Effects of litter‐overlapping on emotionality,stress response,and reproductive functions in male and female rats

In rats, mating at postpartum estrus and delayed dispersal of the young would result in the overlapping of two different‐age litters. As a consequence, newborn pups' early experience will include not only that acquired during the interaction with the mother and age‐matched littermates, but also with older siblings. As early‐life experience modulates rodents' brain function, behavior and reproduction, we aimed to assess how changes in the early environment provoked by the overlapping of litters would affect emotionality, stress response and reproductive functions of male and female pups during adulthood. Results showed that both male and female overlapped reared pups exhibited a reduced behavioral inhibition in the open field test during adulthood. In addition, overlapped reared adult females, but not males, showed a blunted corticosterone response to an acute stressor during diestrus and a reduction in sexual behavior. In summary, natural changes in early experience provoked by the overlapping of litters, long‐term modulate affective and reproductive behaviors, and the endocrine stress response in a sex dimorphic manner. © 2008 Wiley Periodicals, Inc. Dev Psychobiol 51: 259–267, 2009     

Neonatal social isolation alters both maternal and pup behaviors in rats

The development of emotional behavior is dependent on the early experiences of the infant and the quality of maternal care. In these experiments, the effects of social isolation during the preweaning period on both pup behavior and maternal responsivity were examined. In the first study, the number of ultrasonic vocalizations (USVs) emitted after brief maternal separation was measured in neonatal rats with differing histories of social isolation. The social isolation procedure consisted of 5 days of daily separation from the dam and littermates for either 3 or 6 hr. At both ages tested, socially isolated pups vocalized significantly less than control pups. In the second study, the effects of prior isolation either daily for 5 previous days (Chronic Isolation) or for 4 hr prior to testing (Acute Isolation) were examined in a T-maze choice test. Pup vocalizations in the presence of the dam and dams' maternal behavior were assessed. When the dam was confined to the start box or during the maternal free access period, both Chronic and Acute Isolates vocalized less than pups that had never left the home nest. Dams spent more time with and licked and groomed more frequently and for a longer time both Chronic and Acute Isolates compared to pups that had always been with dams in the home nest. These results suggest that early isolation experience can alter subsequent responses to separation stress in neonatal rats and that maternal behavior is sensitive to the prior experiences of offspring.     

Incubator rearing of infant rats without the mother: Effects on adult emotionality and learning

Eight newborn rats, from 3 litters, were separated from the mother and reared during the usual 3-week nursing period in an artificial environment which included an incubator, a warm, moist, pulsating surrogate mother, and special feeding procedures. The incubator animals showed some superiority over mother-reared littermates in performance on the Hebb-Williams test; and, on measures taken in the open field, the incubator animals showed a greater change over trials. Contrary to previous experimental results, our findings indicate that, at least in the rat, maternal deprivation may affect behavioral patterns but does not necessarily and inevitably result in a deficit in adult behavior.     

Effects of male odor during infancy on the maturation, behavior, and reproduction of female mice

Infant female mice who were exposed to the odor of adult male mice of the same strain in the presence or absence of the mother were compared with mice who were not exposed with respect to maturation, open-field behavior, and reproductive success. Exposure lasted 4 hr daily during days 4–18 post-partum. No significant differences were found between the groups in their rates of growth or the age of ear, eye, and vaginal opening. However, the exposed groups displayed first estrus significantly earlier than non-exposed groups: the group exposed in the presence of the mothers showing the earliest first estrus of all 4 groups.     

Effects of preweaning exposure to novel maternal odors on maternal responsiveness and selectivity in adulthood

We examined the effects of odor exposure in the nest on the offspring's subsequent adult responsivity to pups scented with the same odor or a different odor. It was hypothesized that animals receiving exposure to the odor in the nest would be more maternally responsive to pups scented with the (same) exposed odor than to unscented (water-scented) pups. In the first part of the study (Part A), Sprague-Dawley female rat pups (days 1-18 of age) either received exposure to an artificial lemon odor or to the natural (water) odor in the nest. In the second part of the study (Part B), rat pups were exposed daily to lemon or neutral odorants in an incubator at a distance from the mother and the nest. On day 21, animals received odor preference tests for lemon versus neutral pine bedding. On day 60, animals were mated and their pups were removed at 15-min intervals at the time of parturition. Animals were then tested for maternal behavior to foster pups on day 1 or 7 after parturition. Foster pups were scented either with the lemon odor or with water (unscented). Early exposure to lemon in the nest context enhanced animals' attraction to the lemon odor in juvenile tests. In adult maternal tests, exposure to odor on the mother and in the nest had two effects. It increased the latency for animals to express maternal behavior; however, once mothers expressed maternal behavior, they spent more time licking and crouching over pups scented with the same odorant to which they had been exposed earlier on their own mothers. Simple exposure to the lemon odorant out of context of the nest had no effect on adult maternal latencies or behavior.     

Maternally separated rats show deficits in maternal care in adulthood

Although there is considerable research on the phenomenology, neuroendocrinology, neuroanatomy, and sensory control of maternal behavior, little is known about the influences of early postnatal and postweaning experiences on the development of maternal behavior. The purpose of this study was to assess how early life separation from the mother rat affects development of the offspring's juvenile and adult maternal behavior. From postnatal Days 1 to 17, 3 female rats within each litter were separated (SEP) from the mother and the rest of the litter for 5 hr daily while 3 of their sisters were not maternally separated (NSEP). On postnatal Day 21, all subjects were weaned and randomly assigned to one of three juvenile conditions. One female from both SEP and NSEP groups was either isolated (I), given a social conspecific (S), or given 1- to 4-day-old pups (P) for 5 consecutive days. Maternal behavior of SEP and NSEP animals was assessed and recorded on each of the 5 days. Once all animals reached adulthood, they were mated, gave birth, and were assessed for their maternal behavior. We found that the effects of maternal separation on juvenile maternal-like behaviors were minimal. On the other hand, maternal separation reduced adult maternal licking and crouching over pups. In addition, there was a significant interaction between postnatal and juvenile experience on maternal crouching in maternal animals. These results are discussed in terms of the variety of possible behavioral, endocrine, and neurochemical mechanisms that mediate the effects of early life experiences on adult maternal behavior.     

Effects of adrenalectomy on maternal behavior in rats

One week prior to mating, female rats were adrenalectomized or sham-operated and, immediately following parturition, each was given a foster litter of 10 newborn pups from a mother in the same group. Retrieving measures at the time of fostering revealed no significant differences between the 2 groups. Over 16 days of maternal behavior observations the adrenalectomized mothers spent more time in the nest, more time in an active suckling position, and tended to keep the pups in the nest over a longer period of time. These results provide evidence that a functioning adrenal is not necessary for the initiation or maintenance of maternal responsiveness in rats.     

Effects of early deprivation and maternal separation on pup-directed behavior and HPA axis measures in the juvenile female rat

Juvenile female rats show maternal-like behavior toward pups. The purpose of the following experiment was to investigate whether the HPA axis, through the use of early separation manipulations that alter HPA functioning in rats, plays a role in the juvenile response to foster pups. Female rats were early deprived or maternally separated for 5 hours daily from PND 2 to 14 and compared to animal facility-reared rats. Deprivation or separation increased CRH-R1 IR in the juvenile PVN, but had no other effects on other HPA measures or on maternal behavior. Pup-exposure during the juvenile period blunted corticosterone levels after acute and repeated pup-exposures when compared to exposure to novelty and conspecifics respectively. Repeated exposures to pups also increased CRH-R1 IR relative to isolation during the juvenile period. Overall, the data suggest that although pup-exposure affects corticosterone levels, the HPA axis does not relate to juvenile maternal behavior in the present experiments.     

Maternal care affects the development of maternal behavior in inbred mice

The present study investigated the effects of variations in maternal behavior on the development of maternal behavior of female offspring in BALB/c and CBA/Ca inbred mice. In Experiment 1, we conducted fostering within or between the two strains and observed the maternal behaviors of mothers and female offspring for 2 weeks postpartum. Although fostering changed the maternal behavior of mothers in both strains, CBA mothers generally showed greater frequency of nursing posture and pup licking than BALB mothers. BALB female offspring reared by CBA mothers showed more body licking than those reared by BALB mothers, whereas fostering did not affect the maternal behavior of CBA female offspring. In Experiment 2, we examined the maternal behavior of females of F1 hybrids derived from reciprocal crosses between the two strains to confirm the maternal effect demonstrated in Experiment 1. Female F1 hybrids from CBA mothers showed more arched‐back nursing, body licking, and nest building than those from BALB mothers. These results suggested that maternal care affect the development of maternal behavior in inbred mice, though the contributions of genetic and prenatal factors cannot be ignored. © 2009 Wiley Periodicals, Inc. Dev. Psychobiol 51: 345–357, 2009.     

Sexual behavior of male and female septal lesioned rats

Gonadectomized male and female rats were given septal lesions (SL) or sham surgery at approximately 60 days of age. After 3 weeks lordosis behavior tests were initiated. Females were tested after daily injections of 2 μg estradiol benzoate (EB) for 3 days, while males were tested after EB only (2 μg×3 days), and after EB plus progesterone (Prog). The mean lordosis quotients (LQ) of septal lesioned female rats were significantly higher than those of sham operated controls. No increase in lordosis responding was seen in male rats with either EB alone or EB+Prog. Following an additional 3 week interval without steroid treatment masculine behavior tests began. All animals received a pretest and were tested again on Day 4, 7, 11 and 15 daily tesosterone propionate (150 μg/day) treatment. No alterations in masculine sexual behavior (relative to that of controls) were found in either male or female septal lesioned rats. It is concluded that the increased hormone sensitivity is specific for lordosis behavior, at least when the SL are given in adulthood.     

Maternal food restriction: Effects on offspring behavior and development

Pregnant rats were placed on reduced food intake or remained on adequate diet during gestation and lactation. Offspring were cross-fostered to provide for independent experiences of prenatal and/or postnatal mother malnutrition. All offspring were placed on an ad lib diet at time of weaning. When evaluated in adulthood, offspring whose mother was food-deprived during the lactation period showed body weight deficits and increased errors on the Hebb-Williams maze as compared to controls. There were no observed effects of the prenatal deprivation.     

Mother-infant interactions in two strains of rats: Implications for dissociating mechanism and function of a maternal pattern

Mother-infant interaction was observed in Long-Evans and Fischer 344 rats after fostering within or across strains. Interactions immediately following introduction of foster pups to the cage as well as undisturbed interactions with resident litters were examined. Some differences were related to alien status, some to strain of pups, and others to strain of dams. Greater responsiveness to pups of the maternal strain was exhibited in retrieval and body licking. Long-Evans pups received more crouching from dams of both strains 3-12 days postpartum, perhaps because they are significantly larger. Regardless of pup strain, Long-Evans dams engaged in more maternal licking than did F344 dams, and this was more likely directed to the anogenital region. Dams of both strains were more likely to lick male than female pups, regardless of pup strain. The strain difference in maternal licking is consistent with adult strain differences in water and salt appetite and may contribute developmentally to the superior copulatory performance of Long-Evans males. © 1997 John Wiley & Sons, Inc. Dev Psychobiol 30: 310–312, 1997     

Induction of maternal behavior in adult female rats following chronic morphine exposure during puberty

The peripubertal period in the female rat is the time when the stimulatory effects of opioids on prolactin (PRL) secretion develop. In the adult rat, the administration of chronic high-dose morphine has been shown to attenuate the ability of opiates to stimulate PRL secretion. One function of PRL in adult virgin rats is the induction of maternal behavior. The present study examined whether chronic high-dose morphine exposure during the peripubertal period alters PRL-mediated induction of maternal behavior in adult female rats. Two groups of juvenile female rats were administered increasing doses of morphine or vehicle (s.c.) from age 30 to 50 days. As adults, these females either remained intact, or were ovariectomized and treated with a PRL-dependent, steroid hormone regimen that stimulates a rapid onset of maternal behavior. All females were then exposed daily to rat foster pups to determine whether peripubertal morphine exposure affected their latencies to induce maternal behavior. Morphine treatment resulted in a delay in vaginal opening and a temporary reduction in the rate of weight gain; however, the rate of onset of maternal behavior was unaffected by peripubertal morphine treatment. Thus, chronic morphine exposure in the pubertal female did not impact the expression of pup-induced maternal care.     

Intergenerational transmission of maternal behavior in rhesus macaques and its underlying mechanisms

Thirteen group-living rhesus macaque females that were crossfostered shortly after birth were followed longitudinally until they gave birth for the first time. Their maternal behavior was compared to the behavior of both their foster and their biological mothers, and analyzed in relation to the cerebrospinal fluid (CSF) concentrations of serotonin, dopamine, and norepinephrine metabolites (5-HIAA, HVA, and MHPG) measured in their second year of life. Crossfostered females were similar to their foster mothers in their rates of maternal rejection and grooming, whereas their contact-making behavior was more similar to that of their biological mothers. Crossfostered females with lower CSF concentrations of 5-HIAA exhibited higher rates of maternal rejection than females with higher CSF 5-HIAA. In a related article (Maestripieri et al., 2006), we reported that rhesus infants reared by highly rejecting mothers had lower CSF 5-HIAA in their first 3 years of life. Taken together, these findings suggest that early social experience and experience-related long-term changes in serotonergic function may play a role in the intergenerational transmission of maternal rejection from mothers to daughters.     

Effects of copulation on reproductive function in aged female rats

Old female rats in persistent vaginal estrus (PVE) were exposed to varying degrees of copulatory stimulation. While limited mating experiences had no noticeable effects on reproductive function, cohabitation with sexually vigorous males or other forms of exposure to extended mating experiences disrupted the PVE state. Prolonged diestrus, irregular cycles, pseudopregnancy and pregnancy were observed subsequent to extensive copulatory experiences. Except for a tendency to be less receptive to initial mounts old females displayed sexual behavior comparable to that observed in younger, virgin animals. Ten or more intromissions disrupted the PVE. Induction of pregnancy or pseudopregnancy appears to require 30 or more intromissions in these animals. It is concluded that the PVE observed in aged female rats is at least partly due to the absence of coital stimulation. These observations are taken to suggest that age-related changes in the reproductive capacity of female rats may be attributable to alterations in the sensitivity of ovulatory and progestational mechanisms to hormonal and sensory influences.     

Long-term effects of postnatal manipulation on emotionality are prevented by maternal anxiolytic treatment in mice

This study investigated the role of maternal behavior on the long-term effects of postnatal manipulation (15 min of daily separation from the dam and exposure to clean bedding from Day 1 to Day 14 of postnatal life) on emotionality in the mouse. Mothers were treated with an antianxiety agent (Chlordiazepoxide: 5 mg/kg), daily upon removal of the litter from the nest. Emotionality in adult offspring was tested in the elevated plus maze. Mice manipulated during postnatal development were more explorative and less anxious than unhandled mice, but this effect was not observable in the offspring of Chlordiazepoxide-treated dams. No effect of maternal Chlordiazepoxide was observed in unhandled offspring. The pharmacological treatment of the mother did not affect either pups' ultrasonic calling during separation, or maternal behavior far apart from the daily manipulation sessions. By contrast, Chlordiazepoxide-treated dams were less responsive toward pups upon reunion following daily separation. This alteration of dams' behavior was not related to alterations in the amount of ultrasonic calls emitted by pups during reunion. Finally, when dams were daily injected with Chlordiazepoxide far apart from pups' removal, the pharmacological treatment was devoid of effects. These results support the view that the mother–infant interaction which follows separation plays a major role in determining the effects of postnatal manipulations on adult emotionality. © 1998 John Wiley & Sons, Inc. Dev Psychobiol 32: 225–234, 1998