Sex-dependent effects of social status on the regulation of arginine-vasopressin (AVP) V1a, oxytocin (OT), and serotonin (5-HT) 1A receptor binding and aggression in Syrian hamsters (Mesocricetus auratus).

Dominance status in hamsters is driven by interactions between arginine-vasopressin V1a, oxytocin (OT), and serotonin 1A (5-HT1A) receptors. Activation of V1a and OT receptors in the anterior hypothalamus (AH) increases aggression in males, while decreasing aggression in females. In contrast, activation of 5-HT1A receptors in the AH decreases aggression in males and increases aggression in females. The mechanism underlying these differences is not known. The purpose of this study was to determine if dominance status and sex interact to regulate V1a, OT, and 5-HT1A receptor binding. Same-sex hamsters (N = 47) were paired 12 times across six days in five min sessions. Brains from paired and unpaired (non-social control) hamsters were collected immediately after the last interaction and processed for receptor binding using autoradiography. Differences in V1a, OT, and 5-HT1A receptor binding densities were observed in several brain regions as a function of social status and sex. For example, in the AH, there was an interaction between sex and social status, such that V1a binding in subordinate males was lower than in subordinate females and V1a receptor density in dominant males was higher than in dominant females. There was also an interaction in 5-HT1A receptor binding, such that social pairing increased 5-HT1A binding in the AH of males but decreased 5-HT1A binding in females compared with unpaired controls. These results indicate that dominance status and sex play important roles in shaping the binding profiles of key receptor subtypes across the neural circuitry that regulates social behavior.

Development of social play in hamsters: Sex differences and their possible functions.

In several rodent species social play appears to be necessary for proper deployment of species-specific patterns of aggressive and reproductive behavior. Specifically, in male Syrian hamsters (Mesocricetus auratus), play has been linked to the development of adult aggression. We quantified several types of social play behavior in same-sex peer groups of Syrian hamsters three times per week for three consecutive weeks after weaning, which included postnatal days 22-42 (PD22 to PD42). Male hamsters increased playful contact during PD36-PD42, whereas females showed peak playful contact during PD29-PD35. These findings suggest that the motivation for social play increases during mid-adolescence in males, but dissipates in females. To investigate the effects of social play deprivation, one hamster per litter remained pair-housed with its mother forthree weeks after weaning its littermates. In adulthood, both play-deprived and play-exposed animals received acute social defeat stress followed by social interaction testing. Play deprivation led to increased defeat-induced social avoidance in both males and females. In males, play deprivation increased fighting back during social defeat stress, whereas in females it reduced aggressive behavior during conditioned defeat testing. We suggest that social play deprivation disrupts neural circuits regulating aggression in a sex-specific manner, perhaps related to sex differences in territorial defense, but has similar effects on neural circuits regulating stress responsivity. Overall, these findings suggest that juvenile social play functions to promote coping with stress and appropriate social behavior in adulthood.

Winning agonistic encounters increases testosterone and androgen receptor expression in Syrian hamsters.

Winning aggressive disputes is one of several experiences that can alter responses to future stressful events. We have previously tested dominant and subordinate male Syrian hamsters in a conditioned defeat model and found that dominant individuals show less change in behavior following social defeat stress compared to subordinates and controls, indicating a reduced conditioned defeat response. Resistance to the effects of social defeat in dominants is experience-dependent and requires the maintenance of dominance relationships for 14days. For this study we investigated whether winning aggressive interactions increases plasma testosterone and whether repeatedly winning increases androgen receptor expression. First, male hamsters were paired in daily 10-min aggressive encounters and blood samples were collected immediately before and 15min and 30min after the formation of dominance relationships. Dominants showed an increase in plasma testosterone at 15min post-interaction compared to their pre-interaction baseline, whereas subordinates and controls showed no change in plasma testosterone. Secondly, we investigated whether 14days of dominant social status increased androgen or estrogen alpha-receptor immunoreactivity in brain regions that regulate the conditioned defeat response. Dominants showed more androgen, but not estrogen alpha, receptor immuno-positive cells in the dorsal medial amygdala (dMeA) and ventral lateral septum (vLS) compared to subordinates and controls. Finally, we showed that one day of dominant social status was insufficient to increase androgen receptor immunoreactivity compared to subordinates. These results suggest that elevated testosterone signaling at androgen receptors in the dMeA and vLS might contribute to the reduced conditioned defeat response exhibited by dominant hamsters.

Inference in a social context: A comparative study of capuchin monkeys (Cebus apella), tree shrews (Tupaia belangeri), hamsters (Mesocricetus auratus), and rats (Rattus norvegicus).

Four species (capuchin monkeys, tree shrews, rats, and hamsters) performed an inference task situated in a social context. In Experiment 1, capuchin monkeys first explored food sites under 1 of 2 conditions: In 1 condition, food was refilled after it was eaten (replenished condition), whereas it was not refilled (depleted condition) in the other condition. Two food sites were presented for each condition. In the test phase, a subject watched a conspecific demonstrator visit 1 of the food sites in either the replenished or depleted condition. A screen placed in front of the sites prevented the subject from seeing the demonstrator actually eat the food. When the demonstrator was removed, the subject explored the cage. Three of 4 monkeys tended to go to the unvisited sites in the depleted condition, but tended to go to the visited site in the replenished condition. This suggests that they inferred that there was no food because the demonstrator had eaten it. In Experiment 2, using the same procedure, 2 nongroup-living species (tree shrews and hamsters) were indifferent to demonstrator behavior and visited sites only randomly, and group-living rats showed a strong tendency to follow demonstrators, irrespective of the type of food site. These tendencies were unchanged when olfactory information was added in Experiment 3 and when motivation to compete increased in Experiment 4. These results suggest that only capuchin monkeys have the ability to solve an inference task when cued by social information.

Immediate post-defeat infusions of the noradrenergic receptor antagonist propranolol impair the consolidation of conditioned defeat in male Syrian hamsters.

Social defeat occurs when an animal is attacked and subjugated by an aggressive conspecific. Following social defeat, male Syrian hamsters fail to display species-typical territorial aggression and instead exhibit submissive or defensive behaviors even when in the presence of a non-aggressive intruder. We have termed this phenomenon conditioned defeat (CD). The mechanisms underlying CD are not fully understood, but data from our lab suggest that at least some of the mechanisms are similar to those that mediate classical fear conditioning. The goal of the present experiment was to test the hypothesis that noradrenergic signaling promotes the consolidation of CD, as in classical fear conditioning, by determining whether CD is disrupted by post-training blockade of noradrenergic activity. In Experiment 1, we determined whether systemic infusions of the noradrenergic receptor antagonist propranolol (0, 1.0, 10, or 20mg/kg) given immediately after a 15 min defeat by a resident aggressor would impair CD tested 48 h later. Hamsters that were given immediate post-training infusions of propranolol (1.0, but not 10 or 20mg/kg) showed significantly less submissive behavior than did those given vehicle infusions supporting the hypothesis that there is noradrenergic modulation of the consolidation of a social defeat experience. In Experiment 2, we demonstrated that propranolol (1.0mg/kg) given immediately, but not 4 or 24h, after defeat impaired CD tested 48 h after defeat indicating that the window within which the memory for social defeat is susceptible to beta-adrenergic modulation is temporary. In Experiment 3, we examined whether central blockade of noradrenergic receptors could recapitulate the effect of systemic injections by giving an intracerebroventricular infusion of propranolol immediately after defeat and examining the effect on CD 24h later. Centrally administered propranolol (20 µg/3 µl but not 2 µg/3 µl) was also effective in dose-dependently reducing consolidation of CD. Collectively, the present results indicate that noradrenergic activity promotes the consolidation of CD and suggest that CD is a valuable model to study the processes by which emotion and stress modulate memory in an ethologically relevant context. These data also suggest that the popular conception in the clinical literature that the anxiolytic effect of propranolol is primarily due to the drug's peripheral effects may need to be reconsidered.

Mate preference for dominant vs. subordinate males in young female Syrian hamsters (Mesocricetus auratus) following chemically-accelerated ovarian follicle depletion.

Life history theory predicts that selectivity for mates generally declines as females age. We previously demonstrated this phenomenon in Syrian hamsters (Mesocricetus auratus), in that older females showed reduced preference for dominant over subordinate males. To test the hypothesis that decreased reproductive quality due to aging reduces mate preference, we decoupled reproductive and chronological age by treating young female hamsters with 4-vinylcyclohexene diepoxide (VCD), which destroys ovarian follicles and functionally accelerates ovarian follicle depletion without compromising the general health of rodents. In this study, VCD effectively reduced follicle numbers in young Syrian hamsters. VCD-treated and control females were allowed to choose between a dominant and a subordinate male in a Y-maze on the day of proestrus. Both VCD-treated and control females demonstrated preference for the dominant male by leaving a greater proportion of vaginal scent marks near him, which is a behavior that females display when soliciting prospective mates. However, there was no effect of treatment on the proportion of vaginal scent marks left for the dominant male. Furthermore, ovarian follicle numbers were not significantly correlated with any behaviors in either group. We conclude that accelerated ovarian follicle depletion does not reduce mate preference in young female hamsters.

PSA-NCAM in the posterodorsal medial amygdala is necessary for the pubertal emergence of attraction to female odors in male hamsters.

During puberty, attention turns away from same-sex socialization to focus on the opposite sex. How the brain mediates this change in perception and motivation is unknown. Polysialylated neural cell adhesion molecule (PSA-NCAM) virtually disappears from most of the central nervous system after embryogenesis, but it remains elevated in discrete regions of the adult brain. One such brain area is the posterodorsal subnucleus of the medial amygdala (MePD). The MePD has been implicated in male sexual attraction, measured here as the preference to investigate female odors. We hypothesize that PSA-NCAM gates hormone-dependent plasticity necessary for the emergence of males' attraction to females. To evaluate this idea, we first measured PSA-NCAM levels across puberty in several brain regions, and identified when female odor preference normally emerges in male Syrian hamsters. We found that MePD PSA-NCAM staining peaks shortly before the surge of pubertal androgen and the emergence of preference. To test the necessity of PSA-NCAM for female odor preference, we infused endo-neuraminidase-N into the MePD to deplete it of PSAs before female odor preference normally appears. This blocked female odor preference, which suggests that PSA-NCAM facilitates behaviorally relevant, hormone-driven plasticity.

Effects of inescapable versus escapable social stress in Syrian hamsters: the importance of stressor duration versus escapability.

Social avoidance is a common characteristic of many clinical psychopathologies and is often triggered by social stress. Our lab uses Syrian hamsters to model stress-induced social avoidance, and we have previously established that both inescapable and escapable social defeat result in increased social avoidance when compared with no-defeat controls. Our previous work suggested, however, that social avoidance was significantly greater after inescapable defeat. The goal of this study was to determine if this difference in behavior after the two types of defeat was due to experimental differences in the controllability (i.e., escapability) of the defeat or simply to differences in the overall duration of the defeat. In Experiment 1, we used a yoked design to hold constant the duration of defeat between escapable and inescapable defeat conditions. This design resulted in only a very brief social defeat, yet when comparing defeated animals with no-defeat controls, a significant increase in social avoidance was still observed. In Experiment 2, we also used the yoked design, but the escape task was made more difficult to ensure a longer defeat experience. Again, we observed no effect of controllability. Together, these data suggest that the ability to escape a social stressor does not reduce the impact of the stressful experience. These results emphasize that social stressors need not be prolonged or uncontrollable to produce marked effects on subsequent behavior.

A new method for studying social eavesdropping using male golden hamsters.

Social eavesdropping is a special type of social learning and it is defined as the act of extracting information from social interactions between conspecifics. Social eavesdropping has advantages in information gathering and has attracted increasing attention. Emerging studies on social eavesdropping have been reported in several species, but the lack of suitable and manipulable laboratory rodent models remains a challenge to the study of the underlying mechanisms of social eavesdropping. The aim of this study was to take advantage of golden hamsters and their agonistic behaviors to develop a new laboratory method to study social eavesdropping. Male hamsters with or without a defeat experience were used as bystanders and were exposed to either a fighting interaction or a neutral encounter between two male demonstrators in a social learning chamber for a 3-day social learning. The behavioral responses of the bystanders toward observed demonstrators were tested in a U-shaped maze before and after the 3-day social learning. We found that (1) bystanders were attracted to the winning demonstrators in both short-term and long-term tests in experiment 1; (2) bystanders with a brief defeat experience displayed the opposite behavioral pattern and avoided approaching the winning demonstrator in experiment 2. It is evident that these hamsters acquired information about the relative qualities and dominance of the demonstrators and behaved differently toward different conspecifics afterward. Collectively, male hamsters are capable of social eavesdropping and prior experience of defeat has a significant impact on their consequent behaviors. Our newly developed behavioral method offers several advantages and it is useful for the study of social eavesdropping and its underlying mechanisms.

A modified anxious behavior test for hamsters.

BACKGROUND: Latency to feed in a novel environment assesses anxious behavior in rodents, but it is unclear whether it distinguishes anxiety from consumption or appetite. NEW METHOD: The anxiety-related feeding/exploration conflict (AFEC) test was used here to assess anxious behavior in Syrian hamsters for which increased cheek-pouching of food, but not overconsumption of it, reflects appetitive drive, and orexigenic stimuli do not increase consumption. The setup of the test prevented cheek-pouching. COMPARISON WITH EXISTING METHODS: Latency to approach test food provided an additional control for non-emotional effects of treatments. Feed and approach latencies in the test cage were normalized to those in the home cage to factor out non-emotional effects. RESULTS: Feed latency and the feed latency ratio (test cage/home cage) were reduced by acute treatment with benzodiazepine, diazepam, or beta-adrenergic receptor antagonist, propranolol, or chronic treatment with norepinephrine reuptake inhibitor, desipramine. Reductions of feed latency and the feed latency ratio were not associated with hyperphagia, and these behaviors were unaltered by acute treatment with opioid receptor antagonist, naltrexone. Latency to approach food in the test cage, with and without normalization, was unaltered by these treatments. Finally, overnight fasting elevated feed latency without hyperphagia, and this effect was attenuated by chronic desipramine treatment. CONCLUSIONS: These results suggest that the AFEC test assesses anxious, but not appetitive or consummatory, behavior, and that its sensitivity increases with food deprivation of hamsters.

Copulatory and agonistic behavior in Syrian hamsters following social defeat.

Syrian hamsters are highly aggressive animals that reliably defend their home territory. After social defeat, however, hamsters no longer defend their home cage but instead display submissive and defensive behavior toward an intruder, a response that we have termed conditioned defeat. Plasma testosterone is significantly reduced in Syrian hamsters following repeated defeat suggesting that social defeat might also impair copulatory behavior. The present study aimed to determine whether copulatory behavior in male Syrian hamsters is suppressed following repeated social defeats and additionally whether exposure to a hormone-primed stimulus female after social defeat reduces the behavioral response to defeat. Hamsters were paired with an aggressive opponent for one or nine defeats using a resident-intruder model, while controls were placed into the empty cage of a resident aggressor. On the day after the last treatment, half of the hamsters were paired with a receptive female for 10 min. There were no significant differences in the copulatory behavior of defeated versus non-defeated hamsters, and the opportunity to copulate had no effect on subsequent conditioned defeat testing, as defeated animals displayed significantly more submissive behavior than did non-defeated animals. The current data suggest that conditioned defeat is not necessarily a maladaptive response to social stress, at least in terms of reproductive behavior, but may instead represent a viable behavioral strategy adopted by losing animals following social defeat. Further, these data indicate that conditioned defeat is relatively persistent and stable, as the opportunity to copulate does not reduce the subsequent display of submissive behavior.

Sex ratio adjustment by sex-specific maternal cannibalism in hamsters.

Mammalian offspring sex ratios can be biased via prenatal and postnatal mechanisms, including sperm selection, sex-specific embryo loss, and differential postnatal investment in males and females. Syrian hamsters routinely cannibalize some of their pups in the first days after birth. We present evidence that short day lengths, typically predictive of poor autumn and winter field conditions, are associated with male-biased sex ratios, achieved in part through selective perinatal maternal infanticide of female offspring. Higher peak litter sizes were associated with increased cannibalism rates, decreased final litter counts, and increased body mass of pups surviving to weaning. To our knowledge this is the first report of sex ratio adjustment by offspring cannibalism.

Asymmetric learning to avoid heterospecific males in Mesocricetus hamsters.

If a female mates with a male of a closely related species, her fitness is likely to decline. Consequently, females may develop behavioral mechanisms to avoid mating with heterospecific males. In some species, one such mechanism is for adult females to learn to discriminate against heterospecific males after exposure to such males. We have previously shown that adult, female Syrian hamsters (Mesocricetus auratus) learn to discriminate against male Turkish hamsters (Mesocricetus brandti) after exposure to a single heterospecific male during 8 days across a wire-mesh barrier. Here we repeated that experiment but this time we exposed female Turkish hamsters to a male Syrian hamster for 8 days and then measured sexual and aggressive behaviors towards that heterospecific male and towards a conspecific male. In contrast to female Syrian hamsters, female Turkish hamsters did not differ in their latency to go into lordosis or in any measure of aggression towards either type of male. Female Turkish hamsters spent less time in lordosis with the heterospecific male, but the percentage of trials in which females copulated with conspecific and heterospecific males did not differ. When comparing females from both species that had been exposed to a heterospecific male for 8days, female Syrian hamsters copulated less and were more aggressive towards the heterospecific male compared to the behavior of female Turkish hamsters. We discuss how this asymmetric response between females of the two species may be due to the much larger geographical range of Turkish hamsters compared to Syrian hamsters.

Hamsters' (Mesocricetus auratus) memory in a radial maze analog: the role of spatial versus olfactory cues.

The golden hamster's (Mesocricetus auratus) performance on radial maze tasks has not been studied a lot. Here we report the results of a spatial memory task that involved eight food stations equidistant from the center of a circular platform. Each of six male hamsters depleted the food stations along successive choices. After each choice and a 5-s retention delay, the hamster was brought back to the center of the platform for the next choice opportunity. When only one baited station was left, the platform was rotated to evaluate whether olfactory traces guided hamsters' choices. Results showed that despite the retention delay hamsters performed above chance in searching for food. The choice distributions observed during the rotation probes were consistent with spatial memory and could be explained without assuming guidance by olfactory cues. The radial maze analog we devised could be useful in furthering the study of spatial memory in hamsters.

Organization of mating behavior in male hamsters (Mesocricetus auratus).

Factor analysis was applied to standard measures of sexual behavior in 73 male hamsters (Mesocricetus auratus) as they interacted with hormone-primed females. The results suggest that 5 factors, or conceptual mechanisms, function in the organization of the behaviors observed in the first 2 copulatory series. Of these, the 3 that relate to the behaviors in the first copulatory series were compared to those emerging from prior analyses of other rodents. These comparisons revealed similarities and differences in factor structure across species. Whereas all of these analyses identify factors related to the initiation and efficiency of copulatory behavior, hamsters seem to differ from other species in the measures that best define these factors. In addition, the copulatory rate factor that has been prominent in previous analyses of rats seems to be absent in hamsters. These results suggest that male sexual behavior in hamsters is organized differently from that in other rodents. In more general terms, they suggest that even species with generally similar copulatory patterns can show significant differences in behavioral organization, in turn suggesting the need for additional factor analytic studies to better establish the extent of these species differences.

Behavioural and endocrinological changes in Syrian hamsters (Mesocricetus auratus) under domestication.

This study aimed to quantify differences in response to stress between two strains of Syrian hamsters to evaluate the consequences of domestication in this species by measuring behavioural traits in the open-field, adrenal gland masses (ADR), and faecal and blood corticosterone concentrations (CC). We studied a laboratory (lab)- and a wild-derived population (wild). The lab hamsters were significant heavier than the wild hamsters. The lab males had the highest ADR, and it was independent of their high body mass (BM). The ADR of lab females and wild hamsters was linearly dependent of BM. The lab males had the highest faecal and blood CC, whereas the lab females had the lowest CC. In the open field, the lab hamsters began later to groom, groomed shorter, groomed less frequently, began later to rear, reared longer and reared less frequently. In the lab population, females reared more often and groomed longer than males. The sex differences in the behaviours of the lab population and the differences between the populations mirror the differences neither in the ADR nor in the CC. The founder effect and the breeding history of lab Syrian hamsters are discussed as causes of the differences between the studied populations.

Physiological mechanisms for food-hoarding motivation in animals.

The study of ingestive behaviour has an extensive history, starting as early as 1918 when Wallace Craig, an animal behaviourist, coined the terms 'appetitive' and 'consummatory' for the two-part sequence of eating, drinking and sexual behaviours. Since then, most ingestive behaviour research has focused on the neuroendocrine control of food ingestion (consummatory behaviour). The quantity of food eaten, however, is also influenced by the drive both to acquire and to store food (appetitive behaviour). For example, hamster species have a natural proclivity to hoard food and preferentially alter appetitive ingestive behaviours in response to environmental changes and/or metabolic hormones and neuropeptides, whereas other species would instead primarily increase their food intake. Therefore, with the strong appetitive component to their ingestive behaviour that is relatively separate from their consummatory behaviour, they seem an ideal model for elucidating the neuroendocrine mechanisms underlying the control of food hoarding and foraging. This review focuses on the appetitive side of ingestive behaviour, in particular food hoarding, attempting to integrate what is known about the neuroendocrine mechanisms regulating this relatively poorly studied behaviour. An hypothesis is formed stating that the direction of 'energy flux' is a unifying factor for the control of food hoarding.

A magnetic field effect on learning in male golden hamsters.

The aim of this experiment was to investigate the influence of repeated exposure to 10, 20, 30 or 40 Hz magnetic fields at 0.1T on the learning of male golden hamsters in a Skinner box, in which the animals learned to press a lever to receive a food reward. The latency of the first response was not affected by exposure to the magnetic fields used in this experiment. No significant field-dependent effects on the performance of the task were observed in males exposed to 10 and 20 Hz magnetic fields at 0.1T. However, exposure significantly improved the learning of the task in animals exposed to 30 and 40 Hz magnetic fields at 0.1T.

Memory for individuals: hamsters (Mesocricetus auratus) require contact to develop multicomponent representations (concepts) of others.

In humans, individuals recognize other individuals by numerous types of independent information, such as the quality of the voice, appearance of the face, smell, gait, and posture. Humans also have integrated memories of others--that is, in response to a face or a voice the individual is recognized by name and other information about that individual is remembered. In many nonhuman species, individual recognition also occurs. Although observational studies suggest that individuals of some nonhuman species may be able to use several different cues for individual recognition, little experimental proof for this is available. Golden hamsters have at least 5 individually distinctive odors and they develop integrated, multi-odor memories (concepts) of familiar individuals, as shown by across-odor habituation experiments. Little is known, however, about the conditions that are necessary to develop such integrated memories. In these experiments we investigated what kinds of experiences were necessary for male hamsters to develop multiodor memories of females. The results show that exposure to all of the odors of another individual was not sufficient to develop such multiodor memories but that physical contact between the subjects and stimulus animals was necessary. Multiodor representations were developed after interactions with anesthetized individuals, confirming the finding that physical contact was important but also showing that interaction with an awake, behaving individual was not necessary to form multiodor representations of other individuals. We are not aware of experimental proof for integrated, multicomponant memories in any other nonhuman species.

Cohabitation impaired physiology, fitness and sex-related chemosignals in golden hamsters.

This study investigated the impact of long-term paternal presence (cohabitation) on several physiological parameters such as body weight, adrenal weight, cortisol of parents, and the survival of pups compared with brief daily encounters (isolation) of male-female pairs in golden hamsters (Mesocricetus auratus). We showed that females were affected more by cohabitation as evidenced by increased body and adrenal weights, elevated cortisol concentrations, and heavier uteri and spleens as compared with cohabiting male and isolated females. Furthermore, we found that tetradecanoic and hexadecanoic acids of the flank glands were sexually dimorphic, for which they were putative female pheromones. These two compounds were suppressed in females and elevated in males by cohabitation, suggesting that cohabitation impaired sex chemosignals. Overall, we concluded that housing females and males together had deleterious effects on adults and the survival of their pups in the golden hamster.