Joel C. Wommack

Repeated social stress and the development of agonistic behavior: individual differences in coping responses in male golden hamsters.

In male golden hamsters, repeated social subjugation during puberty accelerates the development of adult aggressive behavior and enhances its intensity in the presence of smaller individuals. The current study is focused on the characterization of the hormonal and behavioral responses to social subjugation during puberty. Subjugation consisted of daily exposure to an aggressive adult for 20-min periods from postnatal day 28 (P-28) to P-42, while controls were placed into an empty clean cage. Plasma cortisol levels were measured prior to or immediately after treatment on P-28 and P-42. On P-28, exposure to an aggressive adult or a clean and empty cage caused an increase in plasma cortisol levels. However, only social subjugation resulted in elevated cortisol levels on P-42, showing that juvenile hamsters habituate to an unfamiliar environment but not to social subjugation. In addition, we found a relationship between the frequency of submissive responses during social subjugation and the development of aggressive behavior. The transition from play fighting to adult aggression was most accelerated in the least submissive animals. These data show that behavioral response to social subjugation determines the development of aggressive behavior in golden hamsters. Our data also suggest that submissive behavior is a form of coping that attenuates the behavioral consequences of social subjugation in male golden hamsters.

Stress and the development of agonistic behavior in golden hamsters

Aggressive behavior can be studied as either offensive or defensive responses to a stimulus. The studies discussed in this review are focused on the peripubertal development of offensive aggression in male golden hamsters and its responsiveness to repeated social stress. Quantitative and qualitative changes in offensive responses were analyzed during this period. Quantitative changes in offensive responses were observed as decreased frequency of attacks. Qualitative changes were observed as changes in attack types, as animals reorient their attacks gradually from the face to the lower belly and rump. These developmental changes were altered by repeated exposure to social stress during early puberty. Daily exposure to aggressive adults during early puberty accelerated the qualitative development of offensive responses and the onset of adult-like offensive responses. In contrast, social stress had little effect on the quantitative changes associated with early puberty. However, social stress was associated with higher attack frequency during adulthood. These effects of stress during early puberty contrast with those observed with animals in late puberty. At that time, repeated exposure to aggressive adults inhibits offensive aggression. These data constitute the basis for a new theory on the development of agonistic behavior that includes the following hypotheses. First, it is hypothesized that mid-puberty is marked by a change in responsiveness to repeated social stress. As such, differences in stress responsiveness from social interactions are interpreted as a basic distinction between play fighting and adult aggression. Second, it is also hypothesized that a common neural circuitry mediates the activation of offensive responses during play fighting and adult aggressive interactions.

Repeated exposure to social stress alters the development of agonistic behavior in male golden hamsters

In male golden hamsters, exposure to social stress during puberty alters aggressive behavior. Interestingly, agonistic behavior undergoes two major transitions during puberty: a decline in attack frequency and a shift from play fighting to adult-like aggression. Based on previous observations, we developed an approach for characterizing offensive responses as play fighting or adult-like. The present studies had two aims. First, we validated our approach by looking at the development of attack types during puberty. Second, we looked at the effects of repeated social stress on the development of agonistic behavior by repeatedly exposing individuals to aggressive adults during puberty. In the first phase of the study, our results point to three different developmental periods. Initially, animals engage in agonistic behavior though attacks targeted at the face and cheeks. This period lasts from Postnatal Day 20 (P-20) to P-40 (early puberty). This phase corresponding to play fighting is followed by a transitional period characterized by attacks focused on the flanks (from P-40 to P-50, mid-puberty). Afterward, animals perform adult-like aggression characterized by attacks focused on the belly and rear. Our data also show that repeated exposure to aggressive adults has two separate effects on the development of agonistic behavior. Repeated social stress accelerated the onset of adult-like agonistic responses. Furthermore, attack frequency, while decreasing during puberty, remained at a higher level in early adulthood in stressed animals. These results show that repeated exposure to social stress during puberty alters the development of agonistic behavior both qualitatively and quantitatively.

Behavioural and Neuroendocrine Adaptations to Repeated Stress during Puberty in Male Golden Hamsters

In adult animals, the consequences of stress are often severe and long lasting. Repeated subjugation in adult male golden hamsters inhibits aggression and increases submissive and avoidant behaviours. By contrast, subjugation during puberty enhances offensive aggression. The goals of this study were to characterize behavioural and neuroendocrine responses of naïve and repeatedly subjugated juveniles to social defeat and to assess potential recovery from social stress. From the onset of puberty on postnatal day 28 (P28) to mid puberty (P42), animals were either socially subjugated or placed in a clean and empty cage for 20 min daily. The subjugated and control groups were further divided into subgroups and sacrificed under basal conditions or after social defeat on P28, P35 (early puberty), P45 (mid puberty) and P70 (early adulthood). On P35 and P45, repeatedly subjugated juveniles showed a complete inhibition of olfactory investigation (i.e. risk assessment) towards aggressive adults. Repeatedly subjugated also animals had lower postdefeat cortisol levels than controls on P45. Interestingly, basal cortisol levels increased gradually during puberty but did not differ between treatment groups at any point. Repeated subjugation was also associated with increased tyrosine hydroxylase immunoreactivity (ir‐TH) within the extended medial amygdala. After a 4‐week recovery period, none of these variables differed between subjugated and control groups. In an additional experiment, subjugated adults also had increased ir‐TH in the medial extended amygdala, suggesting that these neurones are particularly responsive to social stress. In conclusion, puberty may be a developmental period characterized by behavioural and neuroendocrine plasticity in stress responsiveness. Furthermore, peri‐pubertal changes in stress hormones may explain why juvenile hamsters are more resilient to social stress than adults.

Stress, Aggression, and Puberty: Neuroendocrine Correlates of the Development of Agonistic Behavior in Golden Hamsters

During puberty, agonistic behaviors undergo significant transitions. In golden hamsters, puberty is marked by a transition from play fighting to adult aggression. During early puberty, male golden hamsters perform play-fighting attacks. This response type is gradually replaced by adult attacks over the course of puberty. Interestingly, this behavioral transition does not appear to be controlled by changes in gonadal steroids. Instead, the shift from play fighting to adult aggression in male golden hamsters is driven by pubertal changes in glucocorticoid levels. Specifically, the transition from play fighting to adult aggression coincides with developmental increases in glucocorticoid levels, and external manipulations such as social stress or treatment with corticosteroid receptor agonists accelerate this behavioral shift. Moreover, the consequences of social stress differ greatly between juvenile and adult male golden hamsters. Although a single defeat during adulthood causes severe and long lasting behavioral and neuroendocrine consequences, socially subjugated juveniles show only transient behavioral effects. As such, it is likely that pubertal changes in the HPA axis are not only linked to the maturation of offensive responses but also determine the consequences of social stress. Combined, these studies in golden hamsters provide a novel mechanism for the development of agonistic behavior and suggest that age related differences in behavioral plasticity are mediated by the development of the HPA axis.

Glucocorticoids and the Development of Agonistic Behaviour during Puberty in Male Golden Hamsters

During puberty, the agonistic behaviour of male golden hamsters undergoes a transition from play fighting to adult aggression. Repeated exposure to social stress early in puberty accelerates this transition. The present study investigated the possible role of glucocorticoids on the maturation of agonistic behaviour. First, we compared serum cortisol levels following a 20‐min restraint stress during early puberty, mid‐puberty or adulthood. Across puberty, animals exhibited a two‐fold increase in post‐restraint cortisol levels. We also compared corticotrophin‐releasing hormone (CRH) immunoreactive fibres projecting to the median eminence between animals in early puberty and adulthood. The CRH fibre density was two‐fold greater in adults compared to juveniles. Furthermore, we investigated the effects of stress hormones on the maturation of agonistic behaviour. Male hamsters were injected daily with dexamethasone, a corticosteroid receptor type II agonist (0, 10 or 40 µg/100 g), early in puberty from postnatal day 31 (P‐31) to P‐36. When paired with a smaller and younger intruder on P‐37, attack frequency did not differ between groups. However, dexamethasone‐treated animals showed a dose‐dependent decrease in the percentage of play‐fighting attacks and an increase in the percentage of adult attacks. In summary, puberty can be described as a period of increasing hypothalamic‐pituitary‐adrenal activity in male golden hamsters. Moreover, increasing glucocorticoid levels influence the maturation of agonistic behaviour. These data shed new light on the neuroendocrine mechanisms that regulate the maturation of social behaviours during puberty.

Acculturation, depressive symptoms, estriol, progesterone, and preterm birth in Hispanic women

We examined the effects of acculturation, depressive symptoms, progesterone, and estriol (E3) as predictors of preterm birth (PTB) in pregnant Hispanic women. This cross-sectional study recruited a sample of 470 Hispanic women between 22- and 24-week gestation from physician practices and community clinics. We used the CES-D to measure maternal depressive symptoms. We measured acculturation by English proficiency on the Bidimensional Acculturation Scale, residence index by years in the USA minus age, nativity, and generational status. Serum progesterone and E3 were analyzed by EIA. Ultrasound and medical records determined gestational age after delivery. In χ2 analysis, there were a significantly greater percentage of women with higher depressive scores if they were born in the USA. In a structural equation model (SEM), acculturation (English proficiency, residence index, and generational status) predicted the estriol/progesterone ratio (E/P), and the interaction of depressive symptoms with the E/P ratio predicted PTB. Undiagnosed depressive symptoms during pregnancy may have biological consequences increasing the risk for PTB.

Chronic social stress during puberty enhances tyrosine hydroxylase immunoreactivity within the limbic system in golden hamsters

The present study was carried out to determine the effects of chronic exposure to social stress during puberty on the dopamine system in male golden hamsters. Experimental animals were socially subjugated between postnatal days 28 (P28) and 42. All animals were sacrificed on P46 and their brains processed for immunocytochemistry to tyrosine hydroxylase (TH). A large increase in the number of TH-immunoreactive (TH-ir) neurons was noted within the posterior portion of the medial amygdaloid nucleus and the posterior portion of the medial division of the bed nucleus of the stria terminalis in subjugated animals as compared to controls. This effect appeared to be site-specific as no difference was seen between groups in the periventricular nucleus, another steroid receptor-rich area. The data suggest that these dopamine neurons may play an important role in the behavioral changes associated with chronic social stress during puberty.

Acculturation and biobehavioral profiles in pregnant women of Hispanic origin: generational differences.

In Hispanics, acculturation may lead to negative health outcomes. This study used a cross-sectional design to investigate the psychosocial and biological risks in acculturating pregnant women of Hispanic origin (n = 470). Psychosocial risks—depressive symptoms, anxiety, and stress—were assessed by self-report, whereas biological measures included stress-related and reproductive hormones. Mental health deteriorated across generations, with worsening depression, anxiety, and stress with successive generations. Stress and reproductive hormone levels decreased across generations, whereas body mass index and number of sexual partners increased. These data provide potential biobehavioral explanations of the relationship between acculturation and declining health among Hispanic women in the United States.

Cortisol controls the pubertal development of agonistic behavior in male golden hamsters via type II corticosteroid receptors

In male golden hamsters, agonistic behavior undergoes a pubertal transition from play fighting to adult aggression. Previous studies have shown that this aspect of behavioral development is associated with pubertal increases in glucocorticoids and that daily social stress or injections of a synthetic glucocorticoid accelerate the transition. The goals of this study were to confirm the effects of cortisol on the development of agonistic behavior and to investigate the role of type II corticosteroid receptors in this process. First, animals treated with cortisol during early puberty [from postnatal days 31 (P-31) to P-36] showed an accelerated transition from play fighting to adult aggression. In a second experiment, the behavioral effects of cortisol were blocked by a co-treatment with a type II corticosteroid receptor antagonist. These findings are the first to show a facilitating role for type II corticosteroid receptors in the pubertal development of a social behavior. As such, these findings provide new insights into the neuroendocrine mechanisms controlling behavioral development during puberty.