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Brian C Trainor

Publications and source records attributed to Brian C Trainor.

11 recordsLinked to original sources

Paternal behavior influences development of aggression and vasopressin expression in male California mouse offspring.

Parental care has been demonstrated to have important effects on offspring behavioral development. California mice (Peromyscus californicus) are biparental, and correlational evidence suggests that pup retrieving by fathers has important effects on the development of aggressive behavior and extra-hypothalamic vasopressin systems. We tested whether retrievals affected these systems by manipulating paternal retrieval behavior between day 15 and 21 postpartum. Licking and grooming behavior affect behavioral development in rats, so we also experimentally reduced huddling and grooming behavior by castrating a subset of fathers. Experimentally increasing the frequency of paternal pup retrieving behavior decreased attack latency in resident-intruder in both male and female adult offspring, whereas experimental reduction of huddling and grooming had no effect. In a separate group of male offspring, we examined vasopressin immunoreactivity (AVP-ir) in two regions of the posterior bed nucleus of the stria terminalis (BNST): the dorsal fiber tracts (dBNST) and the ventral cell body-containing region (vBNST). Experimentally increasing retrievals led to an apparent shift in AVP-ir distribution. Specifically, offspring from the high retrieval group had more AVP-ir than offspring from the sham retrieval group in the dBNST, whereas the opposite was observed in the vBNST. Experimental reduction of paternal grooming was associated with increased AVP-ir in the paraventricular nucleus and also increased corticosterone and progesterone, similar to observed effects of maternal grooming on HPA function. This study provides further evidence that paternal behavior influences the development of aggression and associated neural substrates.

Aggression↗

Somatostatin regulates aggressive behavior in an African cichlid fish.

Animals respond to environmental and social change with plasticity in the neural substrates underlying particular behavioral states. In the African cichlid fish Astatotilapia burtoni, social dominance status in males is accompanied by reduced somatic growth rate as well as increased somatostatin neuron size in the preoptic area. Although somatostatin is commonly studied within the context of growth, we show here for the first time that this ancient neuropeptide also plays a role in controlling social behavior. Somatostatin antagonists increased aggressive behavior in a dose-dependent fashion and the potent somatostatin agonist octreotide decreased aggression. We cloned and sequenced the genes encoding two somatostatin receptor subtypes in this species to study transcription in the gonads. When we examined somatostatin receptor gene expression in testes, expression of the somatostatin type 3 receptor was negatively correlated with an aggressive display and androgen levels. However, octreotide treatment did not reduce plasma testosterone or 11-ketotestosterone levels, suggesting that the behavioral effects of somatostatin are not mediated by androgens. These results show that somatostatin has important effects on social behavior. In dominant male A. burtoni, somatostatin may function to contain energetically costly processes such as somatic growth and aggressive behavior.

Aggression↗

Individual differences in estrogen receptor alpha in select brain nuclei are associated with individual differences in aggression.

Steroid hormones play an important role in modulating social behavior in many species. Estrogens are thought to act on an interconnected network of hypothalamic and limbic brain areas to affect aggressive behavior, although the specific nuclei unknown remain unspecified. We show that individual variation in estrogen receptor alpha (ERalpha) immunoreactivity in the lateral septum (LS), ventral bed nucleus of the stria terminalis (vBNST), and anterior hypothalamus (AHA) of CD-1 mice is positively correlated with aggressive behavior. When males were treated with fadrozole (an aromatase inhibitor), aggressive behavior was reduced, although castration did not reduce aggression. These results suggest that estrogens modulate aggressive behavior by acting on a circuit that includes the LS, vBNST, and AHA and that the source of estrogens is non-gonadal. Fadrozole also decreased c-fos expression in the lateral septum following aggressive encounters. Although the effects of estrogen on aggression appear to involve regulation of neuronal activity in the LS, additional processes are likely involved. These results suggest that estrogen acts in a specific subset of a complex network of nuclei to affect aggressive behavior.

Aggression↗

Social and photoperiod effects on reproduction in five species of Peromyscus.

At temperate latitudes, mammals and birds use changes in day length to time their reproductive activities to coincide with seasonal fluctuations in the environment. Close to the equator, however, conditions permissive of breeding do not track changes in day length as well, so other cues may be more important than photoperiod. In a variety of vertebrates, social interactions regulate breeding condition. We hypothesized that individuals of different species of Peromyscus mice found closer to the equator would respond more strongly to housing with an opposite sex conspecific than they would to photoperiod. To test this hypothesis, we compared the effects of long and short day lengths versus 8 days of pair housing with a female on reproductive tissue weights and testosterone (T) concentrations in five species of Peromyscus (P. aztecus, P. eremicus, P. maniculatus, P. melanophrys, and P. polionotus). After 13 weeks of short days (8L:16D), P. maniculatus, P. melanophrys, and P. polionotus significantly reduced relative testes mass compared to long day (16L:8D) housed animals. Social housing, however, had no effect on tissue weights in any species. However, male P. polionotus paired with females for 8 days increased T concentrations compared to single-housed males, whereas paired P. maniculatus reduced T. These data suggest that mechanisms of photoperiodic and social regulation of reproductive function are mediated by different physiological mechanisms among closely-related species and that both phylogeny and environmental factors contribute to patterns of reproductive plasticity.

Animals↗

Estrogenic encounters: how interactions between aromatase and the environment modulate aggression.

Initial investigations into the mechanistic basis of aggression focused on the role of testosterone (T) and a variety of studies on non-human animals found that elevated T levels promote aggression. However, many correlational studies have not detected a significant association between aggression and peripheral T levels. One reason for this inconsistency may be due to differential metabolism of T within the brain, in particular, the conversion of T to estrogen by aromatase. Thus, differences in aromatase enzyme activity, estrogen receptor expression, and related cofactors may have important effects on how steroids affect aggressive behavior. Hormone manipulation studies conducted in a wide variety of species indicate that estrogens modulate aggression. There is also growing evidence that social experience has important effects on the production of estrogen within the brain, and some cases can not be explained by androgenic regulation of aromatase. Such changes in central aromatase activity may play an important role in determining how social experiences affect the probability of whether an individual engages in aggressive behavior. Although studies have been conducted in many taxa, there has been relatively little integration between literatures examining aggression in different species. In this review, we compare and contrast studies examining aggression in birds, mammals, and humans. By taking an integrative approach to our review, we consider mechanisms that could explain species differences in how estrogen modulates aggression.

Aggression↗

Testosterone and photoperiod interact to affect spatial learning and memory in adult male white-footed mice (Peromyscus leucopus).

Gonadal hormones affect spatial learning and memory in mammals and circulating gonadal hormone concentrations fluctuate by season. Most nontropical rodents are spring/summer breeders and males display higher testosterone concentrations during the breeding season compared with the nonbreeding season (fall/winter). Seasonal patterns of testosterone concentration (as well as many other seasonal modifications of physiology, morphology, and behaviour) are induced by manipulation of photoperiod (day length; i.e. short or long days) in the laboratory. Coincident with reducing testosterone concentration, short days also impair spatial learning and memory performance in male white-footed mice (Peromyscus leucopus) compared with long days. We hypothesized that short-day-induced reduction of testosterone concentrations inhibits spatial learning and memory performance compared with long days. Adult male white-footed mice were maintained in long (16 h light/day) or short (8 h light/day) days for 14 weeks following sham-castration, castration plus saline implant, or castration plus testosterone implant treatment. Spatial learning and memory was assessed using a water maze, and photoperiod-evoked changes in gene expression of sex steroid receptors within the hippocampus were also examined. Castrated, short-day mice with testosterone replacement displayed enhanced water maze performance compared with other short-day mice, but no differences among testosterone treatments were observed in long-day mice. Photoperiod did not affect hippocampal androgen, oestrogen alpha, or oestrogen beta receptor gene expression. These results suggest that photoperiod modulates the effects of testosterone on spatial learning performance by mechanisms indirect of the hippocampus.

Animals↗

Pleiotropic contributions of nitric oxide to aggressive behavior.

Male mice with targeted deletion of the genes encoding the neuronal (NOS-1-/- or nNOS-/-) isoform of nitric oxide synthase display altered aggressive behaviors. Male nNOS-1-/- mice are more aggressive than wild-type (WT) mice in all testing paradigms. Testosterone is necessary, but not sufficient, for evoking the persistent aggression, and that serotonin (5-HT) metabolism is altered in male nNOS-1-/- mice. The specific deletion of the nNOS-1 gene not only results in a lack of nNOS-1 protein, but in common with many genes, affects several 'down-stream' processes. In this review, we address whether the elevated aggression in male nNOS-1-/- mice reflects pleiotropic effects of the nNOS-1 gene on pain sensitivity, 'anxiety-like', or 'depressive-like' behaviors. For example, male nNOS-1-/- mice display increased sensitivity to painful stimuli, which may prolong aggressive interactions. Despite elevated corticosterone concentrations, nNOS-1 knockout mice appear to be less 'anxious' or fearful than WT mice. Male nNOS-1-/- mice display longer latencies to right themselves on an inverted platform and spend more time in the center of an open field than WT mice. Because of reduced serotonin turnover, the excessive aggressiveness displayed by nNOS-1-/- mice may be symptomatic of a depressive-like syndrome. However, nNOS-1-/- mice rarely display behavioral 'despair' when assessed with the Porsolt forced swim test; rather, nNOS-1-/- mice show vigorous swimming throughout the assessment suggesting that the aggressive behavior does not represent depressive-like behavior. Importantly, aggressive behavior is not a unitary process, but is the result of complex interactions among several physiological, motivational, and behavioral systems, with contributions from the social as well as the physical environment. Lastly, the multiple, and often unanticipated, effects of targeted gene disruption on aggressive behavior are considered.

Aggression↗

Opposing hormonal mechanisms of aggression revealed through short-lived testosterone manipulations and multiple winning experiences.

Territorial aggression is influenced by many social and environmental factors. Since aggression is a costly behavior, individuals should account for multiple factors such as population density or reproductive status before engaging in aggression. Previous work has shown that male California mice (Peromyscus californicus) respond to winning aggressive encounters by initiating aggression more quickly in future encounters, and we investigated the physiological basis for this effect. We found that injections that produced a transient increase in testosterone (T) following an aggressive encounter caused males to behave more aggressively in an encounter the following day. Experience alone was not enough to change aggression, as males treated with saline injections showed no change in aggression. The effect of T injections on aggression was androgen-based, as the inhibition of aromatase did not block the T injections from increasing aggression. Aromatase inhibition did, however, increase aggression in the initial aggression tests (before application of T or saline injections), and aromatase activity in the bed nucleus of the stria terminalis (BNST) was negatively correlated with aggression. A previous study suggested that aromatase activity in the BNST decreases after males become fathers. Thus, distinct neuroendocrine mechanisms allow male California mice to adjust aggressive behavior in response to changes in social and reproductive status.

Aggression↗

Arginine vasotocin interacts with the social environment to regulate advertisement calling in the gray treefrog (Hyla versicolor).

Arginine vasotocin (AVT) has different effects on social behaviors across species with different social systems. However, less attention has been directed towards the way environmental stimuli interact with AVT to affect social behaviors. Previous work found that AVT affects the production of advertisement calls and the outcome of competitive interactions between male gray treefrogs (Hula versicolor). We conducted a field study to investigate how the presence of other males in a chorus influenced the production of advertisement calls in males treated with AVT or saline. After hormone treatment we placed individuals in call sites either within 50 cm of another calling male (proximate), or more than 2 m away from any calling male (distant). Males treated with AVT produced significantly longer calls with more pulses when placed at proximate call sites, but not distant call sites. Nonsignificant trends indicated that these increases in call length coincided with a decrease in call rate. There was no effect of call site distance on advertisement calls when males were treated with saline. These results indicate that the social environment can modulate the action of AVT on an important reproductive behavior, and that AVT does not influence call duration and pulse number unless another male is nearby. Understanding how social stimuli regulate the action of AVT on behavior could provide insight on the diversity of AVT function across species.

Animals↗

Variation in aromatase activity in the medial preoptic area and plasma progesterone is associated with the onset of paternal behavior.

The effects of aromatase within the brain on sexual behavior have been studied in a wide variety of species. Relatively few non-mating behaviors have been considered, despite evidence that estrogen affects many social behaviors. Testosterone promotes paternal behavior in California mouse (Peromyscus californicus) fathers, acting primarily via aromatization to estradiol. Virgin male California mice rarely exhibit paternal behavior, so we investigated whether aromatase in the brain changed with the onset of paternal behavior in California mouse fathers. In the medial preoptic area (MPOA), a brain area known to regulate parental behavior in rodents, we found that fathers had significantly more aromatase activity than mated males without pups, suggesting that an increase in estrogen production in this brain area contributes to the onset of paternal behavior. We also found that progesterone (P(4)) levels were lower in fathers compared to sexually inexperienced males and that P(4) was negatively correlated with aromatase activity in the MPOA. These P(4) findings agree with a recent study that found an inhibitory effect of P(4) on paternal behavior. Overall, we found that aromatase activity and P(4) levels change in association with an important life history transition, and may provide a mechanistic basis for plasticity in paternal behavior.

Animals↗

Testosterone promotes paternal behaviour in a monogamous mammal via conversion to oestrogen.

Although high testosterone (T) levels inhibit paternal behaviour in birds breeding in temperate zones many paternal mammals have a very different breeding biology, characterized by a post-partum oestrus. In species with post-partum oestrus, males may engage in T-dependent behaviours such as aggression and copulation simultaneously with paternal behaviour. We previously found that T promotes paternal behaviour in the California mouse, Peromyscus californicus. We examine whether this effect is mediated by the conversion of T to oestradiol (E(2)) by aromatase. In the first experiment, gonadectomized males treated with T or E(2) implants showed higher levels of huddling and pup grooming behaviour than gonadectomized males treated with dihydrotestosterone or empty implants. In the second experiment, we used an aromatase inhibitor (fadrozole) (FAD) to confirm these results. Gonadectomized males treated with T + vehicle or E(2) + FAD showed higher levels of huddling and pup grooming behaviour than gonadectomized males treated with T + FAD or empty implants. Although E(2) is known to promote the onset of maternal behaviour to our knowledge our results are the first to demonstrate that E(2) can promote paternal behaviour in a paternal mammal. These results may explain how mammals express paternal behaviour while T levels are elevated.

Animals↗