Elizabeth A. Becker

Paternal behavior increases testosterone levels in offspring of the California mouse

Paternal care during early development influences pup survivorship in the monogamous and biparental California mouse, Peromyscus californicus. Moreover, paternal pup retrievals impact development of adult offspring aggression and the neuropeptide vasopressin, yet little is known about the underlying mechanisms of these developmental changes. Because testosterone can increase arginine vasopressin and aggression, we hypothesized that paternal pup retrievals increase testosterone levels in prepubertal male P. californicus pups. Male pups were assigned to one of three groups: hormonal baseline, nonretrieval control, or retrieval. On postnatal days 18-21, all pups and the mother were removed from the cage, and the focal male pup was placed either outside of the nest to elicit paternal retrievals (retrieval group) or in the nest to discourage paternal retrievals (nonretrieval group). Testosterone was elevated at 45-min, but not 90-min, post-manipulation in retrieved compared to nonretrieved pups. Moreover, there was a significant positive correlation between pup retrievals and testosterone in the 45-min group. This rapid testosterone rise in response to paternal retrievals may facilitate an increase in aggression and vasopressin in adult offspring. Therefore, this period of development previously viewed as hormonally quiescent may be more active in response to paternal behavior than previously thought.

Deciding to win: interactive effects of residency, resources and 'boldness' on contest outcome in white-footed mice

Various environmental and social factors can bias who wins and who loses a fight, but less is known about how these factors interact with each other to affect contest outcome. We examined this issue in the white-footed mouse, Peromyscus leucopus, as males of this species illustrate great flexibility in aggressive and territorial tactics in the field and in the laboratory. We found that the effects of both residency status and resource abundance (food, water and cover from predators) increased winning ability; however, there was no interaction between these two effects. As such, the impacts of residency and resource abundance on winning might represent two distinct behavioural phenomena that manifest via different mechanisms. We also found that mice that urine-marked an open arena at a high frequency were more likely to win fights in resource-rich environments compared to resource-poor environments. Meanwhile, mice that urine-marked the same type of environment at a substantially lower frequency did not show this behavioural difference between contexts. Because urinary marking behaviour is allied with aspects of risk-taking behaviour and social status, this result implies that males integrate information about their relative ‘boldness’ with information from their environment to make context-appropriate tactical decisions about fighting. We speculate that our data illustrate real-time, decision-making processes that are a necessary component of conditional strategies used to optimize fitness.

A comparison of scent marking between a monogamous and promiscuous species of peromyscus: pair bonded males do not advertise to novel females.

Scent marking can provide behavioral and physiological information including territory ownership and mate advertisement. It is unknown how mating status and pair cohabitation influence marking by males from different social systems. We compared the highly territorial and monogamous California mouse (Peromyscus californicus) to the less territorial and promiscuous white-footed mouse (P. leucopus). Single and mated males of both species were assigned to one of the following arenas lined with filter paper: control (unscented arena), male scented (previously scent-marked by a male conspecific), or females present (containing females in small cages). As expected, the territorial P. californicus scent marked and overmarked an unfamiliar male conspecifics scent marks more frequently than P. leucopus. Species differences in responses to novel females were also found based on mating status. The presence of unfamiliar females failed to induce changes in scent marking in pair bonded P. californicus even though virgin males increased marking behavior. Pair bonding appears to reduce male advertisement for novel females. This is in contrast to P. leucopus males that continue to advertise regardless of mating status. Our data suggest that communication through scent-marking can diverge significantly between species based on mating system and that there are physiological mechanisms that can inhibit responsiveness of males to female cues.

Postcontest Blockade of Dopamine Receptors Inhibits Development of the Winner Effect in the California Mouse (Peromyscus californicus)

The winner effect is an accumulation of previous wins that increase future winning. A primary unanswered question about the winner effect is how do individuals integrate information about previous wins? Dopamine (DA) has been implicated because phosphorylated tyrosine hydroxylase (pTH), the rate-limiting enzyme for DA biosynthesis, is elevated following multiple winning experiences. Moreover, DA receptor blockers and agonists influence aggression when administered prior to male-male contests. In the current study, we administered D1- and D2-like DA receptor antagonists immediately after a contest and examined the development of the winner effect in the territorial California mouse, Peromyscus californicus. During a 3-contest training phase, resident males experienced winning contests, followed immediately by a peripheral injection of either a DA receptor antagonist or vehicle or a handling experience (without injection). The DA receptor antagonists used in this study did not influence locomotion. To assess the cumulative effects of previous winning, males were subjected to a final test contest with a more competitive intruder. The winner effect was significantly decreased by both D1- and D2-like receptor antagonists administered during training. During the test contest, attack behavior was significantly reduced by previous administration of both types of DA receptor antagonists compared with controls. D1-like receptor blockade also diminished chasing behavior, whereas D2-antagonist treated animals continued to pursue opponents. During training against a less competitive intruder, there was no difference in aggressive behaviors between experimental and controls males. Our data indicate that DA activity between contests is concomitant with the competitive advantage gained from multiple winning experiences.

The Effects of Paternal Behavior on Offspring Aggression and Hormones in the Biparental California Mouse

Series of experiments with Peromyscus combined with studies from other species reveal interesting effects of parental behavior on aggression. Both paternal pup retrievals and some aspect(s) of maternal separation (MS) appear to influence aggression of offspring. Paternal retrievals, however, may have a unique effect on offspring aggression that function in part through changes to the arginine vasopressin neurochemical system associated with the bed nucleus of the stria terminalis. In comparison, MS and paternal huddling and grooming may function through the paraventricular nucleus as a result of stress, although effects on aggression appear to vary depending on species. The effects of paternal behavior were not uniform such that pup retrievals, but not huddling and grooming appeared to influence aggression. Thus, paternal effects on aggression may operate through mechanisms different than those traditionally associated with stress. This is also supported by preliminary data indicating a change in testosterone levels of pups in response to paternal retrievals. Despite the lack of an effect of changes in paternal huddling and grooming of offspring on aggression, it is possible that paternal separation in California mice may cause changes in aggression similar to those of MS in either rats or house mice. A careful comparison of aspects of aggression that are influenced by paternal retrievals vs. parental separation could be very illuminating in that one might predict different outcomes for different types of aggression.

Paternal retrievals increase testosterone levels in both male and female California mouse (Peromyscus californicus) offspring

The importance of maternal care on offspring development has received considerable attention, although more recently, researchers have begun to focus on the significance of paternal contributions. In the monogamous and bi-parental California mouse, fathers provide high levels of care, and therefore serve as a model system for studying paternal effects on behavior and underlying neuroendocrine mechanisms. Paternal retrievals in this species influence long term changes in brain (expression of arginine vasopressin-AVP) and behavior (aggression and parenting) in adult male offspring. Further, paternal retrievals induce a transient increase in testosterone (T) in male offspring, which is thought to mediate the relationship between paternal retrievals and AVP expression. Although the father-son relationship has been well characterized, few studies have examined father-daughter interactions. In California mice, paternal retrievals increase aggression in female offspring. Although T has been implicated in the regulation of female aggression, it remains unclear whether T may underlie long-term changes in female offspring aggression in response to paternal retrievals. In the current study, we examined the influence of paternal retrievals on T in both male and female offspring. Retrievals were manipulated experimentally by displacement of the pup and trunk blood was collected from retrieved, non-retrieved, and non-manipulated (baseline) pups. We found that fathers expressed similar levels of retrievals towards sons and daughters, and that T levels were elevated in retrieved, as compared to non-retrieved offspring. Similar to what has been previously described in male offspring and replicated here, female offspring that were retrieved had higher T levels than non-retrieved females. Neither females nor males experienced a change in corticosterone levels in response to retrievals suggesting offspring do not mount a stress response to paternal care. Therefore, our data suggest that paternal retrievals may serve similar functions in shaping adult behavior in both male and female offspring via modulation of hormone levels.

Increased vasopressin expression in the BNST accompanies paternally induced territoriality in male and female California mouse offspring

Abstract While developmental consequences of parental investment on species‐typical social behaviors has been extensively characterized in same‐sex parent‐offspring interactions, the impact of opposite‐sex relationships is less clear. In the bi‐parental California mouse (Peromyscus californicus), paternal retrieval behavior induces territorial aggression and the expression of arginine vasopressin (AVP) in adult male offspring. Although similar patterns of territorially emerge among females, the sexually dimorphic AVP system has not been considered since it is generally thought to regulate male‐typical behavior. However, we recently demonstrated that male and female P. californicus offspring experience increases in plasma testosterone following paternal retrieval. Since AVP expression is androgen‐dependent during development, we postulate that increases in AVP expression may accompany territoriality in female, as well as male offspring. To explore this aim, adult P. californicus offspring that received either high or low levels of paternal care (retrievals) during early development were tested for territoriality and immunohistochemical analysis of AVP within the bed nucleus of the stria terminalis (BNST), paraventricular nucleus (PVN), and supraoptic nucleus (SON). Consistent with previous studies, high care offspring were more aggressive than low care offspring. Moreover, high care offspring had significantly more AVP immunoreactive (AVP‐ir) cells within the BNST than low care offspring. This pattern was observed within female as well as male offspring, suggesting an equally salient role for paternal care on female offspring physiology. Regardless of early social experience, sex differences in AVP persisted in the BNST, with males having greater expression than females. HighlightsWe tested consequences of paternal retrievals on aggression and AVP in offspring.Increased aggression and BNST AVP‐ir in females in response to paternal retrievals.We replicated findings of increased BNST AVP‐ir and aggression in male offspring.Frequency of paternal retrievals associated with offspring BNST AVP‐ir.

Paternal Care Impacts Oxytocin Expression in California Mouse Offspring and Basal Testosterone in Female, but Not Male Pups

Natural variations in parenting are associated with differences in expression of several hormones and neuropeptides which may mediate lasting effects on offspring development, like regulation of stress reactivity and social behavior. Using the bi-parental California mouse, we have demonstrated that parenting and aggression are programmed, at least in part, by paternal behavior as adult offspring model the degree of parental behavior received in development and are more territorial following high as compared to low levels of care. Development of these behaviors may be driven by transient increases in testosterone following paternal retrievals and increased adult arginine vasopressin (AVP) immunoreactivity within the bed nucleus of the stria terminalis (BNST) among high-care (HC) offspring. It remains unclear, however, whether other neuropeptides, such as oxytocin (OT), which is sensitive to gonadal steroids, are similarly impacted by father-offspring interactions. To test this question, we manipulated paternal care (high and low care) and examined differences in adult offspring OT-immunoreactive (OT-ir) within social brain areas as well as basal T and corticosterone (Cort) levels. HC offspring had more OT-ir within the paraventricular nucleus (PVN) and supraoptic nucleus (SON) than low-care (LC) offspring. Additionally, T levels were higher among HC than LC females, but no differences were found in males. There were no differences in Cort indicating that our brief father-pup separations likely had no consequences on stress reactivity. Together with our previous work, our data suggest that social behavior may be programmed by paternal care through lasting influences on the neuroendocrine system.

BACLOFEN DOES NOT COUNTERACT THE ACUTE EFFECTS OF ETHANOL ON FLASH-EVOKED POTENTIALS IN LONG-EVANS RATS

This experiment examined the separate and combined effects of baclofen (5.0 mg/kg, i.p.), a GABAB receptor agonist, and ethanol (2.0 g/kg, i.p.) on flash-evoked potentials (FEPs) recorded from both the visual cortex (VC) and superior colliculus (SC) of chronically implanted male Long-Evans rats. In the VC, ethanol significantly decreased the amplitude of positive component P87, but increased P37 and P47. Other component amplitudes were not significantly altered. In contrast, baclofen reduced the amplitude of negative component N31 to such an extent that it became positive. Although P47 was also reduced by baclofen, the amplitude of most other components was increased. Only P24 and P87 were unchanged by baclofen. The combination of baclofen and ethanol resulted in amplitudes very similar to ethanol alone for secondary components P47, N62, and P87, but very similar to baclofen alone for primary component N31 and late components N147 and P230. In the SC, component amplitudes were generally decreased by ethanol, baclofen, and the combination treatment. Latencies of most components in both structures were increased by the drug treatments. Each drug treatment produced significant hypothermia. Locomotor behavior was also altered. These results demonstrate: (1) pharmacological differences between the primary and late components versus the secondary components of the cortical FEP, (2) that baclofen does not counteract significant effects of ethanol on cortical or collicular component amplitudes, and (3) that baclofen enhances N147-P230 amplitude, suggesting reduced cortical arousal.