of AR mRNA labeling in the temporal lobe was associated with the cortical amygdaloid nucleus and the pyramidal cells of the hippocampus. All areas that contained P450AROM mRNA-expressing cells also contained AR mRNA-expressing cells, but there were areas in which AR mRNA was expressed but not P450AROM mRNA. The apparent relative differences in the expression of P450AROM and AR mRNA-containing neurons within the monkey brain suggests that T acts through different signaling pathways in specific brain areas or within different cells from the same region.

Antagonism of central vasopressin receptors blocks hypoglycemic stress induced inhibition of luteinizing hormone release in male rhesus macaques.

The first objective of this study was to investigate whether the inhibitory effect of insulin-induced hypoglycemia (IIH) on luteinizing hormone (LH) secretion was the same in unrestrained adult male rhesus macaques as has been previously reported in restrained female macaques. Since IIH did inhibit pulsatile LH secretion in adult male macaques, and some previous studies have implicated arginine vasopressin (AVP) as a central mediator of this inhibition, the second objective was to investigate whether antagonism of AVP action could reverse the IIH-induced inhibition of LH release in males. Ten adult male rhesus macaques (Macaca mulatta) were studied during 15-h periods (07.00-22.00 h), with blood samples collected every 15-min. There were three experimental groups; controls (n = 5), IIH (n = 6) and IIH plus vasopressin antagonist (AVPa; n = 6). During the hypoglycemia studies, the first 5 h served as a control for that occasion and an insulin bolus of 1 U/kg was administered intravenously at 12.00 h. During the IIH plus AVPa, the vasopressin antagonist was infused intravenously from 12.00 h to 17.00 h. LH and testosterone decreased progressively after the insulin bolus in the IIH group reaching a minimum value at 4 h after the infusion. However, compared to the preinfusion levels, secretion of LH and testosterone was not suppressed by hypoglycemia in the group treated with the AVP antagonist. The present study shows that in male macaques not subjected to the psychological stress of restraint, IIH suppresses LH and testosterone secretion. This inhibition of LH release can be blocked in some animals by antagonism of central vasopressin receptors, suggesting that vasopressin is involved in the suppression of gonadotropin releasing hormone/LH release induced by hypoglycemia.

Speed selectivity for optic flow in area 7a of the behaving macaque.

Area 7a, in the inferior parietal lobe, has been implicated in optic flow processing to obtain spatial information about the environment. Optic flow, angle-of-gaze and center-of-motion dependencies are already documented, but the selectivity of area 7a to speed is unknown. Such information is crucial as area 7a provides the final step in visual motion analysis that begins at the lateral geniculate nucleus and passes through MT, MST and LIP/VIP. Macaque area 7a neurons were tested with optic flows with speeds of 0.5-128 degrees /s. Of 161 neurons tested in four hemispheres of two adult male macaques, 53% (86/161) were speed selective at either the time of stimulus onset, at the end of the trial, or at both times. Speed selec- tivities resembling the basic filter types (band-pass, band-reject, high-pass, low-pass, broadband) were found. Area 7a neurons exhibited two novel properties not previously reported elsewhere. Speed selectivity was found to be dynamic in that many cells gained, lost or changed speed tuning over the course of a trial. In addition, speed dependence and optic flow selectivity interacted. For example, a cell could preferentially respond to one type of naviga- tional optic flow at a slow speed and a different navigational optic flow at a fast speed. The presence of speed selectivity combined with other properties of area 7a neurons indicates that these neurons may have a role in the concurrent representation of heading as well as multiple object speeds and directions.

Neuroendocrine Consequences of Fasting in Adult Male Macaques: Effects of Recombinant Rhesus Macaque Leptin Infusion

Fasting inhibits the gonadotropic axis and stimulates the corticotropic and somatotropic axes. Since leptin is a product of fat cells that has been implicated in the control of both reproduction and metabolism, we hypothesized that the decrease in leptin observed during fasting was responsible for these effects on reproductive and metabolic hormones. Recombinant rhesus leptin (rrhLep) produced in our laboratory was infused (100 µg/h) into fasted adult male rhesus macaques (6–9 kg) beginning at midnight after the first missed meal and continuing until the end of the study. Bioactive luteinizing hormone (LH), testosterone, cortisol and growth hormone (GH) were measured in plasma from samples collected at 15-min intervals for the last 15 h (42–57 h) of the fast. We analyzed pulsatile LH and GH secretion by deconvolution analysis and the orderliness of pulsatile LH and GH release by the approximate entropy (ApEn) statistic. There was no difference in LH pulse frequency between control and fasted groups, but there was a significant decrease in the mean concentration of LH released (7.6 ± 1.4 ng/ml control vs. 2.7 ± 0.65 ng/ml fasted) that was not relieved with rrhLep infusions (2.8 ± 0.83 ng/ml). Model-free Cluster analysis confirmed these inferences and also indicated that the peak height was lower in the fasted (4.6 ± 1.0 ng/ml) and the fasted + rrhLep (2.85 ± 1.0 ng/ml) groups compared to controls (16.3 ± 1.4 ng/ml). Testosterone levels reflected those of LH. Fasting resulted in an increase in GH secretory pulse frequency (5.3 ± 0.95 pulses/15 h control vs. 12.8 ± 1.4 pulses/15 h fasted) and this increase was not affected by rrhLep infusion (12.5 ± 1.4 pulses/15 h). In addition, fasting also increased the ApEn (decreased the orderliness) of pulsatile GH secretion, and this characteristic was not relieved with rrhLep infusions. Cortisol levels in fasted animals were 2- to 3-fold higher than those observed in control studies, and this increase was particularly pronounced at the time when the animals expected their first meal of the day. The increase in circulating cortisol observed in fasted animals was not affected by rrhLep infusion. Glucose levels at the end of the sampling period were 80 mg/dl in controls, 48 mg/dl in fasted animals and 58 mg/dl in the fasted + rrhLep group. Circulating leptin levels averaged 1.2 ± 0.37 ng/ml in control animals, 0.7 ± 0.2 ng/ml in fasted animals and 10.1 ± 5.6 ng/ml in fasted animals infused with rrhLep. These studies suggest that intravenous replacement with homologous leptin does not reverse the acute changes in GH, LH and cortisol secretion observed with fasting in the adult male macaque.

Self-Injurious Behavior Is Decreased by Cyproterone Acetate in Adult Male Rhesus (Macaca mulatta)

Self-injurious behavior (SIB) presents a serious problem in laboratory macaques that cannot be socially housed for scientific reasons and among institutionalized children and adults where it is often associated with different forms of brain dysfunction. We have experienced limited success in reducing SIB in macaques by enhancing their environment with enrichment devices. Psychotropic drugs also help, but problems are associated with their use. Because sexual and aggressive behavioral problems in men have been treated with progestational drugs, we tested the efficacy of cyproterone acetate (CA, 5–10 mg/kg/week) on reducing SIB in 8 singly housed, adult male rhesus macaques. The main findings were: (1) SIB and other atypical behaviors were significantly reduced during CA treatment; (2) serum testosterone was significantly reduced during CA treatment; (3) cerebral spinal fluid (CSF) levels of 5HIAA and HVA, metabolites of serotonin and dopamine, respectively, declined significantly during CA treatment; (4) the duration of SIB positively correlated with levels of 5HIAA in CSF; but (5) sperm counts were not reduced during treatment. Thus, CA was a partially effective treatment (3 months) for adult male macaques whose behavioral problems include SIB. In summary, CA reduced SIB, overall aggression, serum testosterone, CSF 5HIAA, and CSF HVA. We hypothesized that the progestin activity of CA represses the hypothalamic gonadal axis and decreases testosterone, which in turn decreases SIB. In addition, we speculate that the decrease in 5HIAA and HVA in CSF may have been caused by progestins decreasing the activity of MAO. Therefore, the reduction of SIB may also be related to an increase in the availability of active monoamines in the CNS.

Social Relationships and Intergroup Transfer of Young Adult Male Japanese Macaques Pre- and Post-Fission of the Katsuyama A Group

The social relationships of 10 young adult males in a free-ranging group of Japanese macaques at Katsuyama, Okayama Prefecture, were examined pre- and post-fission. Before group fission, higher-ranking young adult males interacted less frequently with not only their mothers, but also with other matrilineally-related females than did lower-ranking males. Six-year-old males clearly formed two subgroups according to their relative rank, even though they did not form any clear subgroups at the age of two.Higher-ranking males spent more time away from females of the group than did lower-ranking males. However, when it was time for artificial feeding, higher-ranking males obtained scattered food more frequently than lower-ranking males. After group fission, four of the five higher-ranking males and one of the five lower-ranking males remained in the main group, while three of the five lower-ranking males were in the fission group.These differences in the social relationships of young adult males might reflect the female subgroups which appeared prior to group fission.

The change of the locomotor pattern caused by the inclination of the substrata in a Japanese macaque

In order to clarify the condition of the change from the horizontal quadrupedal walking to the vertical climbing in a Japanese macaque, we made an experiment on the inclined substrata. The subject was an adult male Japanese macaque. It freely moved on the substrata, a bamboo pole (8cm diameter). The inclination of the substrata was changed from 15 degrees to 65 degrees with each 5 degrees and the number of the steps was eleven. We put the surface extrodes and telemetry transmitters on the subject to record the activity of the triceps brachii and the biceps brachii. The patterns of the electromyography were clearly different between the horizontal quadrupedal walking and the vertical climbing.The palm of the Japanese macaque touched the substrata on the behind side in the vertical climbing. It was found that this type of forelimb use was observed in the inclination of 50 degrees or more. The cycle duration also decreased at the inclination of 50 degrees or more. The relative duration of stance phase of the forelimb decreased at the inclination of 65 degrees and that of the hindlimb increased at the inclination of 55 degrees or more. The electromyography study showed three stages. The first stage was similar to the horizontal quadrupedal walking and it was seen at the inclination of 15 degrees or less. The second stage was the intermediate type and it was observed between the inclination of 20 degrees and 50 degrees. The last stage was similar to the pattern of vertical climbing at the inclination of 55 degrees or more. These results of electromyography were related to the difference in the locomotor function of the forelimb at different degrees of inclination.

Long-term effects of chronic social stress on serotonergic indices in the prefrontal cortex of adult male cynomolgus macaques

We examined the effects of chronic social stress and social rank on monoamine concentrations in the prefrontal cortex (PFC) in adult male cynomolgus macaques ( Macaca fascicularis). Seventy-five animals were housed in five-member social groups for 28 months and were exposed to three experimental conditions. A ‘no-stress’ condition was comprised of animals housed in groups of stable membership throughout the study. Animals assigned to a ‘past-stress’ condition had their group memberships reorganized at monthly intervals during the first (but not last) 14 months of the study, and a third ‘recent-stress’ condition consisted of social groups reorganized only during the last 14 months. At necropsy, the brains were collected and frozen at −70°C until analyzed. Prefrontal orbital cortex was assayed for monoamines (serotonin (5-HT), dopamine (DA), norepinephrine (NE)), metabolites (5-hydroxyindoleacetic acid (5-HIAA), homovanillic acid (HVA), 3-methoxy-4-hydroxyphenethyleneglycol (MHPG)), and tryptophan using high-performance liquid chromatography with electrochemical detection. Animals in the past-stress condition had significantly lower PFC 5-HIAA concentrations compared to those in the no-stress condition ( P < 0.05). PFC 5-HT concentrations of animals in the past-stress condition were significantly lower than those in the no-stress and recent-stress conditions ( P < 0.01). The concentrations of DA, HVA, NE and MHPG were not altered. These data suggest that exposure to chronic social stress is associated with long-term selective reductions in serotonergic activity in the PFC. This effect may underlie the association in human beings between reduced serotonergic function and conditions such as pathological grief and posttraumatic stress disorder.

Acquisition and long-term patterning of joystick selection of food-pellet vs social-video reward by Bonnet Macaques

Five individually housed, adult male bonnet macaques ( Macaca radiata ) that were highly experienced in single-target joystick tasks were trained to discriminate targets associated with food-pellet and live-social-video rewards; the social video afforded viewing of a social group of bonnet macaques. Most subjects more rapidly acquired the discrimination for their preferred reward. Following discrimination training, the remaining three subjects were given 34 weeks with a simultaneous choice between food-pellet and social-video; the subjects selected a reward by simply using a joystick to direct a cursor to contact the target associated with that reward. Despite some change over time, both types of reward remained effective for the extended period. Different daily patterns of responding for the two rewards were identified.

The effects of finasteride (Proscar) on hair growth, hair cycle stage, and serum testosterone and dihydrotestosterone in adult male and female stumptail macaques (Macaca arctoides)

The effects of finasteride (Proscar) on hair growth, hair cycle stage, and serum testosterone and dihydrotestosterone in adult male and female stumptail macaques (Macaca arctoides)

The effects of finasteride (Proscar) on hair growth, hair cycle stage, and serum testosterone and dihydrotestosterone in adult male and female stumptail macaques (Macaca arctoides).

Finasteride, a 5 alpha-reductase inhibitor, was administered orally (1 mg/kg.day) for 6 months to six male and five female stumptail macaques. Vehicle was given to five male and five female animals over the same period of time. Hair weights in a defined 1-in.2 area of frontal scalp were measured periodically every 1-2 months, and serum was collected for measurement of testosterone and dihydrotestosterone. In addition, scalp biopsies were taken before and 6 months after treatment to evaluate the micromorphometry of hair follicles. Results showed that both male and female serum dihydrotestosterone levels were significantly reduced (60-70%) by finasteride treatment. Both males and females showed statistically significant increases in mean hair weight over the treatment period compared to controls (P = 0.034). In addition, there was a statistically significant increase in mean follicle length (measured histologically in scalp biopsies) compared to baseline in the finasteride-treated animals (P = 0.028). These data show that an inhibition of 5 alpha-reductase in the stumptail macaque can reverse the balding seen with age in both the male and female animals.

A primate model for chancroid.

Adult pigtailed macaques (Macaca nemestrina) were evaluated for their usefulness as a primate model for chancroid. To initiate infection, 10(7)-10(8) cfu of Haemophilus ducreyi were inoculated into the foreskins of 5 adult males and into the vaginal labia of 4 adult females. Lesions developed in the male macaques that were similar in appearance, histopathologic changes, and progression to those of human disease, including the development of ulcers 6-12 days after infection. In addition, H. ducreyi could be recovered from the lesions up to 20 days after inoculation, humoral antibodies were induced beginning 1 week after inoculation, and inguinal lymphadenopathy was noted in 4 of the 5 males. None of the 4 female macaques inoculated with the same preparation of live H. ducreyi developed comparable lesions. Thus, experimental chancroid in adult male macaques closely resembles human disease and should be useful for future studies of the pathogenesis of chancroid.

Immunocytochemical Localization of Androgen Receptors in the Scalp of the Stumptail Macaque Monkey, a Model of Androgenetic Alopecia

The purpose of this study was to identify the distribution of androgen receptors in the bald and hairy scalp of adult male and female stumptail macaque monkeys by light microscopic biotin-avidin immunocytochemistry with a highly purified rat monoclonal antibody against the cloned human androgen receptor. Consistent, intense nuclear and minimal cytoplasmic immunostaining was observed in several distinct cell populations of the pilosebaceous unit including the dermal papilla, hair epithelium, outer root sheath, dermal sheath, and sebaceous gland. A similar distribution of androgen receptors was found in miniaturized and terminal anagen and telogen follicles of the bald and hairy scalp, respectively. Binding of androgen receptor antibody was also detected in dermal fibroblasts, basal and intermediate layers of the interfollicular epidermis, and duct and glandular cells of eccrine sweat glands. This investigation demonstrates the presence of androgen receptors in the pilosebaceous unit of the scalp of the stumptail macaque and also shows that their distribution is comparable to that previously reported for humans.

Neuroendocrine responses to fenfluramine challenge are influenced by exposure to chronic social stress in adult male cynomolgus macaques

This study was designed to investigate the effect of chronic social stress on central serotonergic responsivity in adult male cynomolgus monkeys ( Macaca fascicularis). The influences of social stress and dominance status (social rank) on adrenocorticotropin hormone (ACTH) and cortisol responses to acute administration of an indirect serotonergic agonist (fenfluramine) were evaluated in 75 cynomolgus macaques that were housed in five-member social groups for 28 mo. These groups either remained stable in composition (No-Stress) or had their composition periodically reorganized in the first (Early-Stress) or second (Late-Stress) halves of the study. At the end of the 23rd month, a fenfluramine challenge was done. Animals in the Late-Stress condition had significantly higher ACTH responses compared to those in the No-Stress condition ( p < .05) and significantly higher cortisol responses compared to those in the Early-Stress condition ( p < .05). No differences between dominant and subordinate animals in ACTH or cortisol responses to challenge were identified. These data suggest that social stress produces a “state”-related augmentation of hypothalamic-pituitary-adrenal responsivity to fenfluramine (serotonergic) challenge in cynomolgus macaques.

Coalitions and Alliances in Humans and Other Animals.

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