Cortisol and behavioral responses to separation in mother and infant guinea pigs

In Experiment 1, lactating guinea pigs 3 days postpartum exhibited an elevation of plasma levels of cortisol when their litters were taken from the home cage and placed out of auditory range for 30 min. If pups were left within auditory range during the period of separation, or if the litter was disturbed but not removed, no increase in plasma cortisol levels was observed. In Experiment 2, 11/12- and 18/19-day-old guinea pig pups placed alone in a novel environment for 30 min displayed levels of plasma cortisol and vocalizations that were greater than those of pups tested in the same environment but with their mother. Pups tested with littermates but not with their mother exhibited plasma cortisol levels that were as great as those of pups tested alone. Pups tested with littermates vocalized much less than pups tested alone but more than pups tested with their mother. These results indicate that brief mother-infant separation can activate the pituitary-adrenal system in mother as well as infant guinea pigs and they provide further evidence for the existence of a reciprocal mother-infant attachment in this species.     

Maternal aggression in rats: Changes over pregnancy and lactation in a sprague-dawley strain

Maternal aggression in a Sprague-Dawley strain of laboratory rat (Charles River CD) was explored from Day 1 after mating on Day 0 through Day 24 of lactation (L0-L24). Aggression toward unfamiliar male “intruders” during 10-min tests was low among nonpregnant, nonlactating females and during the first 10 days of gestation. Frequency of attack on intruders increased moderately but significantly by Gestation Day 16 (G16; Experiment 1) or G21 (Experiment 2), a prepartum phenomenon not previously reported in laboratory rats. Levels of aggression were highest, however, during the first 9 days of lactation, when attacks averaged more than 6 per 10-min session. Attacks declined sharply in frequency after L14 and by L24 did not exceed levels observed among nonpregnant females. Experiment 3 examined the importance of the test site (home cage with nest and pups, if any, vs unfamiliar cage without nest or pups) to agonistic behavior associated with pregnancy and lactation. Late pregnant females tested in a novel cage were not aggressive; however, females tested shortly after delivering their pups were highly aggressive, averaging over four attacks per 5-min session. In novel cage tests frequency of attack remained high through L4 but declined significantly by L7. These data are consistent with the hypothesis that maternal aggression at its onset is primarily under hormonal control, but becomes increasingly dependent upon external factors, presumably pup stimulation, during the postpartum period.     

Sensory control of maternal aggression in Rattus norvegicus

Female rats become aggressive toward adult conspecifics during lactation. This change in social affect is dependent on the presence of the offspring, because maternal aggression disappears when the pups are removed. It was found that a similar decline occurs when the litter is placed in a glass flask while remaining in the home cage. In contrast, maternal aggression persists following placement of the pups in a nylon mesh bag. The pups did not vocalize while being in the mesh bags, so it appears that olfactory cues from the offspring constitute a critical element in the maintenance of maternal aggression in the rat. It has been suggested that the odor not only of the pups but also of the intruder may contribute to eliciting aggressive behavior in lactating rodents. In line with this proposal, it was found that mother rats spend about one third of the time preceding the first attack sniffing the body of the intruder. In contrast to findings in mice, housing of the prospective intruder behind a double wire mesh partition in the lactating female's home cage failed to reduce her aggressiveness toward him. Rats, then, may require more intimate contact with an individual than do mice for the aggression-reducing effect of familiarization to be observed.     

Chronic exposure to a novel odor increases pups' vocalizations, maternal care, and alters dopaminergic functioning in developing mice

This study was designed to assess the stress effect of manipulation of the olfactory environment in developing mice. In a first experiment it was found that mouse pups could be stressed (as measured by an increase in ultrasonic calls) by removing the litter from the dam for 15 min/day for the first 14 days of life and exposing them to a novel odor (clean bedding). This stress procedure also produced a long-term modification in maternal behavior. The stress response (ultrasounds) and the modification of maternal behavior were prevented by providing the litter with home cage bedding during maternal separation. In a second experiment it was demonstrated that early stress influenced apomorphine-induced wall climbing behavior in 15-day-old mice, suggesting stress-induced alterations in the dopaminergic system. Pups exposed to clean bedding during infancy exhibited more wall climbing behavior than pups never separated from the mother. Moreover, preventing the early stress response during mother-offspring separation, by providing pups with home cage bedding, eliminated the increase in apomorphine-induced wall climbing. Taken together these results suggest that olfactory cues are decisive in characterizing stressful situations inducing both immediate and long-lasting effects in mouse pups.     

Factors affecting incidence of infanticide and discrimination of related and unrelated neonates in male Mus musculus

Infanticide by males was examined in two strains (C57B1 and DBA) of the house mouse (Mus musculus). Males that had contact with a female within the previous 2-3 weeks rarely committed infanticide when introduced to the home cage of a female and her 1-day-old neonates, even when the female and neonates were of a different strain and from a different colony. In contrast, 90% of C57B1 males that had no contact with a female for more than 7 weeks killed pups when placed in the female's home cage, and 60% killed when a 1-day-old pup was introduced to the male's home cage. No difference in levels of infanticide occurred when grouped males were compared to isolated males. These results indicate that infanticide is not dependent upon recognition of the pups or the female, but depends on the male's previous exposure to females. Infanticidal behavior is not directly determined by genetic relationship, but the factors that inhibit this behavior reduce the probability that a male will kill his own offspring.     

Maternal separation alters later consumption of novel liquids in the squirrel monkey

The consumption of novel, fruit-flavored drinks was measured in juvenile squirrel monkeys that had either had their mother removed from the home cage for 2 h on 80 occasions prior to weaning or had not undergone this separation procedure. Among previously separated animals, males drank more than did females during the first 30 min following presentation, whereas there was no difference in the drinking of nonseparated males and females at this time. Further, the amount of liquid consumed during the 20 h following presentation increased across days of exposure in the nonseparated, but not in the previously separated monkeys. These results show that brief maternal separation can affect the later behavior of squirrel monkeys, and are consistent with findings in rhesus macaques that maternal separation alters later exploratory behavior.     

Effect of postweaning social experience on response of Siberian hamsters (Phodopus sungorus sungorus) toward young

Between 18 and 50 days of age, Siberian hamsters were housed either with same-sex littermates, opposite-sex littermates, opposite-sex littermates and parents, or opposite-sex littermates, parents, and a younger litter. When adults, these animals were presented with two 3-8-day-old pups for 8 hr, and their responses were recorded. Rearing conditions did not affect behavior of females. Males housed with female littermates in the absence of a younger litter showed fewer pup attacks and more nesting with pups than did males housed only with other males. Thus, housing with females in the early postweaning period may influence males' later (adult) responses toward pups. Only among hamsters housed with same-sex littermates did males and females differ in their response to pups, a result emphasizing that sex differences in behavior may depend on early social rearing.     

Effects of motherless rearing on basal and stress-induced corticosterone secretion in rat pups

Rearing of rat pups without a mother, artificial rearing (AR), produces substantial changes in the pups' behavior in later life. These changes are similar to those produced by the stress of repeated mother-pup separations. The predominant interpretation is that the long-term effects of disruptions to the mother-pup relationship are mediated by exposure to elevated levels of corticosterone which affect the development of neurobiological systems underlying cognition and behavior. Indeed, repeated separation of pups from the mother sensitizes the pups' corticosterone response to stress. This study examined basal and stress-induced corticosterone release in AR pups. Corticosterone levels were increased immediately following implantation of feeding cannulae. One day after the start of AR, circulating concentrations of corticosterone were not increased unless AR pups were challenged with an additional stressor (injection). Corticosterone levels were lowest when cannulation and AR started on postnatal day (PND) 5 compared with earlier PNDs. On PND 12, there was no evidence of increased corticosterone levels in AR pups at baseline or in response to stress, indicating that AR did not result in persistent sensitization of corticosterone release. The long-term effects of motherless rearing on rat behavior are mediated by mechanisms that are independent of sustained early corticosterone exposure.     

Rat pups prefer their siblings to their mothers: Possible implications for the development of kin recognition

Previous experiments have indicated that for rat pups some learning of their kin's characteristics is required for kin recognition. By differentially scenting the mother and litter with artificial odours, the possible role of each in the development of this ability can be assessed. 12- and 20-day-old rat pups were given a preference tests between the odour associated with their mother and an odour associated with their littermates. It was hypothesized that, because of the importance of the mother to her pups, individuals would preferentially acquire information from her and thus exhibit a preference for that odour. The results, however, did not support this: Both 12- and 20-day-old rat pups were found to prefer their littermate's odour to that of their mother. A further experiment revealed this did not reflect an aversion to their mother's odour. This preference for sibling littermates probably reflects the greater exposure of littermates to one another. The possible advantages of learning about one's kin from littermates are discussed.     

Maternal discrimination and the development of sex differences in exploratory behaviour in infant spiny mice (Acomys cahirinus)

The present paper reports sex differences in exploratory behaviour by infant Spiny Mice, Acomys cahirinus, that may, in part, be related to differences in maternal behaviour towards pups; like some other rodents, mother Acomys differentiate behaviourally between male and female pups. In Experiment 1 infant Acomys were allowed to explore a novel arena. This experiment showed that even by Day 3 (the day of birth=Day 1) female Acomys explored a novel environment more than males; they entered the arena sooner than males and spent more time in contact with a novel object. Experiment 2 showed that infant females were more active than males when observed in the home cage in the presence of their parents and made more approaches to the mother. Mothers, on the other hand, directed more licking behaviour towards males. Experiment 3 focused on the exploratory behaviour of individual pups in the presence of the mother. Given access to a large, complex arena, female pups explored more than males. The results also showed that mothers direct more of their social interactions towards sons than daughters, particularly when pups are about a week old. Some mothers appear to “direct” the movement of their offspring, by blocking their forward movement; this was done more often to male than to female pups. The data suggest that the previously observed changes in exploratory behaviour at this time, and the emergence of sex differences in exploration, may in part depend upon the mothers' reactions to pups by sex.     

The persistence of some effects of handling in infancy on the behaviour of the adult rat

An attempt was made to discover how persistent the effects of handling before weaning are on activity, grooming, emotional elimination and learning in adult rats; whether there is an interaction of the effects of handling and the effects of cage size on the behaviour of rats; and whether the daily removal of the mother during nursing has any effects on the pups.

Since all differences between handled and undisturbed animals found at 50 or 100 days were found at 220 days, it was concluded that the effects of handling in infancy are persistent. The hypothesis that cage size and removal of the mother during nursing significantly affect adult behaviour was not supported by the results.     

Interfemale aggression in adult bank voles (Clethrionomys glareolus)

Agonistic interaction may play a large role in shaping the social structure and spatial distribution of rodents such as Clethrionomys glareolus. Aggressive and non-aggressive behaviors of adult bank vole females were investigated with a home cage test during 10 min sessions. The number of attacks was significantly higher in virgin females kept with intact adult males than in singly reared females or those exposed to male urine. Bulbectomy of the tested females completely inhibited the male stimulating effect. This indicates that males influence the behavior of females by activating their olfactory systems. Aggressive behavior in pregnant or lactating females, which is linked to maternal behavior, was also tested. Female bank voles between 11 and 17 days of pregnancy or lactating at 3–4 days or 9–10 days attacked their partners significantly more frequently than virgins did. Females that had direct contact with males, even if they were not fertilized, appeared to be more successful in same-sex competition. Aggr. Behav. 24:53–61, 1998. © 1998 Wiley-Liss, Inc.     

Social organization predicts nature of infant-adult interactions in two species of wild guinea pigs (Cavia aperea and Galea monasteriensis)

The authors compared interactions of infants with mothers and unfamiliar females in a novel environment in 2 caviomorph rodent species: the harem-living Cavia aperea, the probable progenitor of the domestic guinea pig; and the pair-living Galea monasteriensis. In C. aperea, interactions with mothers and unfamiliar females were largely similar; in G. monasteriensis, interactions with the mother, but not unfamiliar female, were characterized by physical closeness and sociopositive behavior. In G. monasteriensis, plasma cortisol levels were lower when with the mother than when with the unfamiliar female. Results are consistent with the species' social organizations and suggest that behavioral interactions of pups with mothers and other females in domestic guinea pigs reflect primarily the social organization of the progenitor species rather than domestication.     

Substance P is involved in terminating the hypothalamo- pituitary-adrenal axis response to acute stress through centrally located neurokinin-1 receptors

The neurokinin substance P (SP) has been previously shown to inhibit basal hypothalamo-pituitary-adrenal (HPA) axis activity. This study was designed to investigate the effects of central injection of the specific neurokinin-1 receptor antagonist RP67580 on the HPA axis response to acute restraint stress. In non-restrained rats injected with RP67580, plasma ACTH and corticosterone levels were elevated at 30 and 60 min compared to rats injected with vehicle, but there were no differences between vehicle and RP67580 groups at 4h. In restrained rats injected with vehicle, plasma ACTH and corticosterone levels were significantly elevated at 30 min and 60 min following initiation of the stress but had returned to basal levels at 4h. In restrained rats injected icv with RP67580, plasma corticosterone and ACTH levels were significantly elevated at 30 min and 60 min, with no significant differences compared to the restraint stressed vehicle-injected group. However, in the RP67580-injected group, corticosterone and ACTH levels remained significantly elevated at 4h following onset of restraint compared to those in the restraint stressed vehicle-injected group. Corticotrophin-releasing factor mRNA levels in the parvocellular subdivision of the paraventricular nucleus of the hypothalamus and POMC mRNA levels in the anterior pituitary were significantly increased in the stressed group 4h following injection with RP67580 compared to the stressed group injected with vehicle alone. These data show that endogenous SP does not inhibit the initial magnitude of the HPA axis response to restraint stress, but does act through neurokinin-1 receptors at a central level to reduce the duration of the response to stress. This suggests that SP may be an important central agent controlling the transition between acute and chronic stress.     

Acute predator stress impairs the consolidation and retrieval of hippocampus-dependent memory in male and female rats

We have studied the effects of an acute predator stress experience on spatial learning and memory in adult male and female Sprague-Dawley rats. All rats were trained to learn the location of a hidden escape platform in the radial-arm water maze (RAWM), a hippocampus-dependent spatial memory task. In the control (non-stress) condition, female rats were superior to the males in the accuracy and consistency of their spatial memory performance tested over multiple days of training. In the stress condition, rats were exposed to the cat for 30 min immediately before or after learning, or before the 24-h memory test. Predator stress dramatically increased corticosterone levels in males and females, with females exhibiting greater baseline and stress-evoked responses than males. Despite these sex differences in the overall magnitudes of corticosterone levels, there were significant sex-independent correlations involving basal and stress-evoked corticosterone levels, and memory performance. Most importantly, predator stress impaired short-term memory, as well as processes involved in memory consolidation and retrieval, in male and female rats. Overall, we have found that an intense, ethologically relevant stressor produced a largely equivalent impairment of memory in male and female rats, and sex-independent corticosterone-memory correlations. These findings may provide insight into commonalities in how traumatic stress affects the brain and memory in men and women.     

Maternal aggression toward infanticidal males of different social status in wild house mice (Mus musculus domesticus)

Maternal aggression was examined in wild female mice (Mus musculus domesticus) derived from animals trapped in Alberta, Canada. Lactating females were tested for their behavior toward intruder males during the time of postpartum estrus while housed in a two-cage apparatus containing a defensible nest area. Prior to being used as intruders, sexually naive males were screened for their behavior toward a newborn pup (83% exhibited infanticide). Only infanticidal males were then housed in pairs and allowed to establish a dominance hierarchy. Dominance status was further verified by a urine marking test. The dominant and subordinate infanticidal males were then placed into a lactating female's cage and observed for 1 hr. The test was terminated immediately when a male began to attack the pups. Lactating females attacked the males in both groups, but subordinate males received more intense attacks than dominant males. Dominant males elicited significantly more fear/defense behavior than subordinate intruders. All of the dominant males and only one submissive male attacked the pups. Females were thus successful in blocking infanticide only by infanticidal subordinate males. Since females do not persist in attacking males with high fighting ability, one function of maternal aggression could be to assess the fighting, and resource holding, potential of a future mate. © 1994 Wiley-Liss, Inc.     

Responses of virgin mice, and of maternal females, to normal and caesarian-section delivered pups.

Pups were presented to adult mice of the Porton strain. Significantly more mothers and virgin females retrieved pups to the nest than did virgin males. More virgin females than males licked pups, built nests and assumed lactation posture. Differences were significant even if males that attacked pups were excluded from consideration. Latencies to first appearance of maternal activities were higher than reported by most other workers. Possible genetic strain differences in the response of virgin mice to pups are discussed. In Experiment 2 pups delivered by caesarian section with placentas attached were used. More mothers than either virgin males or females cleaned and accepted pups, indicating that pup cleaning may be controlled by factors different from those influencing other maternal activities.     

The effects of acute stress and pubertal development on metabolic hormones in the rat

A dramatic change in stress responsiveness occurs during pubertal development such that stress-induced corticosterone secretion in prepubertal animals takes 45-60 min longer to return to baseline compared to adults. Though corticosterone is known to influence energy mobilization, it is presently unknown whether stressors affect other hormones important in energy utilization and metabolism differentially in animals before and after pubertal development. Therefore, we exposed prepubertal (28 days of age) and adult (77 days of age) male rats to a single 30 min session of restraint stress in either the light or dark phase of the animals' light-dark (LD) cycle and measured plasma glucose, insulin and thyroid hormones (thyroxine (T4) and triiodothyronine (T3)). We found similar stress-induced increases in plasma glucose levels in prepubertal and adult animals in the LD phase of the LD cycle. We also found that prepubertal animals have lower circulating insulin and total and free T4 levels, but higher total and free T3 levels compared to adults in both the light and dark phases (LD). Interestingly, insulin and thyroid hormone levels were unaffected by acute stress at either age or time of day. These data indicate that, despite prepubertal animals showing an extended glucocorticoid stress response after a single acute exposure to stress, glucose levels are similarly affected by acute stress in prepubertal and adult animals. Furthermore, though stage of development significantly affects the levels of peripheral metabolic hormones such as insulin, T4 and T3, acute stress does not appreciably influence their secretion before or after puberty.     

Risk assessment behaviors associated with corticosterone trigger the defense reaction to social isolation in rats: role of the anterior cingulate cortex

The extent to which the hypothalamic-pituitary-adrenal axis is activated by short-term and long-term consequences of stress is still open to investigation. This study aimed to determine (i) the correlation between plasma corticosterone and exploratory behavior exhibited by rats subjected to the elevated plus maze (EPM) following different periods of social isolation, (ii) the effects of the corticosterone synthesis blocker, metyrapone, on the behavioral consequences of isolation, and (iii) whether corticosterone produces its effects through an action on the anterior cingulate cortex, area 1 (Cg1). Rats were subjected to 30-min, 2-h, 24-h, or 7-day isolation periods before EPM exposure and plasma corticosterone assessments. Isolation for longer periods of time produced greater anxiogenic-like effects on the EPM. However, stretched attend posture (SAP) and plasma corticosterone concentrations were increased significantly after 30?min of isolation. Among all of the behavioral categories measured in the EPM, only SAP positively correlated with plasma corticosterone. Metyrapone injected prior to the 24?h isolation period reversed the anxiogenic effects of isolation. Moreover, corticosterone injected into the Cg1 produced a selective increase in SAP. These findings indicate that risk assessment behavior induced by the action of corticosterone on Cg1 neurons initiates a cascade of defensive responses during exposure to stressors.